Divergent Seasonal Reproductive Patterns in Syntopic Populations of Two Murine Species in Southern Spain, Mus spretus and Apodemus sylvaticus

Abstract

In most mammals with seasonal reproduction, males undergo testis regression during the non-breeding period. We performed a morphological, hormonal, functional, and molecular study of the testes of sexually inactive males of two species of murine rodents, the wood mouse, Apodemus sylvaticus, and the Algerian mouse, Mus spretus, in syntopic populations of southern Iberian peninsula. Both species reproduce during most of the year, but wood mice stop breeding in the summer whereas Algerian mice do it in winter. Sexually inactive males of A. sylvaticus show complete testis regression with reduced levels of serum testosterone and abnormal distribution of cell-adhesion molecules. Contrarily, inactive males of M. spretus maintain almost normal spermotogenesis despite a significant reduction of androgenic function. The lack of an evident explanation for the divergent seasonal breeding patterns found in southern populations of A. sylvaticus and M. spretus, compared with northern ones, implies that very subtle species/population-specific features and/or non-conspicuous environmental cues probably operate to determine their seasonal breeding pattern. These results also support the notion that multiple models of circannual testis variation are possible for different populations of the same species, showing that the mechanisms controlling seasonal reproduction are in fact very plastic and fast evolving.

Cellular Modifications in Spermatogenesis during Seasonal Testicular Regression: An Update Review in Mammals

“…In two of the species, the Algerian mouse, Mus spretus, and the greater white-toothed shrew, Crocidura russula, the epithelium does not undergo important cellular changes during the winter, which is the non-breeding season [85]. By contrast, in the other two species, the wood mouse, Apodemus sylvaticus, and the Mediterranean pine vole, Microtus duodecimcostatus, testis regression occurs (facultatively in the latter species) during the non-reproductive period, which takes place in summer [55,58]. These authors concluded that the phylogeny does not seem to be associated with the existence (or not) of seasonal testis regression.…”

“…They consider that this apoptosis is only the cause of the epithelium that remains arrested after suffering regression through the desquamation of the germ cells. However, only by continuously studying the regression period would it be possible to know if this hypothesis is true [55]. In contrast, a study of apoptosis, proliferation, and seasonal body changes in various organs in male bank voles (Myodes glareolus) found that there were changes in the number of testicular cells in the testes due to an increase in apoptotic cells in the seminiferous epithelium during testicular regression [56].…”

“…In addition to these species, the histology of the testes of several rodents during the non-reproductive period has recently been described: The wood mouse, Apodemus sylvaticus, and the Algerian mouse, Mus spretus, in syntropic populations of the south of the Iberian Peninsula [55]. Wood mice do not breed in summer and Algerian mice do not breed in winter.…”

“…In contrast, the histological pattern of Algerian mice is different in the non-breeding season. On the one hand, involutional changes of the seminiferous epithelium are not observed, even though there In addition to these species, the histology of the testes of several rodents during the non-reproductive period has recently been described: The wood mouse, Apodemus sylvaticus, and the Algerian mouse, Mus spretus, in syntropic populations of the south of the Iberian Peninsula [55]. Wood mice do not breed in summer and Algerian mice do not breed in winter.…”

Cell adhesion and immune response, two main functions altered in the transcriptome of seasonally regressed testes of two mammalian species

“…In females, ovaries entry in anoestrus (Das & Khan, 2010) and sexual receptivity is either reduced or abolished, as shown in the musk shrew, Suncus murinus (Temple, 2004). In males of several species, a process of testis regression takes place by which gonad volume is remarkably reduced and spermatogenesis is arrested, as described in the Syriam hamster, Mesocricetus auratus (Seco-Rovira et al, 2015; Martínez-Hernández et al, 2020), the black bear, Ursus americanus (Tsubota et al, 1997), the Iberian mole, Talpa occidentalis (Dadhich et al, 2010; Dadhich et al, 2013), the large hairy armadillo Chaetophractus villosus (Luaces et al, 2013), the wood mouse, Apodemus sylvaticus (Massoud et al, 2021) and the Mediterranean pine vole, Microtus duodecimcostatus (Lao-Pérez et al, 2021), among others.…”