Terrestrial reproduction as an adaptation to steep terrain in African toads

Abstract

How evolutionary novelties evolve is a major question in evolutionary biology. It is widely accepted that changes in environmental conditions shift the position of selective optima, and advancements in phylogenetic comparative approaches allow the rigorous testing of such correlated transitions. A longstanding question in vertebrate biology has been the evolution of terrestrial life histories in amphibians and here, by investigating African bufonids, we test whether terrestrial modes of reproduction have evolved as adaptations to particular abiotic habitat parameters. We reconstruct and date the most complete species-level molecular phylogeny and estimate ancestral states for reproductive modes. By correlating continuous habitat measurements from remote sensing data and locality records with life-history transitions, we discover that terrestrial modes of reproduction, including viviparity evolved multiple times in this group, most often directly from fully aquatic modes. Terrestrial modes of reproduction are strongly correlated with steep terrain and low availability of accumulated water sources. Evolutionary transitions to terrestrial modes of reproduction occurred synchronously with or after transitions in habitat, and we, therefore, interpret terrestrial breeding as an adaptation to these abiotic conditions, rather than an exaptation that facilitated the colonization of montane habitats.

Global patterns of terrestriality in amphibian reproduction

“…These data suggest that the occurrence of terrestrial species is associated with high humidity in tropical and subtropical areas and is constrained by lower temperatures. Also, an association between terrestrial breeding habits and humid, montane environments has been proposed for a long time (Alcala, 1962;Goin & Goin, 1962) and is supported by local and regional evidence (Jimenez-Robles, Guayasamin, Ron, & Riva, 2017;Liedtke et al, 2017). The mechanism behind this pattern is related to high humidity provided by forest cover and mostly by the scarcity of suitable water bodies in the steep-terrain landscape, where water fails to accumulate in still water bodies and runs as fast-flowing streams (Liedtke et al, 2017;Muller et al, 2013).…”

“…World‐wide, amphibian diversity depends greatly on water availability (Buckley & Jetz, ), and we demonstrated that this assumption is valid for both terrestrial and aquatic breeding species. However, although aquatic breeding species depend more on rainfall patterns and availability of aquatic environments (lotic and lentic), the diversity of terrestrial species depends greatly on steeper terrains, which are related to altitude, milder temperatures and higher relative air humidity (Alcala, ; Liedtke et al, ). These differences not only impact amphibian ecology but also have practical consequences for conservation.…”

A new earless species of Poyntonophrynus (Anura, Bufonidae) from the Serra da Neve Inselberg, Namibe Province, Angola

“… Van Bocxlaer et al (2010) first confirmed the long-suspected close phylogenetic relationship between the species recognized by Frost et al (2006) as Mertensophryne and Poyntonophrynus . This result was expanded upon recently by Liedtke et al (2017) who included new data for seven of the ten species included by Frost et al (2006) in Poyntonophrynus .…”

“…Sequence assembly was performed using BioEdit 7.0.5.3 ( Hall 1999 ), and new sequences were deposited in GenBank (Table 1 ). The new sequences were then integrated into a data set consisting of all Poyntonophrynus , Mertensophryne , and Capensibufo sequences used in Liedtke et al (2017) , which include 16S and RAG-1, but also sequences of 12S, CO1, ND2, and CXCR4 (Table 1 ). All previously sequenced species of Poyntonophrynus and Mertensophryne were included in that particular data set.…”

“…There are currently ten recognized species in the genus Poyntonophrynus , all of which are small terrestrial toads with inconspicuous parotoid glands and lacking a tarsal fold. One East African species, however, Poyntonophrynus lughensis (Loveridge, 1932), was recently demonstrated to be more closely related to Mertensophryne ( Liedtke et al 2017 ). The remaining nine species are found in sub-Saharan Africa, with most of the diversity concentrated in Angola and Namibia.…”