Whole-genome analysis of multiple wood ant population pairs supports similar speciation histories, but different degrees of gene flow, across their European range

Abstract

The application of demographic history modeling and inference to the study of divergence between species is becoming a cornerstone of speciation genomics. The demographic history is usually reconstructed by analysing a single population from each species, assuming that the divergence history inferred between these populations represents the actual speciation history. However, this assumption is rarely explicitly tested, and it may not be met when species diverge with gene flow. For instance, secondary contact between two species after a range expansion may be confined into a specific geographic region. In this study, we tested to what extent the divergence history inferred from two heterospecific populations would vary depending on their geographic locations, using mound-building red wood ants. The wood ant species Formica polyctena and F. aquilonia have contrasting distributions in Europe and naturally hybridize in Finland. We first performed whole-genome resequencing of 20 individuals sampled in multiple populations across both species ranges. We then reconstructed the divergence histories of distinct heterospecific population pairs using a coalescent-based approach. We found that the analysis of these different population pairs always supported a scenario of divergence with gene flow, suggesting that species divergence started in the Pleistocene (ca. 500 kya) and occurred with continuous asymmetrical gene flow from F. aquilonia to F. polyctena until a recent time, when migration stopped (2-19 kya, depending on the population pair considered). However, we found support for contemporary gene flow in the sympatric population pair from Finland, where hybrids have been described. Overall, our results suggest that divergence histories reconstructed from a few individuals may be reliable and applicable at the species level. Nonetheless, the geographical context of populations chosen to represent their species should be taken into account, as it may affect estimates of migration rates between species when gene flow is heterogeneous across their geographical ranges.

Rapid and predictable genome evolution across three hybrid ant populations

“…We collected unmated queens from Bunkkeri (n = 10) and Långholmen (n W = 10, n R = 9) in Spring 2018 and workers from Pikkala (n = 10) in Spring 2015 (S1 Table ). Data generated by Portinha and colleagues [40] were used as F. aquilonia and F. polyctena reference panels. Briefly, it consists of 10 workers (diploid females) per species sampled from several monospecific colonies across Europe (Fig 1A and S1 Table).…”

Rapid and repeatable genome evolution across three hybrid ant populations

“…We collected unmated queens from Bunkkeri (n = 10) and Långholmen (nW = 10, nR = 9) in Spring 2018 and workers from Pikkala (n = 10) in Spring 2015 (Table S1). Data generated by Portinha et al (8) were used as F. aquilonia and F. polyctena reference panels. Briefly, it consists of ten workers (diploid females) per species sampled from several locations across Europe (Fig.…”

“…Both the hybrid samples generated for this study and the F. aquilonia and F. polyctena samples from Portinha et al (8) were processed and sequenced at the same time, and all data went through the same pipeline. DNA was extracted with a Sodium Dodecyl Sulfate (SDS) protocol from whole bodies and sequencing libraries were built with NEBNext DNA Library Prep Kits (New England Biolabs) by Novogene (Hong Kong).…”

“…The data set used for demographic modeling hence comprises 1,537,053 SNPs. We used the composite-likelihood method implemented in FASTSIMCOAL2 (v2.6, 12) to compare alternative demographic models to demographic parameters inferred from the site frequency spectrum (SFS) following Portinha et al (8). We ran each model 100 times with 80 iterations per run for likelihood maximization and the expected SFS was approximated through 200,000 coalescent simulations per iteration.…”

“…Generation time was assumed to be 2.5 years (8). Finally, we used the best speciation history inferred by Portinha et al (8) to constrain parameter range prior to the admixture event in our demographic models.…”