Spermatogenesis in cultured blue mussel (Mytilus edulis) from a cold-ocean environment: Seasonal spatiotemporal expression of three gamete-associated molecular markers

To understand the seasonality of spermatogenesis in cultured males of Mytilus edulis from a cold-ocean environment, we investigated the cellular transitions occurring within the spermatogenic epithelium of the testicular acini during early and advancing spermatogenesis, with specific reference to the histology of the epithelium, gene specific spermatogenic response, condition, culture environment, and season. A combination of histological evaluation, qPCR analysis, and in situ hybridization was used to examine the cellular transitions taking place in the germinal epithelium from late winter through to a seasonal spawn in summer. We observed clear seasonal transitionary changes in the spermatogenic cell population making up the germinal epithelium (i.e., spermatogonial stem cells, spermatocytes, spermatids, and spermatozoa) extending from February to July. These seasonal transitions in spermatogenic cell type coincided with significant variation in the spatiotemporal expression of two molecular markers for spermatogenesis (i.e., Kelch-like protein 10 [KLHL10] and Armadillo repeat-containing protein 4 isoform X2 [ARMC4]) but not for expression of a gamete-specific Mitochondrial cytochrome oxidase I (MT-COI). The spatiotemporal expression of these genes is directly linked to the cellular changes taking place in the germinal epithelium during spermatogenesis. These observations not only corresponded to seasonal changes in physiological condition but also environmental temperature and chlorophyll a, thus further supporting the link between male gametogenesis and environment in higher latitude regions.