Abstract

Simple SummaryIn temperate zones of the Earth, most species reproduce in seasons providing the most favourable environmental conditions. Producing gametes is expensive in energetical terms, so both males and females either reduce or abolish gametogenesis during the non-breeding period. We thoroughly studied the testes of sexually inactive males of two rodents, the wood mouse, Apodemus sylvaticus, and the Algerian mouse, Mus spretus, in southern Iberian peninsula. These populations are syntopic, that is, animals of the two species share their territories and resources, so one would expect them to show similar or identical seasonal reproduction patterns. Contrarily, we found that both species reproduce during most of the year, but wood mice stop breeding in the summer whereas Algerian mice do it in winter. These divergent seasonal breeding patterns imply that either very subtle animal features and/or environmental cues operate to determine reproduction timing and support the notion that multiple models of circannual reproduction patterns are possible for different populations of the same species, showing that the mechanisms controlling seasonal reproduction are in fact very plastic and fast evolving. Hence, small mammals probably have multiple ways available to get adapted to the unstable environmental conditions derived from the ongoing global climate change.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.

Highlights

  • In temperate zones of the Earth most species concentrate the reproductive effort in those seasons with the most favourable environmental conditions

  • Apoptosis was the only cellular process known to be involved in seasonal testis regression, and it is the main cause of germ cell depletion in several mammalian species

  • Sylvaticus males analysed in the present study showed no difference between sexually active and inactive males (Figure 1A; Supplementary Table S4)

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Summary

Introduction

In temperate zones of the Earth most species concentrate the reproductive effort in those seasons with the most favourable environmental conditions. Two main aspects of seasonal breeding are currently being investigated: (1) the mechanisms of cyclic gonadal regression and recrudescence (mainly in the males), and (2) the environmental cues controlling circannual rhythms of reproduction. Two main cellular mechanisms of germ cell depletion have been described during testis regression in seasonally breeding mammals: apoptosis and desquamation (sloughing) [1]. Apoptosis was the only cellular process known to be involved in seasonal testis regression, and it is the main cause of germ cell depletion in several mammalian species. Most studies have been performed in the Syrian hamster, which has become a model species in the field of seasonal reproduction [16,17,18,19,20]

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