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

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.

North-Western Palaearctic species of Pristiphora (Hymenoptera, Tenthredinidae)

“…About 21% of the species (out of 47 where it was possible to give an assessment) appear not to be clearly identifiable based on nuclear data, but morphological separation of most of these ten or so species is also problematic (P. glauca and P. wesmaeli, ruficornis subgroup, armata subgroup, P. staudingeri and P. luteipes). Roux et al (2016) found in a recent study based on genome-scale data for 61 animal species/population pairs, that an intermediate "grey zone" of speciation exists. This zone, where taxonomy is often controversial, spanned from 0.5% to 2% of net synonymous divergence.…”

“…excluding within population diversity). Among the 61 species/population pairs that Roux et al (2016) studied, gene flow between populations was always found to be prevalent when net synonymous divergence was below 0.5% and always absent when net synonymous divergence exceeded 2%. In the intermediate zone (net synonymous divergence 0.5%-2.0%), all degrees of reproductive isolation, from complete to none at all, were found (Roux et al 2016).…”

Coadapted genomes and selection on hybrids: Fisher's geometric model explains a variety of empirical patterns

“…These species fall at the high end of the continuum of divergence during which introgression persists among incipient species (Roux et al. 2016). We used experimentally bred F2 and BC1, with selection imposed implicitly, by the method of fertilization, and by our genotyping only individuals who survived to reproductive age (Bierne et al.…”

A genomic perspective timely needed for re-evaluating the species delimitations, evolutionary trajectories, and conservation strategies of the Galapagos giant tortoises

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Genome-wide data obtained from even a small number of individuals can provide unprecedented levels of detail about the evolutionary history of populations and species [1], determinants of genetic diversity [2], species boundaries and the process of speciation itself [3]. Loire and Galtier [4] present a clear example, using the emblematic Galápagos giant tortoise (Chelonoidis nigra), of how multi-species comparative population genomic approaches can provide valuable insights about population structure and species delimitation even when sample sizes are limited but the number of loci is large and distributed across the genome.

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