Meiotic drive adaptive testes enlargement during early development in the stalk-eyed fly

Abstract

The sex ratio (SR) X-linked meiotic drive system in stalk-eyed flies destroys Y-bearing sperm. Unlike other SR systems, drive males do not suffer fertility loss. They have greatly enlarged testes which compensate for gamete killing. We predicted that enlarged testes arise from extended development with resources re-allocated from the accessory glands, as these tend to be smaller in drive males. To test this, we tracked the growth of the testes and accessory glands of wild-type and drive males over 5–6 weeks post-eclosion before males attained sexual maturity. Neither of the original predictions is supported by these data. Instead, we found that the drive male testes were enlarged at eclosion, reflecting a greater allocation of resources to the testes during pupation. Testes grow at a higher rate during early adult development in drive males, but there was no evidence that this retards the growth of the accessory glands. Further experiments are proposed to investigate whether smaller accessory glands only arise in drive males post-copulation or when flies are subjected to nutritional stress. Our experimental findings support the idea that enlarged testes in drive males arise as an adaptive allocation of resources to traits that enhance male reproductive success.

A selfish genetic element and its suppressor causes abnormalities to testes in a fly

“…XCMD and their suppressors generate potent genetic conflict that may also be a force influencing gonad development, morphology and evolution (31,32). In this study, we examined whether the intragenomic conflicts created by SR sub and its suppressor affects gonad morphology in D. subobscura .…”

“…In stalk-eyed flies, males that carry XCMD have enlarged testes to compensate drive induced sperm mortality, and XCMD males produce an equivalent number of sperm to normal males (31). The compensation of male testes also appears to occur from an early development stage (32). Compensation may also be the effect that we have observed in D. subobscura .…”

“…Here, we demonstrate that the presence of XCMD and its suppressor can cause significant morphological changes to male gonads. This is the second system, that we are aware of, where XCMD strongly influences male gonad development (31,32). Unlike the XCMD system in stalk-eyed flies, where morphological changes were deemed a compensation mechanism against drive, our evidence suggests that XCMD in D. subobscura inflicts gross abnormalities on male gonads that becomes even more severe in the presence of its suppressor.…”

“…Despite the lack of sperm produced, drive carrying males do not often show fertility costs in single matings when compared to wildtype males (18,26–29). Indeed, XCMD in stalk eyed flies even appears to have resulted in the response to the loss of sperm created by drive through compensation (30–32). Here, males carrying XCMD have an increased testes size that allows them to produce an equivalent amount of sperm to standard males.…”

“…Despite the lack of sperm produced, drive carrying males do not often show fertility costs in single matings when compared to wildtype males (18,(26)(27)(28)(29). Indeed, in stalk eyed flies, the presence of sperm-killing XCMD appears to have driven the evolution of a compensatory increase in the testes size of XCMD males (30)(31)(32) . This allows them to produce a similar amount of sperm to non-XCMD males.…”