Genetic control of seasonal reproductive cycle in Talpa occidentalis

The production of gametes (gametogenesis) is a requisite for sexual reproduction. Depending on environmental factors, mainly latitude, species may have continual reproduction, which implies uninterrupted gametogenesis, or seasonal reproduction, in which gametogenesis (gonads) activate and inactivate cyclically every year. Testis physiology and its genetic and endocrine control has been studied for many decades in model species like mice, rats and human, which are continual breeding species. However, very little efforts have been made to study seasonal reproduction, which provides us an excellent opportunity to study naturally established mechanisms by which gametogenesis function may be accommodated to the environmental requirements. Most studies carried out on the control of seasonal breeding have been performed in domesticated animals, mainly hamsters, or in semi-wild animals like the roe deer. Studies made in wild animals like the brown hare have been very scarce and focused on particular aspects of seasonal breeding. Hence, to date no wild animal had been the subject of a comprehensive study in which the different aspects of seasonal breeding control were approached. In the present study we have studied Talpa occidentalis, a species of mole, which shows seasonal reproduction. This species breed during the winter and inactivate during summer. Many morphological changes occur in the gonads of both males and females throughout the annual reproductive cycle. In males, testes are larger during the breeding season and smaller during the non-breading season, so that testicular weight in December may quadruple that in July. Most cells present in the germinative epithelium of fertile testes disappear when they become non-fertile testes, and appear again in the next autumn, when testis function reactivates. In this species, we have studied, for the first time, the main aspects of seasonal variations in the testis, including: 1) the expression patterns of several genes involved in testis development, like SOX9, DMRT1, SF1 and AMH, 2) androgen levels and the localization and expression levels of their receptors, 3) seasonal dynamics of somatic and germ cells, 4) apoptosis and cell proliferation, 5) seasonal variations in cell junctions and the status of the blood- testis barrier, and 6) the structural integrity of the lamina propria of seminiferous tubules. This comprehensive study has provided several interesting results. We have shown that the seasonal breeding in the mole is not regulated at the level of meiosis onset, as this is maintained at a constant rhythm throughout the year. Our data suggest that there is a hormonal control exerted by the hypothalamic-pituitary-gonadal axis and that genes like SOX9 and DMRT1 may be a part of the testicular mechanism that respond to this hormonal control. We have also shown that inactive adult and pre-pubertal testes are very similar but not identical to each other as genes like AMH and OCT4 which are active in the former, remain permanently repressed in the later. The spermatogonial pool in the mole testis probably fluctuates throughout the breeding cycle due to an imbalance between the cellular processes controlling it: apoptosis, cell proliferation and the rhythm of meiosis onset. In addition, we have shown that apoptosis is not responsible for the massive depletion of germ cells that occurs during testis involution. Rather, it a consequence of cell junction disruption, which may lead to Sertoli-germ cell detachment. The disorganization of the blood-testis barrier in testes of non-breeding moles supports this hypothesis. In temperate areas of the earth the climatic conditions vary seasonally and lead living organisms to modulate their activity also according to a seasonal rhythm. Reproduction is the biological process in which this influence becomes more evident. The current climate change proceeds inexorably and its negative influence on the fitness of seasonal breeding vertebrates remains uncertain, but may be potentially irreversible in many cases. Hence, having a precise knowledge of the environmental and genetic factors controlling seasonal breeding is an essential tool to face and counteract those probable negative effects. The present study in the mole may increase our understanding of these biological processes.