Ancient forest fragmentation or recent radiation? Testing refugial speciation models in chameleons within an African biodiversity hotspot

Abstract

Aim East Africa is one of the most biologically diverse regions, especially in terms of endemism and species richness. Hypotheses put forward to explain this high diversity invoke a role for forest refugia through: (1) accumulation of new species due to radiation within refugial habitats, or (2) retention of older palaeoendemic species in stable refugia. We tested these alternative hypotheses using data for a diverse genus of East African forest chameleons, Kinyongia.Location East Africa.Methods We constructed a dated phylogeny for Kinyongia using one nuclear and two mitochondrial markers. We identified areas of high phylogenetic diversity (PD) and evolutionary diversity (ED), and mapped ancestral areas to ascertain whether lineage diversification could best be explained by vicariance or dispersal.Results Vicariance best explains the present biogeographic patterns, with divergence between three major Kinyongia clades (Albertine Rift, southern Eastern Arc, northern Eastern Arc) in the early Miocene/Oligocene (> 20 Ma). Lineage diversification within these clades pre-dates the Pliocene (> 6 Ma). These dates are much older than the Plio-Pleistocene climatic shifts associated with cladogenesis in other East African taxa (e.g. birds), and instead point to a scenario whereby palaeoendemics are retained in refugia, rather than more recent radiations within refugia. Estimates of PD show that diversity was highest in the Uluguru, Nguru and East Usambara Mountains and several lineages (from Mount Kenya, South Pare and the Uluguru Mountains) stand out as being evolutionarily distinct as a result of isolation in forest refugia. PD was lower than expected by chance, suggesting that the phylogenetic signal is influenced by an unusually low number of extant lineages with long branch lengths, which is probably due to the retention of palaeoendemic lineages. Main conclusionsThe biogeographic patterns associated with Kinyongia are the result of long evolutionary histories in isolation. The phylogeny is dominated by ancient lineages whose origins date back to the early Miocene/Oligocene as a result of continental wide forest fragmentation and contraction due to long term climatic changes in Africa. The maintenance of palaeoendemic lineages in refugia has contributed substantially to the remarkably high biodiversity of East Africa.

<strong>The “<em>Rhampholeon</em> <em>uluguruensis</em> complex” (Squamata: Chamaeleonidae) and the taxonomic status of the pygmy chameleons in Tanzania</strong>

“…Turner & Channing 2008;Tolley et al 2010). This is probably due to a long history of isolation in forest fragments, similar to chameleons in the genus Kinyongia (Tolley et al 2011;Mariaux et al 2008), which occur in the same forest fragments as the Rhampholeon species in our study. Despite the large genetic differentiation between the candidate species, the phenotypes are extremely similar and particularly difficult to distinguish using traditional morphological characters.…”

Large-scale phylogeny of chameleons suggests African origins and Eocene diversification

“…Aside from short episodic climatic optima (ca 15 and 24 Myr), the climate has remained comparatively cool, which has induced dry conditions, resulting in fragmentation and reduction of forests [36]. Given that most chameleon species (both terrestrial and arboreal) are closely associated with forested/wooded habitats [32], fragmentation of forests could have led to vicariance causing the species formation observed within most genera during this period. Some species that use large perches were also apparently able to make the transition from closed canopy forests to open woodlands (savannah, dry forests of Madagascar) allowing colonization of that niche as closed canopy forests diminished.…”

“…Transition out of habitats with large perches into habitats with fine structure (i.e. grassland and heathland) has only occurred for a few clades [32,34], and primarily since the Pliocene (figure 2) when these habitats became present in the African landscape [69][70][71][72].…”

“…However, relationships among the remaining chameleon genera still lack a well-supported phylogenetic hypothesis, possibly owing to a lack of extensive taxon sampling and inclusion of too few markers, or possibly because a rapid initial radiation caused a 'true' polytomy [14,15,[29][30][31]. Analyses with extensive taxon sampling are limited to single genera [30,[32][33][34][35], and these have usually recovered Oligocene/ Miocene origins for genera. This in turn suggests the possibility of a collective explanation for generic-level diversification, i.e.…”

Allometry for sexual dimorphism in millipedes (Diplopoda)

“…[74] The absence of any relationships between size and mating was documented for the tropical millipede Nyssodesmus pythos [13] . My evidence for sexual selection on dimorphism is based on the relative size dimorphism in Centrobolus which shows size is important in determining the outcome of mating [47,73,76,77] . The mechanism is based on a conflict of interests [77] .…”