Expression of Genes Controlling Testicular Development in Adult Testis of the Seasonally Breeding Iberian Mole

Abstract

Most testicular features undergo major circannual variation in seasonal breeding species. Although the ultimate cause of these variations is known to be the photoperiod in most cases, very little is known about the genetic mechanisms by which these changes are modulated in the testis. Many genes involved in testis development are known to be expressed in the adult testis as well. Since these genes encode genetic regulatory factors, it is reasonable to suspect that they could play some role in the control of the adult testis function. Using immunological detection techniques and RT-Q-PCR, we have studied the spatio-temporal expression pattern of WT1, SF1, SOX9, AMH, and DMRT1 in 4 representative stages of the circannual cycle of the testes of Talpa occidentalis, a mole species with strict seasonal reproduction. AMH is not expressed at any stage of the cycle, showing that inactive adult testes are functionally different from pre-pubertal, juvenile ones. The continuous presence of primary spermatocytes may explain the permanent repression of AMH in the mole testis. WT1 and SF1 are down-regulated and SOX9 is up-regulated in regressed mole testes, suggesting that the modulation of the expression of these genes may be involved in the control of circannual gonad variation. Furthermore, SOX9 and DMRT1 show clear spermatogenic stage-dependent expression patterns. Both genes are expressed more intensely during the proliferative stages of spermatogonia, although SOX9 expression is limited to Sertoli cells, whereas DMRT1 is expressed in both Sertoli and spermatogonial cells. Available data suggest that intratesticular levels of testosterone could regulate circannual spermatogenic variations of seasonal breeders by modulating the expression of DMRT1 to control spermatogonial proliferation.

The testis of greater white‐toothed shrew Crocidura russula in Southern European populations: A case of adaptive lack of seasonal involution?

“…It is noteworthy that the seasonal breeding cycle in the southern populations appears to be inverted with respect to that of northern ones, where reproductive inactivity occurs in winter. This is not surprising as the same phenomenon also occurs in populations of other mammalian species living in the same region near the city of Granada, including the Iberian mole (Jiménez et al, ; Dadhich et al, ) and two rodents, Microtus duodecimcostatus and Apodemus sylvaticus (our unpublished data). The extreme drought that characterizes summer in the southeastern Iberian Peninsula probably determines this reversed cycle as it is at this time when small mammals face the harshest life conditions in this region.…”

“…This precludes us from studying the mechanism of testis regression in this species in these populations, but permits us to compare the aforementioned protein‐expression patterns in shrew with those of other mammalian species. Several proteins, including SOX9, Claudin 11, and DMC1, showed no expression differences with respect to those of the mouse and the Iberian mole (Dadhich et al, ), confirming a high degree of evolutionary conservation of their respective functions in the testis. Spermatogenic stage‐depending expression of SOX9 in all species studied to date, including rats (Fröjdman et al, ), mice, moles (Dadhich et al, ), and shrews (present article) suggest an important role for this protein in the control of spermatogenesis, and probably also in seasonal testis involution as expression is even stronger in seasonally regressed testes of moles (Dadhich et al, ).…”

“…We investigated in the testes of C. russula the expression pattern of several proteins, which have previously been found to show seasonal variations in another species of the order Eulipotyphla, the Iberian mole Talpa occidentalis (Dadhich et al, ). However, again, no differences were detected between the two study groups of C. russula (compare left and right columns in Fig.…”

“…Also, we studied the expression pattern of DMRT1, a protein that in T. occidentalis was shown to mark both Sertoli cells and spermatogonia, but not spermatocytes (Dadhich et al, ). As described in the mole, two types of seminiferous tubules can be identified in the testes of C. russula males according to the number of cells expressing DMRT1.…”

Circannual Testis Changes in Seasonally Breeding Mammals

“…This finding is consistent with the data reported by Brambell [1935], who showed that the beginning, and probably also the end, of the breeding season in another shrew, Sorex araneus , is determined by the female and not by the male. Thus, the seasonal breeding cycle in the southern populations of C. russula is inverted with respect to that of northern ones, where reproduction is halted in winter, as occurs in populations of other mammalian species living in the same region, including the Iberian mole [Jiménez et al, 1990;Dadhich et al, 2010Dadhich et al, , 2011Dadhich et al, , 2013 and 2 rodents [unpubl. data].…”