Secondary sympatry amongst sister lineages is strongly associated with genetic and ecological divergence. This pattern suggests that for closely related species to coexist in secondary sympatry, they must accumulate differences in traits that mediate ecological and/or reproductive isolation. Here, we characterized inter- and intraspecific divergence in three giant tree frog species whose distributions stretch across West and Central Africa. Using genome-wide single-nucleotide polymorphism data, we demonstrated that species-level divergence coincides temporally and geographically with a period of large-scale forest fragmentation during the late Pliocene. Our environmental niche models further supported a dynamic history of climatic suitability and stability, and indicated that all three species occupy distinct environmental niches. We found modest morphological differentiation amongst the species with significant divergence in tympanum diameter and male advertisement call. In addition, we confirmed that two species occur in secondary sympatry in Central Africa but found no evidence of hybridization. These patterns support the hypothesis that cycles of genetic exchange and isolation across West and Central Africa have contributed to globally significant biodiversity. Furthermore, divergence in both ecology and reproductive traits appear to have played important roles in maintaining distinct lineages. At the intraspecific level, we found that climatic refugia, precipitation gradients, marine incursions, and potentially riverine barriers generated phylogeographic structure throughout the Pleistocene and into the Holocene. Further studies examining phenotypic divergence and secondary contact amongst these geographically structured populations may demonstrate how smaller scale and more recent biogeographic barriers contribute to regional diversification.

La sympatrie secondaire parmi les espèces sœurs est fortement associée à la divergence génétique et écologique. Ce modèle suggère que pour que des espèces étroitement liées coexistent en sympatrie secondaire, elles doivent accumuler des différences dans les traits qui contribuent à l'isolement écologique ou reproductif. Ici, nous avons caractérisé la divergence inter- et intra-spécifique chez trois espèces de grenouilles arboricoles géantes dont les distributions s'étendent à travers l'Afrique de l'Ouest et Centrale. Avec des données génétiques, nous avons démontré que la divergence au niveau des espèces coïncide temporellement et géographiquement avec une période de fragmentation forestière à la fin du Pliocène. Nos modèles de niches environnementales ont soutenu une histoire dynamique de stabilité climatique, et ont indiqué que les trois espèces occupent des niches environnementales distinctes. Nous avons trouvé une différenciation morphologique modeste parmi les trois espèces mais une divergence significative dans le diamètre du tympan et les cris des mâles. De plus, nous avons confirmé que deux espèces sont présentes en sympatrie secondaire en Afrique Centrale mais n'avons trouvé aucune preuve d'hybridation. Ces résultats soutiennent l'hypothèse que les cycles d'échange génétique et d'isolement à travers l'Afrique de l'Ouest et Centrale ont contribué à une profonde concentration de biodiversité dans la région. De plus, la divergence des traits écologiques et reproducteurs semble avoir joué un rôle important dans le maintien de lignées distinctes. Au niveau intra-spécifique, nous avons constaté que les refuges climatiques, les gradients de précipitation, les incursions marines et potentiellement les barrières fluviales ont généré une structure phylogéographique pendant le Pléistocène et jusqu'à l'Holocène. Des études examinant la divergence phénotypique et le contact secondaire entre ces populations géographiquement structurées pourraient démontrer comment des barrières biogéographiques à échelle plus petite et plus récentes contribuent à la diversification régionale.

Amphibian and Reptile Diversity Research Center Department of Biology University of Texas at Arlington Arlington Texas USA

Bioko Biodiversity Protection Project Drexel University Philadelphia Pennsylvania USA

Chair of Wildlife Ecology and Wildlife Management University of Freiburg Freiburg Germany

CIBIO InBio Centro de Investigação em Biodiversidade e Recursos Genéticos Universidade do Porto Campus de Vairão Vairão Portugal

Département d'Ecologie et Biodiversité des Ressources Aquatiques Centre de Surveillance de la Biodiversité Université de Kisangani Kisangani République Démocratique du Congo

Département d'Ecologie et Biodiversité des Ressources Terrestres Centre de Surveillance de la Biodiversité Université de Kisangani République Démocratique du Congo Kisangani

Department of Biological Sciences University of Texas at El Paso El Paso Texas USA

Department of Biology Adrian College Michigan USA

Department of Biology and Burke Museum of Natural History and Culture University of Washington Seattle Washington USA

Department of Biology University of Florida Florida USA

Department of Ecology and Evolutionary Biology Princeton University New Jersey USA

Department of Integrative Biology W K Kellogg Biological Station Michigan State University Michigan USA

Department of Natural History Florida Museum of Natural History University of Florida Gainesville Florida USA

Department of Vertebrate Zoology National Museum of Natural History Smithsonian Institution Washington DC USA

Department of Zoology Faculty of Science University of Lagos Lagos Nigeria

Department of Zoology National Museum Prague Czech Republic

Ecology Evolution and Behavior Program Michigan State University Michigan USA

Faculdade de Ciências da Universidade do Porto Porto Portugal

Fundação Kissama Luanda Angola

Gabon Biodiversity Program Smithsonian Conservation Biology Institute Gamba Gabon

Herpetology Department Institute for Biodiversity Science and Sustainability California Academy of Sciences San Francisco California USA

Institut National de Recherche en Sciences Exactes et Naturelles Brazzaville République du Congo

Institute de Recherches Agronomiques et Forestières Libreville Gabon

Institute of Conservation Science and Learning Bristol Zoological Society Bristol UK

Institute of Vertebrate Biology Czech Academy of Sciences Brno Czech Republic

Instituto Superior de Ciências da Educação da Huíla Rua Sarmento Rodrigues Lubango Angola

Laboratoire d'Herpétologie Département de Biologie Centre de Recherche en Sciences Naturelles République Démocratique du Congo Lwiro

Leibniz Institute for Evolution and Biodiversity Science Museum für Naturkunde Berlin Germany

Museum of Zoology Senckenberg Natural History Collections Dresden Dresden Germany

School of Natural Resources and Environment University of Florida Florida USA

Section of Research and Collections North Carolina Museum of Natural Sciences North Carolina USA

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