Diversity and Evolution of Frog Visual Opsins: Spectral Tuning and Adaptation to Distinct Light Environments.

Visual systems adapt to different light environments through several avenues including optical changes to the eye and neurological changes in how light signals are processed and interpreted. Spectral sensitivity can evolve via changes to visual pigments housed in the retinal photoreceptors through gene duplication and loss, differential and coexpression, and sequence evolution. Frogs provide an excellent, yet understudied, system for visual evolution research due to their diversity of ecologies (including biphasic aquatic-terrestrial life cycles) that we hypothesize imposed different selective pressures leading to adaptive evolution of the visual system, notably the opsins that encode the protein component of the visual pigments responsible for the first step in visual perception. Here, we analyze the diversity and evolution of visual opsin genes from 93 new eye transcriptomes plus published data for a combined dataset spanning 122 frog species and 34 families. We find that most species express the four visual opsins previously identified in frogs but show evidence for gene loss in two lineages. Further, we present evidence of positive selection in three opsins and shifts in selective pressures associated with differences in habitat and life history, but not activity pattern. We identify substantial novel variation in the visual opsins and, using microspectrophotometry, find highly variable spectral sensitivities, expanding known ranges for all frog visual pigments. Mutations at spectral-tuning sites only partially account for this variation, suggesting that frogs have used tuning pathways that are unique among vertebrates. These results support the hypothesis of adaptive evolution in photoreceptor physiology across the frog tree of life in response to varying environmental and ecological factors and further our growing understanding of vertebrate visual evolution.

The bii4africa dataset of faunal and floral population intactness estimates across Africa's major land uses.

Sub-Saharan Africa is under-represented in global biodiversity datasets, particularly regarding the impact of land use on species' population abundances. Drawing on recent advances in expert elicitation to ensure data consistency, 200 experts were convened using a modified-Delphi process to estimate 'intactness scores': the remaining proportion of an 'intact' reference population of a species group in a particular land use, on a scale from 0 (no remaining individuals) to 1 (same abundance as the reference) and, in rare cases, to 2 (populations that thrive in human-modified landscapes). The resulting bii4africa dataset contains intactness scores representing terrestrial vertebrates (tetrapods: ±5,400 amphibians, reptiles, birds, mammals) and vascular plants (±45,000 forbs, graminoids, trees, shrubs) in sub-Saharan Africa across the region's major land uses (urban, cropland, rangeland, plantation, protected, etc.) and intensities (e.g., large-scale vs smallholder cropland). This dataset was co-produced as part of the Biodiversity Intactness Index for Africa Project. Additional uses include assessing ecosystem condition; rectifying geographic/taxonomic biases in global biodiversity indicators and maps; and informing the Red List of Ecosystems.

Giant Tree Frog diversification in West and Central Africa: Isolation by physical barriers, climate, and reproductive traits.

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.