Phylogenomic approach reveals strong signatures of introgression in the rapid diversification of neotropical true fruit flies (Anastrepha: Tephritidae)

Abstract

New sequencing techniques have allowed us to explore the variation on thousands of genes and elucidate evolutionary relationships of lineages even in complex scenarios, such as when there is rapid diversification. That seems to be the case of species in the genus Anastrepha, which shows great species diversity that has been divided into 21 species groups, several of which show wide geographical distribution. The fraterculus group has several economically important species and it is also an outstanding model for speciation studies, since it includes several lineages that have diverged recently possibly in the presence of interspecific gene flow. Our main goal is to test whether we can infer phylogenetic relationships of recently diverged taxa with gene flow, such as what is expected for the fraterculus group and determine whether certain genes remain informative even in this complex scenario. An analysis of thousands of orthologous genes derived from transcriptome datasets of 10 different lineages across the genus, including some of the economically most important pests, revealed signals of incomplete lineage sorting, vestiges of ancestral introgression between more distant lineages and ongoing gene flow between closely related lineages. Though these patterns affect the phylogenetic signal, the phylogenomic inferences consistently show that the morphologically identified species here investigated are in different evolutionary lineages, with the sole exception involving Brazilian lineages of A. fraterculus, which has been suggested to be a complex assembly of cryptic species. A tree space analysis suggested that genes with greater phylogenetic resolution have evolved under similar selection pressures and are more resilient to intraspecific gene flow, which would make it more likely that these genomic regions may be useful for identifying fraterculus group lineages. Our findings help establish relationships among the most important Anastrepha species groups, as well as bring further data to indicate that the diversification of fraterculus group lineages, and even other lineages in the genus Anastrepha, has been strongly influenced by interspecific gene flow.