Abstract
Understanding how incipient species are maintained with gene flow is a fundamental question in evolutionary biology. Whole genome sequencing of multiple individuals holds great potential to illustrate patterns of genomic differentiation as well as the associated evolutionary histories. Kentish (Charadrius alexandrinus) and the white-faced (C. dealbatus) plovers, which differ in their phenotype, ecology and behavior, are two incipient species and parapatrically distributed in East Asia. Previous studies show evidence of genetic diversification with gene flow between the two plovers. Under this scenario, it is of great importance to explore the patterns of divergence at the genomic level and to determine whether specific regions are involved in reproductive isolation and local adaptation. Here we present the first population genomic analysis of the two incipient species based on the de novo Kentish plover reference genome and resequenced populations. We show that the two plover lineages are distinct in both nuclear and mitochondrial genomes. Using model-based coalescence analysis, we found that population sizes of Kentish plover increased whereas white-faced plovers declined during the Last Glaciation Period. Moreover, the two plovers diverged allopatrically, with gene flow occurring after secondary contact. This has resulted in low levels of genome-wide differentiation, although we found evidence of a few highly differentiated genomic regions in both the autosomes and the Z-chromosome. This study illustrates that incipient shorebird species with gene flow after secondary contact can exhibit discrete divergence at specific genomic regions and provides basis to further exploration on the genetic basis of relevant phenotypic traits.
Highlights
Understanding the conditions in which speciation occurs is a fundamental question in evolutionary biology
All the bird captures and sampling were performed with permission from the respective authorities (Beijing Normal University to PQ and Sun Yat-sen University to YL) and blood and tissue collection procedures conform to the regulations of the animal experimental and medical ethics committee of Sun Yat-sen University
With ABC simulations, we found that the genome-wide polymorphism patterns in KP and WFP fit best with the secondary contact model, suggesting that the two plover species experienced gene flow after secondary contact
Summary
Understanding the conditions in which speciation occurs is a fundamental question in evolutionary biology. Of equal importance is the understanding of how newly diverged species (incipient species) are maintained, as it is likely that interspecific gene flow is a common occurrence between diverging species (Payseur and Rieseberg, 2016). A physical barrier acts to prevent gene flow across the whole genome (Via, 2012) and pre- and post-zygotic mechanisms of reproductive isolation can evolve to facilitate divergence. Even infrequent gene flow can erode species barriers (Lindtke and Buerkle, 2015). In the more contentious geographical context, such as parapatric or sympatric speciation (Bird et al, 2012; Bolnick and Fitzpatrick, 2007), disentangling the relative role of gene flow and other diverging conditions and forces remains challenging (Shaner et al, 2015; Wang et al, 2017)
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