Testing the role of trait reversal in evolutionary diversification using song loss in wild crickets

Funding: UK Natural Environment Research Council Grants NE/I027800/1, NE/G014906/1, and NE/L011255/1 (to N.W.B.) and Leverhulme Trust Grant RPG-2014-284 (to F.M.-Z.) The mechanisms underlying rapid macroevolution are controversial. One largely untested hypothesis that could inform this debate is that evolutionary reversals might release variation in vestigial traits, which then facilitates subsequent diversification. We evaluated this idea by testing key predictions about vestigial traits arising from sexual trait reversal in wild field crickets. In Hawaiian Teleogryllus oceanicus, the recent genetic loss of sound-producing and -amplifying structures on male wings eliminates their acoustic signals. Silence protects these “flatwing” males from an acoustically orienting parasitoid and appears to have evolved independently more than once. Here, we report that flatwing males show enhanced variation in vestigial resonator morphology under varied genetic backgrounds. Using laser Doppler vibrometry, we found that these vestigial sound-producing wing features resonate at highly variable acoustic frequencies well outside the normal range for this species. These results satisfy two important criteria for a mechanism driving rapid evolutionary diversification: Sexual signal loss was accompanied by a release of vestigial morphological variants, and these could facilitate the rapid evolution of novel signal values. Widespread secondary trait losses have been inferred from fossil and phylogenetic evidence across numerous taxa, and our results suggest that such reversals could play a role in shaping historical patterns of diversification. Postprint