Genetic Tests for Ecological and Allopatric Speciation in Anoles on an Island Archipelago

Abstract

From Darwin's study of the Galapagos and Wallace's study of Indonesia, islands have played an important role in evolutionary investigations, and radiations within archipelagos are readily interpreted as supporting the conventional view of allopatric speciation. Even during the ongoing paradigm shift towards other modes of speciation, island radiations, such as the Lesser Antillean anoles, are thought to exemplify this process. Geological and molecular phylogenetic evidence show that, in this archipelago, Martinique anoles provide several examples of secondary contact of island species. Four precursor island species, with up to 8 mybp divergence, met when their islands coalesced to form the current island of Martinique. Moreover, adjacent anole populations also show marked adaptation to distinct habitat zonation, allowing both allopatric and ecological speciation to be tested in this system. We take advantage of this opportunity of replicated island coalescence and independent ecological adaptation to carry out an extensive population genetic study of hypervariable neutral nuclear markers to show that even after these very substantial periods of spatial isolation these putative allospecies show less reproductive isolation than conspecific populations in adjacent habitats in all three cases of subsequent island coalescence. The degree of genetic interchange shows that while there is always a significant genetic signature of past allopatry, and this may be quite strong if the selection regime allows, there is no case of complete allopatric speciation, in spite of the strong primae facie case for it. Importantly there is greater genetic isolation across the xeric/rainforest ecotone than is associated with any secondary contact. This rejects the development of reproductive isolation in allopatric divergence, but supports the potential for ecological speciation, even though full speciation has not been achieved in this case. It also explains the paucity of anole species in the Lesser Antilles compared to the Greater Antilles.

A likelihood framework analysis of an island radiation: phylogeography of the Lesser Antillean geckoSphaerodactylus vincenti, in comparison with the anoleAnolis roquet

“…(). This complex history has had a profound impact on the molecular genetic diversity of another lizard, Anolis roquet , where very divergent lineages evolved in allopatry on distinct proto‐islands before coming into secondary contact once the islands coalesced (Thorpe & Stenson, ; Thorpe et al ., , ). However, with this anole and other Lesser Antillean anoles, it is generally adaptation to the environmental zonation that determines its appearance (colour and pattern) and traditional subspecies (Thorpe & Stenson, ), rather than these geo‐historical processes (Thorpe et al ., ).…”

Colonization history and genetic diversity: adaptive potential in early stage invasions

“…Quantitative traits of Anolis may vary along altitudinal gradients and correlative studies, molecular studies, parallels and field‐based natural selection experiments (Malhotra & Thorpe 1991b, 1997b; Ogden & Thorpe 2002; Thorpe et al. 2004, 2005; 2010) all indicate that this is in response to current ecological conditions rather than past processes such as genetic drift.…”

Comparative tests of the role of dewlap size in Anolis lizard speciation

“…Mainland anole species have relatively large geographical ranges [53] which may increase the opportunity for populations to become isolated in different environments that may favour different signalling traits, and potentially to come into secondary contact. Island anole speciation also likely involves adaptation to different macrohabitats [51], but if more speciation events involve dispersal between islands, then the probability of secondary contact may be reduced. The other obvious differences between island and mainland anoles are the more diverse range of predators and the lower population density of anoles on the mainland.…”