Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence.

Camille Roux,Nicolas Bierne,Christelle Fraïsse,Jonathan Romiguier,Nicolas Galtier,Yoann Anciaux,Craig Moritz

doi:10.1371/journal.pbio.2000234

Abstract

Speciation results from the progressive accumulation of mutations that decrease the probability of mating between parental populations or reduce the fitness of hybrids—the so-called species barriers. The speciation genomic literature, however, is mainly a collection of case studies, each with its own approach and specificities, such that a global view of the gradual process of evolution from one to two species is currently lacking. Of primary importance is the prevalence of gene flow between diverging entities, which is central in most species concepts and has been widely discussed in recent years. Here, we explore the continuum of speciation thanks to a comparative analysis of genomic data from 61 pairs of populations/species of animals with variable levels of divergence. Gene flow between diverging gene pools is assessed under an approximate Bayesian computation (ABC) framework. We show that the intermediate "grey zone" of speciation, in which taxonomy is often controversial, spans from 0.5% to 2% of net synonymous divergence, irrespective of species life history traits or ecology. Thanks to appropriate modeling of among-locus variation in genetic drift and introgression rate, we clarify the status of the majority of ambiguous cases and uncover a number of cryptic species. Our analysis also reveals the high incidence in animals of semi-isolated species (when some but not all loci are affected by barriers to gene flow) and highlights the intrinsic difficulty, both statistical and conceptual, of delineating species in the grey zone of speciation.

Highlights

An important issue in evolutionary biology is understanding how the continuous-time process of speciation can lead to discrete entities—species
Speciation proceeds by the accumulation at specific loci of mutations that reduce the fitness of hybrids, preventing gene flow—the so-called species barriers
Heterogeneous effective population size was considered in all the models, while heterogeneous migration rate was considered in models with gene flow (IM, ancient migration (AM), and secondary contact (SC))

Summary

Introduction

An important issue in evolutionary biology is understanding how the continuous-time process of speciation can lead to discrete entities—species. There is usually no ambiguity about species delineation when distant lineages are compared. The continuous nature of the divergence process, causes endless debates about the species status of closely related lineages [1]. A major problem is that distinct markers do not diverge in time at the same rate [2]. Morphology is almost unchanged between lineages that show high levels of molecular divergence [4]. The erratic behavior and evolution of the various criteria is such that in a wide range of between-lineage divergence—named the grey zone of the speciation continuum—distinct species concepts do not converge to the same conclusions regarding species delineation [2]

Methods

Results

Discussion

Conclusion