Abstract

Host-parasite interactions are predicted to drive the evolution of defences and counter-defences, but the ability of either partner to adapt depends on new and advantageous traits arising. The loss of male song in Hawaiian field crickets (Teleogryllus oceanicus) subject to fatal parasitism by eavesdropping flies (Ormia ochracea) is a textbook example of rapid evolution in one such arms race. Male crickets ordinarily sing to attract females by rubbing their forewings together, which produces sound by exciting acoustic resonating structures formed from modified wing veins (‘normal-wing’). The resulting song is the target of strong sexual selection by conspecific females. However, male song also attracts female flies that squirt larvae onto males or nearby female crickets; the larvae then burrow into, consume, and ultimately kill the host. The flies thus impose strong natural selection on male song, producing silent males, which have spread rapidly in populations on two islands – Kauai and Oahu. On both islands, song loss is caused by genetic mutations that drastically reduce or eliminate sound-producing structures on the male forewing by feminising wing venation – these males are called ‘flatwing’. On recent visits to parasitized cricket populations, we discovered two additional wing phenotypes – ‘small-wing’ and ‘curly-wing’. These two phenotypes differ noticeably from flatwing, and from each other, but all have the effect of eliminating or reducing acoustic signals that attract the parasitoid fly. These discoveries illustrate how the evolutionary process can repeatedly, and through a remarkable variety of independent mechanisms, drive adaptation to the same selection pressure.