Putative Mitochondrial Sex Determination in the Bivalvia: Insights From a Hybrid Transcriptome Assembly in Freshwater Mussels

Bivalves exhibit an astonishing diversity of sexual systems, with genetic and environmental determinants of sex, and possibly the only example of mitochondrial genes influencing sex determination pathways in animals. In contrast to all other animal species in which strict maternal inheritance (SMI) of mitochondria is the rule, bivalves possess a system known as doubly uniparental inheritance (DUI) of mitochondria in which maternal and paternal mitochondria (and their corresponding female-transmitted or F mtDNA and male-transmitted or M mtDNA genomes) are transmitted within a species. Species with DUI also possess sex-associated mtDNA-encoded proteins (in addition to the typical set of 13), which have been hypothesized to play a role in sex determination. In this study, we analyzed the sex-biased transcriptome in gonads of two closely-related freshwater mussel species with different reproductive and mitochondrial transmission modes: the gonochoric, DUI species, Utterbackia peninsularis, and the hermaphroditic, SMI species, Utterbackia imbecillis. Through comparative analysis with other DUI and non-DUI bivalve transcriptomes already available, we identify common male and female-specific genes, as well as SMI and DUI-related genes, that are probably involved in sex determination and mitochondrial inheritance in this animal group. Our results contribute to the understanding of what could be the first animal sex determination system involving the mitochondrial genome.