Possible Epigenetic Origin of a Recurrent Gynandromorph Pattern in Megachile Wild Bees

SIMPLE SUMMARY: Gynandromorphs, i.e., individuals with a mix of male and female body parts, are known for many species of insects and other animals with separate sexes. This anomaly is generally regarded as the result of localized genetic mutations in sex-determining genes. We analyzed the specific mix of male and female characters in naturally occurring gynandromorphs of 21 species of the wild bee genus Megachile and found a recurrent pattern. Based on the regularity of this pattern, and the current knowledge on sex determination and sex differentiation in the relatively closely-related honey bee, we argue that the origin of these composite phenotypes is possibly epigenetic, rather than genetic, i.e., produced by some defects in the maintenance of the regulatory signals that control sex differentiation at the level of single cell lineages, rather than triggered by genetic mutations. ABSTRACT: Gynandromorphs, i.e., individuals with a mix of male and female traits, are common in the wild bees of the genus Megachile (Hymenoptera, Apoidea). We described new transverse gynandromorphs in Megachile pilidens Alfkeen, 1924 and analyze the spatial distribution of body parts with male vs. female phenotype hitherto recorded in the transverse gynandromorphs of the genus Megachile. We identified 10 different arrangements, nine of which are minor variants of a very general pattern, with a combination of male and female traits largely shared by the gynandromorphs recorded in 20 out of 21 Megachile species in our dataset. Based on the recurrence of the same gynandromorph pattern, the current knowledge on sex determination and sex differentiation in the honey bee, and the results of recent gene-knockdown experiments in these insects, we suggest that these composite phenotypes are possibly epigenetic, rather than genetic, mosaics, with individual body parts of either male or female phenotype according to the locally expressed product of the alternative splicing of sex-determining gene transcripts.