Does non-Mendelian chromosome transmission and unusual sex determination affect male mate choice in the fly Bradysia coprophila?

Abstract

Mate quality and the cost of mating affect the evolution of mating preferences and is one reason females often show stronger mate preferences than males. Fungus gnats in the family Sciaridae (Diptera) are a family in which we might expect to see the evolution of strong male mate preferences. Many Sciaridae species are monogenic, where females exclusively produce offspring of one sex. Sciaridae species also exhibit paternal genome elimination, a reproductive system where males only transmit maternally inherited chromosomes to offspring. Therefore, Sciaridae males would benefit from exhibiting mating preferences for females that produce female offspring, as a males genes are only transmitted to future generations through his daughters, not his sons. We explore male mate choice in the sciarid fly Bradysia (formerly Sciara) coprophila. We find that mating is costly, as males become sperm limited through multiple matings, and that males exhibit preferences for larger females, suggesting that males are selected to be choosy. However, we do not find male preferences for females that produce female offspring, instead we find that males prefer mating with females that produce male offspring. We speculate that this seemingly maladaptive behaviour may be due to female receptivity rather than male preference, or that males are unable to distinguish between females of different types, which is perhaps surprising since these females differ genetically by 1000s of genes (through a large paracentric inversion on the X chromosome). Together we show how the interplay between unusual genetics and sex determining systems may affect mating system evolution. Summary statementIn the fungus gnat Bradysia coprophila females are genetically predetermined to produce broods of just one sex and males only transmit maternally inherited genes to offspring. These factors suggest males should have strong mating preferences for females that produce daughters, which we explore. We find that while males would benefit from being "choosy", they appear unable to distinguish the two female types, possibly because females are selected to hide their sex determining phenotype.