Rivers, not refugia, drove diversification in arboreal, sub-Saharan African snakes

Allen, Kaitlin E.; Greenbaum, Eli; Hime, Paul M.; Nkonmeneck, Walter Paulin Tapondjou; Sterkhova, Viktoria; Kusamba, Chifundera; Rödel, Mark‐Oliver; Penner, Johannes; Peterson, A. Townsend; Brown, Rafe M.

doi:10.22541/au.158880203.33695479

Cited by 3 publications

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“…For instance, we found distinct lineages of L . millsoni on either side of the Sanaga and Congo Rivers, and both rivers coincide with intra‐ and interspecific levels of divergence in a range of taxa including the ground dwelling long‐fingered frogs (Hirschfeld et al, 2015), swamp rats (Bohoussou et al, 2015), arboreal snakes (Allen et al, 2021), and chimpanzees (Hey, 2010). Likewise, our ENMs identify several regions within West and Central African rainforests as climatically suitable throughout the late Pleistocene to present day for L .…”

Section: Discussionmentioning

confidence: 92%

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

et al. 2021

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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.

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Section: Discussionmentioning

confidence: 92%

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

et al. 2021

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“…Pirani et al (2019) indicated that divergence-time across river basins varies, suggesting that river barriers can be dynamic considering connection and isolation induced by climatic ameliorations. By contrast, forest-living snakes in the Congo River basin exhibit divergence across the river independent of isolation by climatic ameliorations (Allen et al, 2021). The strength of the dispersal barrier is, however, variable, being stronger where the river is wider (Allen et al, 2021).…”

Section: Rivers As a Biogeographic Barriermentioning

confidence: 99%

“…By contrast, forest-living snakes in the Congo River basin exhibit divergence across the river independent of isolation by climatic ameliorations (Allen et al, 2021). The strength of the dispersal barrier is, however, variable, being stronger where the river is wider (Allen et al, 2021). Similarly, in a recent study of 33 animal taxa along the Colorado River, Dolby et al (2019) suggested that rivers should be viewed as leaky barriers, that filter rather than prevent gene flow.…”

Section: Rivers As a Biogeographic Barriermentioning

confidence: 99%

Pseudocongruent phylogeography reflects unique responses to environmental perturbations in a biodiversity hotspot

Busschau

Jordaan

Conradie

et al. 2022

Journal of Biogeography

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Aim: Comparative phylogeographic studies provide important insights into the biogeographic processes shaping regional patterns of diversity. Yet, comparative studies are lacking for southern African herpetofauna, despite their high diversity. We statistically compare phylogeographic structure and divergence-time estimates among five co-distributed forest-living herpetofaunal taxa to assess rivers, climatic refugia and climatic gradients as congruent drivers of phylogeographic diversity.Location: Maputoland-Pondoland-Albany biodiversity hotspot, Southern Africa. Taxon: herpetofauna (reptiles and amphibians).Methods: Phylogeographic structure and divergence-times within species were estimated from mitochondrial and nuclear DNA sequence data. Phylogeographic concordance factors were used to estimate the degree of phylogeographic congruence among sympatric localities. Full-likelihood Bayesian comparisons were used to estimate synchronous divergence between phylogeographic regions and across a putative river barrier. Palaeoclimatic niche models were compared among taxa to identify congruent climatic refugia. Nonparametric statistics were used to identify climatic differences between regions and among populations within each species. Finally, redundancy analyses were used to assess geographic distance, climate and the putative river barrier as explanatory variables to genetic diversity. Results: There is comprehensive phylogeographic structuring within each species, comprising distinct northerly and southerly clades. Phylogeographic concordance factors generally support co-diversification in a north/south axis. Yet, analyses of the divergence-time estimates through the Mio/Plio/Pleistocene indicate asynchronous phylogeographic histories. Climatic niche models identified idiosyncratic responses to palaeoclimatic change. Climatic variables are significantly different among populations in all species and correlated with latitude. A combined model of distance, climate and rivers explained the greatest proportion of genetical diversity in most taxa, of which climate explained the highest variance. Main Conclusions: Ancient and recent species-specific responses to climatic and geological processes resulted in pseudo congruent phylogeographic histories among the five co-distributed species. The presence of a congruent north/south pattern in multiple taxonomic groups occupying different forested microhabitats, from fossorial to arboreal, supports latitudinal gradients as global drivers of phylogeographic diversity along the east coast of South Africa.

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“…There have since been other simulations purporting to show that NCPA has a high false positive rate, with the most recent being Panchal and Beaumont (2010). All of these are based on serious misrepresentations of NCPA, and when these misrepresentations are corrected, the type I error rate is at or below the pre-set level of 0.05 (Templeton, 2009, 2015, Allen et al, 2021. Finally, NCPA does not require a prior phylogeographic model, but rather phylogeographic inferences are built up directly from the data by retaining only statistically significant inferences.…”

Section: Phylogenetic Analysismentioning

confidence: 99%

“…Both Darwin and Wallace recognized the role of rivers in dividing populations and isolating them for periods of time sufficient to accumulate morphological differences between the populations they separate (Wallace, 1849;Darwin, 1872). Studies in many taxa, including frogs, birds, rodents, and primates, have elaborated on the river barrier hypothesis (Sick, 1967;Capparella, 1988;Ayres and Cluttonbrock, 1992;Patton et al, 1994;Lougheed et al, 1999;Aleixo, 2004;Nicolas et al, 2011Nicolas et al, , 2019Voelker et al, 2013;Kopuchian et al, 2020;Allen et al, 2021;de Fraga and Carvalho, 2021). In general, river size (width, flow-rate, discharge) is expected to positively correlate with indices of differentiation between populations separated by rivers.…”

Section: Introductionmentioning

confidence: 99%

Population genetics of the naked mole-rat Heterocephalus glaber: The role of rivers in shaping genetic structure

et al. 2022

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We used nested clade phylogeographic analysis (NCPA) of mitochondrial DNA sequence data to examine the processes contributing to population structure in naked mole-rats. We examined sequence variation in the (1097 bp) control region D-loop of the mitochondrial genome in 303 individuals from 174 colonies of naked mole-rats (Heterocephalus glaber) located mainly within an 870 km2 area in Meru National Park, Kenya. Four rivers were found to be correlated to a significant fragmentation inference in the NCPA. The largest pairwise divergence between haplotypes from populations separated by rivers was 2.74%, which was well over half of the divergence reported between the extremes of the distribution from southern Ethiopia to southern Kenya (4.6%). However, the size of the river (measured in current discharge) was not a good predictor of the amount of sequence divergence between populations separated by a river. It appears that a large-scale historical fragmentation event may have conflated fragmentation patterns on a smaller scale, when recent colonization and range expansion brought two old lineages together at a location with a relatively small river separating them.

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Rivers, not refugia, drove diversification in arboreal, sub-Saharan African snakes

Abstract: This is an open access article under the terms of the Creative Commons Attribution License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.

Cited by 3 publications

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

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

Pseudocongruent phylogeography reflects unique responses to environmental perturbations in a biodiversity hotspot

Population genetics of the naked mole-rat Heterocephalus glaber: The role of rivers in shaping genetic structure

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