Non-equilibrium estimates of gene flow inferred from nuclear genealogies suggest that Iberian and North African wall lizards (Podarcis spp.) are an assemblage of incipient species

Catarina Pinho,D James Harris,Nuno Ferrand

doi:10.1186/1471-2148-8-63

Catarina Pinho, D James Harris + Show 1 more

Open Access

https://doi.org/10.1186/1471-2148-8-63

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Abstract

BackgroundThe study of recently-diverged species offers significant challenges both in the definition of evolutionary entities and in the estimation of gene flow among them. Iberian and North African wall lizards (Podarcis) constitute a cryptic species complex for which previous assessments of mitochondrial DNA (mtDNA) and allozyme variation are concordant in describing the existence of several highly differentiated evolutionary units. However, these studies report important differences suggesting the occurrence of gene flow among forms. Here we study sequence variation in two nuclear introns, β-fibint7 and 6-Pgdint7, to further investigate overall evolutionary dynamics and test hypotheses related to species delimitation within this complex.ResultsBoth nuclear gene genealogies fail to define species as monophyletic. To discriminate between the effects of incomplete lineage sorting and gene flow in setting this pattern, we estimated migration rates among species using both FST-based estimators of gene flow, which assume migration-drift equilibrium, and a coalescent approach based on a model of divergence with gene flow. Equilibrium estimates of gene flow suggest widespread introgression between species, but coalescent estimates describe virtually zero admixture between most (but not all) species pairs. This suggests that although gene flow among forms may have occurred the main cause for species polyphyly is incomplete lineage sorting, implying that most forms have been isolated since their divergence. This observation is therefore in accordance with previous reports of strong differentiation based on mtDNA and allozyme data.ConclusionThese results corroborate most forms of Iberian and North African Podarcis as differentiated, although incipient, species, supporting a gradual view of speciation, according to which species may persist as distinct despite some permeability to genetic exchange and without having clearly definable genetic boundaries. Additionally, this study constitutes a warning against the misuse of equilibrium estimates of migration among recently-diverged groups.

Highlights

The study of recently-diverged species offers significant challenges both in the definition of evolutionary entities and in the estimation of gene flow among them
For example, attempts to reconstruct relationships among such taxa are often hampered by a poor resolution of relationships, by lack of monophyly inferred from individual gene genealogies due to incomplete lineage sorting or, when multiple loci are analysed, by discordant scenarios portrayed by distinct genealogies
There is a single common pattern emerging from the study. This situation of polyphyly in nuclear genealogies relative to mitochondrial data is not uncommon. This discordance could suggest that mitochondrial DNA-defined species of Iberian and North African Podarcis do not correspond to true evolutionary entities and that this differentiation is the result of stochastic or deterministic effects acting only on the mitochondrial genome

Summary

Introduction

The study of recently-diverged species offers significant challenges both in the definition of evolutionary entities and in the estimation of gene flow among them. Iberian and North African wall lizards (Podarcis) constitute a cryptic species complex for which previous assessments of mitochondrial DNA (mtDNA) and allozyme variation are concordant in describing the existence of several highly differentiated evolutionary units. These studies report important differences suggesting the occurrence of gene flow among forms. Closelyrelated species are likely to retain some permeability to the exchange of genes, which may affect some loci more than others [1,2] These features become even more striking when more than two species are involved; in rapidly radiating taxa the chance of incomplete lineage sorting increases and complex patterns of admixture often arise, complicating the recognition of species boundaries in the context of both biological and phylogenetic species definition criteria [3,4,5,6]. Recent analytical methods [10,11], in contrast, do not assume equilibrium and allow the analysis of gene flow and divergence in the same framework, being appropriate tools to evaluate migration rates among recently diverged taxa

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