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

Kaitlin E Allen,Walter P Tapondjou N,A Townsend Peterson,Eli Greenbaum,Mark-Oliver Rödel,Johannes Penner,Rafe M Brown,Paul M Hime,Chifundera Kusamba,Viktoria V Sterkhova

doi:10.1002/ece3.7429

Abstract

The relative roles of rivers versus refugia in shaping the high levels of species diversity in tropical rainforests have been widely debated for decades. Only recently has it become possible to take an integrative approach to test predictions derived from these hypotheses using genomic sequencing and paleo‐species distribution modeling. Herein, we tested the predictions of the classic river, refuge, and river‐refuge hypotheses on diversification in the arboreal sub‐Saharan African snake genus Toxicodryas. We used dated phylogeographic inferences, population clustering analyses, demographic model selection, and paleo‐distribution modeling to conduct a phylogenomic and historical demographic analysis of this genus. Our results revealed significant population genetic structure within both Toxicodryas species, corresponding geographically to river barriers and divergence times from the mid‐Miocene to Pliocene. Our demographic analyses supported the interpretation that rivers are indications of strong barriers to gene flow among populations since their divergence. Additionally, we found no support for a major contraction of suitable habitat during the last glacial maximum, allowing us to reject both the refuge and river‐refuge hypotheses in favor of the river‐barrier hypothesis. Based on conservative interpretations of our species delimitation analyses with the Sanger and ddRAD data sets, two new cryptic species are identified from east‐central Africa. This study highlights the complexity of diversification dynamics in the African tropics and the advantages of integrative approaches to studying speciation in tropical regions.

Highlights

Three major allopatric diversification mechanisms have been proposed in the classical literature to explain species diversity in the tropics
The “river hypothesis” in which species and populations diverged across riverine barriers (Ayres & Clutton-Brock, 1992; Bates, 1863; Hershkovitz, 1977; Mayr, 1942; Sick, 1967; Wallace, 1853); the “refuge hypothesis” in which forests fragmented during the cold, dry Pleistocene glaciation cycles, causing isolation and divergence in small forest patches (Haffer, 1969, 1974, 1982; Prance, 1982; Vanzolini, 1973; Vanzolini & Williams, 1970); and an amalgamate “river-refuge hypothesis,” in which speciation was promoted by a combination of river barriers and climate-driven vegetation changes (Ayres & Clutton-Brock, 1992; Haffer, 1992, 1993)
The complexity of geographic barriers in West and Central Africa, and the association of refugia with areas of high surface relief or riparian zones (Hofer et al, 1999, 2000; Figure 1), makes it extremely difficult to untangle the relative importance of different diversification mechanisms with distribution data alone (Leaché et al, 2019; Portik et al, 2017)

Summary

Introduction

Three major allopatric diversification mechanisms have been proposed in the classical literature to explain species diversity in the tropics. Based on pollen core records (Bonnefille & Riollet, 1988; Brenac, 1988; Girese et al, 1994; Maley, 1987, 1989, 1991; Maley & Brénac, 1987; Maley & Livingstone, 1983; Sowunmi, 1991) and species distribution data (Colyn, 1987, 1991; Richards, 1963; Rietkerk et al, 1995; Sosef, 1991), Maley (1996) proposed several Pleistocene rainforest refugia for sub-Saharan Africa that are still considered today (e.g., Bell et al, 2017; Hughes et al, 2017; Huntley et al, 2019; Jongsma et al, 2018; Larson et al, 2016; Penner et al, 2011; Portik et al, 2017; Figure 1) Many of these hypothesized refugia are located in highland areas (e.g., the Cameroon Volcanic Line and the Albertine Rift; Figure 1, refugia 4 and 10, respectively). A major fluvial refuge, that is, a refugium associated with a river, located in the gallery forests around the Congo River (Figure 1, refugium 9), has been supported by pollen core data (Maley, 1996), and distributional patterns of multiple bird (Huntley et al, 2018; Levinsky et al, 2013), mammal (Colyn et al, 1991; Levinsky et al, 2013), and plant taxa (Robbrecht, 1996)

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Discussion

Conclusion