Stereological and histological characterization of spermatogenesis in Atlantic salmon (Salmo salar)

Male Atlantic salmon display variation in life history strategies, where sexual maturation occurs during the freshwater phase as parr, after smoltification as jacks, as grilse after one, or after multiple winters at sea as anadromous adults, each strategy exhibiting evolutionary trade-offs. Spermatogenesis starts during puberty, salmon being a typical example for the unrestricted spermatogonia type of cystic spermatogenesis. If and how life history strategies affect the process of spermatogenesis is unknown. We characterized the germ cell stages appearing during spermatogenesis histologically and determined the increasing number of germ and Sertoli cells stereologically. We found 9 mitotic divisions and a loss of 64% of germ cells occurring during development, the highest ratio found in teleost fish yet. This may relate to the observation that salmon showed, with 207, the so far highest number of germ cells supported per Sertoli cell in vertebrates. We hypothesize that next to circulating hormones, such as follicle-stimulating hormone, local mechano-transduction pathways regulate changes in Sertoli cell number. Such changes accompany the development of spermatogenic cysts, apparently in response to the increasing and then again decreasing volume of individual germ cell clones. This coordinates Sertoli cell number with spermatogenic cyst maturation. No major differences in spermatogenesis were found between parr and two sea winter Atlantic salmon, consistent with a genetic fixation of the major traits of spermatogenesis, as found in most vertebrates. • Salmon spermatogonia complete 9 mitotic cell cycles before entering meiosis. • One Sertoli cell can support 207 spermatids, the highest efficiency found thus far. • Apoptotic germ cell loss during spermatogenesis (64%) is one of the highest in fish. • Hormones and mechanotransduction may coordinate germ and Sertoli cell proliferation. • Spermatogenesis is similar in parr and 2SW adults but the latter produce more cysts.