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

Roger S Thorpe,Helena Johansson,Yann Surget-Groba,Bruce Walsh

doi:10.1371/journal.pgen.1000929

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.

Highlights

Speciation generates biodiversity and is a key process in evolution and ecology, and the relative importance of factors contributing to speciation in sexually reproducing animals, such as genetic drift in spatial isolation, natural selection, sexual selection and mutation-order, remains an active area of research [1,2,3,4,5,6,7,8]
Over the last 150 years, since Darwin’s study of islands and his ‘‘Origin of Species,’’ island archipelagos have played a central role in the understanding of evolution and how species multiply
Islands epitomise the conventional view of geographic speciation, where genomes diverge in isolation until accumulated differences result in reproductive isolation and the capacity to coexist without interbreeding

Summary

Introduction

Speciation generates biodiversity and is a key process in evolution and ecology, and the relative importance of factors contributing to speciation in sexually reproducing animals, such as genetic drift in spatial isolation, natural selection, sexual selection and mutation-order, remains an active area of research [1,2,3,4,5,6,7,8]. While there has been growing paradigm shift towards models [10] and processes such as ecological speciation [1,5,7,8] that are not dependent on allopatry, there have been few critical tests of allopatric speciation in systems which are regarded as exemplifying the process, such as island archipelagos [9,11,12,13,14,15,16,17] This is primarily because, from a contemporary perspective, genetic isolation cannot be assessed in spatially isolated populations. The island ages, molecular clock and geographic distribution of the lineages link closely to suggest that the precursor islands of Martinique (together with Barbados) had separate anole allospecies for up to about 8mybp, before central uplifting joined the Martinique precursors to form a single island (with Barbados remaining independent) [21]

Author Summary

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Methods