Abstract

BackgroundThe impacts of hybridization on the process of speciation are manifold, leading to distinct patterns across the genome. Genetic differentiation accumulates in certain genomic regions, while divergence is hampered in other regions by homogenizing gene flow, resulting in a heterogeneous genomic landscape. A consequence of this heterogeneity is that genomes are mosaics of different gene histories that can be compared to unravel complex speciation and hybridization events. However, incomplete lineage sorting (often the outcome of rapid speciation) can result in similar patterns. New statistical techniques, such as the D-statistic and hybridization networks, can be applied to disentangle the contributions of hybridization and incomplete lineage sorting. We unravel patterns of hybridization and incomplete lineage sorting during and after the diversification of the True Geese (family Anatidae, tribe Anserini, genera Anser and Branta) using an exon-based hybridization network approach and taking advantage of discordant gene tree histories by re-sequencing all taxa of this clade. In addition, we determine the timing of introgression and reconstruct historical effective population sizes for all goose species to infer which demographic or biogeographic factors might explain the observed patterns of introgression.ResultsWe find indications for ancient interspecific gene flow during the diversification of the True Geese and were able to pinpoint several putative hybridization events. Specifically, in the genus Branta, both the ancestor of the White-cheeked Geese (Hawaiian Goose, Canada Goose, Cackling Goose and Barnacle Goose) and the ancestor of the Brent Goose hybridized with Red-breasted Goose. One hybridization network suggests a hybrid origin for the Red-breasted Goose, but this scenario seems unlikely and it not supported by the D-statistic analysis. The complex, highly reticulated evolutionary history of the genus Anser hampered the estimation of ancient hybridization events by means of hybridization networks. The reconstruction of historical effective population sizes shows that most species showed a steady increase during the Pliocene and Pleistocene. These large effective population sizes might have facilitated contact between diverging goose species, resulting in the establishment of hybrid zones and consequent gene flow.ConclusionsOur analyses suggest that the evolutionary history of the True Geese is influenced by introgressive hybridization. The approach that we have used, based on genome-wide phylogenetic incongruence and network analyses, will be a useful procedure to reconstruct the complex evolutionary histories of many naturally hybridizing species groups.

Highlights

  • The impacts of hybridization on the process of speciation are manifold, leading to distinct patterns across the genome

  • All analyses supported a scenario of gene flow during divergence with low levels of recent gene flow because the histograms all displayed one peak corresponding to the initial species split

  • Using genomic datasets and modern analysis tools, such as the D-statistic and pairwise sequentially Markovian coalescent (PSMC) analysis, in combination with network analyses based on gene tree discordance, we were able to determine patterns of introgressive hybridization in the True Geese

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Summary

Introduction

The impacts of hybridization on the process of speciation are manifold, leading to distinct patterns across the genome. A consequence of this heterogeneity is that genomes are mosaics of different gene histories that can be compared to unravel complex speciation and hybridization events. Incomplete lineage sorting (often the outcome of rapid speciation) can result in similar patterns New statistical techniques, such as the D-statistic and hybridization networks, can be applied to disentangle the contributions of hybridization and incomplete lineage sorting. Hybridization may slow down or even reverse species divergence It may accelerate speciation via adaptive introgression or contribute to species diversity through the formation of new hybrid taxa. These diverse effects occur at different spatial scales and during different stages across the speciation continuum [2]. The pattern of hybridization is only a single snapshot of a complex and continuously changing interaction

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