Rapid Convergent Evolution in Wild Crickets

The earliest stages of convergent evolution are difficult to observe in the wild, limiting our understanding of the incipient genomic architecture underlying convergent phenotypes [1, 2]. To address this, we capitalized on a novel trait, flatwing, that arose and proliferated at the start of the 21stcentury in a population of field crickets (Teleogryllus oceanicus) on the Hawaiian island of Kauai [3]. Flatwing erases sound-producing structures on male forewings. Mutant males cannot sing to attract females, but they are protected from fatal attack by an acoustically orienting parasitoid fly (Ormia ochracea). Two years later, the silent morph appeared on the neighboring island of Oahu. We tested two hypotheses for the evolutionary origin of flatwings in Hawaii: (1) that the silent morph originated on Kauai and subsequently introgressed into Oahu and (2) that flatwing originated independently on each island. Morphometric analysis of male wings revealed that Kauai flatwings almost completely lack typical derived structures, whereas Oahu flatwings retain noticeably more wild-type wing venation. Using standard genetic crosses, we confirmed that the mutation segregates as a single-locus, sex-linked Mendelian trait on both islands. However, genome-wide scans using RAD-seq recovered almost completely distinct markers linked with flatwing on each island. The patterns of allelic association with flatwing on either island reveal different genomic architectures consistent with the timing of two mutational events on the X chromosome. Divergent wing morphologies linked to different loci thus cause identical behavioral outcomes - silence - illustrating the power of selection to rapidly shape convergent adaptations from distinct genomic starting points.