Sex‐specific evolution of relative leg size in Drosophila prolongata results from changes in the intersegmental coordination of tissue growth

Abstract

Evolution of relative organ size is the most prolific source of morphological diversity, yet the underlying molecular mechanisms that modify growth control are largely unknown. Models where organ proportions have undergone recent evolutionary changes hold the greatest promise for understanding this process. Uniquely among Drosophila species, Drosophila prolongata displays a dramatic, male‐specific increase in the size of its forelegs relative to other legs. By comparing leg development between males and females of D. prolongata and its closest relative Drosophila carrolli, we show that the exaggerated male forelegs are produced by a sex‐ and segment‐specific increase in mitosis during the final larval instar. Intersegmental compensatory control, where smaller leg primordia grow at a faster rate, is observed in both species and sexes. However, the equilibrium growth rates that determine the final relative proportion between the first and second legs have shifted in male D. prolongata compared both to conspecific females and to D. carrolli. We suggest that the observed developmental changes that produce new adult proportions reflect an interplay between conserved growth coordination mechanisms and evolving organ‐specific growth targets.

Pupal Cues Increase Sperm Production but Not Testis Size in an Insect

“…In a study where testis size is measured and sperm are counted [19], the male larvae exposed to larval cues, regardless of sex, produce smaller testes but more fertile sperm. These discoveries suggest that in response to their social environment, male larvae are able to dedicate varying portions of testis volumes to spermatogenesis and other functions [41], resulting in potential trade-offs between traits of different functions [19,[42][43][44]. However, there is no report that insects can alter their testis size in response to the socio-sexual environment experienced at the adult stage.…”

Pupal Cues Increase Sperm Production but Not Testis Size in an Insect

“…In a study where testis size is measured and sperm are counted [19], the male larvae exposed to larval cues regardless of sex produce smaller testes but more fertile sperm. These discoveries suggest that in response to their social environment, male larvae are able to dedicate varying portions of testis volumes to spermatogenesis and other functions [41], resulting in potential trade-offs between traits of different functions [19,[42][43][44]. However, there is no report that insect adults can alter their testis size in response to the socio-sexual environment.…”

A courtship behavior that makes monandrous females polyandrous

“…2014; Kudo et al. 2015; Luecke and Kopp 2019). Males of D. prolongata are hyperaggressive and fight with their enlarged forelegs (Kudo et al.…”

“…Drosophila prolongata is a fruit fly that has morphological and behavioral characters different from the other Drosophila species (Setoguchi et al 2014). First, the body and foreleg size of D. prolongata are sexually dimorphic, with both being larger in males (Rohner et al 2018a;Rohner et al 2018b;Setoguchi et al 2014;Kudo et al 2015;Luecke and Kopp 2019). Males of D. prolongata are hyperaggressive and fight with their enlarged forelegs (Kudo et al 2017).…”