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

Abstract

Males of all seasonal breeding mammals undergo circannual periods of testis involution resulting in almost complete ablation of the germinative epithelium. We performed a morphometric, histological, hormonal, and gene-expression study of the testes from winter and summer males of the greater white-toothed shrew, Crocidura russula, in populations of the southeastern Iberian Peninsula. Unexpectedly, we found no significant differences between the two study groups. Surprisingly, female data confirmed a non-breeding period in the summer, evidencing that males retain full testis function even when most females are not receptive. This situation, which has not been described before, does not occur in northern populations of the same species where, in addition, the reproductive cycle is inverted with respect to those in the south, as the non-breeding period occurs in winter instead in summer. Considering that the non-reproductive period shortens at lower latitude locations, we hypothesize that in southern populations the non-breeding period is short enough to make testis regression inefficient in terms of energy savings, because: (1) testes of C. russula are very small, a condition derived from their monogamy that implies low investment in spermatogenesis; and (2) the spermatogenic cycle of this species is slow and long. The inverted seasonal breeding cycle and the lack of seasonal testis regression described here are new adaptive processes that deserve further research, and provide evidence that the genetic and hormonal mechanisms controlling reproduction timing in mammals are more plastic and versatile than initially suspected.

Sox9 and Sox8 protect the adult testis from male-to-female genetic reprogramming and complete degeneration

“…Nothing is known on the role of SOX9 in the adult testis, where it is expressed by Sertoli cells in a spermatogenic stage-dependent manner in several mammalian species ( Fröjdman et al, 2000 ; Dadhich et al, 2011 ; Massoud et al, 2014 ). Here we report the use of two Sertoli-cell-specific Cre lines ( Wt1-CreERT2 and Sox9-CreERT2 ) to induce Sox9 ablation on a Sox8 -/- background in the adult testis, starting at postnatal day 60 (P60).…”

Circannual Testis Changes in Seasonally Breeding Mammals

“…Massoud et al [2014] considered that this is a new adaptive mechanism not described before. The authors hypothesized that in southern populations the non-breeding period is short enough to make testis regression inefficient in terms of energy savings for 2 reasons.…”

“…data]. Massoud et al [2014] suggested that the extreme summer drought in south-eastern Spain probably causes this reversed cycle, small mammals facing better life conditions in the moderate winters of this region.…”

“…Massoud et al [2014] recently studied males from some populations from near the city of Granada, southern Spain, in order to determine the mechanism of testis regression in this species. The authors expected to find a shorter non-breeding period in these southern populations as the length of the reproductive period of a particular species is known to increase as latitude decreases, as shown in talpid moles [Jiménez et al, 1990].…”

“…To explain the female-driven non-breeding period of C. russula in southern populations, Massoud et al [2014] suggested that this species, and probably many others, tend to reproduce continuously throughout the year, but females may undergo a transient receptivity drop if they face survival difficulties such as food restriction, as evidenced in the musk shrew S. murinus [Temple, 2004]. This phenomenon is controlled by the GnRH-II hormone, a different and an evolutionarily well-conserved form of the GnRH family [Kauffman, 2004], which has been shown to modulate the mating behavior in this species [Temple et al, 2003].…”