Vestigial singing behaviour persists after the evolutionary loss of song in crickets

Abstract

The evolutionary loss of sexual traits is widely predicted. Because sexual signals can arise from the coupling of specialized motor activity with morphological structures, disruption to a single component could lead to overall loss of function. Opportunities to observe this process and characterize any remaining signal components are rare, but could provide insight into the mechanisms, indirect costs and evolutionary consequences of signal loss. We investigated the recent evolutionary loss of a long-range acoustic sexual signal in the Hawaiian field cricket Teleogryllus oceanicus. Flatwing males carry mutations that remove sound-producing wing structures, eliminating all acoustic signalling and affording protection against an acoustically-orientating parasitoid fly. We show that flatwing males produce wing movement patterns indistinguishable from those that generate sonorous calling song in normal-wing males. Evolutionary song loss caused by the disappearance of structural components of the sound-producing apparatus has left behind the energetically costly motor behaviour underlying normal singing. These results provide a rare example of a vestigial behaviour and raise the possibility that such traits could be co-opted for novel functions.

A silent orchestra: convergent song loss in Hawaiian crickets is repeated, morphologically varied, and widespread

“…2B; comparing songs measured in the lab using a CEM DT-805 (CEM, Shenzhen, China) sound level meter 5 cm from test subjects). Flatwing males also attempt to sing (Schneider et al 2018), but the amplitude of acoustic stimuli produced during wing movement did not differ between CwNw and Fw males (N = 13, P = 1.000). Like Fw males, CwNw males produced variable, but lower-amplitude, peak frequencies ( Fig.…”

“…Flatwing males also attempt to sing (Schneider et al. ), but the amplitude of acoustic stimuli produced during wing movement did not differ between CwNw and Fw males ( N = 13, P = 1.000). Like Fw males, CwNw males produced variable, but lower‐amplitude, peak frequencies (Fig.…”

Sexual signal loss in field crickets maintained despite strong sexual selection favoring singing males

“…Despite the prediction that evolution by sexual selection should be common and relatively rapid, there are comparatively few examples of contemporary evolution (either gain or loss) of novel traits by sexual selection (Svensson and Gosden ; Schneider et al. ; Tinghitella et al. ).…”

“…Although affected males retain their stridulatory behaviors, they cannot produce song (Schneider et al. ). The obligately silent phenotype, termed “flatwing,” is caused by a Mendelian sex‐linked gene (Tinghitella , Pascoal et al.…”

“…In response to this intense selection against singing, mutations have spread through populations in Hawaii that destroy the wing structures males use to produce and radiate sound (Zuk et al 2006;Pascoal et al 2014). Although affected males retain their stridulatory behaviors, they cannot produce song (Schneider et al 2018). The obligately silent phenotype, termed "flatwing," is caused by a Mendelian sex-linked gene (Tinghitella 2008, Pascoal et al 2014.…”