Hybrid zone genomics supports candidate species in Iberian Alytes obstetricans

Christophe Dufresnes,Íñigo Martínez-Solano

doi:10.1163/15685381-20191312

Christophe Dufresnes, Íñigo Martínez-Solano

Open Access

https://doi.org/10.1163/15685381-20191312

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Abstract

Abstract While estimates of genetic divergence are increasingly used in molecular taxonomy, hybrid zone analyses can provide decisive evidence for evaluating candidate species. Applying a population genomic approach (RAD-sequencing) to a fine-scale transect sampling, we analyzed the transition between two Iberian subspecies of the common midwife toad (Alytes obstetricans almogavarii and A. o. pertinax) in Catalonia (northeastern Spain), which putatively diverged since the Plio-Pleistocene. Their hybrid zone was remarkably narrow, with extensive admixture restricted to a single locality (close to Tarragona), and congruent allele frequency clines for the mitochondrial (13 km wide) and the average nuclear genomes (16 km wide). We also fitted clines independently for 89 taxon-diagnostic SNPs: most of them behave like the nuclear background, but a subset (13%) is completely impermeable to gene flow and might be linked to barrier loci involved in hybrid incompatibilities. Assuming that midwife toads are able to disperse in the area of contact, we conclude that these taxa experience partial reproductive isolation and represent incipient species, i.e. Alytes almogavarii and Alytes obstetricans. Interestingly, their evolutionary age and mitochondrial divergence fall below the thresholds proposed in molecular systematics studies, emphasizing the difficulty of predicting the outcome of secondary contacts between young lineages entering the grey zone of speciation.

Highlights

In the wake of recent attempts to relate theThe delimitation of cryptic species by phylogeographers is inherently challenged by the continuous and dynamic nature of speciation processes (Avise, 2000; Heethoff, 2018; Struck et al, 2018; Chenuil et al, 2019)
In the era of the “molecularisation of taxonomy” (Lee, 2004), evolutionary biologists may never agree on how much reproductive isolation and genetic differentiation is required to consider diverging populations as incipient species (Coyne and Orr, 2004; De Queiroz, 2007; Padial et al, 2010)
As theoretically and empirically supported, reproductive isolation tends to increase rapidly due to the accumulation of barrier loci after a certain degree of genetic divergence, above which the probability to merge back and reverse the speciation process is considerably reduced (Barton, 1983; Orr, 1995; Gourbiere and Mallet, 2009; Singhal and Moritz, 2013)

Summary

Introduction

In the wake of recent attempts to relate theThe delimitation of cryptic species by phylogeographers is inherently challenged by the continuous and dynamic nature of speciation processes (Avise, 2000; Heethoff, 2018; Struck et al, 2018; Chenuil et al, 2019). In the era of the “molecularisation of taxonomy” (Lee, 2004), evolutionary biologists may never agree on how much reproductive isolation and genetic differentiation is required to consider diverging populations as incipient species (Coyne and Orr, 2004; De Queiroz, 2007; Padial et al, 2010). As theoretically and empirically supported, reproductive isolation tends to increase rapidly due to the accumulation of barrier loci after a certain degree of genetic divergence, above which the probability to merge back and reverse the speciation process is considerably reduced (Barton, 1983; Orr, 1995; Gourbiere and Mallet, 2009; Singhal and Moritz, 2013). If properly characterized and implemented, this checkpoint should facilitate the delimitation of incipient species.

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