A feedback between dispersal and hybridization may facilitate the repeated emergence of flight in field crickets

Abstract

Dispersal and hybridization can reinforce one another in a feedback loop when species that disperse farther are more likely to encounter and mate with close relatives, resulting in gene flow that can reintroduce dispersal-enhancing alleles in their descendants. This dynamic could help explain why complex dispersal-related traits, such as flight in insects, appear to evolve repeatedly within a clade, but this idea has rarely been tested with genomic data. North American Gryllus field crickets, in which flight capability appears to have been regained from flightless ancestors at least nine independent times, offer a powerful system to do so. Using a genome-wide dataset, we test three predictions about the origins of phylogenetic discordance in Gryllus and the role of dispersal-related traits. First, we find that both incomplete lineage sorting (ILS) and hybridization contribute to extensive gene tree conflict observed across the Gryllus phylogeny, but several conflicting patterns cannot be explained by ILS alone. Multiple lines of evidence reveal introgression at both deep and recent nodes, producing a mosaic evolutionary history with reticulation across many lineages. Second, hybridization is disproportionately concentrated among flight-capable lineages, supporting the idea that dispersal ability increases opportunities for interspecific gene flow. Third, introgression from flight-capable lineages could help explain repeated trait reversal across the phylogeny, suggesting that allele flow may have contributed to the re-emergence of flight in descendants of flightless ancestors. These results are consistent with a dispersal-hybridization feedback shaping both the reticulated phylogenetic history of Gryllus and the repeated emergence of flight. More broadly, models of character evolution built on bifurcating trees may overestimate the number of independent trait origins when reticulate processes are ignored.