Abstract

Introgression should no longer be considered as rare a phenomenon as once thought, since several studies have recently documented gene flow between closely related and radiating species. Here, we investigated evolutionary relationships among three closely related species of fruit flies of the Anastrepha fraterculus group (Anastrepha fraterculus, A. obliqua and A. sororcula). We sequenced a set of 20 genes and implemented a combined populational and phylogenetic inference with a model selection approach by an ABC framework in order to elucidate the demographic history of these species. The phylogenetic histories inferred from most genes showed a great deal of discordance and substantial shared polymorphic variation. The analysis of several population and speciation models reveal that this shared variation is better explained by introgression rather than convergence by parallel mutation or incomplete lineage sorting. Our results consistently showed these species evolving under an isolation with migration model experiencing a continuous and asymmetrical pattern of gene flow involving all species pairs, even though still showed a more closely related relationship between A. fraterculus and A. sororcula when compared with A. obliqua. This suggests that these species have been exchanging genes since they split from their common ancestor ∼2.6 MYA ago. We also found strong evidence for recent population expansion that appears to be consequence of anthropic activities affecting host crops of fruit flies. These findings point that the introgression here found may have been driven by genetic drift and not necessary by selection, which has implications for tracking and managing fruit flies.

Highlights

  • IntroductionThere is increased attention on the study of evolutionary relationships among recently diverged and radiating species (Beltran et al, 2002; Buckley et al, 2006; Maddison and Knowles, 2006; Carstens and Knowles, 2007; Mallet et al, 2007; Nunes et al, 2010; Martin et al, 2013; Cruickshank and Hahn, 2014; Meyer et al, 2016), because they tend to be affected by incongruence among gene trees, as initially reviewed by Pamilo and Nei (1988) and Maddison (1997)

  • Our phylogenetic inference performed in BUCKy using the complete gene set identified A. fraterculus, A. obliqua and A. sororcula as different lineages but failed to find sublineages that would be compatible with putative cryptic species

  • Because this analysis performs a posteriori clustering of samples considering only the phylogenetic signal derived from all genes sequenced in a coalescent framework (Larget et al, 2010), the absence of sublineages in A. fraterculus is not impacted by our decision to treat A. fraterculus as sensu latu, since the program does not use a priori species information

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Summary

Introduction

There is increased attention on the study of evolutionary relationships among recently diverged and radiating species (Beltran et al, 2002; Buckley et al, 2006; Maddison and Knowles, 2006; Carstens and Knowles, 2007; Mallet et al, 2007; Nunes et al, 2010; Martin et al, 2013; Cruickshank and Hahn, 2014; Meyer et al, 2016), because they tend to be affected by incongruence among gene trees, as initially reviewed by Pamilo and Nei (1988) and Maddison (1997) This is Evidence for Introgression in Anastrepha Species often due to the stochasticity of the coalescent process, which is more likely the larger population sizes are relative to the divergence times (Pamilo and Nei, 1988), leading to incomplete lineage sorting (ILS). That may be the case of the fruit fly Rhagoletis pomonella, where it has been suggested that introgression may be playing a relevant role during its speciation (Feder et al, 1999; Xie et al, 2007; Michel et al, 2010; Arcella et al, 2015)

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