The ability to gain matings, not sperm competition, reduces the success of males carrying a selfish genetic element in a fly

Abstract

Females are expected to avoid low-quality males fathering their offspring. X chromosome meiotic drive (XCMD) makes males very low-quality mates. XCMDs are X chromosomes that, in males, cause the failure of all Y chromosome sperm, so all functional sperm carry the driving X and produce daughters. This transmission advantage can allow the XCMD to spread through populations. However, XCMD males typically have low fertility, are very poor at sperm competition, only produce daughters, and bear low fitness alleles associated with XCMD. This imposes significant costs on females that mate with these males. Recently, several studies have shown that females can reduce the risk of their offspring inheriting XCMDs by mating with multiple males (polyandry), as XCMD males typically lose out to normal males in sperm competition. Hence it has been suggested that increased polyandry may be likely to evolve whenever a costly XCMD is common in a population, and that polyandry may be a key factor in preventing XCMDs spreading through populations. We tested this by examining the fruit fly Drosophila subobscura, in which females are known to mate only once in European populations where XCMDs are absent. However, in North African populations an XCMD, referred to as ‘SRs’, occurs. If the association between XCMDs and polyandry is true, then these North African populations should have evolved polyandry. However, we found no evidence of polyandry in North African D. subobscura populations. Instead, we found some evidence that males that carry SRs are slightly less successful at gaining matings in noncompetitive situations. These results show that polyandry does not necessarily evolve in response to the presence of harmful X chromosome drive. With both sperm competition and female choice both being unlikely to substantially reduce the success of XCMD in D. subobscura, the factors that prevent SRs spreading through these populations remain mysterious.