Sex-Specific Transcriptome Signatures in Pacific Oyster Hemolymph

Sex determination and differentiation exhibit remarkable molecular diversity across taxa, driven by genetic, epigenetic, and environmental factors. Invertebrates with sequential hermaphroditism, such as the Pacific oyster (Magallana gigas), represent a poorly understood system despite their role as keystone species and contribution to a substantial aquaculture industry.

To identify sex-related molecular markers during gametogenesis, we repeatedly sampled hemolymph from artificially conditioned oysters over two months, and sex phenotypes were assigned at the end of the experiment by biopsy.

RNA-sequencing analysis of five males and five females revealed subtle yet consistent sex-specific transcriptional signatures in hemolymph. We show that gametogenesis proceeds asynchronously among oysters, even within the same sex individuals. Complex physiological trade-offs were discovered between sexes during gonad maturation; in early stages of sexual maturation, females prioritized cell division, whereas males suppressed it. Females exhibited higher expression of solute carrier family (SLC) genes, suggesting enhanced nutrient exchange during oogenesis. Temporal dynamics highlighted differential expression of genes regulating cross-membrane ion gradients (e.g., transient receptor potential channels) and signal transduction (e.g., signal transducer and activator of transcription), previously linked to environmental sex determination (ESD) in some reptilian species.

Together, these findings underscore that gametogenesis in Pacific oysters is complex and dynamic, and that molecular pathways of ESD may be partially conserved between invertebrate and vertebrate species.