Speciation in the Deep Sea: Multi-Locus Analysis of Divergence and Gene Flow between Two Hybridizing Species of Hydrothermal Vent Mussels

Baptiste Faure,François Bonhomme,Nicolas Bierne,Didier Jollivet,Arnaud Tanguy,Craig R Mcclain

doi:10.1371/journal.pone.0006485

Abstract

BackgroundReconstructing the history of divergence and gene flow between closely-related organisms has long been a difficult task of evolutionary genetics. Recently, new approaches based on the coalescence theory have been developed to test the existence of gene flow during the process of divergence. The deep sea is a motivating place to apply these new approaches. Differentiation by adaptation can be driven by the heterogeneity of the hydrothermal environment while populations should not have been strongly perturbed by climatic oscillations, the main cause of geographic isolation at the surface.Methodology/Principal FindingSamples of DNA sequences were obtained for seven nuclear loci and a mitochondrial locus in order to conduct a multi-locus analysis of divergence and gene flow between two closely related and hybridizing species of hydrothermal vent mussels, Bathymodiolus azoricus and B. puteoserpentis. The analysis revealed that (i) the two species have started to diverge approximately 0.760 million years ago, (ii) the B. azoricus population size was 2 to 5 time greater than the B. puteoserpentis and the ancestral population and (iii) gene flow between the two species occurred over the complete species range and was mainly asymmetric, at least for the chromosomal regions studied.Conclusions/SignificanceA long history of gene flow has been detected between the two Bathymodiolus species. However, it proved very difficult to conclusively distinguish secondary introgression from ongoing parapatric differentiation. As powerful as coalescence approaches could be, we are left by the fact that natural populations often deviates from standard assumptions of the underlying model. A more direct observation of the history of recombination at one of the seven loci studied suggests an initial period of allopatric differentiation during which recombination was blocked between lineages. Even in the deep sea, geographic isolation may well be a crucial promoter of speciation.

Highlights

Reconstructing the history of divergence and gene flow between closely-related organisms is a difficult task of evolutionary genetics that has recently received much attention [1]
Secondary introgression can be difficult to separate from ongoing primary differentiation with gene flow, because the high stochasticity of the coalescence process often leads to a full range of situations, from reciprocal monophyly to extensive allele sharing [6]
Genetic variation To avoid a sampling bias in estimates and tests that assume random sampling, we used one multiple captured allele per individual, this allele being the most frequently captured in our mark-recapture cloning procedure [27]

Summary

Introduction

Reconstructing the history of divergence and gene flow between closely-related organisms is a difficult task of evolutionary genetics that has recently received much attention [1]. The analysis of DNA sequence polymorphism at multiple loci associated with new statistical coalescence-based inferences provides an elegant approach to test for the existence of gene flow during the divergence process [2] This approach has been applied to a number of closely related species [3], [4]. Secondary introgression can be difficult to separate from ongoing primary differentiation with gene flow (i.e. parapatry), because the high stochasticity of the coalescence process often leads to a full range of situations, from reciprocal monophyly to extensive allele sharing [6]. Differentiation by adaptation can be driven by the heterogeneity of the hydrothermal environment while populations should not have been strongly perturbed by climatic oscillations, the main cause of geographic isolation at the surface

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