Shedding light on the grey zone of speciation along a continuum of genomic divergence

C. Roux, C. Fraisse, J. Romiguier, Y. Anciaux, N. Galtier, N. Bierne, PLoS Biology 14 (2016).

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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.
Publishing Year
Date Published
2016-12-27
Journal Title
PLoS Biology
Acknowledgement
European Research Council (ERC) https://erc.europa.eu/ (grant number ERC grant 232971). PopPhyl project. The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. French National Research Agency (ANR) http://www.agence-nationale-recherche.fr/en/project-based-funding-to-advance-french-research/ (grant number ANR-12-BSV7- 0011). HYSEA project. We thank Aude Darracq, Vincent Castric, Pierre-Alexandre Gagnaire, Xavier Vekemans, and John Welch for insightful discussions. The computations were performed at the Vital-IT (http://www.vital-it.ch) Center for high-performance computing of the SIB Swiss Institute of Bioinformatics and the ISEM computing cluster at the platform Montpellier Bioinformatique et Biodiversité.
Volume
14
Issue
12
Article Number
e2000234
IST-REx-ID

Cite this

Roux C, Fraisse C, Romiguier J, Anciaux Y, Galtier N, Bierne N. Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biology. 2016;14(12). doi:10.1371/journal.pbio.2000234
Roux, C., Fraisse, C., Romiguier, J., Anciaux, Y., Galtier, N., & Bierne, N. (2016). Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biology, 14(12). https://doi.org/10.1371/journal.pbio.2000234
Roux, Camille, Christelle Fraisse, Jonathan Romiguier, Youann Anciaux, Nicolas Galtier, and Nicolas Bierne. “Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence.” PLoS Biology 14, no. 12 (2016). https://doi.org/10.1371/journal.pbio.2000234.
C. Roux, C. Fraisse, J. Romiguier, Y. Anciaux, N. Galtier, and N. Bierne, “Shedding light on the grey zone of speciation along a continuum of genomic divergence,” PLoS Biology, vol. 14, no. 12, 2016.
Roux C, Fraisse C, Romiguier J, Anciaux Y, Galtier N, Bierne N. 2016. Shedding light on the grey zone of speciation along a continuum of genomic divergence. PLoS Biology. 14(12).
Roux, Camille, et al. “Shedding Light on the Grey Zone of Speciation along a Continuum of Genomic Divergence.” PLoS Biology, vol. 14, no. 12, e2000234, Public Library of Science, 2016, doi:10.1371/journal.pbio.2000234.
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