Identification of Live Germ-Cell Desquamation as a Major Mechanism of Seasonal Testis Regression in Mammals: A Study in the Iberian Mole (Talpa occidentalis)1

Abstract

In males of seasonally breeding species, testes undergo a severe involution at the end of the breeding season, with a major volume decrease due to massive germ-cell depletion associated with photoperiod-dependent reduced levels of testosterone and gonadotropins. Although it has been repeatedly suggested that apoptosis is the principal effector of testicular regression in vertebrates, recent studies do not support this hypothesis in some mammals. The purpose of our work is to discover alternative mechanisms of testis regression in these species. In this paper, we have performed a morphological, hormonal, ultrastructural, molecular, and functional study of the mechanism of testicular regression and the role that cell junctions play in the cell-content dynamics of the testis of the Iberian mole, Talpa occidentalis, throughout the seasonal breeding cycle. Desquamation of live, nonapoptotic germ cells has been identified here as a new mechanism for seasonal testis involution in mammals, indicating that testis regression is regulated by modulating the expression and distribution of the cell-adhesion molecules in the seminiferous epithelium. During this process, which is mediated by low intratesticular testosterone levels, Sertoli cells lose their nursing and supporting function, as well as the impermeability of the blood-testis barrier. Our results contradict the current paradigm that apoptosis is the major testis regression effector in vertebrates, as it is clearly not true in all mammals. The new testis regression mechanism described here for the mole could then be generalized to other mammalian species. Available data from some previously studied mammals should be reevaluated.

Testicular histomorphometry and the proliferative and apoptotic activities of the seminiferous epithelium in Syrian hamster (Mesocricetus auratus) during regression owing to short photoperiod

“…Although there are some species of mammals in which apoptosis is known not to be the main cellular mechanism in testicular regression, its function being the control of proliferation (Blottner et al, 2007;Dadhich et al, 2013), in other animal species it is considered to be the main mechanism involved in this process. Some species like the Brown Hare, in which spermatogenesis arrest, in the non-breeding season, occurs in spermatocytes, only spermatocytes and rarely spermatogonia undergo apoptosis (Strbenc et al, 2003).…”

“…In contrast, in the white-footed mouse, starling (Young & Nelson, 2001) or the crow (Jenkins et al, 2007;Islam et al, 2012) it has been observed that, in addition to apoptosis in spermatocytes, apoptosis also occurs in round spermatids and spermatogonia, although to a lesser extent, while spermatogenesis arrest, occurs in spermatogonia. To date, the Syrian hamster has been classified as a species where apoptosis is important but not the main mechanism of testicular regression, owing to the lack of data concerning the changes that occur during testicular regression (Dadhich et al, 2013), although it is known that spermatocyte apoptosis is crucial for maintaining regression once it is already established (Morales et al, 2002). In this study, the effect of short photoperiod has been studied throughout the whole process of testicular regression, so that it is possible to conclude that apoptosis plays an essential role in the atrophy of the seminiferous epithelium during the non-breeding season.…”

Circannual Testis Changes in Seasonally Breeding Mammals

“…The panels in figure 1 depict the aspect of active and inactive testes in 2 mammalian species, the Iberian mole, Talpa occidentalis , and the wood mouse, Apodemus sylvaticus . In both species, the inactive testis maintains some meiotic activity, as meiosis onset is not completely interrupted and some few primary spermatocytes are still present in the regressed seminiferous tubules [Dadhich et al, 2010[Dadhich et al, , 2013. This situation appears to be quite common in many species that undergo seasonal testis regression, as observed in the Japanese redbellied newt, Cynops pyrrhogaster [Yazawa et al, 2000], the silver fox, Vulpes vulpes [Andersen Berg et al, 2001], the Syrian hamster [Morales et al, 2002[Morales et al, , 2007, the Chinese soft-shelled turtle, Pelodiscus sinensis [Zhang et al, 2008], and the Japanese jungle crow, Corvus macrorhynchos [Islam et al, 2012], as well as in the Mediterranean pine vole, Microtus duodecimcostatus [unpubl.…”

“…The structure and functionality of the BTB has been investigated in 3 seasonally breeding mammals: the mink, Mustela vison [Pelletier, 1988], the Djungarian hamster, Phodopus sungorus [Tarulli et al, 2008], and the Iberian mole [Dadhich et al, 2013]. Molecular-tracer experiments have shown that in all 3 species the BTB becomes permeable in the non-breeding period, allowing the tracer to reach the adluminal compartment of the seminiferous epithelium ( fig.…”

“…In some species, spermatogenesis is completely arrested, and the animals are unable to breed for several months. This occurs in a variety of species, including hamsters [Bex and Bartke, 1977], deer [Brown et al, 1979;Clarke et al, 1995], brown bears [Tsubota et al, 1997], moles [Dadhich et al, 2010[Dadhich et al, , 2013, and armadillos [Luaces et al, 2013[Luaces et al, , 2014.In mammals, reproduction is a complex feature that is induced and controlled by the hypothalamus-pituitarygonad axis (HPG). The hypothalamic neurons release the decapeptide GnRH (gonadotropin-releasing hormone) in the portal venous system, which in turn causes the release of gonadotrophic hormones LH (luteinizing hormone) and FSH (follicle stimulating hormone) in the anterior pituitary (hypophysis), which activates spermatogenesis and the production of gonadal steroids [Hayes et…”