Impact of the processes of testicular regression and recrudescence in the prostatic complex of the bat Myotis nigricans (Chiroptera: Vespertilionidae)

Abstract

Myotis nigricans is a species of vespertilionid bat, whose males show two periods of total testicular regression during the annual reproductive cycle in the northwest São Paulo State, Brazil. Thus, the aim of this study was to investigate the impact of total testicular regression on the prostatic morphophisyology and its regulation. The prostatic complex (PC) of animals from the four periods of the reproductive cycle (active, regressing, regressed, and recrudescence) was analyzed by different histological, morphometric, and immunohistochemical procedures to characterize its variations, analyze its hormonal regulation and evaluate whether the prostate is affected by the processes of testicular regression and recrudescence. The results indicated a decrease in the prostatic parameters from the active to regressed periods, which are related to decreases in the testicular production of testosterone and in the prostatic expression of androgen receptor (AR), estrogen receptor α (ERα) and aromatase. However, in regressed-recrudescence periods, the prostatic expression of AR, ERα and aromatase increased, indicating the reactivation of the PC. Despite this, the PC appears to have a slower reactivation and seems not to follow the testicular recrudescence in morphological and morphometric terms. With these data, we demonstrate that the prostatic physiology is directly affected by total testicular regression and conclude that it is regulated by testosterone and estrogen, via the production of testosterone by the testes, its conversion to dihydrotestosterone by 5α-redutase and to estrogen by aromatase, and the activation/deactivation of AR and ERα in epithelial cells, which regulate cell expression and proliferation.

Comparative analysis of male reproductive accessory glands in bats Histiotus velatus (Vespertilionidae), Molossus rufus (Molossidae), and Peropteryx leucoptera (Emballonuridae)

“…Similarly, the absence of ampullary glands and seminal vesicles is not exclusive to the three species analyzed here. This absence was also reported in all Neotropical bat species studied histologically (Albernaz et al, 2021; Beguelini et al, 2015, 2016; Christante et al, 2015; Martins et al, 2015, 2016; Negrin et al, 2014; Puga et al, 2013, 2014, 2016, 2017; Santos et al, 2018), as well as in bats from families of the Old World, such as Hipposideridae (Pal, 1983) and Rhinolophidae (Bernard, 1985). The meaning of the absence of these two glandular types in these bats is still uncertain; however, we corroborate the hypothesis postulated by Beguelini et al (2016), which proposes that the absence of these glands, possibly, indicates that their secretion is not necessary for these bats, or that their function has been assumed by any of the glands still present in the complex.…”

“…Despite these great variations in the composition of RAGs, all the three species of bats analyzed in the present study, as well as all other species already histologically studied in the literature, present similarities in the ventral prostate. In all species, this region have an atypical epithelium, which varies markedly in morphology, due to its holocrine pattern of secretion (Albernaz et al, 2021; Beguelini et al, 2015, 2016; Christante et al, 2015; Martins et al, 2015, 2016; Negrin et al, 2014; Puga et al, 2013; Santos et al, 2018). Holocrine secretion has never been described for the reproductive glands of any other mammal in the current literature.…”

The prostate of the bat Artibeus lituratus: Seasonal variations, abiotic regulation, and hormonal control

“…Tropical bats may present monoestric or polyestric patterns or continuous reproduction throughout the year (Taddei, 1980;Zortéa, 2003). In some cases, the reproduction of the a bat species may vary geographically, presenting different patterns in regions with markedly divergent climatic conditions (Beguelini et al, 2013(Beguelini et al, , 2014(Beguelini et al, , 2015aBeguelini et al, 2015b;Beguelini et al, 2020;Krutzsch, 1979;Soares et al, 2020;Wilson & Findley, 1971).…”

“…The binding of DHT to AR in prostatic epithelial cells triggers different cascades of reactions that primarily regulate prostatic secretions (Prins et al, 1991). Conversely, circulating testosterone that reaches prostatic stroma could be converted into estradiol (E2) by the aromatase enzyme, which is present mainly in the cytoplasm of prostatic stromal cells (Beguelini et al, 2015a).Estradiol is an estrogen hormone that is essential for the prostate and has an opposite role in the regulation of prostatic tissue with the activation of estrogen receptor alpha (ERα), triggering proliferation, and estrogen receptor beta (ERβ), causing anti-proliferative effects (apoptosis), which could balance the proliferative action of androgens on the epithelium (Ellem & Risbridger, 2009;Heldring et al, 2007).…”

“…Conversely, the ventral region differs from the reproductive glands described in other mammals, by presenting holocrine secretion (Puga et al, 2013). In addition to this anatomical variation, studies have indicated relevant changes in the morphology and physiology of the prostate during the annual reproductive cycle of the few bat species already studied (Beguelini et al, 2015a;Christante et al, 2015;Negrin et al, 2014;Puga et al, 2014;Swami & Lall, 1982). Generally, prostatic parameters increase as a preparation for the reproductive peak of the species.…”