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

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.

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

“…We have recently reported the changes that the testicular transcriptome of the Mediterranean pine vole, Microtus duodecimcostatus, undergo during its seasonal reproductive cycle in southeastern Iberian Peninsula (Lao-Pérez et al, 2021). The inactive testes of this species show a clear difference with those of the Iberian mole: meiosis initiation is completely stopped, so that no zygotene or pachytene cells are present in the regressed seminiferous tubules.…”

“…Hence, to normalize the data and focus on the study of gene expression in somatic cells, we decided to remove transcripts expressed in germ cells from the General Feature Format (GFF) file of the Iberian mole that we have recently generated (Real et al, 2020). For this, we used previously published cell signatures in single cell RNA sequencing studies (scRNA-seq) (Hermann et al, 2018;Green et al, 2018), as described in Lao-Pérez et al (Lao-Pérez et al, 2021). We removed all genes included in clusters 1-13 and 16 from the Hermann et al (Hermann et al, 2018) study, belonging to different germ cell types, and those from spermatogonia, spermatocyte, round spermatid, and elongating spermatid from the Green et al (Green et al, 2018) one.…”

“…We also found that inactive testes have lost the "immune privilege" (reduced immune response) that operates normally in active testes. Finally, we performed an inter-species comparative analysis against analogous datasets we reported for the Mediterranean pine vole (Lao-Pérez et al, 2021), finding that a large number of genes are commonly deregulated in the inactive testes of both species. These genes are enriched in pathways such as the MAPK and regulation of the immune response, indicating the existence of conserved molecular mechanisms of testis involution across seasonal breeding mammals.…”

“…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.…”

“…The copyright holder for this preprint this version posted January 12, 2022. ; https://doi.org/10.1101/2022.01.12.476048 doi: bioRxiv preprint European beaver, Castor fiber (Bogacka et al, 2017), the plateau pika, Ochotona curzoniae and the Mediterranean pine vole, Microtus duodecimcostatus (Lao-Pérez et al, 2021). However, the number and identity of the deregulated genes vary substantially from study to study, mainly due to differences in either the profiling technologies used or the bioinformatic analysis performed.…”