Parallel Diversification of the African Tree Toad Genus Nectophryne (Bufonidae)

Molecular Phylogenetics and Evolution 162 (2021) 107184 Contents lists available at ScienceDirect Molecular Phylogenetics and Evolution journal homepage: www.elsevier.com/locate/ympev Parallel diversification of the African tree toad genus Nectophryne (Bufonidae) H. Christoph Liedtke a,*, Diego J. Soler-Navarro a, Ivan Gomez-Mestre a, Simon P. Loader b, Mark-Oliver Rodel¨ c a Ecology, Evolution and Development Group, Department of Wetland Ecology, Estacion´ Biologica´ de Donana~ (CSIC), 41092 Sevilla, Spain b Life Sciences Department, Natural History Museum, London SW7 5BD, UK c Museum für Naturkunde – Leibniz Institute for Evolution and Biodiversity Science, Biodiversity Dynamics, Invalidenstr. 43, Berlin 10115, Germany ARTICLE INFO ABSTRACT Keywords: African amphibian diversity remains underestimated with many cryptic lineages awaiting formal description. An Central Africa important hotspot of amphibian diversification is the Guineo-Congolian rainforest in Central Africa, its richness Amphibia attributable to present day and ancestral range fragmentation through geological barriers, habitat expansion and Diversity hotspot contraction, and the presence of steep ecological gradients. The charismatic Nectophryne tree toads present an Phylogeography interesting case study for diversificationin this region. The two formally described species comprising this genus Lower Guinea forests Guineo-Congolian forest show nearly identical geographic distributions extending across most of the Guineo-Congolian rainforest, but Sympatry show little morphological disparity. Both species harbour extensive genetic diversity warranting taxonomic re Character displacement visions, and interestingly, when comparing the subclades within each, the two species show remarkably parallel diversification histories, both in terms of timing of phylogenetic splits and their geographic distributions. This indicates that common processes may have shaped the evolutionary history of these lineages. 1. Introduction for physical barriers. Evidence for these have been found in numerous taxa. For example, the Sanaga River in southern Cameroon in particular, The Guineo-Congolian rainforest constitutes the second largest but also the Dja, Ogooué and Mbini rivers (Fig. 1) have been implicated contiguous area of lowland tropical moist broadleaf forests after the as barriers to gene flowin primates (Anthony et al., 2007; Mitchell et al., Amazonian rainforest (Bele et al., 2015), and boasts an exceptional 2015), reptiles (Kindler et al., 2016), bats (Hassanin et al., 2015), birds species richness and endemism (Myers et al., 2000; Plana, 2004; White, (Huntley and Voelker, 2016) and amphibians (Jongsma et al., 2017; 1979). Amphibians are no exception and the region has some of the Leache´ et al., 2019). Centres of ancient forest refugia (Plana, 2004; highest diversity on all of continental Africa (Jenkins et al., 2013). The Fig. 1) and Pleistocene climate stability correlate with the diversification true diversity likely remains underestimated, with broad scale phylo patterns of forest dependent amphibian species (Bell et al., 2017; Charles genetic and biogeographic studies in recent years highlighting the need et al., 2018; Leaché et al., 2019; Portik et al., 2017). A north–south for systematic and taxonomic revisions of major groups of African am seasonal inversion, often referred to as a ‘climatic hinge’ along the phibians (Jongsma et al., 2017; Leaché et al., 2019; Liedtke et al., 2016; southern border of Cameroon as well as a coastal-inland climatic Portik et al., 2017). gradient, seems to have contributed to species diversification in rain The extraordinary species diversity in the Guineo-Congolian region forest trees (Hardy et al., 2013), primates (Mitchell et al., 2015), reptiles has most frequently been attributed to three biogeographic processes: (Freedman et al., 2010) and amphibians (Bell et al., 2017; Jongsma vicariance by rivers acting as either past or present barriers to gene flow, et al., 2017; Leaché et al., 2019). vicariance by repeated habitat fragmentation and contraction, espe For amphibians, these processes have contributed to the diversity of cially of tropical forests, throughout the Oligocene – Miocene right up to representatives of Arthroleptidae (Portik et al., 2017), Hyperoliidae the Pleistocene, and dispersal across pronounced ecological gradients (Bell et al., 2017; Charles et al., 2018), Ranidae (Jongsma et al., 2017) followed by local adaptation, resulting in divergence without the need and Rhacophoridae (Leache´ et al., 2019), but not all species share the * Corresponding author. E-mail address: [email protected] (H.C. Liedtke). https://doi.org/10.1016/j.ympev.2021.107184 Received 25 June 2020; Received in revised form 14 April 2021; Accepted 26 April 2021 Available online 29 April 2021 1055-7903/© 2021 The Authors. Published by Elsevier Inc. This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/). H.C. Liedtke et al. Molecular Phylogenetics and Evolution 162 (2021) 107184 same degree of sensitivity to the different processes. This idiosyncrasy 1981; Laurent, 1950; Tihen, 1960), form a monophyletic clade that appears to rest, at least in part, on the ecology of species. For example represents an evolutionarily independent lineage to all other African savanna specialized reed frogs (Hyperolius spp.) experienced different bufonids (Liedtke et al., 2016). This represents a third amphibian diversification history to closely related forest specialists (Bell et al., example of a relatively recent Afro-Asian exchange, in addition to Chi 2017), and in turn, both types of reed frogs are less restricted by rivers as romantis and Amnirana (Leaché et al., 2019). This clade of toads are all barriers than is the African foam-nest frog Chiromantis rufescens (Leaché habitat specialists, many restricted to forests and Liedtke et al. (2017) et al., 2019) and the Gabon forest frog Scotobleps gabonicus (Portik et al., places their divergence from Asian lineages at the early Miocene which 2017). To gain a complete picture of the drivers of diversification of coincides with global expansion of forests and the physical connection of amphibians in this region therefore relies on investigating patterns in Africa and Eurasia through the Arabian Peninsula (Lonnberg,¨ 1929). phylogenetically and ecologically diverse taxa. Currently, there are two formally recognized species in the genus Nectophryne are small, arboreal forest toads (Amphibia: Bufonidae) Nectophryne: N. afra Buchholz and Peters, 1875 and N. batesii Boulenger, found across Central Africa and represent a phylogenetically and 1913 (Barbour, 1938; Frost, 2018). However, recent molecular work ecologically distinct taxon to the above listed amphibians. Species of this suggests cryptic genetic diversity in both taxa (Deichmann et al., 2017; genus are largely restricted to lowland forest and forest edges (Laurent, Liedtke et al., 2016). The two species show sympatric, essentially 1972) and have unique morphological adaptations to an arboreal life entirely overlapping distributions (IUCN, 2019; Laurent, 1972; Nobel, style. This includes digits heavily beset with lamellae comparable to 1924), an unexpected biogeographic pattern for sister species with those of geckos (Boulenger, 1900), and a specialized reproductive mode. apparently little morphological, behavioural or niche segregations. In Nectophryne lay relatively few, large eggs in water-filled tree cavities fact, species identification based on morphology alone is difficult and (Channing and Rodel,¨ 2019; Liedtke et al., 2014) and at least one species there are few definitive diagnostic features differentiating the two. The provides post-hatching parental care (Scheel, 1970), which is a rare original description of N. batesii diagnosed that “the snout of N. batesii, evolutionary occurrence in amphibians (Furness and Capellini, 2019; sp. n., [that] is shorter than that of N. afra, and, seen from below, pro Schulte et al., 2020; Vagi´ et al., 2019). Nectophryne, together with the jects far less considerably beyond the mouth; seen in profile, it is much genera Wolterstorffina,Werneria and in all likelihood the data deficient, less obliquely truncate” (Boulenger, 1913). Laurent (1987) found that in monotypic Laurentophryne parkeri (Blackburn et al., 2017; Grandison, addition to snout shape differences, N. batesii appears to have longer Fig. 1. Geographic distribution and sampling effort of Nectophryne afra (above) and N. batesii (below). Maps show IUCN Red List predicted species ranges, morphological and genetic sampling of current study and the known or suspected (“?”) type localities. Political borders, major rivers, current forest extent and past forest refugia (sensu Plana, 2004) are also shown. (For interpretation of the references to colour in this figure legend, the reader is referred to the web version of this article.) 2 H.C. Liedtke et al. Molecular Phylogenetics and Evolution 162 (2021) 107184 extremities, and he found that there may be sexual dimorphism in (accession numbers: MT721160-MT721174, MT724570-MT724593, forearm width as well as geographic variation in thigh width when MT733062-MT733084, SI1). comparing N. batesii from western and eastern populations. The gene dataset was supplemented with sequences from GenBank, This study aims to shed light on the evolutionary history of the including COI sequences where available. The complete dataset con charismatic genus of

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