Circannual Testis Changes in Seasonally Breeding Mammals

Abstract

In the non-equatorial zones of the Earth, species concentrate their reproductive effort in the more favorable season. A consequence of seasonal breeding is seasonal testis regression, which implies the depletion of the germinative epithelium, permeation of the blood-testis barrier, and reduced androgenic function. This process has been studied in a number of vertebrates, but the mechanisms controlling it are not yet well understood. Apoptosis was assumed for years to be an important effector of seasonal germ cell depletion in all vertebrates, including mammals, but an alternative mechanism has recently been reported in the Iberian mole as well as in the large hairy armadillo. It is based on the desquamation of meiotic and post-meiotic germ cells as a consequence of altered Sertoli-germ cell adhesion molecule expression and distribution. Desquamated cells are either discarded alive through the epididymis, as in the mole, or subsequently die by apoptosis, as in the armadillo. Also, recent findings on the reproductive cycle of the greater white-toothed shrew at the meridional limits of its distribution area have revealed that the mechanisms controlling seasonal breeding are in fact far more plastic and versatile than initially suspected. Perhaps these higher adaptive capacities place mammals in a better position to face the ongoing climate change.

Trade-off between somatic and germline repair in a vertebrate supports the expensive germ line hypothesis

“…Drosophila lines exposed to X-ray irradiation, for example, evolved increased resistance to DNA damage but this resistance was lost after cessation of exposure to X-ray, further supporting the idea that increased DNA maintenance is costly (36). The cost of germline maintenance can also be inferred from the fact that many mammals and birds reduce the size of their germ line to a minimum outside the breeding season (37,38) and that germline ablation in C. elegans nematodes and male D. melanogaster fruitflies results in an increase in lifespan (29,39). Further indirect evidence comes from studies showing that castration in males results in a significant increase in lifespan in rats (40) and humans (41).…”

Germ cell desquamation-based testis regression in a seasonal breeder, the Egyptian long-eared hedgehog, Hemiechinus auritus

“…This is necessary if the non-breeding period is long enough to make testis regression efficient in terms of energy saving, as spermatogenesis is too expensive to be maintained when it is not needed [ 6 ]. After the study of a number of seasonal breeding mammals, it seems evident that there is not a unique mechanism of testis regression, existing two main cellular processes by which germ cells are massively depleted: apoptosis and desquamation [ 7 ]. However, more species must be studied to determine their relative prevalence and, maybe, to discover new testis regression mechanisms.…”

“…In addition to germ cells, Leydig cells also show species-specific differences in the regressed testis [ 7 ].…”

Sertoli-immature spermatids disengagement during testis regression in the armadillo

“…In seasonal reproducers, the mechanisms regulating the process of germ cell desquamation during testis regression is still poorly known. These wild animals have strong hormonal response to the natural succession of breeding and non-breeding seasons, showing, during the non-breeding season, very low circulating and intra-testicular testosterone levels (for a review, Jimenez et al 2015). Both testosterone and gonadotropins are known to regulate the expression of cell adhesion proteins in the testis , Tarulli et al 2008, McCabe et al 2010) and, in testosteronesuppressing experiments in the rat, it has been shown that dissociation of the adhesion complexes at the apical ES contributes to the massive sloughing of immature spermatids (Zhang et al 2005).…”

“…Seasonal reproduction in the non-equatorial regions of the planet is an adaptive strategy aimed at assuring newborns the best environment for survival. During the non-reproductive season, block of the ovarian function and reduction or interruption of the testis activity determines the inability to produce offspring (for a review Jimenez et al 2015). Spermatogenetic arrest has been described in several mammalian species including the Iberian mole (Dadhich et al 2010(Dadhich et al , 2013, the hamster (Bex & Bartke 1977), the black bear (Tsubota et al 1997), the white-footed mouse (Young et al 1999) and the large hairy armadillo Chaetophractus villosus whose seminiferous epithelium undergoes, once a year, rapid regression (Luaces et al 2013(Luaces et al , 2014.…”