UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO POSGRADO EN CIENCIAS BIOLÓGICAS FACULTAD DE CIENCIAS SISTEMÁTICA BIOGEOGRAFÍA EVOLUTIVA DE LAS ISLAS DEL PACÍFICO MEXICANO TESIS QUE PARA OPTAR POR EL GRADO DE: DOCTORA EN CIENCIAS PRESENTA: PATRICIA GUADALUPE GARCÍA NAVARRETE TUTOR PRINCIPAL DE TESIS: DR. JUAN JOSÉ MORRONE FACULTAD DE CIENCIAS, UNAM. MIEMBROS DEL COMITÉ TUTOR: DRA. TANIA ESCALANTE ESPINOSA FACULTAD DE CIENCIAS, UNAM DR. DAVID NAHUM ESPINOSA ORGANISTA FACULTAD DE ESTUDIOS SUPERIORES ZARAGOZA, UNAM Ciudad Universitaria, CDMX. Octubre, 2024 UNAM – Dirección General de Bibliotecas Tesis Digitales Restricciones de uso DERECHOS RESERVADOS © PROHIBIDA SU REPRODUCCIÓN TOTAL O PARCIAL Todo el material contenido en esta tesis esta protegido por la Ley Federal del Derecho de Autor (LFDA) de los Estados Unidos Mexicanos (México). El uso de imágenes, fragmentos de videos, y demás material que sea objeto de protección de los derechos de autor, será exclusivamente para fines educativos e informativos y deberá citar la fuente donde la obtuvo mencionando el autor o autores. Cualquier uso distinto como el lucro, reproducción, edición o modificación, será perseguido y sancionado por el respectivo titular de los Derechos de Autor. PROTESTA UNIVER" "CT 02 TT HONESTIDAD ACADÉMICA Y PROFESIONAL (Graduación con trabajo escrito) De conformidad con lo dispuesto en los artículos 87, fracción V, del Estatuto General, 68, primer párrafo, del Reglamento General de Estudios Universitarios y 26, fracción I, y 35 del Reglamento General de Exámenes, me comprometo en todo tiempo a honrar a la institución y a cumplir con los principios establecidos en el Código de Ética de la Universidad Nacional Autónoma de México, especialmente con los de integridad y honestidad académica. De acuerdo a lo anterior, manifiesto que el trabajo escrito titulado: BIOGEOGRAFÍA EVOLUTIVA DE LAS ISLAS DEL PACÍFICO MEXICANO Que presenté para obtener el grado de DOCTOR(A) EN CIENCIAS, es original, de mí autoría y lo realicé con rigor metodológico exigido por el Programa de Posgrado en Ciencias Biológicas, citando las fuentes de ideas, textos, imágenes, gráficos u otro tipo de obras empleadas para su desarrollo. En consecuencia, acepto que la falta de cumplimiento de las disposiciones reglamentarias y normativas de la Universidad, en particular las ya referenciadas en el Código de Ética, llevará a la nulidad de los actos de carácter académico administrativo del proceso de obtención de mi grado académico. Atentamente M GARCIA NAVARRETE PATRICIA GUADALUPE No. de cuenta UNAM: 517007569 (Nombre, firma y número de cuenta del estudiante) UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO POSGRADO EN CIENCIAS BIOLÓGICAS FACULTAD DE CIENCIAS SISTEMÁTICA BIOGEOGRAFÍA EVOLUTIVA DE LAS ISLAS DEL PACÍFICO MEXICANO TESIS QUE PARA OPTAR POR EL GRADO DE: DOCTORA EN CIENCIAS PRESENTA: PATRICIA GUADALUPE GARCÍA NAVARRETE TUTOR PRINCIPAL DE TESIS: DR. JUAN JOSÉ MORRONE FACULTAD DE CIENCIAS, UNAM. MIEMBROS DEL COMITÉ TUTOR: DRA. TANIA ESCALANTE ESPINOSA FACULTAD DE CIENCIAS, UNAM DR. DAVID NAHUM ESPINOSA ORGANISTA FACULTAD DE ESTUDIOS SUPERIORES ZARAGOZA, UNAM Ciudad Universitaria, CDMX. Octubre, 2024 COORDINACIÓN GENERAL DE ESTUDIOS DE POSGRADO COORDINACIÓN DEL POSGRADO EN CIENCIAS BIOLÓGICAS FACULTAD DE CIENCIAS OFICIO: CGEP/CPCB/FC/0364/2024 ASUNTO: Oficio de Jurado M. en C. Ivonne Ramírez Wence Directora General de Administración Escolar, UNAM Presente Me permito informar a usted que en la reunión ordinaria del Comité de Posgrado en Ciencias Biológicas, celebrada el día 26 de febrero de 2024 se aprobó el siguiente jurado para el examen de grado de DOCTORA EN CIENCIAS de la estudiante GARCÍA NAVARRETE PATRICIA GUADALUPE con número de cuenta 517007569 con la tesis titulada: “Biogeografía evolutiva de las islas del Pacífico mexicano”, realizada bajo la dirección del DR. JUAN JOSÉ MORRONE: Presidente: DR. ANTONIO ALFREDO BUENO HERNÁNDEZ Vocal: DRA. MARÍA HILDA FLORES OLVERA Vocal: DR. ENRICO ALEJANDRO RUIZ CASTILLO Vocal: DRA. IRENE GOYENECHEA MAYER-GOYENECHEA Secretario: DRA. TANIA ESCALANTE ESPINOSA Sin otro particular, me es grato enviarle un cordial saludo. ATENTAMENTE “POR MI RAZA HABLARÁ EL ESPÍRITU” Ciudad Universitaria, Cd. Mx., a 02 de mayo de 2024 COORDINADOR DEL PROGRAMA COORDINACIÓN c. Cc. p. Expediente del alumno ACBB/AAC/GEMF/EARR/mnm COORDINACIÓN DEL POSGRADO EN CIENCIAS BIOLÓGICAS Unidad de Posgrado, Edificio D, 1 Piso. Circuito de Posgrados, Ciudad Universitaria Alcaldía Coyoacán. C. P 04510 CDMX Tel. (+5255)5623 7002 http://pcbiol. posgrado. unam.mx/ AGRADECIMIENTOS INSTITUCIONALES Al Posgrado en Ciencias Biológicas de la Universidad Nacional Autónoma de México (UNAM). Al Consejo Nacional de Humanidades, Ciencias y Tecnologías (CONAHCyT) por su contribución al fortalecimiento de las comunidades científicas y por brindar apoyo a mi investigación a través del programa de becas nacionales (CVU: 444876). A la Universidad Nacional Autónoma de México, a la Facultad de Ciencias y al Museo de Zoología “Alfonso L. Herrera” (Entomología). A mi tutor principal, Dr. Juan José Morrone, y a los miembros del Comité Tutor, Dra. Tania Escalante Espinosa y Dr. David Nahum Espinosa Organista AGRADECIMIENTOS A TÍTULO PERSONAL A mis tutores: Juan José Morrone, Tania Escalante y David Espinosa. A los sinodales de mi candidatura: Dra. Mercedes Isolda Luna Vega, Dra. María Patricia Velasco de León, Dr. José Luis Villaseñor Ríos, Dr. Octavio Rafael Rojas Soto y la Dra. Tania Escalante Espinosa. Al jurado de mi examen de grado: Dr. Antonio Alfredo Bueno Hernández, Dra. María Hilda Flores Olvera, Dr. Enrico Alejandro Ruíz Castillo, Dra. Irene Goyenechea Mayer-Goyenechea y Dra. Tania Escalante Espinosa. Al Dr. Luis Antonio Sánchez-González, Dr. Constantino González Salazar, Dra. Leticia Ochoa Ochoa, M. en C. Gerardo Soria Ortiz y M. en C. Armando Rincón Gutiérrez por su contribución y orientación en los artículos de investigación y proyectos. A mi familia, los García-Navarrete. A mi familia, los Gutiérrez-García. A mis compañeros de oficina: Isvi y Brandy DEDICATORIA A las mujeres en la ciencia A la comunidad científica A las generaciones venideras, con la esperanza de que encuentren en la educación una senda amplia y accesible hacia el conocimiento sin importar género ni origen. ¡Que este trabajo contribuya a un futuro donde la ciencia esté al servicio de los mexicanos! ¡Qué solo y amplio el mar Pacífico! ¡Qué rumores hostiles e inexorables bajo sus olas sin costa! Porque el Pacífico era, sin duda, el más viejo de los mares, el primero de todos ellos, cuando en el mundo no había tierra y todo consistía solamente en un errar sin meta y sin principio. [...] ¿Qué pueden ser las Islas? No una tierra sino un gesto; escena pura, drama monstruosamente simple y apagado, sin recurso hacia la vida, como un golpe pequeño y débil que se diera en lo más hondo del mar. Algo lejano y amarillo, sin referencia. [...] Las Islas Marías son, a lo más, una idea, un concepto, nunca un lugar situado en el tiempo y en el espacio. Los muros de agua José Revueltas ÍNDICE RESUMEN..................................................................................................................................... 1 ABSTRACT .................................................................................................................................. 3 INTRODUCCIÓN GENERAL.................................................................................................... 5 CAPÍTULO I: Biogeografía evolutiva del Archipiélago Revillagigedo, México ..................... 8 Publicación: García-Navarrete P.G., Escalante T., Espinosa D., Morrone J.J. 2023.Evolutionary biogeography of the Revillagigedo Archipelago, Mexico. Journal of Natural History. 57: 9-12, 685-709. https://doi.org/10.1080/00222933.2023.2203337 .... 8 CAPÍTULO II: Afidades biogeográficas de la biota de las Islas Marías, Mexico................. 34 Publicación: García-Navarrete P.G., Sánchez-González L.A., Morrone J.J. 2023. Biogeographical affinities of the biota of the Tres Marías Islands, Mexico. Biological Journal of the Linnean Society, blad101 https://doi.org/10.1093/biolinnean/blad101 .... 34 DISCUSIÓN GENERAL Y CONCLUSIONES ....................................................................... 51 REFERENCIAS BIBLIOGRÁFICAS ...................................................................................... 55 ANEXO: PUBLICACIONES INDEPENDIENTES DEL TEMA DE TESIS. RESULTADO DE ACTIVIDADES ACADÉMICAS COMPLEMENTARIAS .................... 58 I.Interacciones potenciales parásito-hospedero entre Dendroctonus y Pinus en México...... 58 Publicación: García-Navarrete P.G., Soria-Ortiz G.J., González-Salazar C. 2021. Interacciones potenciales parásito-hospedero entre el escarabajo Dendroctonus (Coleoptera: Scolytidae) y Pinus (Pinaceae) en México. Revista de Biología Tropical, 69(3): 1004-1022. https://dx.doi.org/10.15517/rbt.v69i3.45910 ........... 58 II. ... Distribución potencial de los híbridos entre Crocodylus acutus y Crocodylus moreletii en la costa del Pacífico mexicano fuera de su zona natural de hibridación .................................. 59 Publicación: Soria-Ortiz G.J., García-Navarrete P.G., Ochoa-Ochoa L.M., Rincón-Gutiérrez A. 2022. Potential distribution of hybrids between Crocodylus acutus and Crocodylus moreletii on the Mexican Pacific coast outside the natural hybridistion zone. Herpetological Journal, 32(3): 93-101. http://doi.org/10.33256/32.393101 ........................................................................ 59 1 RESUMEN Los elementos insulares en México, aunque representan solo el 0.3% de la superficie total del país, desempeñan un papel crucial en la biodiversidad como hábitats clave para la alimentación, reproducción y refugio de diversas especies. Aunque se han aplicado varios enfoques de estudio a las islas, se observa la falta de un análisis integral de ellas y sus comunidades biológicas. En respuesta a esta necesidad, en esta tesis se propone la aplicación de la biogeografía evolutiva como un método multidisciplinario que integra diversos enfoques y métodos biogeográficos, permitiendo una comprensión más exhaustiva de la historia biogeográfica de las islas. En este sentido, el Archipiélago de Revillagigedo y las Islas Marías emergen como ecosistemas de investigación fundamentales. La ubicación de estas islas es estratégica en el Pacífico mexicano, así como sus características geológicas y bióticas distintivas, las cuales las convierten en laboratorios ideales para explorar los procesos de evolución y especiación. Este estudio se centra en un análisis biogeográfico integral de los archipiélagos de Revillagigedo y las Islas Marías en el Pacífico mexicano. El objetivo principal fue inferir la historia biogeográfica de la biota insular y describir su relación con la región continental de México. A través de diversos análisis, se busca clarificar la conexión de estos archipiélagos con el continente y presentar un escenario geobiótico singular en el centro del Pacífico mexicano. El análisis biogeográfico evolutivo aplicado en islas facilita la determinación y corroboración de los componentes bióticos insulares. Este enfoque integra la escala espaciotemporal mediante la identificación de cenocrones y la propuesta de un escenario geobiótico, proporcionando un marco para comprender la posible formación de la biota de las islas. La presente tesis se estructura en dos capítulos, cada uno abordando aspectos específicos de las islas, su biota y su relación con el contexto geográfico y geológico. El primer capítulo analiza la biota de Revillagigedo, proponiendo un marco biogeográfico histórico. En este capítulo se utilizó un análisis de parsimonia de endemismos con eliminación progresiva de caracteres y un análisis cladístico. El Archipiélago se identificó como un nodo biogeográfico, se clasificó como un distrito dentro de la provincia de las Tierras Bajas del Pacífico. La hipótesis geobiótica sugiere la llegada de cenocrones Neártico y Neotropical durante e Plioceno-Pleistoceno. En el segundo capítulo se aborda la afinidad biogeográfica de la biota de las Islas Marías. El análisis se realizó 2 en tres etapas: identificación de componentes bióticos, evaluación biogeográfica cladística y mapeo de patrones de afinad utilizando la información filogenética. Se identificaron tres componentes bióticos y tres patrones de afinidad (Neotropical, Sonorense-Neotropical, Neártico- Neotropical). La historia biogeográfica de las islas se vincula con eventos tectónicos y fluctuaciones del nivel del mar que permitieron procesos de vicarianza y dispersión. En conjunto, estos capítulos ofrecen una visión detallada de la evolución biogeográfica de ambos archipiélagos en el contexto histórico. Los procesos de colonización y dispersión desde el continente hacia las islas han jugado un papel crucial en la formación de su biota. Esta investigación destaca al ser pionera en analizar la información de dos archipiélagos del Pacífico mexicano con el propósito de comprender la historia evolutiva de la región insular del Pacífico de México, con base en la formulación y contrastación de hipótesis biogeográficas que, a su vez, contribuirán a la conservación de estos ecosistemas insulares. 3 ABSTRACT Insular elements in Mexico, though they represent only 0.3% of the country’s total surface area, play a crucial role in biodiversity as key habitats for feeding, reproduction, and refuge of diverse species. Although several studies have been applied to the islands, there is a lack of a comprehensive analysis of these ecosystems and their biological communities. In response to this need, this thesis proposes the application of evolutionary biogeography as a multidisciplinary method that integrates diverse biogeographic approaches and methods, allowing for a more comprehensive understanding of the biogeographic history of the islands. In this sense, the Revillagigedo Archipelago, and the Tres Marías Islands emerge as fundamental research ecosystems. The strategic location of these islands in the Mexican Pacific, as well as their unique geological and biotic characteristics, make them ideal laboratories for studying the processes of evolution and speciation. This study focuses on a comprehensive biogeographic analysis of the Revillagigedo and Tres Marías archipelagos in the Mexican Pacific. The main objective was to infer the biogeographic history of the island’s biota and to describe its relationship with the Mexican mainland. Through diverse analyses, it seeks to clarify the connection of these archipelagos with the mainland and to present a unique geobiotic scenario in the central Mexican Pacific. Evolutionary biogeographic analysis applied to islands facilitates the identification and corroboration of island biotic components. This approach integrates the spatiotemporal scale through the identification of cenocrons and the proposal of a geobiotic scenario, providing a framework for understanding the possible assembly of the biota of the islands. This thesis is structured in two chapters, each one addressing specific aspects of the islands, their biota, and their relationship with the geographic and geological context. The first chapter analyzes the biota of Revillagigedo, proposing a historical biogeographical framework. This chapter utilized a parsimony analysis of endemism with progressive character elimination and a cladistic analysis. The archipelago was identified as a biogeographic node and classified as a district within the Pacific Lowlands province. The geobiotic hypothesis suggests the arrival of Nearctic and Neotropical cenocrons during the Pliocene-Pleistocene. The second chapter discusses the biogeographic affinity of the biota of the Tres Marías Islands. The analysis was conducted in three stages: identification of biotic components, cladistic biogeographic 4 evaluation, and mapping of affinity patterns using phylogenetic information. Three biotic components and three affinity patterns (Neotropical, Sonoran-Neotropical, Nearctic-Neotropical) were identified. The biogeographic history of the islands is linked to tectonic events and sea level fluctuations that allowed vicariance and dispersal processes. Together, these chapters provide a detailed overview of the biogeographic evolution of both archipelagos in the historical context. Colonization and dispersal processes from the continent to the islands have played a crucial role in the formation of their biota. This research stands out as a pioneer in the analysis of the information from two Mexican Pacific archipelagos to understand the evolutionary history of the Pacific Island region of Mexico, based on the formulation and falsification of biogeographic hypotheses that, in turn, will contribute to the conservation of these ecosystems. 5 INTRODUCCIÓN GENERAL México, con una extensión territorial de 1,964,375 km2, alberga un conjunto de islas que representan aproximadamente el 0.3% de su superficie total, abarcando 5,127 km2. Estos elementos insulares comprenden una variada gama de formas geográficas como islas verdaderas, islotes, arrecifes, cayos y rocas, sumando más de 4,000 en todo el territorio nacional (INEGI, 2019). En el Pacífico mexicano las islas se pueden dividir en tres áreas: el Golfo de California, en donde las islas más representativas son Pelícano, Montague, Tiburón y Ángel de la Guarda; la costa oeste de la península de Baja California, en donde se encuentran las islas Cedros y Guadalupe; y el Pacífico central mexicano, donde se localiza el archipiélago de Revillagigedo y las Islas Marías (INEGI, 2016). Los ecosistemas insulares de México se caracterizan por la presencia de numerosas especies endémicas, lo cual resalta la singularidad y la riqueza de su biodiversidad; además las islas tienen un papel fundamental como hábitats clave para la alimentación, reproducción, anidación y refugio de especies migratorias (Tershy y Croll, 1994; Lara-Lara et al., 2008; Aguirre Muñoz et al., 2010). En este contexto, las islas son escenarios de estudio privilegiados para la investigación de procesos evolutivos. El aislamiento y las dinámicas ecológicas y geológicas de las islas las convierte en auténticos laboratorios naturales, que permiten analizar los mecanismos que modelan el establecimiento, la adaptación y la especiación de taxones aislados del continente (MacArthur y Wilson, 1967; Whitehead y Jones, 1969; Fernández-Palacios, 2004). Las islas del Pacífico mexicano y su biota han sido objeto de estudio desde diversos conjuntos y enfoques (e. g. Brattstrom, 1990; Casas-Andreu, 1992; Donlan et al., 2000; Tershy et al., 2002; CONANP, 2004; Lara-Lara et al., 2008; Aguirre Muñoz et al., 2010). No obstante, es evidente la ausencia de un enfoque biogeográfico integral que permita una comprensión de estos ecosistemas insulares y sus comunidades biológicas. En este sentido, la biogeografía evolutiva como campo multidisciplinario se presenta como un método con aplicación en el análisis integral de las islas. Este campo implica la implementación de distintos enfoques y métodos biogeográficos en una secuencia de etapas de un mismo análisis, lo cual permite resolver de manera más completa la historia biogeográfica de los taxones que habitan un área determinada (Morrone, 2007). 6 La biogeografía evolutiva de islas ha sido abordada previamente, pero son escasos los trabajos donde se hayan aplicado todas las etapas del análisis propuestas por Morrone (2007). En otros casos, se han empleado métodos biogeográficos, pero su enfoque ha sido más limitado, sin incluir información diversa de manera integral (Vázquez-Miranda et al., 2007; Morrone, 2011; Posadas et al., 2011; Murray y Crother, 2019). La biogeografía evolutiva aplicada en sistemas insulares tiene como objetivos identificar las afinidades de la biota insular, analizar la relación de la biota con el área ancestral, inferir la evolución de los organismos colonizadores e identificar los procesos involucrados en el ensamblaje biótico (Whittaker y Fernández-Palacios, 2007; Morrone, 2011). La aplicación de la biogeografía evolutiva en ecosistemas insulares presenta ventajas significativas. Este enfoque presta atención a las características únicas y propias de cada sistema insular, analiza a las especies establecidas como conjuntos de taxones, describe patrones e infiere procesos, considera las escalas espaciotemporales y ofrece una posible explicación para la evolución simultánea de los taxones y las áreas, con base en eventos geológicos y climáticos (Morrone, 2007, 2009). Dada la escasez de estudios biogeográficos integrativos centrados en ecosistemas insulares, la presente tesis propone utilizar el análisis biogeográfico evolutivo para formular y contrastar hipótesis relacionadas con la evolución biótica de los dos archipiélagos principales del Pacífico mexicano: Revillagigedo y las Islas Marías. A través de diversos análisis, se pretende esclarecer la relación de estas islas con el continente, al mismo tiempo que se busca presentar un escenario geobiótico propio de esta región central del Pacífico mexicano. Esta tesis se compone de dos capítulos, cada uno con enfoques y alcances distintos, donde se abordan aspectos específicos de las islas, su biota y su relación con el contexto geográfico y geológico. Esto proporciona una visión completa y detallada de la evolución de estas islas en el contexto biogeográfico de México. En el primer capítulo se realiza un análisis de la biota del Archipiélago de Revillagigedo con el propósito de proponer un marco biogeográfico histórico, siguiendo los pasos de un análisis biogeográfico evolutivo: 1) identificación de componentes bióticos, 2) comprobación de las relaciones entre estos componentes bióticos, 3) regionalización, 4) identificación de cenocrones, y 5) construcción de un escenario geobiótico. En este capítulo se examinan las afinidades 7 bióticas de Revillagigedo con las regiones Neártica y Neotropical y se investiga si la colonización principal de la biota del archipiélago se llevó a cabo mediante dispersión atravesando la barrera oceánica. El segundo capítulo aborda la afinidad biogeográfica de la biota de las Islas Marías. Este análisis incluyó tres etapas de análisis, en primer lugar, se identificaron los componentes bióticos mediante un Análisis de Parsimonia de Endemismos para generar una hipótesis biogeográfica primaria sobre las relaciones de las áreas. En segundo lugar, se realizó un análisis biogeográfico cladístico de las especies endémicas de las islas para poner a prueba la hipótesis biogeográfica primaria utilizando datos filogenéticos. Por último, se utilizó la información filogenética de las especies endémicas para representar los patrones de distribución geográfica de sus grupos hermanos. Esta información integrada aporta evidencia para comprender la relación de las especies de las Islas Marías con las áreas adyacentes y formular hipótesis sobre el ensamblaje biótico de las islas. El Archipiélago de Revillagigedo y las Islas Marías destacan como dos ecosistemas fundamentales en la biodiversidad mexicana. Esta investigación se erige como un pilar fundamental para comprender la historia biogeográfica de la biota de Revillagigedo y las Islas Marías. Esta investigación aspira no sólo a contribuir al entendimiento de la biogeografía evolutiva de las islas del Pacífico mexicano, sino también a establecer una base sólida para estudios futuros que exploren los mecanismos de ensamblaje de la biota en contextos insulares. Los resultados potencialmente enriquecerán no solo el campo de la biogeografía, sino también la conservación y gestión de los ecosistemas insulares, aportando significativamente a la biodiversidad global. 8 CAPÍTULO I: Biogeografía evolutiva del Archipiélago Revillagigedo, México Publicación: García-Navarrete P.G., Escalante T., Espinosa D., Morrone J.J. 2023.Evolutionary biogeography of the Revillagigedo Archipelago, Mexico. Journal of Natural History. 57: 9-12, 685-709. https://doi.org/10.1080/00222933.2023.2203337 JOURNAL OF NATURAL HISTORY : (5) Taylor 8. Francis 2023, VOL. 57, NOS. 9-12, 685-709 A l https://doi.org/10.1080/00222933.2023.2203337 aylor 8 Francis Group (M) Check for updates Evolutionary biogeography of the Revillagigedo Archipelago, Mexico Patricia G. García-Navarrete (5**, Tania Escalante (5, David Espinosa (3% and Juan J. Morrone(3* “Museo de Zoología “Alfonso L. Herrera”, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), Mexico City, Mexico; *Posgrado en Ciencias Biológicas, Unidad de Posgrado, Edificio D, 1* Piso, Circuito de Posgrados, Ciudad Universitaria, Coyoacán, Mexico City, Mexico; “Grupo de Biogeografía de la Conservación, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), Mexico City, Mexico; “Facultad de Estudios Superiores Zaragoza, Universidad Nacional Autónoma de México (UNAM), Mexico City, Mexico ABSTRACT ARTICLE HISTORY The biotic assembly of the Revillagigedo Archipelago, Mexico, was Received 17 August 2021 analysed under an evolutionary biogeographic framework. We Accepted 12 April 2023 undertook a parsimony analysis of endemicity with progressive char- Published online acter elimination of 194 plant and animal species, which allowed us 12 June 2023 to identify the archipelago as a complex area or node where Nearctic KEYWORDS and Neotropical biotic components overlap. We undertook a cladistic biotic components; dispersal; biogeographic analysis using the phylogenetic information of 42 endemism; island taxon-area cladograms, from which one general-area cladogram biogeography was obtained: (Revillagigedo, (Sonoran, (Baja California, (Veracruzan, Pacific Lowlands)))). These results suggest that the Revillagigedo Archipelago may be classified as a province, although we prefer to keep it as a district of the Pacific Lowlands province. We identified two cenocrons (temporally integrated set of taxa) that can be dated to the Pliocene-Pleistocene: one Nearctic that dispersed from the Baja California Peninsula, and another Neotropical where the species dispersed from the Pacific coast to the islands. The geological information and the general-area cladograms allowed us to propose a geobiotic scenario for the archipelago where the islands are probably the result of volcanism associated with the oceanic Mathematician Ridge, and the arrival of the cenocrons to the archi- pelago may have occurred during the Pliocene-Pleistocene, after the islands were available for colonisation. Introduction Wallace (1881) recognised three types of islands according to their geological origin: ancient continental, recent continental, and oceanic. Recently, Ali (2017) proposed to classify islands according to the colonisation process of their founding ancestors: recent land bridge, recent ice sheet, deep time vicariant and overwater dispersed islands. “Oceanic islands' and 'overwater dispersed islands' refer to islands that derived from events of volcanism or tectonic uplift and that never had a connection with the CONTACT Juan J. Morrone o morroneGciencias.unam.mx Oo Supplemental data for this article can be accessed online at https://doi.org/10.1080/00222933.2023.2203337. O 2023 Informa UK Limited, trading as Taylor 8: Francis Group Published online 12 Jun 2023 9 686 ¡(a P. G. GARCÍA-NAVARRETE ET AL. continental masses (Menard 1986; Santamarta-Cerezal 2016; Ali 2017), hence their biota must have arrived through the ocean or evolved from ancestors that crossed it (MacArthur and Wilson 1967; Paulay 1994; Whittaker et al. 2014). The probability of colonisation of these islands is influenced by the geography, the environmental config- uration, and the attributes of the organisms (MacArthur and Wilson 1967). The biotas of oceanic islands usually lack land birds, mammals, and amphibians that cannot disperse over wide oceans without artificial help, whereas volcanic islands have a good number of birds and insects, and often abundant lizards (Wallace 1881). Oceanic islands have played an important role in the development of biogeography due to their diversity and uniqueness, providing fundamental insights into evolutionary patterns and processes (Darwin 1859; Wallace 1881; MacArthur and Wilson 1967; Whittaker et al. 2014; Ali 2017). At the end of the twentieth century, interest in the biogeography of oceanic islands decreased because the distribution of plants and animals in these environments is strongly modelled by dispersal and it was argued that this process cannot be methodically tested as it is based on random events (Peake 1981; McLennan and Brooks 2002; Halas et al. 2005). The last two decades, however, have shown a renewed interest as it has been acknowledged that dispersal to oceanic islands plays a fundamental role in evolutionary and speciation processes, and in the generation of endemic biotas (Givinish and Renner 2004; Renner 2004; Cook and Crisp 2005; de Queiroz 2005). The Revillagigedo Archipelago is situated in the Northeast Pacific, approximately 720 km west of the state of Colima and 450 km south of the Baja California peninsula, Mexico. It extends over ca. 156 km? and is composed of four islands (Figure 1): Socorro, Clarión, San Benedicto and Roca Partida (Brattstrom 1990; CONANP 2004). Numerous studies have focused on the Revillagigedo Archipelago, mostly on Socorro island, dealing with the geology (Richards 1959, 1964, 1965); conservation and impact caused by intro- duced animals and the removal of exotic species (Rodríguez-Estrella et al. 1991, 1992, 1996; Ortega-Rubio et al. 1992; Arnaud et al. 1993; Ortega-Rubio and Castellanos-Vera 1994; Álvarez-Cárdenas et al. 2000; CONANP 2004; Izquierdo et al. 2005; Walter and Levin 2007; Martínez-Gómez et al. 2010; Carlson et al. 2013; López-Higareda et al. 2014; Brattstrom 2015; Ortiz-Alcaraz 2016; Ortiz-Alcaraz et al. 2019); floristic studies (López- Caamal et al. 2004); and faunistic studies on arthropods (Jiménez et al. 1994; Pérez-Chi 2005), reptiles (Ortega-Rubio et al. 1991; Feldman et al. 2011; Mulcahy et al. 2014) and birds (Parkes 1990; Walter 1990; Castellanos and Rodríguez-Estrella 1993; Johnson and Clayton 2000; Barber et al. 2004; Martínez-Gómez and Jacobsen 2004; Martínez-Gómez et al. 2005, 2015, 2017; Yanga et al. 2011; Sosa-López et al. 2012; Martínez-Gómez and Matías-Ferrer 2013; Evans et al. 2015). Brattstrom (1990) provided a preliminary account of the biogeography of the islands, based on vertebrate taxa. Hahn et al. (2012) conducted a biogeographic analysis of the birds on the Mexican Pacific coast, finding a correlation between the taxonomic hierarchy and the isolation gradient from the coast to the islands. Socorro island is located at 18.699 N and 110.942W. It is the largest island of the Revillagigedo Archipelago and has an extent of 132 km?. This island consists of one central volcano, the Evermann, and 12 secondary craters; it has temporary and permanent ponds and sinks. The first eruptions that created the island date from the Miocene, and the raising of Socorro Island above sea level probably occurred in the Early Pleistocene (Brattstrom 1990; CONANP 2004). Socorro is the most 10 JOURNAL OF NATURAL HISTORY (e) 687 San Benedicto Roca Partida TON Socorro Figure 1. Islands of the Revillagigedo Archipelago. diverse island of the archipelago in fauna and flora. lts vegetation is complex, consisting of species of Bryopsida, Liliopsida, Lycopodiopsida, Magnoliopsida and Polypodiopsida. The endemic flora is represented by Acianthera unguicallosa, Aristolochia socorroensis, Bidens socorrensis, Botrychium socorrense, Castilleja socor- rensis, Cestrum pacificum, Coreocarpus insularis, Coreopsis insularis, Critoniopsis littor- alis, Erigeron socorrensis, llex socorroensis, Muhlenbergia solisii and Salvia pseudomisella (Johnston 1931; Levin and Moran 1989; Ortega-Rubio et al. 1991; León-de la Luz et al. 1994; CONANP 2004; León-de la Luz and Chiang 2004; Flores- Palacios et al. 2009). Some animal species are endemic to Socorro (Palacios-Vargas et al. 1982; García-Aldrete et al. 1992; Galina-Tessaro et al. 1994; Jiménez et al. 1994; Félix Lizárraga et al. 2015), eg the grasshopper Schistocerca socorro, the lizard Urosaurus auriculatus, and the birds Mimus graysoni, Psittacara brevipes, Troglodytes sissonii and Zenaida graysoni, the last extinct in the wild (Castellanos and Rodríguez-Estrella 1993; Johnson and Clayton 2000; Song 2006; Hahn et al. 2012). Three introduced mammals (Felis catus, Mus musculus and Ovis orientalis) have been reported (Arnaud et al. 1993; Álvarez-Cárdenas et al. 2000; CONANP 2004; López-Higareda et al. 2014). 11 688 («) P.G. GARCÍA-NAVARRETE ET AL. Clarión Island is located at 18.12N and 110.942W. It is the second island of the Revillagigedo Archipelago in order of decreasing size, with 19.80 km?. lt was formed with the material of volcanic eruptions from the Eocene-Miocene. Its rise above sea level has been dated to the early Pliocene, and fossil records suggest that it could be the oldest island. This island has two temporary ponds on the low flat southern portion (Brattstrom 1990; CONANP 2004). Its vegetation consists of species of Asteraceae, Fabaceae, Lamiaceae, Poaceae, Rubiaceae, Sapotaceae and Zygophillaceae. Aristida tenuifolia has been reported as endemic to Clarión (CONANP 2004). Scarce studies list the animals that occur specifically on Clarión, or at least on Socorro and Clarión (Everett 1988; García-Aldrete et al. 1992; Wanless et al. 2009; González-Zamora et al. 2016). San Benedicto Island is located at 18.699%N and 114.716"W. It has an extent of 4.8 km?. lt has a volcanic origin, and it is the northernmost and youngest island of the Revillagigedo Archipelago. The last volcanic activity was in 1952 when the Bárcena volcano erupted. As a consequence of the eruption, the fauna and flora were nearly exterminated; nonetheless, the island was repopulated (Richards 1959, 1965; Brattstrom 1990). San Benedicto Island has low vegetation, consisting of species of Liliopsida and Magnoliopsida (eg Cenchrus myosuroides, Eragrostis prolifera, Ipomoea pes-caprae, Perityle socorrosensi and Teucrium townsendii). Erigeron crenatus and Aristolochia islandica have been reported as endemic species (Johnston 1931; CONANP 2004; Brattstrom 2015). The main lists of the biota are from Pitman and Ballance (2002) and Brattstrom (2015), who reported the repopulation of the island by Bulbostylis nesiotica, Eragrostis prolifera, Phaethon aethereus, P. rubricauda, Phoebastria immutabilis, Sula dactylatra, S. granti, S. leucogaster, S. nebouxii and S. sula. Roca Partida Island is located at 19N and 112.083"W. It is the smallest and most inhospitable island of the Revillagigedo Archipelago; it has an extent of 0.014 km?. It is the summit of a large stratovolcano with an underwater origin, which has been eroded by wave action. Its precise geological age has not been determined, but some authors have suggested that it is older than San Benedicto and Socorro (Richards 1964; Brattstrom 1990). There are no records of plant species and only seabirds are known (CONANP 2004). Some biogeographic regionalisation schemes proposed for Mexico have not consid- ered the Revillagigedo Archipelago (Smith 1941; Stuart 1964; Cabrera and Willink 1973; Arriaga et al. 1997; Morrone et al. 2002; Morrone 2005); others included it within the Pacific Lowlands province (Morrone et al. 2017) or treated it explicitly as a biogeographic district assigned to this province (Goldman and Moore 1945; Morrone 2014). Some authors have considered the Revillagigedo Archipelago an independent province (Goldman and Moore 1945; Udvardy 1975; Rzedowski 1978; Rzedowski and Reyna- Trujillo 1990; Arriaga et al. 1997), whereas others have treated it as a province within the Arid Tropical North American region (Espinosa et al. 2008). The Revillagigedo Archipelago is relevant in the framework of biodiversity conserva- tion, which has led the Mexican government to declare ¡it a Natural Protected Area, with the character of a Biosphere Reserve in 2007, and as a National Park in 2017 (DOF 2017). Despite this, some natural phenomena and human activities have caused ecological changes such as soil erosion, vegetation disturbance, reduction in native populations, the introduction of species and extinction of endemic species (Ortega-Rubio et al. 1991; Arnaud et al. 1993; CONANP 2004; Aguirre-Muñoz et al. 2011). Among the natural phenomena that have affected the biotic composition of the islands, the most 12 JOURNAL OF NATURAL HISTORY e 689 outstanding factors are hurricanes and volcanic eruptions (Richards 1959; Brattstrom 2015). The biodiversity of the Revillagigedo Archipelago has a high value, although the plants and animals of the islands are still poorly known. Previous studies focused on the management of the wildlife resources of the Revillagigedo Archipelago are not sufficient and it is worth working to collect the existing information. Regarding the ecological issues that affect insular ecosystems, we can mention the presence of introduced species. The presence of exotic species such as sheep (Ovis orientalis), feral cats (Felis catus), wild pigs (Sus scrofa), mice (Mus musculus) and rabbits (Oryctolagus cuniculus), mostly in Socorro, represents a real danger for the native flora and fauna. The presence of these species increases the extinction rate of endemic species, the degradation of the soil and vegeta- tion, and the alteration of trophic chains (Álvarez-Cárdenas et al. 2000; CONANP 2004; Aguirre-Muñoz et al. 2011; López-Higareda et al. 2014). The Revillagigedo Archipelago is worthy of attention due to three main aspects: geology (volcanic origin), high biodiversity, and conservation prioritisation given its endemic and threatened species (Brattstrom 1990; Myers et al. 2000; Whittaker and Fernández-Palacios 2007; DOF 2017). Our objective is to analyse its biota to propose a historical biogeographic framework, following the steps of an evolutionary biogeo- graphic analysis (cf. Morrone 2009, 2011): (1) identification of biotic components, (2) testing the relationships between these biotic components, (3) regionalisation, (4) identi- fication of cenocrons, and (5) construction of a geobiotic scenario. We test the biotic affinities with the Nearctic and Neotropical regions, and whether the main colonisation of the biota of the archipelago was achieved by overwater dispersal. Material and methods Data We compiled a database of terrestrial plant and animal species and seabirds of the Revillagigedo Archipelago, with data from the literature (cited in Supplementary Material File $1), and the electronic repositories CONABIO (2021) and GBIF (2022). This database, which includes 248 families, 485 genera, 667 species and 97 subspecies, was reviewed, verifying each record based on the valid names of each species and its current distribution, using Barriga-Tuñón (2009), Mite Research (2010), Lepage et al. (2014), Bonato et al. (2016), Constantino (2020), Bellinger et al. (2022), Uetz et al. (2022), Bánki et al. (2023), Insecta.pro (2023), Tropicos (2023), World Flora online (2023), World Spider Catalog (2023), and World Register of Marine Species (2023), platforms and specialised literature. Efforts were made to compile a complete database while minimising the erroneous records of names, distributions, situations and sources, for which we collabo- rated with experts to review the lists of plants and birds (see Acknowledgements). Plant species were checked using the Bánki et al. (2023) Checklist, WFO, and Tropicos databases; subsequently, for synonymies, we consulted the “Checklist of the native vascular plants of Mexico” (Villaseñor 2016). Here, we considered endemic species to be those that occur on at least one of the islands of the archipelago and are not distributed on the continent. Exotic species include those purposely or accidentally introduced to the archipelago. For all the analyses, exotic species and birds that do not nest on the islands were excluded. Therefore, only 507 species were considered. 13 690 () P.G. GARCÍA-NAVARRETE ET AL. Evolutionary biogeographic analysis The first step of an evolutionary biogeographic analysis (sensu Morrone 2009, 2011, 2020) is the identification of biotic components, which are groups of taxa that coexist spatio- temporally. A parsimony analysis of endemicity with progressive character elimination (PAE-PCE; Echeverry and Morrone 2010) is useful to identify possible biotic components. PAE-PCE is a procedure in which a parsimony analysis is performed on a matrix of presence-absence data. From this analysis, an area cladogram is obtained, and the species that support each clade (synapomorphies) are removed from the matrix. The resulting data matrix is re-analysed iteratively until there are no further synapomorphies on the cladograms. For this PAE-PCE, the species distributed in all the biogeographic units analysed, those species whose total distribution could not be obtained, those probably extinct, and the species endemic to the islands (autapomorphies) were not considered. Based on the information from the provinces where the species are found, a data matrix of 194 species (columns) versus Revillagigedo and the provinces Baja California, Pacific Lowlands, Sonoran and Veracruzan (rows) was constructed, where the presence or absence of species was coded with “1' or '0', respectively, and a row with zeros was included to root the cladogram (Supplementary Material Table 52). PAE-PCE was applied to the matrix using TNT version 1.5 (Goloboff and Catalano 2016), under equal weights, using the heuristic method of new search strategies (Ratchet), with 20 random seeds, find minimum length 10 times and 5000 iterations. To explore the effect of homoplasy on the results of the first analysis, a second analysis was performed under implied weights (Goloboff 1993), with constants of concavity (k) set to different integer values of 3, 6 and 11, where 1 is the most severely weighted against homoplastic characters. The TNT setk script, developed by Salvador Arias, was used to identify the most appropriate k value using the script of Goloboff et al. (2008). The resulting clades with at least two synapo- morphies were considered to represent biotic components and are represented graphi- cally on the map as generalised tracks (see Craw et al. 1999; Morrone 2009, 2015). Their overlap was interpreted as a complex area or node. To test the relationships between the biotic components, we undertook a cladistic biogeographic analysis, based on the phylogenetic relationships of the taxa and their distributions (Morrone and Crisci 1995; Humphries and Parenti 1999; Morrone 2009; Parenti and Ebach 2009). We applied a primary Brooks parsimony analysis (primary BPA), initially proposed by Wiley (1988). We used the available phylogenetic information of 42 cladograms to construct the taxon-area cladograms (Table 1), replacing the terminal taxa by their distribution data taken from Global Biodiversity Information Facility, Naturalista and bibliographic sources, for which we considered the Baja California, Pacific Lowlands, Sonoran and Veracruzan provinces, and the Revillagigedo area. These cladograms were annotated in parenthetical format to obtain the node matrix for the primary BPA, according to Santos et al. (2021). The text file was uploaded to the BuM platform (Santos et al. 2021) to obtain the primary BPA matrix; however, as this software does not support redundant distributions in paralogous nodes, the cladograms had to be adjusted to remove the paralogy without compromising the clades that included Revillagigedo. In cases where it was not possible to adjust the cladograms, they were removed; therefore, only 35 cladograms were considered (Supplementary Material Table S3). The data matrix was constructed comprising 146 nodes in the columns and five areas 14 JOURNAL OF NATURAL HISTORY e 691 Table 1. List of the taxa selected for the cladistic biogeographic analysis, and the corresponding source of phylogenetic information used to construct the taxon-area cladograms. * = Cladograms that were not used in the final analysis because the BuM platform does not support redundant distributions in paralogy. Group Taxa Source Plants *Asplenium formosum Xu et al. (2020) A. sessilifolium Xu et al. (2020) Coreocarpus insularis Kimball et al. (2003) Euphorbia californica Yang et al. (2012) E. chersonesa Yang et al. (2012) *E. hirta Yang et al. (2012) *E. hyssopifolia Yang et al. (2012) E. misera Yang et al. (2012) *E. thymifolia Yang et al. (2012) lresine diffusa Borsch et al. (2018) Lantana involucrata Marx et al. (2010) Phaseolus lunatus Chacón et al. (2007) Physalis cordata Feng et al. (2016) *P. philadelphica Feng et al. (2016) Polystichum muricatum McHenry and Barrington (2014) Verbena litoralis Marx et al. (2010) Zeltnera wigginsii Mansion and Zeltner (2004) Invertebrates Ataenius liogaster Stebnicka (2005) Erynnis funeralis Zakharov et al. (2009) Leptotes marina Fric et al. (2019) Manduca sexta Kitching et al. (2002) Odontomachus clarus Fernandes et al. (2021) *Papilio thoas Zakharov et al. (2004) Phoebis agarithe Núñez et al. (2020) Schistocerca piceifrons Song et al. (2017) S. socorro Song et al. (2017) Solenopsis geminata Shreve et al. (2020) Vertebrates Accipiter cooperii Breman et al. (2013) Anas acuta Ctenosaura pectinata Haemorhous mexicanus Hypsiglena torquata H. unaocularus Larus delawarensis L. occidentalis *Masticophis anthonyi Mimus graysoni Oceanodroma cheimomnestes O. leucorhoa chapmani O. leucorhoa leucorhoa O. socorroensis Pipilo maculatus Rhogeessa parvula Setophaga auduboni *S, pitiayumi *S, pitiayumi graysoni *Stercorarius longicaudus Sterna paradisaea Tachycineta albilinea T. thalassina Toxostoma bendirei Troglodytes aedon T. sissonii Urosaurus auriculatus U. clarionensis Livezey (1991) Kóhler et al. (2000) Smith et al. (2013) Myers and Mulcahy (2020) Myers and Mulcahy (2020) Pons et al. (2005) Pons et al. (2005) Myers et al. (2017) Valente et al. (2020) Taylor et al. (2017) Taylor et al. (2017) Taylor et al. (2017) Taylor et al. (2017) DaCosta et al. (2009) Hoofer and Van Den Bussche (2001) Valente et al. (2020) Valente et al. (2020) Valente et al. (2020) Chu et al. (2009) Bridge et al. (2005) Stager et al. (2014) Stager et al. (2014) Lovette et al. (2012) Martínez-Gómez et al. (2005) Martínez-Gómez et al. (2005) Feldman et al. (2011) Feldman et al. (2011) 15 692 () P.G. GARCÍA-NAVARRETE ET AL. in the rows, coded as “1' for the presence and '0' for the absence of a node in an area. A hypothetical area coded with zeros was included to root the general-area cladogram (Supplementary Material File S4). The matrix was analysed with TNT (Goloboff and Catalano 2016), using the same methodology, with the setk script, as in the analysis of biotic components. A biogeographic regionalisation is a hierarchical system that classifies areas based on their biota. This system implies the recognition of successively nested areas using five main categories: kingdom, region, dominion, province and district (Escalante 2009; Morrone 2018). The category assigned to the Revillagigedo Archipelago is based on both the number of species that support the biotic components and the relationships depicted in the general-area cladogram. The archipelago may be nested within the Nearctic or Neotropical regions, considering the Sonoran and Baja California provinces Nearctic and the Pacific Lowlands and Veracruzan provinces Neotropical, or it could be proposed as an independent province if there is no strong relationship with any of these areas. Also, it can be argued that an area is a node when it belongs to alternative clades in different general-area cladograms or if different biotic components converge in the area. Once biotic components have been identified, we may proceed to recognise cenocrons, which are sets of taxa that share a biogeographic history and have dispersed synchronically to the area (Morrone 2009, 2020). To better understand the evolutionary biogeography of the areas, it is necessary to give a temporal dimension that supports the hypotheses (Hunn and Upchurch 2001; Morrone 2009). To hypothesise whether the Neotropical and Nearctic biotic components could be considered cenocrons, we searched for dated phylogenies associated to their species. The lineages that are distributed in the Pacific Lowlands and Veracruzan provinces were preliminarily considered to belong to the Neotropical cenocron, and the lineages that are distributed in the Baja California and Sonoran provinces were considered to represent the Nearctic cenocron. Fourteen dated phylogenetic analyses were found, nine of which correspond to the Neotropical cenocron: Canavalia rosea, Dorymyrmex bicolour, Leptotes marina, Phoebis agarithe, Polystichum muricatum, Psittacara brevipes, Schistocerca socorro, Setophaga pitiayumi graysoni and Zenaida graysoni (McHenry and Barrington 2014; Snak et al. 2016; Song et al. 2017; Fric et al. 201 9; Núñez et al. 2020; Valente et al. 2020; Oberski 2022), and five of which correspond to the Nearctic cenocron: Haemorhous mexicanus, Mimus graysoni, Papilio thoas, Turdus assimilis and Zeltnera wigginsii (Mansion and Zeltner 2004; Zakharov et al. 2004; Smith et al. 2013; Batista et al. 2020; Valente et al. 2020). The construction of a geobiotic scenario is the final step in the analysis. lt is obtained by integrating the vicariance events depicted in the general-area cladogram, the dispersal events of the cenocrons, and the dated geological information available for the archipe- lago (Morrone 2009, 2011, 2020). Results Identification of biotic components The PAE-PCE generated a single most parsimonious area cladogram, with a length of 277 steps, a consistency index (Cl) of 0.70, and a retention index (RI) of 0.67. A clade represent- ing the first biotic component included the Revillagigedo and the Pacific Lowlands (Neotropical region), having 86 geographical synapomorphies (Table 2). In the second 16 JOURNAL OF NATURAL HISTORY E 693 Table 2. List of the species that support the biotic components. Neotropical component Nearctic component Abildgaardia mexicana Ardenna bulleri Acalypha umbrosa Argiope argentata Adiantopsis radiata Coniopteryx simplicior Agrotis malefida Cyclosa turbinata Anelosimus studiosus Mareca strepera strepera Anomis editrix Marginitermes hubbardi Anyphaena judicata Argyrodes elevatus Aristida pansa Asplenium formosum Ataenius liogaster Callopistria foridensis Camponotus picipes Chinavia hilaris Chrysopodes collaris Colpocephalum fregili Ctenosaura pectinata Dicyrtoma aurata Ectopsocus meridionalis Epidendrum nitens Epidendrum ramosum Eretes sticticus Eriophora edax Eustala californiensis Folsomides parvulus Frangula discolour Guettarda elliptica Helicobia morionella Hibana cambridgei Hippomane mancinella Hypericum eastwoodianum Hypochthonius rufulus Hypogena tricornis Hypsiglena torquata Ipomoea indica Isotomiella minor Lantana hirta Latiblattella picturata Lepechinia schiedeana Lepidocyrtus pallidus Leucauge venusta Mallodon chevrolatii Megalothorax incertus Meliosma nesites Melipotis famelica Meridiorhantus calidus Mesosphaerum pectinatum Mesosphaerum suaveolens Nanogalactia brachystachys Neoptychodes trilineatus Neoscona oaxacensis Oecanthus varicornis Onychoprion fuscatus crissalis Ophiuche minualis Oreodera glauca Oreopanax xalapensis Peperomia san-joseana Peridroma saucia Perigonia lusca Phalacrocorax brasilianus mexicanus Pityrogramma ebenea (Continued) 17 694 P. G. GARCÍA-NAVARRETE ET AL. Table 2. (Continued). Neotropical component Nearctic component Plumbago zeylanica Polystichum muricatum Ponometia exigua Procecidochares flavipes Pseudosinella violenta Pterodroma externa Pterodroma phaeopygia Puffinus lherminieri Puffinus subalaris Rhomphaea projiciens Schistocerca americana Schistocerca piceifrons piceifrons Solenopsis geminata Sorghastrum nutans Sorghastrum pohlianum Sphaeridia pumilis Sporobolus purpurascens Strymon melinus clarionensis Thalassaphorura parvicornis Thelypteris oligocarpa Thymoites maderae Tramea calverti Wamba crispulus Xenylla humicola Zanthoxylum fagara culantrilo analysis, after removing the synapomorphies that supported the previous clade, a single most parsimonious cladogram resulted, with a length of 1434 steps, Cl of 0.75, and RI of 0.736. In this second cladogram, a clade representing the second biotic component joins the Revillagigedo Archipelago and the Baja California province (Nearctic region), sup- ported by six synapomorphies (Table 2). In the third analysis, the same cladogram as in the second analysis was obtained. Therefore, both biotic components are mapped as generalised tracks and their overlap in the archipelago allowed its recognition as a complex area or node (Figure 2). Testing the relationships among the biotic components The primary BPA generated one most parsimonious area cladogram: (Revillagigedo (Sonoran (Baja California (Veracruzan, Pacific Lowlands)))) (Figure 3), with a length of 203 steps, Cl of 0.71, Rl of 0.53, and a K value of 0.141601. This area cladogram reflects an independent relationship of the Revillagigedo Archipelago with the other areas. Biogeographic regionalisation According to the analysis of the biotic components, the biota of the Revillagigedo Archipelago is related to both the Neotropical and Nearctic biotas, but with a stronger relationship to the former. The overlap of the biotic components in the archipelago (Figure 2) would imply its recognition as a transition zone, but it lacks the typical cenocrons recognised for the Mexican Transition Zone (Halffter and Morrone 2017; Morrone 2020). According to the relationships among the biotic components in the cladistic biogeographic analysis, the Revillagigedo Archipelago may be considered an 18 JOURNAL OF NATURAL HISTORY (4) 695 -. Baja California generalized track ma Pacific Lowlands generalized track (Y node Figure 2. Biotic components overlapping in the Revillagigedo Archipelago. independent province. Following the more recent biogeographic regionalisation of Mexico (Morrone et al. 2017; Morrone 2019), however, we prefer to classify the Revillagigedo Archipelago as a district within the Pacific Lowlands province. Cenocrons Fourteen dated phylogenetic analyses were found, corresponding to three plant genera (Canavalia, Polystichum and Zeltnera), five insect genera (Dorymyrmex, Leptotes, Papilio, Phoebis and Schistocerca), and six bird genera (Haemorhous, Mimus, Psittacara, Setophaga, Turdus and Zenaida) (Figure 4). The analysis of Canavalia (Magnoliopsida: Fabaceae) shows a clade between the Revillagigedo species C. rosea and C. cathartica with a divergence time of 0.2 Ma (Snak et al. 2016). The analysis of Polystichum (Polypodiopsida: Dryopteridaceae) shows that the divergence time between the Revillagigedo species P. muricatum and its sister species occurred at least 1.27 Ma (McHenry and Barrington 2014). The analysis of Mansion and Zeltner (2004) shows the dated phylogenetic relationships within the 19 696 («) P.G. GARCÍA-NAVARRETE ET AL. Root 4 pp — Revillagigedo Archipelago Sonoran Baja California ——- Pacific Lowlands L——— Veracruzan Figure 3. Cladogram obtained through the primary Brooks parsimony analysis. New World endemic Zeltnera (Magnoliopsida: Gentianaceae): in this case, Z. wigginsii has an approximate divergence time from its sister species of 1 Ma. According to the dated insect phylogenetic hypotheses, the Revillagigedo ant Dorymyrmex bicolour (Insecta: Formicidae) diverged from its sister species at least 2 Ma (Oberski 2022). Leptotes marina (Insecta: Lycaenidae) is the sister species of L. cassius and L. trigemmatus, dated approximately 4 Ma (Fric et al. 2019). Papilio thoas (Insecta: Papilionidae) diverged from its sister species P. cresphontes between 19.18 and 8.55 Ma, 12 Ma on average (Zakharov et al. 2004). The clade that includes the Revillagigedo species Phoebis agarithe (Insecta: Pieridae) diverged from its sister taxon approximately 3.5 Ma (Núñez et al. 2020). In the phylogeny of Schistocerca (Orthoptera: Acrididae), there are three species distributed in the Revillagigedo Archipelago, namely S. americana, S. nitens and S. socorro. The clade that includes these species dates to approximately 2.5 Ma. The endemic species S. socorro has a divergence time of 2 Ma; the other species have divergence times of 1.5 (S. nitens) and 1 Ma (S. americana) (Song et al. 2017). Valente et al. (2020) presented a molecular phylogenetic data set of the terres- trial avifauna of oceanic archipelagos. From this work, we took the proposed phylogenies and the calculated branching time of four endemic bird species of the Socorro Island: Mimus graysoni (Mimidae) with an approximate branching time of 1 Ma, Psittacara brevipes (Psittacidae) with 0.55 Ma, Setophaga pitiayumi graysoni (Motacillidae) with 2.5 Ma, and Zenaida graysoni (Columbidae) with 1 Ma. Haemorhous mexicanus (Fringillidae) diverged from its sister species between 15.7 and 5 Ma, 10 Ma on average (Smith et al. 2013). The phylogeny of Turdus (Turdidae) suggests a divergence time of 3.5 Ma between the Revillagigedo species T. asimilis and its sister taxon (Batista et al. 2020). 20 JOURNAL OF NATURAL HISTORY (2) 697 -Canavalia gladiolata faemorhous smithi ¿ptotes cassius .C. lineata a — purpureus . trigemmatus -C. hawaiiensis /. mexicanus * .. Marina. -C. cathartica Ni - callanga o eros (a fimus gilvus apilio anchisiades Polystichum turrialbae. -M. polyglottos E erostratus 17 e muricatum * -M. magnirostris > hectorides P. hartwegil gilvus L————P torquatus P. foumieri E gilvus A astyalls P concinnum -M. graysoni ** > cresphontes R talamancanum (e) (0) hs > thoas * P. alfaroi (h) Psittacara finschi Schistocerca centralis jetophaga americana Turdus obsoletus pq brevipes ** S. americana * 28 pitiayumi T. lawrencii - -P. rubritorquis serialis cubense $ S. pitiayumi graysoni ** T. assimilis * o S. piceifrons dd A ratico S. socorro * o S. nitens * (Mex) o S. nitens (USA) Zeltnera pusilla -Zenaida graysoni ** 1 -Z wigginsii * ! -Z. macroura -Z. stricta -Z. galapagoensis mm 7, quitensis a -Z. auriculata Figure 4. Dated phylogenies used for the identification of the Neotropical cenocron: (a) Canavalia (based on Snak et al. 2016), (b) Dorymyrmex (based on Oberski 2022), (c) Haemorhous (based on Smith et al. 2013), (d) Leptotes (based on Fric et al. 2019), (e) Mimus (based on Valente et al. 2020), (f) Papilio (based on Zakharov et al. 2004), (g) Phoebis (based on Núñez et al. 2020), (h) Polystichum (based on McHenry and Barrington 2014), (i) Psittacara (based on Valente et al. 2020), (j) Schistocerca (based on Song et al. 2017), (k) Setophaga (based on Valente et al. 2020), (l) Turdus (based on Batista et al. 2019), (m) Zeltnera (based on Mansion and Zeltner 2004), (n) Zenaida (based on Valente et al. 2020). Numbers indicate the approximate dates of divergence in millions of years; * = species distributed in Revillagigedo; ** = species endemic to Revillagigedo. In summary, the dated phylogenies suggest that the divergence times between the species of Revillagigedo and their respective sister taxa span from 12 to 0.2 Ma. From the compiled information, we hypothesise the existence of two cenocrons: Nearctic (including Haemorhous, Papilio, Mimus, Turdus and Zeltnera) and Neotropical (including Canavalia, Dorymyrmex, Leptotes, Phoebis, Polystichum, Psittacara, Schistocerca, Setophaga and Zenaida). The arrival of these cenocrons to the archipelago may have occurred during the Pliocene-Pleistocene after the islands were available for colonisation. Geobiotic scenario The Revillagigedo Archipelago is made up of four oceanic islands located at the northern end of the Mathematician Ridge where there was an expansion of the 21 698 P. G. GARCÍA-NAVARRETE ET AL. ocean floor 3.5 Ma ago (Mammerickx et al. 1988). The Mathematician Ridge is currently inactive; however, volcanism is still active due to a weak zone created by faults and fractures. The tectonic framework of the north-western margin of Mexico during the Pliocene and Pleistocene should be considered the starting point of the geobiotic scenario of the Revillagigedo Archipelago. It corresponds to the overlap of the Eastern Pacific Ridge and the assimilation of the oceanic trench. A little farther south the trench remained active, which is manifested in the marginal volcanic arc in present-day Central America. In a later tectonic stage, the southern portion of the current Baja California Peninsula separated from the rest of the continent, and the Pacific oceanic waters flooded that portion (13 to 4.5 Ma). Southern Mexico rose and fractured, thus facilitating the formation of the Transmexican Volcanic Belt in the mainland, from the Pacific Ocean to the Gulf of Mexico; and the Galapagos Ridge was formed in the ocean, joining the eastern Pacific Ridge, and limiting the Cocos plate (Aguayo-Camargo and Marín-Córdova 1987; Mammerickx et al. 1988; Cserna 1989). The Revillagigedo islands are probably the result of volcanism associated with the oceanic Mathematician Ridge, since the times of the active ridge coincide with the approximate dating of the islands based on lithological data. The approximate dating of the Revillagigedo islands indicates that Clarión appeared first, originating from a submarine volcanic eruption in the Eocene-Miocene. The precise geological age of Roca Partida has not been determined yet, but some authors suggest that it is older than both the San Benedicto and Socorro islands. The first eruption that originated on Socorro Island dates from the Miocene, and it has been determined that San Benedicto is the youngest island in the archipelago (Richards 1964; Ortega-Gutiérrez and Sánchez-Rubio 1985; Brattstrom 1990). Clarión, Socorro and San Benedicto islands share the same lithological composition (alkaline mafic rocks), indicating that they had the same volcanic origin and similar age in the Neogene-Quaternary (Reed et al. 2005). The distribution of this lithology may be due to a fissure eruption along a fracture and the subsequent formation of volcanic cones, before emerging above the surface. Roca Partida has different lithological characteristics (inter- mediate rocks) and a different age range (Pliocene-Quaternary; Reed et al. 2005), so the volcanic event that gave rise to it could be different from the one that gave rise to Clarión, Socorro and San Benedicto. According to Brattstrom (1990), the dates of rising above sea level could be Early Pliocene for Clarión (5.3 to 3.6 Ma), Early Pleistocene (2.58 to 1.8 Ma) for Socorro, and Late Pleistocene (1.8 to 0.012 Ma) for San Benedicto. For Roca Partida, Brattstrom (1990) mentioned that its geological age cannot be determined but assumed it to be younger than Clarión and older than the other islands; however, Richards (1964) dated the possible geological age of Roca Partida to the Late Pleistocene (1.8 to 0.012 Mya). Discussion Islands are worth studying due to their endemic species and because they are natural models that allow the isolation of factors and processes when analysing biotic assembly (Whittaker and Fernández-Palacios 2007; Morrone 2011). The Revillagigedo Archipelago is a complex area, where two different biotas converge, one Neotropical (Pacific Lowlands) and another Nearctic (Baja California Peninsula). Because of the recent volcanic origin of 22 JOURNAL OF NATURAL HISTORY e 699 the archipelago, these biotic components represent ancestral biotas assembled by dis- persal events. Previous biogeographic studies have shown that the Pacific Lowlands and Baja California belong to different biotic components. Morrone and Márquez (2003) identiñed a Mesoamerican biotic component that includes the Pacific Lowlands, Veracruzan and Chiapas Highlands provinces, and a Nearctic-Californian component that includes the Baja California province. Escalante et al. (2004) identified a California and a Central-South Pacific generalised track; the former includes the Baja California and California provinces, and the latter the Pacific Lowlands, Transmexican Volcanic Belt, Balsas Basin, Sierra Madre del Sur, Veracruzan and Chiapas Highlands provinces. There are no previous cladistic biogeographic studies that include the Revillagigedo islands; however, in all the studies dealing with the biotic history of continental Mexico (Marshall and Liebherr 2000; Contreras-Medina et al. 2007; Escalante et al. 2007), Baja California and the Pacific Lowlands are considered independent areas. Marshall and Liebherr (2000) analysed montane areas of the Mexican Transition Zone and identified a northern and a southern group; the northern one includes the Arizona Mountains, Sonoran Desert, Sierra Madre Occidental and Sierra Madre Oriental. Contreras-Medina et al. (2007) identified a major clade, which shows the Baja California area as the sister area of the Great Basin and Mojavean provinces, and another that includes six provinces, among them the Veracruzan and Pacific Lowlands. Escalante et al. (2007) identified a clade including the Pacific Lowlands, Baja California and Sonora provinces. This analysis shows that the Revillagigedo Archipelago separated as the first group from the rest of the areas, as in the study of Ríos-Muñoz and Navarro-Sigúenza (2012) on the richness and biogeographic regionalisation of the Mesoamerican avifauna. Although in the cladistic biogeographic analysis the Revillagigedo Archipelago is the sister area to the other four areas, this cannot represent an event of fragmentation/vicariance, as the geological information indicates that the archipelago was never attached to the continent. The results of the cladistic biogeographic analysis suggest that the Revillagigedo Archipelago may be classified as an independent province, as postulated by other authors (Goldman and Moore 1945; Rzedowski 1978; Samek 1988; Rzedowski and Reyna-Trujillo 1990; Escalante et al. 1998; Espinosa et al. 2008). Additionally, the nodal characteristic of this area as a transitional zone, where biotas from the Nearctic and Neotropical regions overlap, may be tested in future studies, although the absence of some of the typical cenocrons, namely Mountain Mesoamerican and Mexican Plateau (see Halffter and Morrone 2017; Morrone 2020), seems to indicate that this is not the case. For the moment, we keep the Revillagigedo Archipelago as a district of the Pacific Lowlands province (Morrone et al. 2017; Morrone 2019). Clarión Island rose above sea level in the Pliocene Zanclean (5.3 to 3.6 Mya) (Brattstrom 1990). Despite harbouring two of the oldest dated lineages, Haemorhous mexicanus and Papilio thoas (12 and 10 Ma, respectively), they might have arrived in the early Pliocene, as part of the Nearctic cenocron. From this time, around 4 Ma, two cenocrons were identi- fied, coming from both regions, one Nearctic and one Neotropical. Socorro Island arose in the Pleistocene Gelasian, 2.58 to 1.8 Ma (Brattstrom 1990), representing an area closer to the continent. This allowed the arrival of more species, which dispersed to the island at least 2.5 Ma from both the Nearctic and Neotropical regions according to the Dorymyrmex, Mimus, Polystichum, Psittacara, Schistocerca, Setophaga, Zeltnera and Zenaida lineages. 23 700 P. G. GARCÍA-NAVARRETE ET AL. The Neotropical taxa of the Revillagigedo Archipelago correspond to the Typical Neotropical cenocron described for the Mexican Transition Zone (Halffter and Morrone 2017), which began to disperse northward massively from South America through the Central American and Mexican lowlands during the Pliocene-Pleistocene. Johnston (1931) considered that the Revillagigedo flora is dominated by two elements: one older, with geographically distant, southern relationships; and another that dispersed from northern and eastern Mexico in more recent times. Brattstrom (1990) considered that there was no evidence of adaptive radiation in the Revillagigedo islands, thus supporting the relatively recent dispersal of their biota. The biotic assembly of these Nearctic and Neotropical cenocrons in the archipelago is worthy of testing in the future with more phylogenetic hypotheses and dated lineages. We inferred the simultaneous arrival of both the Nearctic and Neotropical cenocrons to the Revillagigedo Archipelago during the Pliocene and up to the Pleistocene almost continuously. Their dispersal could have occurred during the Pliocene when Clarión Island had already emerged from the sea: the Nearctic cenocron could have come along the Baja California peninsula, already separated from the mainland, while the Neotropical cenocron could have dispersed during the Pliocene, from South America to continental Mexico (Halffter and Morrone 2017), through Central America and southern Mexico, when the Transmexican Volcanic Belt was already formed, and the species dispersing along the Pacific Lowlands had the opportunity to disperse to the islands. Feldman et al. (2011) considered that the most plausible scenario for the lizards of the genus Urosaurus, which has two sister species in the archipelago, is a western Mexican origin and a single dispersal event to the archipelago, followed by a second dispersal event between the islands. As Urosaurus represents one of the few known examples of adaptive radiations in the Revillagigedo Archipelago, it would be critical to have a dated phylogeny for this genus. Although oceanic dispersal has been underestimated by approaches emphasising vicariance (see de Queiroz 2005), during the last few decades several authors have postulated that the biotic assembly of oceanic islands is mainly due to dispersal, so ocean currents, predominant wind patterns, the geographic arrangement of islands, and bird migration routes may be relevant factors to explain this process (Ziegler et al. 2002; Givinish and Renner 2004; Renner 2004; Cook and Crisp 2005; Halas et al. 2005; McGlone 2005; Cowie and Holland 2006; Whittaker and Fernández-Palacios 2007; Whittaker et al. 2014). The Revillagigedo Archipelago can serve as a model system to address fundamental issues regarding biotic assembly on islands. The present study demonstrates the impor- tance of the archipelago as it is considered related to both the Nearctic and the Neotropical biotas. Yet nowhere is the biodiversity crisis more evident and in need of urgent attention than on islands, and Revillagigedo is no exception. Acknowledgements We appreciate the useful comments by two anonymous reviewers that greatly helped improve our original manuscript. We also thank Luis A. Sánchez-Gonzalez and Susana Ocegueda Cruz for checking the information on the bird and plant species, respectively, of the Revillagigedo Archipelago. The first author thanks the Posgrado en Ciencias Biológicas of the Universidad 24 JOURNAL OF NATURAL HISTORY E 701 Nacional Autónoma de México (UNAM) for academic training and logistic support, and the Consejo Nacional de Ciencia y Tecnología (CONACyT) for a scholarship (CVU: 444876). This paper is part of the requirements for obtaining a doctoral degree at the Posgrado en Ciencias Biológicas, UNAM, of the first author. Support from PAPIIT project IN218520 (DGAPA, UNAM) is acknowledged. Disclosure statement No potential conflict of interest was reported by the authors. Funding This work was supported by the Dirección General de Asuntos del Personal Académico, Universidad Nacional Autónoma de México [IN218520]. ORCID Patricia G. García-Navarrete (13) http://orcid.org/0000-0003-1451-7265 Tania Escalante (13) http://orcid.org/0000-0002-9127-8969 David Espinosa (3) http://orcid.org/0000-0002-9938-4686 Juan J. Morrone (3) http://orcid.org/0000-0001-5566-1189 Geolocation information Revillagigedo Archipelago is located in the Northeast Pacific, approximately 720 km west of Colima and 450 km south of Baja California Sur, Mexico. References Aguayo-Camargo JE, Marín-Córdova S. 1987. Origen y evolución de los rasgos morfotectónicos postcretácicos de México. Bol Soc Bot México. 48:15-39. doi:10.18268/BSGM1987v48n2a2. 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Molecular phylogenetics and classification of Euphorbia subgenus Chamaesyce (Euphorbiaceae). Taxon. 61:764-789. doi:10. 1002/tax.614005. Zakharov EV, Caterin MS, Sperling FAH. 2004. Molecular phylogeny, historical biogeography, and divergence time estimates for swallowtail butterflies of the genus Papilio (Lepidoptera: Papilionidae). Syst Biol. 53:193-215. doi:10.1080/10635150490423403. Zakharov EV, Lobo NF, Nowak C, Hellmann JJ. 2009. Introgression as a likely cause of mtDNA paraphyly in two allopatric skippers (Lepidoptera: Hesperiidae). Heredity. 102:590-599. doi:10. 1038/hdy.2009.26. Ziegler AM, Rees PM, Naugolnykh SV. 2002. The early Permian floras of Prince Edward Island, Canada: differentiating global from local effects of climate change. Can J Earth Sci. 39:223-238. doi:10.1139/e01-075. 33 34 CAPÍTULO II: Afinidades biogeográficas de la biota de las Islas Marías, Mexico Publicación: García-Navarrete P.G., Sánchez-González L.A., Morrone J.J. 2023. Biogeographical affinities of the biota of the Tres Marías Islands, Mexico. Biological Journal of the Linnean Society, blad101 https://doi.org/10.1093/biolinnean/blad101 Biological Journal of the Linnean Society, 2023, XX, 1-16. With 3 figures. Biogeographical affinities of the biota of the Tres Marías Islands, Mexico PATRICIA G. GARCÍA-NAVARRETE?”?, LUIS A. SÁNCHEZ-GONZÁLEZ! and JUAN J. MORRONE”"" ¡Museo de Zoología “Alfonso L. Herrera”, Departamento de Biología Evolutiva, Facultad de Ciencias, Universidad Nacional Autónoma de México (UNAM), 04510 Mexico City, Mexico “Posgrado en Ciencias Biológicas, Unidad de Posgrado, Edificio D, 1? Piso, Circuito de Posgrados, Ciudad Universitaria, Coyoacán, C.P. 04510, Mexico City, Mexico Received 5 May 2023; accepted for publication 30 June 2023 The Tres Marías archipelago in the central Mexican Pacific is a protected area that has a complex geological history due to its tectonic setting. This study describes an integrative analysis of the biogeographical affinities of the biota inhabiting the islands. A biotic component analysis showed a close relationship between the islands and the Pacific Lowlands and Veracruzan biogeographical provinces, whereas a cladistic biogeographical analysis additionally showed a Nearctic affinity with the Sonoran biogeographical province. The biogeographical affinity patterns, based on the distribution of the sister group of each endemic species, revealed three distinct patterns: Neotropical, Sonoran-Neotropical and Nearctic-Neotropical. The study recognized that the Tres Marías Islands are a region of great biological complexity where the biota of the Pacific Lowlands and the Veracruzan provinces intersect, with a predominantly Neotropical affinity. In this biogeographical analysis, information on the biotic assemblage and the geological history of the Tres Marías Islands are integrated and discussed. The biotic assembly of the islands must have occurred via both vicariance and dispersal at different geological times, related to opening of the Gulf of California (Miocene—Pleistocene) as well as to periods of glaciation (Pleistocene). ADDITIONAL KEYWORDS: biogeographical patterns — cladistic biogeographical analysis — dispersal — generalized tracks — vicariance. INTRODUCTION situated in a hydrographically complex area, where thermal fronts form due to the confluence of different water masses, such as the California current, equatorial surface water, tropical subsurface water, intermediate Pacific water and deep Pacific water mass, marking the southernmost point of subarctic waters and the starting point of the northern equatorial current (Bray €: Robles, 1991; Torres-Orozco, 2004). The Tres Marías archipelago is located between the north-west edge of the Middle America Trench and the south-eastern limit of the Tamayo Fracture Zone of the Rivera Plate. The Tres Marías Escarpment lies to the west and south-west. This tectonic context is part of a general subduction regime of the Cocos Plate under the North American Plate (Lonsdale, 1995; Dañobeitia et al., 2016) and the transform boundary between the North American and Pacific Plates. The Tres Marías Islands have intercalations of Mesozoic "Corresponding author. E-mail: morronefciencias.unam.mx andesites and limestones, with Holocene coastal and The Tres Marías Islands archipelago, also known as Islas Marías, was declared a Natural Protected Area and Biosphere Reserve in 2000 (Secretaría de Medio Ambiente, Recursos Naturales y Pesca, 2000) and in 2019, María Madre island ceased to be a federal penal colony. This archipelago is located in the central Mexican Pacific, -130 km north-west of San Blas, Nayarit, and 360 km south-east of the Baja California Peninsula. The archipelago consists of four continental islands: María Madre (140.28 km?), María Magdalena (66.98 km?), María Cleofas (18.75 km?) and San Juanito (9.016 km?) (Subgrupo del Catálogo de Islas Nacionales, 2014). San Juanito island is considered an islet, an extension of the northern part of María Madre island (Peralta € García, 2013). This archipelago is OThe Author(s) 2023. Published by Oxford University Press on behalf of The Linnean Society of London. 1 All ri hts reserved. For permissions, please e-mail: journals.permissionsQoup.com ez oz Je qu ia xd as gz uo Je sn se oi pa ul ol g AU ] I8 U| N Y N N AQ 9/ €6 12 2/ 10 1P el q/ ue su ul jo lq /£ 60 1' 01 /1 0p /a 1o e- so ue ap e/ ue su u1 |o 1q /u o9 'd no oi ua pe se // :s dy y w o p a p e o j u m o g 35 2 P.G.GARCÍA-NAVARRETE ETAL. alluvial deposits (Carreño, 1985; Pompa-Mera et al., 2013; Sistema Geológico Mexicano, 2023). According to the lithostratigraphy of María Madre island (McCloy et al., 1988), the oldest rocks that constitute the basement of the islands originated as a marine volcanic arc resulting from the subduction of the Farallon Plate beneath the North American Plate, prior to the formation of the Gulf of California. During the development of this tectonic event, the Farallon Plate was consumed, bringing with it the volcanic arc, which accreted to the continent. Evidence suggests that the Gulf began to form during the mid-Miocene (16-10 Mya) to Pliocene—Pleistocene (5 Mya) (Zanchi, 1994; Ferrari, 1995; Lonsdale, 1995; Helenes et al., 2009). In the Gulf of California, right-lateral oblique rifting between the North American and Pacific Plates began 12.5 Mya. Approximately 8 Mya, an initial marine embayment formed in the southernmost Gulf of California and 6.3 Mya, a narrow marine seaway was fully developed, connecting the Gulf to the Salton Trough in northern California, USA. The Gulf of California became defined during the middle Pliocene (3.52 Mya), suggesting that the Tres Marías Islands had already been separated from the continent and had reached a position approximating the current one by that time (Aguayo-Camargo €: Marín-Córdova, 1987; Lonsdale, 1989; Dorsey € Umhoefer, 2012; Bennett € Oskin, 2014; Umhoefer et al., 2018). During the Pleistocene, as a result of sea-level change due to periods of glaciation, each island experienced independent events of total or partial emergence and submergence (Hallam, 1981; Brown € Gibson, 1983). In the case of María Madre island, it has been suggested that at least one part emerged at the end of the Pleistocene during the last glacial period (McCloy et al., 1988; Pompa-Mera et al., 2013). Several biotic inventory studies have been conducted on the Tres Marías Islands, including of mammals, amphibians, reptiles, birds, terrestrial molluscs, coastal fish species, stony corals and vascular plants (Grayson, 1871; Merriam, 1898; Nelson, 1899; Stager, 1957; Zweifel, 1960; Grant € Cowan, 1964; Grant, 1965, 1966; Northern, 1965; McDiarmid et al., 1976; García-Aldrete, 1986; Wilson, 1991; Casas-Andreu, 1992; Lenz, 1995; del Prado-Gasca et al., 2006; Pérez-Vivar et al., 2006; Comisión Nacional de Áreas Naturales Protegidas, 2007, 2022; Erisman et al., 2011; Hahn et al., 2012; Nolasco-Luna et al., 2016). However, few biogeographical studies have been conducted on the biota of the Tres Marías Islands. Casas-Andreu (1992) discussed the biogeographical aspects of the herpetofauna and noted that the islands show 75-100% affinity with a continental coastal strip from Sinaloa to Michoacán. A study of stony corals suggested that the Tres Marías Islands might act as a nodal point for coral dispersal to the north, and other studies of coral communities have assessed the importance of the Tres Marías Islands as a steppingstone for species and individuals to and from the Revillagigedo Archipelago, the Gulf of California and the tropical Mexican Pacific, and the entrance of the Gulf of California has been identified as a key area for the immigration of species (Pérez-Vivar et al., 2006; López-Pérez et al., 2015). Hahn et al. (2012) studied the biogeography of birds in Pacific Mexico along an isolation gradient from mainland Chamela (coastal Jalisco), through the Tres Marías Islands and the Revillagigedo Archipelago. Endemic land bird species increased from the mainland to Revillagigedo, whereas total landbird species decreased from Revillagigedo to mainland Chamela. Ríos-Muñoz € Navarro-Sigienza (2012) used parsimony analysis of endemicity to understand the biogeographical relationships of the avifauna of seasonally dry tropical forests in Mesoamerica based on potential distributions, finding a close relationship between the Tres Marías Islands and the provinces of the Northern Group (Baja California, Northeastern Mexico, Northern Pacific Lowlands, Central Balsas Basin, Southern Plateau and Southern Pacific Lowlands). A recent study of bird dispersal suggests that the most well-supported scenario for passerine bird colonization of the Tres Marías Islands occurred via a single event + 120 kya, taking advantage of geographical conditions imposed by Pleistocene climatic changes, which is highly concordant with geological evidence (Ortiz-Ramírez et al., 2018). They also found that the islands could have taxa with different biogeographical origins, which supports complex scenarios for their biotic assembly. Two key features of the Tres Marías Islands have been previously highlighted: the geographical location between two biogeographical regions (Nearctic and Neotropical), and their interesting geological history closely associated with opening of the Gulf of California. The complexity of the islands makes them a biotic mosaic that might include species from both regions. Furthermore, continental biogeographical nodes have been identified near the Tres Marías Islands (Contreras-Medina € Eliosa- León, 2001; García-Marmolejo et al., 2008; Corona et al., 2009), suggesting that different biogeographical processes, such as vicariance and active dispersal from continental regions, might have influenced their biotic assembly. The present study aims to contribute to understanding the biogeographical affinity of the biota of the Tres Marías Islands. Our goal was achieved in three stages: first, we identified biotic components through a parsimony analysis of endemicity with progressive character elimination (PAE-PCE) to generate a primary biogeographical hypothesis on the biogeographical relationships of the areas. Second, we O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1- ez oz Je qu ia jd as gz uo Ja sn se o¡ pa uo !g Au ] 3S Ul N Y N N AQ 9/ €6 /Z 4/ 01 P e1 q/ ue su u1 jo lq /2 60 1' 01 /1 0p /a j9 nu e- so ue rp e/ ue au u1 or q/ uo 9 dn oo ue pe se // :s dy y w o p a p e o ¡ u m o g 36 BIOGEOGRAPHY OF THE TRES MARÍAS ISLANDS 3 performed a cladistic biogeographical analysis of the species endemic to the archipelago to test our primary biogeographical hypothesis using phylogenetic data. Finally, we used the phylogenetic information of endemic species to map the distribution patterns of their sister groups. This integrated information provides evidence to understand the relationship of the species of the Tres Marías Islands with those of adjacent areas and formulate hypotheses on the biotic assembly of the islands. MATERIAL AND METHODS DATA We compiled a database of terrestrial plant and animal species from the Tres Marías Islands, gathering data from the literature (Supporting Information File S1) and electronic repositories (CONABIO, 2022; GBIF, 2022; Lepage, 2022). The database was reviewed, verifying each record based on the valid names of each species and their current distribution following Barriga-Tuñón (2009), Mite Research (2010), Lepage et al. (2014), Bonato et al. (2016), Constantino (2020), Bellinger et al. (2022), Uetz et al. (2022), Bánki et al. (2023), Insecta.pro (2023), POWO (2023), Tropicos (2023), World Spider Catalog (2023) and WoRMS Editorial Board (2023). Our preliminary list contains 838 species and 163 varieties or subspecies, of which 56 are identified as endemic to the Tres Marías Islands. BIOGEOGRAPHICAL AFFINITY ANALYSIS This analysis allowed us to formulate hypotheses on the biogeographical history of the biota inhabiting the Tres Marías Islands. We tested the biogeographical affinity in three steps. First, we approached the relationship between the Tres Marías Islands and adjacent areas by identifying biotic components through an exploratory analysis of generalized tracks. The second step consisted of contrasting the results of the first step, incorporating phylogenetic information of the endemic species of the archipelago, through a cladistic biogeographical analysis. Third, we mapped the distribution of the sister groups of the endemic species used in the cladistic analysis to determine which areas were probably related to the islands. Identification of biotic components PAE-PCE is a procedure for identifying biotic components (Morrone, 2009). This involves performing a parsimony analysis on a matrix of presence-absence data, from which an area cladogram is obtained. Species supporting each resultant clade (synapomorphies) are removed from the matrix and the resulting data matrix isre-analysed iteratively until no more synapomorphies appear on the cladograms. Clades in the study area with at least two synapomorphies are considered to represent biotic components and are represented graphically on the map as generalized tracks (Luna- Vega et al., 2000). The overlap of these tracks is interpreted as a complex area or node. For this PAE- PCE, species distributed in all biogeographical units, of uncertain distribution, probably extinct, introduced and island endemics (autapomorphies) were excluded. Using the information from the provinces where the species are found, we constructed a data matrix containing 495 taxa (columns) and eight areas (rows): Tres Marías Islands, North Baja California, South Baja California, Sonoran, North Pacific Lowlands, South Pacific Lowlands, Balsas and Veracruzan provinces. The presence or absence of species was coded as 1 and “0”, respectively. A row with zeros was also included to root the cladogram (Supporting Information Table S2). PAE-PCE was applied to the matrix using TNT v.1.5 with the implicit enumeration option (Goloboff $. Catalano, 2016). Cladistic biogeographical analysis To test the affinity of the biota of the Tres Marías Islands we conducted a cladistic biogeographical analysis (Morrone € Crisci, 1995; Humphries € Parenti, 1999; Morrone, 2009; Parenti € Ebach, 2009), based on the endemic taxa of the islands for which phylogenetic and distributional information was available. We applied Brooks parsimony analysis (BPA; Brooks, 1990), which requires a matrix of nodes and areas derived from taxon—area cladograms. To include the endemic subspecies not sampled in the original phylogeny, we added a branch to the clade in which the subspecies was expected to be grouped. In the case of Pheugopedius felix, which has two endemic subspecies in the Tres Marías Islands, we selected only P. felix magdalenae. For this analysis, we treated populations on the Tres Marías Islands as endemic species (e.g. Ortiz-Ramírez et al., 2018). To construct taxon—area cladograms, we replaced the terminal taxa with their distribution data. For this analysis, the same eight areas as in the first step and 19 cladograms were considered (Table 1; Supporting Information Table S3). To obtain the node versus area matrix for BPA, we followed a pattern-based method combining supertrees and area cladograms proposed by Santos et al. (2023), which was uploaded to the SAMBA platform to generate the BPA matrix (File S4). The data matrix from SAMBA includes eight areas and 3281 nodes in the columns, plus a hypothetical area coded with zeros to root the general area cladogram (Table S5). We analysed the matrix using TNT v.1.5 with the implicit enumeration option (Goloboff €: Catalano, 2016). O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 ez oz Je qu ia jd as gz uo Ja sn se o¡ pa uw o! lg AU ] 3S Ul WN YN N ÁQ 9 4 € £ 6 4 Z 2 / L 0 1 P e I q / u e s u u i j o l q / £ 6 0 1 ' 0 1 / 1 0 p / a 1 9 / e - s o 0 u e A p e j u e a u u 1 j o 1 q / u o o dnoo1 Wepes e//:s dyy wo , p a p e o j u m o g 37 4 P.G.GARCÍA-NAVARRETE ETAL. Table 1. List of endemic taxa selected for cladistic biogeographical analysis, taxon-area cladograms used in the BPA, areas of distribution of the sister group of the endemic species, and corresponding phylogenetic information source Group Taxa Source Plants Invertebrates (insecta) Vertebrates (birds) Zanthoxylum caribaeum nelsonii Chalcolepidius forreri Danaus eresimus montezuma Amazona oratrix tresmariae Cardinalis cardinalis of Tres Marías Islands Cynanthus latirostirs lawrencei Dryobates scalaris graysoni Granatellus venustus francescae Icterus pustulatus (subsp. graysoni) of Tres Marías Islands Leptotila verreauxi capitalis Pheugopedius felix magdalenae Appelhans et al. (2018) Casari (2008) Aardema $ Andolfatto (2016) Urantówka et al. (2014) Ortiz-Ramírez et al. (2018) Hernández-Baños et al. (2020) Manthey et al. (2019) Klicka et al. (2007) Ortiz-Ramírez et al. (2018) Peters et al. (2022) Mann et al. (2009) Piranga bidentata flammea Setophaga pitiayumi insularis Vireo hypochryseus of Tres Marías Islands Aspidoscelis communis mariarum Vertebrates (reptiles) Phyllodactylus cleofasensis Peromyscus madrensis Rhogeessa parvula parvula Tlacutzin insularis Vertebrates (mammals) Campillo et al. (2019) Baiz et al. (2020) Ortiz-Ramírez et al. (2018) Barley et al. (2019) Ramírez-Reyes et al. (2021) Bradley et al. (2014) Baird et al. (2009) Arcangeli et al. (2018) Biogeographical affinity patterns To determine the biogeographical relationships of the insular species, we used the same 19 cladograms as in step two. We utilized Geographic Information System tools to delineate the distribution areas of the sister groups of each endemic species using freehand dashed lines. To represent the provinces with distribution data in the Nearctic region, we used the biogeographical regionalization of Escalante et al. (2021), and for the distributions in the Neotropical region, we used the regionalization of Morrone et al. (2022). The results of this analysis should be interpreted as indicating biogeographical affinities based on patterns, rather than directional lines or dispersal patterns. RESULTS IDENTIFICATION OF BIOTIC COMPONENTS The first run of PAE-PCE generated a single, most parsimonious area cladogram (Fig. 14), with 809 steps, a consistency index (CI) of 0.61 and a retention index (RI) of 0.68. A clade with 82 geographical synapomorphies represents the first biotic component and includes the Tres Marías Islands and the South Pacific Lowlands (Table 2). After removing the synapomorphies that supported the previous clade, the second run resulted in a single most parsimonious cladogram (Fig. 1B), with 722 steps, CI of 0.57 and RI of 0.66. This second cladogram is supported by 47 synapomorphies and represents a second biotic component joining the Tres Marías Islands with the South Pacific Lowlands and Veracruzan province (Table 2). The third run generated a most parsimonious cladogram (Fig. 1C) of 656 steps, CI of 0.55 and RI of 0.65. This run identified two main clades: one corresponds to Nearctic provinces (North and South Baja California, and Sonoran), and another corresponds to Neotropical provinces (Balsas, Veracruzan, South and North Pacific Lowlands, and the Tres Marías Islands). Additionally, the analysis revealed a connection between the Tres Marías Islands and the North Pacific Lowlands, supported by seven synapomorphies (Table 2). There was no new information in the fourth run, and it produced the same cladogram as the third analysis. Thus, three biotic components were identified as generalized tracks, and their overlap in the archipelago allowed their recognition as a complex area or node (Fig. 2). CLADISTIC BIOGEOGRAPHICAL ANALYSIS The BPA generated one most parsimonious cladogram: (((((Tres Marías Islands, Sonoran), North Pacific Lowlands), South Pacific Lowlands), Balsas), Veracruzan), South Baja California), North Baja California) with 6860 steps, CI of 0.47 and RI of 0.29. This area cladogram revealed a relationship between the Tres Marías Islands and the Sonoran province, which belongs within the Nearctic region (Fig. 1D). O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 ez oz Ja qu aj da s gz uo Ja sn se o¡ pa uo ¡g AU J SU L IN YN N ÁQ 9 4 € 6 / 2 2 / 1 0 1 P e I q / u e s u u I J o l q / £ 6 0 1 ' 0 1 / 1 0 p / a J o n i e - s o u e n p e j u e s u u 1 j o r q / u o 9 d n o ol Wa pe oe // :s dy y Wo J p a p e o j u m o g 38 BIOGEOGRAPHY OF THE TRES MARÍAS ISLANDS 5 Root North Baja California South Baja California Sonoran Balsas North Pacific Lowlands Veracruzan res Marías Islands South Pacific Lowlands Root Balsas North Baja California South Baja California Sonoran North Pacific Lowlands Tres Marías Islands South Pacific Lowlands Veracruzan Root (— North Baja California pe” Baja California Sonoran Balsas Veracruzan South Pacific Lowlands Tres Marías Islands North Pacific Lowlands North Baja California South Baja California Veracruzan Balsas South Pacific Lowlands North Pacific Lowlands Tres Marías Islands A l l Sonoran Figure 1. AC, cladograms resulting from the PAE-PCE analysis, with previous synapomorphies removed in each case. D, cladogram obtained by BPA. BIOGEOGRAPHICAL AFFINITY PATTERNS Sister groups are widely distributed across the continent. To facilitate the presentation of patterns, we selected only a few provinces to represent broader distributions not shown on the map. In the Nearctic region, sister group distributions included 11 provinces, and in the Neotropical region, 28 provinces (Supporting Information File S6). Three affinity patterns of the biota of Tres Marías Islands were identified: Neotropical, Sonoran- Neotropical and Nearctic-Neotropical. The Neotropical pattern corresponds to Zanthoxylum caribaeum (Equisetopsida), Chalcolepidius silbermanni (Insecta), Amazona oratrix (Aves), Cynanthus latirostris (Aves), Icterus pustulatus of Guerrero, Mexico (Aves), Tlacuatzin canescens of the Northern Pacific coastal plain (Mammalia) and Vireo hypochryseus of Tres Marías Islands (Aves). This pattern includes affinities with the Veracruzan and Pacific Lowlands provinces, the Antillean subregion, and Central and South America (Fig. 3A; Table 3). The Sonoran-Neotropical pattern corresponds to Granatellus venustus (Aves), Pheugopedius felix (Aves), Piranga bidentata (Aves), Setophaga pitiayumi (Aves), Aspidoscelis communis (Reptilia) and Rhogeessa parvula (Mammalia). This pattern includes affinities with the Sonoran province of the Nearctic region, and the Balsas Basin, Pacific Lowlands and Veracruzan provinces, as well as Central O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 ez oz Je qu ia jd as gz uo Ja sn se o¡ pa uw o! lg AU ] 3S Ul WN YN N ÁQ 9 4 € £ 6 4 Z 2 / L 0 1 P e I q / u e s u u i j o l q / £ 6 0 1 ' 0 1 / 1 0 p / a 1 9 / e - s o 0 u e A p e j u e a u u 1 j o 1 q / u o o dnoo1 Wepes e//:s dyy wo , p a p e o j u m o g 39 6 P.G.GARCÍA-NAVARRETE ETAL. Table 2. List of taxa that supporting the biotic components of PAE-PCE South Pacific Lowlands South Pacific Lowlands + Veracruzan North Pacific Lowlands Acalypha verbenacea Adelina bifurcata Agave fourcroydes Agave geminiflora Anolis nebuloides Anopliomorpha reticolle Anthonomus amari Aristolochia tresmariae Aspidoscelis communis Ateleia insularis Averrhoidium spondioides Balantiopteryx plicata plicata Belaphotroctes hermosus Chelicerca chamelaensis Cissus verticillata verticillata Cladioneura coriacea Coptocycla febricitans Cordia tinifolia Ctenodon brasilianus Diplotaxis sparsa Drymarchon melanurus rubidus Echmepteryx intermedia Echmepteryx pacifica Echmepteryx yañezi Elaphidion irroratum Esenbeckia nesiotica Euphorbia tresmariae Forchhammeria sessilifolia Glossophaga soricina mutica Gouinia isabelensis Guapira petenensis Gymnanthes insolita Haematopus palliatus frazari Holochroa ochra Hypsaclera holosericea Imantodes gemmistratus gracillimus Imantodes gemmistratus latistratus Justicia nelsonii Lachesilla rena Lampropeltis triangulum Lasiurus frantzit teliotis Lepidaploa canescens Leptogenys ixta Leptophis diplotropis diplotropis Lonchocarpus palmeri Macrotus waterhousii mexicanus Mastigodryas melanolomus Microdesmia arborea Morisonia odoratissima Myotis californicus mexicanus Myotis nigricans carteri Nanopsocus oceanicus Onychoprion fuscatus crissalis Ateleia pterocarpa Averellia coactiliata Bauerus dubiaquercus Bernoullia flammea Canthon corporaali Capraria mexicana Carpodiptera cubensis Carpodiptera cubensis cubensis Citharexylum hexangulare Cordia eriostigma Crematogaster opaca Croton reflexifolius Cyperus aggregatus aggregatus Dalea carthagenensis carthagenensis Dendropanax alaris Doyerea emetocathartica Elaeodendron xylocarpum Erythroxylum areolatum Esenbeckia berlandieri Eumaeus toxea Gouania stipularis Guaiacum sanctum Gymnanthes actinostemoides Helicteres guazumifolia Hippomane mancinella Lachesilla nuptialis Lampropeltis abnorma Leptothorax subditivus Mitracarpus linearifolius Myriocarpa longipes Nasutitermes corniger Neoclytus augusti Neurolaena lobata Oiketicus kirbyi Pappophorum pappiferum Passiflora suberosa litoralis Pheidole bilimeki Phyllanthus adenodiscus Pseudomyrmex cubaensis Randia monantha Rochefortia spinosa Savia sessiliflora Schizolobium parahyba Schnella herrerae Thylacella cubana Zamia loddigesii Zygia longifolia Eretes stricticus Hypogena tricornis Listrochelus venodiola Masticophis mentovarius striolatus Megasoma nogueirai Rhogeessa parvula major Sida cuspidata O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 ez oz Je qu ea jd es gz uo Ja sn se si pa uw ol g AU ] 3S Ul IN YN N ÁQ 9 / € 6 4 Z 4 / 1 0 1 P e 1 q / u e s u u 1 j o l q / 2 6 0 1 ' 0 1 / 1 0 P / a / 9 . e - s o 0 u e A p e / u e s u u o I q / u o 9 dn o o u s p e s e / / : s d y y W o p a p e o j u m o g 40 BIOGEOGRAPHY OF THE TRES MARÍAS ISLANDS 7 Table 2. Continued South Pacific Lowlands South Pacific Lowlands + Veracruzan North Pacific Lowlands Passiflora obtusifolia Paullinia clavigera clavigera Peripsocus potosi Pheidole dwyeri Phyllanthus graveolens Phyllanthus mocinoanus Phyllanthus tequilensis Phyllodactylus tuberculosus Pilocarpus racemosus Pilocarpus racemosus racemosus Plumbago zeylanica Polypsocus corruptus Pseudocaecilius citricola Psoquilla marginepunctata Punctum minutissimum Rhadinaea hesperia Salvia prasiifolia Sporobolus atrovirens Targionia hypophylla Temnoscheila virescens Thouinia serrata Tournefortia candida Turdus graysoni Urosaurus ornatus lateralis Vireo flavoviridis forreri Vireo hypochryseus sordidus Zamia paucijuga Zanthoxylum fagara culantrilo Zenaida asiatica asiatica and South America, of the Neotropical region (Fig. 3B; Table 3). The Nearctic-Neotropical pattern corresponds to Danaus eresimus (Insecta), Cardinalis cardinalis of southern Baja California and north-western Mexico (Aves), Dryobates scalaris (Aves), Leptotila verreauxi (Aves), Phyllodactylus saxatilis, Phyllodactylus nolascoensis, Phyllodactylus sp., Phyllodactylus homolepidirus, Phyllodactylus partidus (Reptilia), Peromyscus beatae, Peromyscus levipes, Peromyscus schmidlyi, Peromyscus boylii, Peromyscus simulus and Peromyscus stephani (Mammilia). This pattern includes affinities with 11 provinces of the Nearctic region and 28 provinces of the Neotropical region (Fig. 3C; Table 3). DISCUSSION The geological history of the Tres Marías Islands may have played a fundamental role in determining the biogeographical composition and affinities of their biota. These islands were formed by a tectonic event that created the Gulf of California. During the early Miocene, the Tres Marías Islands, the Baja California Peninsula and the continent formed a single continental block (Mammerickx, 1980; Lonsdale, 1995; Carreño €: Helenes, 2002), allowing for territorial continuity of the flora and fauna in these areas (Grismer, 2000; Rojas-Soto et al., 2003; Moctezuma €: Halffter, 2019). The separation of the Tres Marías Islands from the mainland suggests that the biota on the islands is probably related to the nearest continental region of the Mexican Pacific, due to vicariance; however, in more recent periods, the archipelago has undergone emergence and subduction events, allowing for dispersal. It is important to consider these geological events when trying to understand the origin and evolution of the biota of the islands. The biotic component analysis revealed a relationship between the Tres Marías Islands and the north and south Pacific Lowlands, as well as with the Veracruzan province. The relationship between the coasts of Mexico (Pacific and Gulf) follows the distribution of different taxa and, therefore, these O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 ez oz Ja qu ia jd as gz uo Je sn se oi pa uo !g AU 3S Ul N V N N ÁQ 9/ €6 /Z 4/ L0 1P EI q/ ue su uI jo l9 /2 60 L' 01 /1 0P /a Jo nu e- so ue Ap e/ ue su uI jo q/ uu oo 'd no “o 1u ap eo e/ /: sd yy uo . p a p e o ¡ u m o g 41 8 P.G.GARCÍA-NAVARRETE ET AL. South Pacific Lowlands == South Pacific Lowlands + Veracruzan North Pacific Lowlands Tres Marías Islands Biogeographical Node Figure 2. Biotic components overlapping in the Tres Marías Islands. areas have been considered part of the Neotropical region (Morrone, 2014; Morrone et al., 2022). Casas- Andreu (1992) postulated a close relationship between the Tres Marías Islands and the Mexican Pacific coast, particularly Sinaloa, Nayarit, Jalisco and Colima. The author attributed these results to both the young age of the islands and their reduced land area. An analysis by the Comisión Nacional de Áreas Naturales Protegidas (2007) evaluated floristic similarity using Sorensen's index among the Tres Marías Islands, the Revillagigedo Archipelago, Chamela Bay in Jalisco and the Baja California Peninsula. Their results showed that the greatest similarity of the Tres Marías Islands was with Chamela Bay (24.5%), while the least similarity was with the Baja California Peninsula (4.84%). The study attributed the floristic similarity of the islands to their proximity to the coast of Jalisco. In addition, the study attributed the difference with Baja California as mainly due to the tropical origin of the insular flora. Our analysis of the biotic components suggests that the Tres Marías Islands are a region of great biological complexity, where the biota of the Pacific lowlands and the Veracruzan provinces intersect. Despite their mostly Neotropical affinity, considering the Tres Marías Islands as a complex or nodal area may be due to the different historical times at which species may have arrived on the islands. The cladistic biogeographical analysis added the Nearctic affinity of the Tres Marías Islands via the Sonoran province. This affinity is closely linked to the geological history of the opening of the Gulf of California, which could be due to two possible scenarios. First, during the Miocene, dispersal occurred when the Gulf of California had not yet formed, and the Baja California Peninsula was attached to areas corresponding to Sonora and Sinaloa, including both Nearctic and Neotropical elements that moved toward the peninsula and islands when they remained as a single block in the continental mass (Cazier, 1948; Riddle, 2000; Murphy € Aguirre-León, 2002; O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 ez oz Ja qu aj da s gz uo Ja sn se o¡ pa wo !g Au ] 38 Ul N V N N ÁQ 9 / £ 6 4 Z 4 / 1 0 1 P e I q / u e a u u i j o l 9 / £ 6 0 1 ' 0 1 / 1 0 p / a J o n 1 e - s o u e n p e j u e s u u o 1 q / u i o o dn o“ o1 us pe oe // :s dy y w o p a p e o ¡ u m o g 42 BIOGEOGRAPHY OF THE TRES MARÍAS ISLANDS 9 —— Amazona oratrix tresmariae —-Chalcolepidius forreri —-Cynanthus latirostris lawrencei —-Icterus pustulatus (subsp. graysoni) —- Tlacuatzin insularis € Vireo hypocryseus (Tres Marías Islands) —-Zanthoxylum caribaeum nelsonii e [Neotropical region ES —-—Aspidoscelis communis mariarum ——Piranga bidentata flammea —-—Rhogeessa parvula parvula —-Setophaga pitiayumi insularis ——Granatellus venustus francescae € Pheugopedius felix magdalenas Sonoran province [Neotropical region ——Danaus eresimus montezuma —-Dryobates scalaris graysoni —-Leptotila verreauxi capitalis , —-Cardinalis cardinalis (Tres Marías Islands) 8 Phyllodactylus cleofasensis —-Peromyscus madrensis Nearctic region Neotropical region ES Figure 3. Biogeographical affinity patterns according to sister groups. A, Neotropical affinity pattern; B, Sonoran- Neotropical affinity pattern; C, Nearctic-Neotropical affinity pattern. O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 ez oz se qu ie jd as gz uo Ja sn se or pa Lu o! g AU] 1 SUl IN VN A ÁQ 9/ €6 2Z ./ L0 1P EI q/ ue su un ol q/ 26 01 '0 1/ 10 P/ a/ o1 /e -S Du en pe Ju ea uu Iy oq /u oo 'd no o1 ep eo e/ /: sd yy Wo J pe pe oj um og 43 10 P.G. GARCÍA-NAVARRETE ET AL. D o w n l o a d e d from h t t p s : / / a c a d e m i c . o u p . c o m / b i o l i n n e a n / a d v a n c e - a r t i c l e / d o i / 1 0 . 1 0 9 3 / b i o l i n n e a n / b l a d 1 0 1 / 7 2 7 9 3 7 6 by U N A M Inst Inv B i o m e d i c a s user on 25 S e p t e m b e r 2 0 2 3 “(UOJUTIOP UB[IZEAG [29.10] PUE UOTUTUIOP DYIDEJ) POLISULY YINOG UL UOLÍ3A [eo1do.1J09N 9YI JO UOIyeyuaseadal = ys (Mbraryo-seusrejung “e2UBUIB[E -OSNJENL) “03 MbSOJA) SIJULAOIA PILISUY [2.qU9) = Y) UOLSAIQNS UBLA]JUY = LNVY “SPUR[S] SELI]A $94, = IN “é9ULA0AId epnsuruad ue7eonA = O/1A '99ULA0Ad UBZNIDBIOA = AL, DULAVIH U S B SeS[eg ="IV8 “SPUB]mo"] 9YI0B YINOS ="]4S SPUB]MO"] DYIOBA YHON ="TAN :uozéas ¡m91d0.309N “oduracid Uedi[neure], = N V fs0utacad Ue Lredio.3sn y = s/1y “souraoad uenqengio = 149 (uexaL, URTUOYLAEN “UBIABUO]N “SESUBY “SYOUBUIO/) SEDUIAOAA YS(] 9YI JO YINOS = YS[IS “S0UILA0IA UBIOUOS = NOS “ETUAOHEO PlEJ YINOS = DAS (UBTUAOH]EO) PULIOJEO Peg YHON = DEN 5401894 9130.4D2N, V O H A A “TVE “IAS “IAN V S A S T H O N O S “DEN 1UuDY days s n o s í u o . a g “snqnurs snoshulo.tag “1I£0Q SNISKULOLIJ “1 p r u y o s snosíuo.lag 'sodi09] snISÉULOLAS “90ID9Q S N I S Á M O L I J s n p y u n d s n 3 k j o 9 o p o n y d “snupidajo v o y s n j k 3 9 0 p o ¡ £ y g “des s n j A 3 0 m p o y d SISUALPDUL SNISÁMWOLIJ L "IAN N O S D A S “$18U9098D]0U S N J A J I D P O J A Y J “ S I D A D S SNRJAJIDPO Y T s1suasoJ09]9 S N I A J I D P O Y T V S V O “ O N A H A I A “TVE “Ids - “ T A N N O S N V L V S A S T H O 1xNDILLIA D ] 0 ) d Y ] sippados 1xnNDILLIA D O d T O N A V O H H A “IVA “IdS - “ I A N N O S “DAS D A N V S A S SIID]DIS SIJDQOLLJ T U O S Á D E SIID]DIS SIJDQOÑLJ ODIXOJA] U-I9]S9M-YJIOU SPUB[S] SELIBIA T6'T "IAN N O S “DAS pue e r u o J I T e o eleg YIMOg Jo s21/DUIPIDI S I D U I P I D O S9.,L JO SI]DUIPADI S I P U I P A D O VS V O “LNV YHHA Teo1ido.1J09N = “ T V 4 “ I d s “ I d N N O S ' S N V s n u l t s a l o S n D U D ( ] D U M Z I J U O U S N U I S I L O S N D U D ( J - 0 T O I L I N - VS V O Y A A “IAS “IAN “NOS m¡naund pssoodoYy mb¿nauod vbnaund vssoodoYy - "IV4 “ I d N “IdS N O S srunuIuIo) s i j a o s o p i d s y UNADIADUL S I U N U U U O S S1J29SOprdsy vS = "VO Y A A “IVA “IAS “ I A N N O S runkoraid o S v y d o j a s siuppnsur n u n k o r a d v s v y d o j a s = VO Y H A “IVA “IAS “ I A N N O S DIDJUIPIQ D S U D M I J D I W U D ] ) DIDJUIPIQ D Í U D I I J = “IAS “ I A N N O S x19/ s n i p a d o 8 n o y d a p u a ¡ o p g b u x1]a/f s m i p a d o 8 n a y g [ e o t d o j 0 9 N - "IdS “ I A N “ N O S s n 3 s n u d a s n ] ] 9 J D U D . L ) 2 D I S I J U D A / S N I S N U I A S N ] ] I J D U D A L ) - U B . I 0 U O S spuers] 8€'0 "IdN Bo[Bu1g jo s n a s K u y o o d k y 09.11p SBLIB]A sa Jo s n a s k u y o o d A y 09.14 Z3'T "IdN ure[d [875809 9YI0BH ULOUJIOU JO SUIISIUDI U I Z I N I D ] Y, S1LD]NSUI UIZINID],L, SPUR[S] SBLIB]A $91] JO (1U0SkDLS 03'0 "Iás ODIXAJA] “019.1IDNL) JO SNJD]NISNA SN.LIJI] “dsqns) s n 3 o n 3 s n d sntapo] - Y H A “IAS “ I A N S1.180.117D] S N Y J U D U L D 19919. MD] S1750.117D] S N Y J U D U L D - VO Y A A “IAS DJD1I7D]0.IND D U O Z D U Y “X1LIDLO D U O Z D U Y IDILDUISIL] XILJDLO D U O Z D U Y - VS V O L N V Y U H A “IAS UUDULLIQ]IS S M I P I A O N D Y D 1.94.0/ sn1p1d3J09]DYD - VS V O “ L N V H H A “IAS “ I A N U N I D Q I I D A U N J Á X O Y J U D Z — 17UOSIQU ULNIDQUIDO U N J Á X O Y F U D Z — TeordorjooN sule3yed au Aqrugge [eo1 2 J U A T I S A L T U O N Q L A J S T P JO SESIY dno13 197518 serads I u s p u g -yde13os3o1g Q U ) 9)U93.19AIP I19Y) Pue “sorpruyye restyde13o09B01q 94) SUYAP 0) pasn dno.3 197518 1194) “SPUB[S] SBLIB]A $9], 94) 07 sotdads 9 I U S P U H “E I I A B L O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 44 BIOGEOGRAPHY OF THE TRES MARÍAS ISLANDS 11 Moctezuma €: Halffter, 2019). The second scenario suggests that this relationship could be the result of recent history, in the early Pliocene, when the Gulf of California had already formed and species of Nearctic origin actively or passively dispersed to colonize the islands from the north through the Baja California Peninsula or directly from Sonora (Davis, 1959; Murphy € Aguirre-León, 2002; Rojas-Soto et al., 2003; Moctezuma éz Halffter, 2019). A third scenario would be a combination of the two previous ones. To determine the most feasible scenario for biotic assembly, it is necessary to have dated phylogenies that suggest species divergence. It is also important to consider the distribution of sister taxa, which may suggest an affinity in distribution with either the Mexican Pacific mainland or the Baja California Peninsula. Analysis of biogeographical affinities defined three patterns. The Neotropical pattern showed affinity with the coasts of the Mexican Pacific slope and the Gulf of Mexico, as determined by the biotic component analysis. Additionally, the areas of Central and South America and the Antilles were identified as part of this pattern. Of the seven endemic species that defined the Neotropical affinity pattern, three had phylogenetic divergence dates: Tlacuatzin insularis (Mammalia), Icterus pustulatus graysoni (Aves) and Vireo hypochryseus (Aves). The phylogeny of Tlacuatzin insularis suggested a divergence time of 1.22 Mya with regard to Tlacuatzin canescens from the northern Pacific Lowlands (Arcangeli et al., 2018). The diversification of this taxon occurred during the Pleistocene, suggesting that climatic changes and geographical barriers such as the Sierra Madre Occidental, the Transmexican Volcanic Belt, the Sierra Madre del Sur and the Isthmus of Tehuantepec influenced the divergence of these populations. This mouse possum might have reached the islands through a terrestrial bridge during a glacial period when sea level was low (Arcangeli ef al., 2018). Regarding populations from the North Pacific Lowlands, insular populations of Vireo hypochryseus showed a divergence time of 0.38 Mya from populations from the North Pacific Lowlands, while /cterus pustulatus graysoni showed a divergence time 0£ 0.20 Mya from populations of I. pustulatus from Guerrero (Ortiz-Ramírez et al., 2018). Fixation indices (F¿p) were significant for V. hypochryseus, but not for [. pustulatus, suggesting that only the insular populations of V. hypochryseus are genetically differentiated. However, populations in these two species are geographically close, which may allow for occasional exchange of migrants. Based on these data, the endemic populations of Tres Marías Islands diverged relatively recently, during the Pleistocene, from their sister groups. Therefore, the biota of the Tres Marías Islands is closely related to the Neotropical region via the lowlands of the Mexican Pacific (Stager, 1957; Zweifel, 1960; García-Aldrete, 1986). Recent divergence has also been postulated for the herpetofauna of the Tres Marías Islands (Casas- Andreu, 1992). The Sonoran-Neotropical affinity pattern, also identified in the cladistic biogeographical analysis, indicates that the Tres Marías Islands might be related to the Nearctic region, due to an extension of Pacific coastal species distributions, as seen in the typical Neotropical pattern (Cazier, 1948; Rzedowski, 1978; Enderson et al., 2009; Halffter € Morrone, 2017). This pattern shows that taxa are distributed along the Pacific and Gulf of Mexico coasts, with their distribution extending slightly further north into Sonora, Tamaulipas and even the USA, but unfortunately we do not have dated phylogenies. Such information would be useful in determining whether this affinity pattern is due to ancient migration before the separation of the Baja California Peninsula, or if it is due to more recent dispersal over the Peninsula after the Gulf of California formed. The Nearctic-Neotropical pattern suggests biotic similarities with both regions. The dated phylogenies showed divergence times of 7 and 1.9 Mya. A lower divergence time occurred between the populations of Cardinalis cardinalis (Aves) from Tres Marías Islands and those from southern Baja California and north-west Mexico (Ortiz-Ramírez et al., 2018). In this case, the fixation indices were significant, and the populations are genetically differentiated; therefore, the affinity of Tres Marias Islands with both southern Baja California and north-west Mexico may be due to recent speciation. Phyllodactylus cleofasenis (Reptilia) and its sister group, which consists of four species, diverged -7 Mya (Ramírez-Reyes et al., 2021), which may reflect the ancient affinities that existed before the formation of the Gulf of California. The genus Phyllodactylus has endemic species not only on the Tres Marías Islands but also in the islands of the Gulf of California and the Baja California Peninsula (Casas-Andreu, 1992; Blair, 2009; Ramírez-Reyes et al., 2020). According to Ramírez-Reyes et al. (2020), Phyllodactylus cleofasensis populations from María Cleofas island diverged from mainland lineages during the early Pliocene. María Cleofas island, like the other islands ofthe archipelago, may have undergone periods of total or partial emergence and submergence due to the periods of glaciation. The last emergence of María Cleofas island probably occurred in the late Pliocene— Pleistocene, similar to that of María Madre (McCloy et al., 1988; Pompa-Mera et al., 2013). The emergence of these islands has enabled the dispersal of taxa from the mainland.The analysis ofOrtiz-Ramírez et al.(2018) on dispersal routes supports the hypothesis that the Tres Marías Islands were colonized by populations from north-western Mexico (Sonora, Sinaloa, Nayarit and O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 ez oz Je qu ia jd as gz uo Ja sn se o¡ pa uw o! lg AU ] 3S Ul WN YN N ÁQ 9 4 € £ 6 4 Z 2 / L 0 1 P e I q / u e s u u i j o l q / £ 6 0 1 ' 0 1 / 1 0 p / a 1 9 / e - s o 0 u e A p e j u e a u u 1 j o 1 q / u o o dnoo1 Wepes e//:s dyy wo , p a p e o j u m o g 45 12 P.G. GARCÍA-NAVARRETE ET AL. Jalisco) due to population expansion during favourable environmental conditions of the Pleistocene. Our analysis of biogeographical affinities suggests that the Tres Marías Islands are related to both the Nearctic and Neotropical regions. However, the Nearctic provinces are only found together with the Neotropical provinces, suggesting a Neotropical origin with subsequent dispersal towards northern Mexico (Cazier, 1948; Rzedowski, 1978; Casas-Andreu, 1992; Enderson et al., 2009; Halffter €: Morrone, 2017; Ortiz- Ramírez et al., 2018). The phylogenetic data showed divergences times ranging from at least 7 Mya to less than 1.5 Mya, suggesting that the biota of the islands was composed of elements from different time periods, from when the peninsula was still part ofthe mainland until the islands reached a position close to that of the present. The biogeographical affinity patterns of the Tres Marías Islands are related to the geological history of the region. The separation of the Baja California Peninsula and its displacement towards the north-west gave rise to different patterns of dispersal, isolation, extinction and speciation in the fauna and flora (Case et al.,2002). The opening ofthe Gulf of Cali ornia resulted from the subduction of the Farallon Plate beneath the North American Plate, causing the Pacific Plate to move north-westward. Eventually, continental rifting was initiated in the North American Plate coupled with the Pacific Plate. The Farallon Plate finished its subduction at the end ofthe Middle Miocene (Lonsdale, 1989; Zanchi, 1994; Carreño €: Helens, 2002; Ferrari et al., 2018; Umhoefer et al., 2018). During the Miocene, continental configurations allowed dispersal to land, leading to subsequent vicariant speciation (e.g. in Phyllodactylus). Our study has only analysed data on taxa with Neotropical affinity, but it is possible that the overland dispersal pattern during the Miocene also occurred in taxa with Nearctic affinity (Moctezuma € Halffter, 2019). During the early Pliocene, the first oceanic crust formed in the Gulf of California, which separated the continental region from the peninsula and created smaller landmasses in the form of islands (Lonsdale, 1989; Bennett € Oskin, 2014; Umhoefer et al., 2018). Later, during the Pleistocene, sea level dropped by between 100 and 200 m during periods of glaciation (Hallam, 1981; Brown € Gibson, 1983), allowing the Tres Marías Islands to become connected to the mainland through land bridges and providing the opportunity for some species (e.g. Tlacuatzin insularis) to reach the islands by dispersal (Casas- Andreu, 1992; Arcangeli et al., 2018; Ortiz-Ramírez et al., 2018). The isolation of the Tres Marías Islands has promoted significant stages of genetic differentiation and the processes of population dynamics on the islands are different from those that occur on the nearby continent (Ortiz-Ramírez el al., 2018). Isolation leads to processes of divergence in insular populations due to highly reduced gene flow (e.g. Phyllodactylus cleofasensis and Tlacuatzin insularis); however, in some instances, insular and continental populations may still maintain some gene flow (e.g. [cterus pustulatus). This study describes a close biogeographical affinity of the Tres Marías Islands with the Neotropical region. Nevertheless, insular areas can host elements of different biogeographical origins. We also describe the Tres Marías Islands as a node or complex area supporting various scenarios of species assembly on the islands, with a biota assembled at different time periods and through different processes. These processes include terrestrial dispersal in a connected area prior to the formation of the Gulf of California; vicariant events due to the separation of the Baja California Peninsula, which isolated populations and led to diversification and speciation; and passive or active dispersal events from the continent to the islands after the formation of the Gulf of California due to sea level fluctuations during the Pleistocene, which led to incipient speciation. ACKNOWLEDGMENTS P.G.G.N. thanks the Posgrado en Ciencias Biológicas of the Universidad Nacional Autónoma de México (UNAM) for academic training and logistical support, and Isvi E. Gutiérrez-Pérez for the revision of the geological information. P.G.G.N. was supported by a grant from the Consejo Nacional de Humanidades, Ciencia y Teconología (CONAHCyT; CVU 444876). We thank Daubian Santos for support with the SAMBA platform. CONFLICTS OF INTEREST The authors declare that they have no potential conflicts of interest. 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The reptile Database. Available at: http://www.reptile- database.org. Umbhoefer PJ, Darin MH, Bennett SE, Skinner LA, Dorsey RJ, Oskin ME. 2018. Breaching of strike-slip faults and successive flooding of pull-apart basins to form the Gulf of California seaway from ca. 8-6 Ma. The Geological Society of America 46: 695-698. Urantówka AD, Mackiewicz P, Strzala T. 2014. Phylogeny of Amazona barbadensis and the Yellow-Headed Amazon Complex (Aves: Psittacidae): a new look at South American Parrot evolution. PLoS One 9:e97228.https://doi.org/10.1371/ journal.pone.0097228 Wilson DE. 1991. Mammals of the Tres Marías Islands. In: Griffiths TA, Klingener D, eds. Contributions to mammalogy in honor of Karl F. Koopman. Bulletin of the American Museum of Natural History 206: 214-250. World Spider Catalog. 2023. World Spider Catalog. Version 23.5. Natural History Museum Bern. Available at: http://wsc. nmbe.ch WoRMS Editorial Board. 2023. World Register of Marine Species. Available at: https://www.marinespecies.org Zanchi A. 1994. The opening of the Gulf of California near Loreto, Baja California, Mexico: from basin and range extension to transtensional tectonics. Journal of Structural Geology 16: 1619-1639. https://doi. org/10.1016/0191-8141(94)90131-7 Zweifel RG. 1960. Results of the puritan-American Museum of Natural History expedition to western Mexico Herpetology of the Tres Marías Islands. Bulletin of the American Museum of Natural History 119: 77-128. SUPPORTING INFORMATION Additional supporting information may be found in the online version of this article on the publisher's website. File S1. References regarding the plant and animal species of the Tres Marías Islands. Table S2. Data matrix of biogeographical units vs. species used in PAE-PCE. Table S3. Taxon-area cladograms used in the BPA. File S4. Text file for the SAMBA platform and the combined matrix used in BPA. Table S5. Combined matrix from SAMBA used in BPA. File S6. Nearctic and Neotropical provinces used to map the distribution of the sister group of endemic species. O 2023 The Linnean Society of London, Biological Journal of the Linnean Society, 2023, XX, 1-16 ez oz Ja eq ua jd as gz uo Ja sn se o¡ pa uw o! g Au ] 38 Ul N V N N ÁQ 9 / £ 6 4 Z 4 / L 0 1 P E I q / u e a u u i j o l 9 / £ 6 0 1 " 0 1 / 1 0 p / a J o p 1 e - s o u e n p e / u e s u u o 1 q / u i o o dn o“ o1 us pe oe // :s dy y w o p a p e o ¡ u m o g 50 51 DISCUSIÓN GENERAL Y CONCLUSIONES En el primer capítulo de esta tesis se examinó la composición biótica del Archipiélago de Revillagigedo en el contexto de la biogeografía evolutiva. La relevancia de este archipiélago en la conservación de la biodiversidad llevó al gobierno de México a designarlo Área Natural Protegida con el carácter de Reserva de la Biósfera en 2007 y como Parque Nacional en 2017 (DOF, 2017). Inicialmente, se llevó a cabo un análisis de parsimonia de endemismos con eliminación progresiva de caracteres (PAE-PCE), lo que permitió identificar al archipiélago como un área compleja o nodo donde se superponen los componentes bióticos Neártico y Neotropical. Posteriormente, se realizó un análisis biogeográfico cladístico utilizando la información filogenética de 42 cladogramas taxonómicos de áreas, a partir de los cuales se obtuvo un cladograma general: (Revillagigedo, (Sonorense, (Baja California, (Veracruzana, (Tierras Bajas del Pacífico))))). Este cladograma reveló una relación independiente del archipiélago con el resto de las áreas. Los resultados sugieren que el Archipiélago de Revillagigedo podría clasificarse como una provincia, aunque se prefiere mantenerlo como un distrito perteneciente a la provincia de las Tierras Bajas del Pacífico debido a que la disparidad en la proporción de sinapomorfías entre las regiones Neotropical y Neártica fue evidente, con 87 sinapomorfías compartidas con el Neotropical y solo 6 con el Neártico. Además, con base en dataciones filogenéticas se identificaron dos cenocrones del Plioceno-Pleistoceno: uno Neártico que posiblemente se dispersó desde la península de Baja California, y otro Neotropical donde las especies se dispersaron desde la costa del Pacífico hacia las islas. En la formulación de una hipótesis para proponer un escenario geobiótico de Revillagigedo, es imprescindible comprender la historia geológica del sitio. La evidencia apunta a que las islas Revillagigedo son probablemente el resultado del vulcanismo asociado con la dorsal oceánica de Matemáticos, ya que los periodos de actividad de la dorsal coinciden con la datación aproximada de las islas con base en los datos litológicos. De acuerdo con dataciones de las islas del archipiélago, Clarión fue la primera isla en emerger, originándose a partir de erupciones volcánicas submarinas en el Eoceno-Mioceno (56 – 5.33 Ma). Aunque la edad geológica precisa de Roca Partida aún no se ha determinado, algunos autores sugieren que es más antigua que San Benedicto y Socorro. La isla Socorro experimentó su primera erupción en el Mioceno (23.3 – 52 5.33 Ma), y se ha determinado que San Benedicto es la isla más joven del archipiélago (Richards 1964; Ortega-Gutiérrez y Sánchez-Rubio 1985; Brattstrom 1990). Con la información geológica del archipiélago y los análisis biogeográficos evolutivos realizados se infiere que el Archipiélago de Revillagigedo es un área compleja donde convergen dos biotas distintas: una neotropical (Tierras Bajas del Pacífico) y otra neártica (Baja California). Debido al origen volcánico del archipiélago, estos componentes representan biotas ancestrales ensambladas por eventos de dispersión durante el Plio-Pleistoceno, después de que las islas estuvieran disponibles para la colonización. La formulación de la hipótesis del escenario geobiótico del Archipiélago de Revillagigedo, basada en la integración de diversos métodos biogeográficos empleados en el análisis del Capítulo I, condujo a la inferencia de un escenario que postula la llegada simultánea de los cenocrones Neártico y Neotropical al Archipiélago de Revillagigedo durante el Plioceno (5.33 Ma) y hasta el Pleistoceno (0.29 Ma), de manera prácticamente continua. La dispersión de estos cenocrones pudo haberse producido durante el Plioceno, época en la cual la isla Clarión ya había emergido sobre el nivel del mar. Se sugiere que el cenocrón Neártico podría haber alcanzado la isla a lo largo de la península de Baja California, ya separada del continente, mientras que el cenocrón Neotropical pudo haberse dispersado durante el Plioceno desde América del Sur, pasando por América Central y el sur de México (Halffter y Morrone 2017). Este proceso pudo ocurrir en un intervalo de tiempo en el que también ocurrieron los eventos volcánicos asociados a la distención tectónica de la Faja Volcánica Transmexicana, permitiendo a las especies moverse a lo largo de la costa del Pacífico mexicano y llegar a las islas del archipiélago de Revillagigedo. En el segundo capítulo de esta tesis se llevó a cabo un análisis integral de las afinidades biogeográficas de la biota de las Islas Marías. Este archipiélago, ubicado en el Pacífico central mexicano, presenta una historia geológica compleja atribuida a su configuración tectónica y ha sido reconocido como un área natural protegida y designado como reserva de la biósfera (Secretaría de Medio Ambiente, Recursos Naturales y Pesca, 2000). El estudio biogeográfico de las Islas Marías se realizó en tres etapas. En la primera etapa se llevó a cabo la identificación de los componentes bióticos mediante un análisis exploratorio de trazos generalizados. En este análisis se identificó un componente biótico que conecta a las Islas Marías con el sur de la Tierras Bajas del Pacífico; otro componente biótico vinculó a las Islas con el sur 53 de las Tierras Bajas del Pacífico y la provincia Veracruzana; y un tercer componente biótico asoció las Islas con el norte de las Tierras Bajas del Pacífico. La superposición de estos componentes en las Islas Marías evidenció su naturaleza de un área compleja o nodo biogeográfico. En la segunda etapa del estudio se llevó a cabo una evaluación biogeográfica cladística que generó el siguiente cladograma de áreas: (((((((Islas Marías, Sonora), Norte de las Tierras Bajas del Pacífico), Sur de las Tierras Bajas del Pacífico), Balsas), Veracruzana), Baja California Sur), Baja California Norte). Finalmente, se utilizó la información filogenética de las especies endémicas, para representar los patrones de distribución geográfica de sus grupos hermanos, con el propósito de identificar las áreas con las que las islas guardan una relación más probable. En este mapeo se identificaron tres patrones de afinidad: Neotropical, Sonorense- Neotropical y Neártico-Neotropical. Al abordar la comprensión del origen y la evolución de la biota de las Islas Marías, es esencial considerar tanto los análisis biogeográficos integrales como los eventos geológicos que dieron forma a la historia biogeográfica de estas islas. La formación de las Islas Marías se atribuye a eventos tectónicos que formaron el Golfo de California. En el Mioceno temprano (23.03 -15.97 Ma), las Islas Marías, la península de Baja California y el continente constituían un bloque continental (Mammericks, 1980; Lonsdale, 1995; Carreño y Helenes, 2002), manteniendo la continuidad territorial de la flora y fauna (Grismer, 2000; Rojas-Soto et al., 2003; Moctezuma y Halffter, 2019). La separación posterior de las Islas Marías del continente sugiere una relación probable de la biota de las islas con la región continental más cercana del Pacífico mexicano, mediada por procesos de vicarianza. No obstante, en periodos más recientes, las Islas Marías han experimentado eventos de cambios en el nivel del mar, permitiendo también la dispersión de especies hacia estas islas. Este estudio revela una afinidad biogeográfica estrecha de las Islas Marías con la región Neotropical. Además, se definió a las islas como un nodo o área compleja que respalda varios escenarios de ensamblaje de especies, con una biota reunida en distintos períodos y mediante diversos procesos. Estos procesos comprenden la dispersión terrestre en un área conectada previa a la formación del Golfo de California; eventos vicariantes ocasionados por la separación de la Península de Baja California, que aislaron poblaciones y fomentaron la diversificación y especiación; y eventos de dispersión, ya sea pasiva o activa, desde el continente hacia las islas 54 después de la formación del Golfo de California, a consecuencia de las fluctuaciones del nivel del mar durante el Pleistoceno, propiciando así la especiación incipiente. En este estudio biogeográfico, se integra y analiza información sobre el ensamblaje biótico y la historia geológica de las Islas Marías. La formación biótica de estas islas pudo haber ocurrido mediante procesos de vicarianza y dispersión en distintos momentos geológicos, vinculados con la apertura del Golfo de California (Mioceno-Pleistoceno) como con periodos de glaciación (Pleistoceno). Este trabajo doctoral proporciona una visión integral de la biogeografía evolutiva de los archipiélagos del Pacífico mexicano. En el primer capítulo se estableció que el Archipiélago de Revillagigedo es una zona compleja o nodo, con componentes bióticos Neárticos y Neotropicales. La datación filogenética indicó la presencia de dos cenocrones en el Plio- Pleistoceno, sugiriendo procesos de dispersión desde Baja California y la costa del Pacífico hacia las islas. En el segundo capítulo, las Islas Marías revelaron una conexión con la región Neotropical, evidenciando eventos vicariantes y de dispersión relacionados con la formación del Golfo de California y fluctuaciones del nivel del mar. El estudio de los archipiélagos de Revillagigedo y las Islas Marías en el Pacífico mexicano proporcionó una comprensión más profunda de la historia biogeográfica y la composición biótica única de estas islas. La identificación de sus componentes bióticos, las relaciones con las regiones Neártica y Neotropical, así como los procesos de colonización, ha destacado aspectos esenciales para la conservación y gestión efectiva de estos ecosistemas insulares. La aplicación de la biogeografía evolutiva en estos archipiélagos no solo contribuye al conocimiento científico fundamental, sino que también sienta las bases para futuras investigaciones sobre la evolución biológica en las islas del Pacífico mexicano y sus implicaciones para la conservación de la diversidad biológica de México. 55 REFERENCIAS BIBLIOGRÁFICAS Aguirre-Muñoz A., Bezaury-Creel J., de la Cueva H., March-Mifsut I., Peters-Recagno E., Rojas S., Santos K. 2010. Islas de México: Un recurso estratégico. 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Interacciones potenciales parásito-hospedero entre Dendroctonus y Pinus en México La presente publicación es de acceso libre: García-Navarrete P.G., Soria-Ortiz G.J., González-Salazar C. 2021. Interacciones potenciales parásito-hospedero entre el escarabajo Dendroctonus (Coleoptera: Scolytidae) y Pinus (Pinaceae) en México. Revista de Biología Tropical, 69(3): 1004-1022. https://dx.doi.org/10.15517/rbt.v69i3.45910 59 II. Distribución potencial de los híbridos entre Crocodylus acutus y Crocodylus moreletii en la costa del Pacífico mexicano fuera de su zona natural de hibridación La presente publicación es de acceso libre: Soria-Ortiz G.J., García-Navarrete P.G., Ochoa-Ochoa L.M., Rincón-Gutiérrez A. 2022. Potential distribution of hybrids between Crocodylus acutus and Crocodylus moreletii on the Mexican Pacific coast outside the natural hybridistion zone. Herpetological Journal, 32(3): 93-101. http://doi.org/10.33256/32.393101