Abstract

Several studies have uncovered a highly heterogeneous landscape of genetic differentiation across the genomes of closely related species. Specifically, genetic differentiation is often concentrated in particular genomic regions (“islands of differentiation”) that might contain barrier loci contributing to reproductive isolation, whereas the rest of the genome is homogenized by introgression. Alternatively, linked selection can produce differentiation islands in allopatry without introgression. We explored the influence of introgression on the landscape of genetic differentiation in two hybridizing goose taxa: the Taiga Bean Goose (Anser fabalis) and the Tundra Bean Goose (A. serrirostris). We re-sequenced the whole genomes of 18 individuals (9 of each taxon) and, using a combination of population genomic summary statistics and demographic modeling, we reconstructed the evolutionary history of these birds. Next, we quantified the impact of introgression on the build-up and maintenance of genetic differentiation. We found evidence for a scenario of allopatric divergence (about 2.5 million years ago) followed by recent secondary contact (about 60,000 years ago). Subsequent introgression events led to high levels of gene flow, mainly from the Tundra Bean Goose into the Taiga Bean Goose. This scenario resulted in a largely undifferentiated genomic landscape (genome-wide FST = 0.033) with a few notable differentiation peaks that were scattered across chromosomes. The summary statistics indicated that some peaks might contain barrier loci while others arose in allopatry through linked selection. Finally, based on the low genetic differentiation, considerable morphological variation and incomplete reproductive isolation, we argue that the Taiga and the Tundra Bean Goose should be treated as subspecies.

Highlights

  • Genetic differentiation between species pairs is often concentrated in a few genomic regions, the so-called islands of differentiation (Wolf and Ellegren 2017). This finding led to the formulation of a verbal model in which such islands diverge over time because they contain loci involved in reproductive isolation, whereas the rest of the genome is homogenized by interspecific gene flow (Wu 2001; Turner et al 2005; Feder et al 2012)

  • We focus on two Bean Goose taxa: the Taiga Bean Goose (Anser fabalis) and the Tundra Bean Goose (A. serrirostris)

  • The principal component analysis (PCA) indicated that the Taiga and the Tundra Bean Goose can be separated using genomic data

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Summary

Introduction

Concentrated in a few genomic regions, the so-called islands of differentiation (Wolf and Ellegren 2017) This finding led to the formulation of a verbal model in which such islands diverge over time (i.e. higher absolute divergence, dXY) because they contain loci involved in reproductive isolation (and originally referred to as “genomic islands of speciation”, Turner et al 2005), whereas the rest of the genome is homogenized by interspecific gene flow (Wu 2001; Turner et al 2005; Feder et al 2012). Genomic regions with high levels of recombination are expected to experience less linked selection because recombination uncouples loci from the advantageous or deleterious variant under selection (Hudson and Kaplan 1995; Nordborg et al 1996) These processes–genetic hitchhiking and background selection— can produce islands of differentiation in allopatry in the absence of gene flow. Verifying the taxonomical position of the Taiga and Tundra Bean Goose is of utmost importance for the correct management of the taxa

Material and methods
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Compliance with ethical standards

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