Mediterranean Pine Vole, Microtus duodecimcostatus: A Paradigm of an Opportunistic Breeder

SIMPLE SUMMARY: In temperate zones of the Earth, some mammalian species reproduce seasonally whereas others do it continuously. Other species are summer breeders in the north and winter breeders in the south. Thus, the reproductive pattern seems not to be a species-specific but a population-specific trait. We investigated the reproduction pattern of the Mediterranean pine vole, Microtus duodecimcostatus, in the area around the city of Granada in Southern Spain, and found that individuals living in wastelands reproduce seasonally whereas those living in close poplar plantations (just 8 km apart) reproduce throughout the year, as did voles captured in wastelands and kept in captivity. These animals represent thus a paradigm of an opportunistic breeder as particular individuals stop breeding or not, depending on the environmental conditions they face at any moment. Sexually inactive male voles undergo complete testis inactivation and their sperm production is halted. The immune system in active testes is depressed, a phenomenon known as “immune privilege” that protect germ cells from autoimmune attack. We studied gene activity in active and inactive testes and our results indicate that such an immune privilege is lost in inactive testes, suggesting an important role for this process during testis regression. ABSTRACT: Most mammalian species of the temperate zones of the Earth reproduce seasonally, existing a non-breeding period in which the gonads of both sexes undergo functional regression. It is widely accepted that photoperiod is the principal environmental cue controlling these seasonal changes, although several exceptions have been described in other mammalian species in which breeding depends on cues such as food or water availability. We studied the circannual reproductive cycle in males of the Mediterranean pine vole, Microtus duodecimcostatus, in the Southeastern Iberian Peninsula. Morphological, hormonal, functional, molecular and transcriptomic analyses were performed. As reported for populations of other species from the same geographic area, male voles captured in wastelands underwent seasonal testis regression in summer whereas, surprisingly, those living either in close poplar plantations or in our animal house reproduced throughout the year, showing that it is the microenvironment of a particular vole subpopulation what determines its reproductive status and that these animals are pure opportunistic, photoperiod-independent breeders. In addition, we show that several molecular pathways, including MAPK, are deregulated and that the testicular “immune privilege” is lost in the inactive testes, providing novel mechanisms linking seasonal testosterone reduction and testis regression.