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New Insights in Testicular Biology of Seasonal Breeders
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New Insights in Testicular Biology of Seasonal Breeders

A special issue of Animals (ISSN 2076-2615). This special issue belongs to the section "Animal Reproduction".

Deadline for manuscript submissions: closed (31 July 2021) | Viewed by 21604

Special Issue Editors

Dr. Ester Beltrán Frutos

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Guest Editor
Department of Cell Biology and Histology, Medical School, IMIB‐Arrixaca, Regional Campus of International Excellence "Campus Mare Nostrum", University of Murcia, 30071 Murcia, Spain
Interests: cell biology; histology; testis; photoperiod; aging
Prof. Dr. Luis Miguel Pastor

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Guest Editor
Department of Cell Biology and Histology, Medical School, IMIB-Arrixaca, Regional Campus of International Excellence “Campus Mare Nostrum”, University of Murcia, 30120 Murcia, Spain
Interests: testes histology; testicular apoptosis; seasonal reproduction; aging testes; sertoli cells; leydig cells

Special Issue Information

Seasonal reproduction is an adaptive reproductive strategy that is used by some species to cope with the energy availability that occurs with seasonal oscillations. In this type of reproduction, the light/dark cycle (photoperiod) determines, among other factors, important changes in the fertility of individuals, which have their origin at the cellular, molecular and tissue level in the reproductive system. In males, part of these changes affect the testis with alterations in both spermatogenesis and testicular interstitium that modify the generation of sperm. Linked to this at the neuroendocrine level, there is a decrease in the main hormones involved in reproduction, such as LH, FSH and testosterone. In recent years, testicular changes have been studied both in species with a short seasonal reproduction (ex: sheep) and in species of a long seasonal reproduction (axis: Syrian hamster) in various vertebrate orders. The purpose of this Special Issue was to update the data on the cellular and molecular mechanisms that occur in the testis in the seasonal reproduction of vertebrates. The comparative approach that is intended to be developed in the Issue will not only help us to better understand the diverse adaptive strategies of the reproductive type in the different vertebrate orders, but also provide us with news insights that can serve as a starting point to improve the reproductive performance of domestic animals. 

Dr. Ester Beltrán Frutos
Prof. Dr. Luis Miguel Pastor García
Guest Editors

Manuscript Submission Information

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Keywords

  • photoperiod
  • testis
  • spermatogenesis
  • testicular interstitium
  • sperm
  • hormones

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Published Papers (7 papers)

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Research

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9 pages, 2886 KiB  
Article
The Effect of Inhibin Immunization in Seminiferous Epithelium of Yangzhou Goose Ganders: A Histological Study
by Muhammad Faheem Akhtar, Ejaz Ahmad, Ilyas Ali, Muhammad Shafiq and Zhe Chen
Animals 2021, 11(10), 2801; https://doi.org/10.3390/ani11102801 - 26 Sep 2021
Cited by 6 | Viewed by 2464
Abstract
The current study investigated the effect of inhibin immunization on germ cell numbers (spermatogonia, spermatocytes, round, and elongated spermatids), seminiferous tubules (ST) diameter, Johnsen’s score, epithelial height (μm), luminal tubular diameter (μm), and number of ST per field (ST/field) of Yangzhou goose ganders. [...] Read more.
The current study investigated the effect of inhibin immunization on germ cell numbers (spermatogonia, spermatocytes, round, and elongated spermatids), seminiferous tubules (ST) diameter, Johnsen’s score, epithelial height (μm), luminal tubular diameter (μm), and number of ST per field (ST/field) of Yangzhou goose ganders. Histological evaluation showed apoptosis and regression of testes after inhibin (INH) immunization, with a concomitantly marked reduction in the round and elongated spermatids in the experiment (INH) group compared to the control group. The diameter of seminiferous tubules (ST) and epithelial height (EH) were positively correlated at 181, 200, and 227 days of age. In comparison, luminal tubular diameter (LD) was negatively correlated on day 227 to ST diameter and epithelial height. On day 227, many seminiferous tubules per field (ST/field) were negatively correlated to ST diameter, EH, and LD. INH immunization elevated ST diameter, EH, and LD, while Johnsen’s score and number of ST/field had reciprocal expression. In conclusion, the concomitant effect of INH immunization and seasonality in breeding regressed germ cells and damaged spermatogenesis in seminiferous epithelium Yangzhou ganders. Full article
(This article belongs to the Special Issue New Insights in Testicular Biology of Seasonal Breeders)
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19 pages, 6892 KiB  
Article
Mediterranean Pine Vole, Microtus duodecimcostatus: A Paradigm of an Opportunistic Breeder
by Miguel Lao-Pérez, Diaa Massoud, Francisca M. Real, Alicia Hurtado, Esperanza Ortega, Miguel Burgos, Rafael Jiménez and Francisco J. Barrionuevo
Animals 2021, 11(6), 1639; https://doi.org/10.3390/ani11061639 - 1 Jun 2021
Cited by 4 | Viewed by 4634
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue New Insights in Testicular Biology of Seasonal Breeders)
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13 pages, 781 KiB  
Article
Seasonal Changes of Nuclear DNA Fragmentation in Boar Spermatozoa in Spain
by Raquel Ausejo, Juan Manuel Martínez, Pedro Soler-Llorens, Alfonso Bolarín, Teresa Tejedor and María Victoria Falceto
Animals 2021, 11(2), 465; https://doi.org/10.3390/ani11020465 - 9 Feb 2021
Cited by 9 | Viewed by 2742
Abstract
There are numerous cases when conventional spermiogram parameters are all within an acceptable range but boar subfertility persists. The total sperm nuclear DNA fragmentation index (tDFI) is a trait related to fertility and prolificacy problems that is not routinely evaluated in commercial AI [...] Read more.
There are numerous cases when conventional spermiogram parameters are all within an acceptable range but boar subfertility persists. The total sperm nuclear DNA fragmentation index (tDFI) is a trait related to fertility and prolificacy problems that is not routinely evaluated in commercial AI boars. The aim of this research was to study the effect of the photoperiod, season and reproductive age of the boar on tDFI (measured by SCSA) of 1279 ejaculates from 372 different boars belonging to 6 different breeds located in 6 AI studs in Spain. tDFI data ranged from 0.018% to 20.1%. Although there was a significant single boar effect in the tDFI occurrence, a negative correlation between the tDFI and the age of the boar was found (p < 0.001). tDFI would decrease due to aging of the boar 0.66% each year old within the observed age range. After including age as a covariate in the ANCOVA, no differences were found in tDFI between photoperiods when the sperm collection date was evaluated. However, when the date of the production of semen in the testis was evaluated, the total percentage of spermatozoa with fragmented nuclear DNA was 1.46% higher in the increasing photoperiod in comparison to the decreasing photoperiod (p < 0.0001). On the other hand, for both dates, the lowest tDFI values corresponded to minimum day length for decreasing photoperiod phase (autumn), while the highest tDFI values were found in summer (maximum day length for decreasing photoperiod phase). Full article
(This article belongs to the Special Issue New Insights in Testicular Biology of Seasonal Breeders)
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11 pages, 6556 KiB  
Article
Assessment of Testicular Lhcgr mRNA Expression Correlated with Testis and Seminal Vesicle Activities in the Libyan jird (Meriones libycus, Rodentia: Muridae) during Breeding Season Compared with Nonbreeding Season
by Radia Boufermes, Mansouria Belhocine, Zaina Amirat and Farida Khammar
Animals 2021, 11(2), 320; https://doi.org/10.3390/ani11020320 - 27 Jan 2021
Cited by 3 | Viewed by 2381
Abstract
The Libyan jird (Meriones libycus, 1823) is a wild desert rodent that is a seasonal breeder species adapted to breed when the environmental conditions can satisfy the energy and hydrous requirements of pregnant and nursing females to ensure that births occur [...] Read more.
The Libyan jird (Meriones libycus, 1823) is a wild desert rodent that is a seasonal breeder species adapted to breed when the environmental conditions can satisfy the energy and hydrous requirements of pregnant and nursing females to ensure that births occur at the most favorable time of the year. We assessed gene expression of testicular luteinizing hormone receptor (Lhcgr) correlated to testis activity. The expression of Lhcgr was evaluated using quantitative Real Time-Polymerase Chain Reaction (qRT-PCR and the testis activity by a histological method in adult male Libyan jirds during the nonbreeding and breeding seasons. Our results showed that Lhcgr mRNA expression increased in autumn during the nonbreeding season and decreased in spring during the breeding season. This expression varied in contrast to testicular structure or function and plasma testosterone levels. These results help to elucidate this desert rodent’s seasonal sexual activity, which is correlated with central regulation. Full article
(This article belongs to the Special Issue New Insights in Testicular Biology of Seasonal Breeders)
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16 pages, 4666 KiB  
Article
Divergent Seasonal Reproductive Patterns in Syntopic Populations of Two Murine Species in Southern Spain, Mus spretus and Apodemus sylvaticus
by Diaa Massoud, Miguel Lao-Pérez, Esperanza Ortega, Miguel Burgos, Rafael Jiménez and Francisco J. Barrionuevo
Animals 2021, 11(2), 243; https://doi.org/10.3390/ani11020243 - 20 Jan 2021
Cited by 15 | Viewed by 2251
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 [...] Read more.
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. Full article
(This article belongs to the Special Issue New Insights in Testicular Biology of Seasonal Breeders)
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13 pages, 1096 KiB  
Article
Global Methylation and Protamine Deficiency in Ram Spermatozoa Correlate with Sperm Production and Quality but Are Not Influenced by Melatonin or Season
by Kelsey R. Pool, Jessica P. Rickard and Simon P. de Graaf
Animals 2020, 10(12), 2302; https://doi.org/10.3390/ani10122302 - 4 Dec 2020
Cited by 4 | Viewed by 2616
Abstract
This study assessed whether the seasonal effects of melatonin that upregulate ram reproductive function alter sperm global methylation or protamine deficiency and whether these parameters corresponded to ram endocrinology, semen production and quality. Ejaculates were assessed from rams that received melatonin implants ( [...] Read more.
This study assessed whether the seasonal effects of melatonin that upregulate ram reproductive function alter sperm global methylation or protamine deficiency and whether these parameters corresponded to ram endocrinology, semen production and quality. Ejaculates were assessed from rams that received melatonin implants (n = 9) or no implants (n = 9) during the non-breeding season. Ejaculates (n = 2/ram/week) were collected prior to implantation (week 0), 1, 6 and 12 weeks post implantation and during the following breeding season (week 30). Flow cytometry was used to assess the sperm global methylation and protamine deficiency in each ejaculate, which had known values for sperm concentration, motility, morphology, DNA fragmentation, seminal plasma levels of melatonin, anti-Mullerian hormone and inhibin A. Serum levels of testosterone and melatonin were also evaluated. Though there was no effect of melatonin or season, sperm protamine deficiency was negatively correlated with sperm production and seminal plasma levels of anti-Mullerian hormone and positively correlated with sperm DNA fragmentation and morphology. Global methylation of spermatozoa was positively correlated with sperm DNA fragmentation, morphology and serum testosterone and negatively correlated with sperm motility. These moderate associations with sperm production and quality suggest that sperm protamine deficiency and global methylation are indicative of ram testicular function. Full article
(This article belongs to the Special Issue New Insights in Testicular Biology of Seasonal Breeders)
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Review

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17 pages, 1608 KiB  
Review
Cellular Modifications in Spermatogenesis during Seasonal Testicular Regression: An Update Review in Mammals
by Ester Beltrán-Frutos, Vicente Seco-Rovira, Jesús Martínez-Hernández, Concepción Ferrer, María Isabel Serrano-Sánchez and Luis Miguel Pastor
Animals 2022, 12(13), 1605; https://doi.org/10.3390/ani12131605 - 22 Jun 2022
Cited by 13 | Viewed by 2247
Abstract
Testicular regression occurs during the non-breeding season in many mammals. This affects spermatogenesis, resulting in decreased or arrested activity. Both lead to a decrease or cessation in sperm production. In recent years, the cellular mechanisms that lead to infertility in males in non-reproductive [...] Read more.
Testicular regression occurs during the non-breeding season in many mammals. This affects spermatogenesis, resulting in decreased or arrested activity. Both lead to a decrease or cessation in sperm production. In recent years, the cellular mechanisms that lead to infertility in males in non-reproductive periods have been studied in very different species of mammals. At the start of the present century, the main mechanism involved was considered as an increase in the apoptotic activity of germ cells during the regression period. The loss of spermatogonia and spermatocytes causes not only a decrease in spermatogenesis, but an arrest of the seminiferous epithelium activity at the end of regression. Recently, in some mammal species, it was found that apoptosis is the usual mechanism involved in epithelium activity arrest, although it is firstly atrophied by massive desquamation of the germ cells that are released from their binding with the Sertoli cells, and which are shed into the lumen of the seminiferous tubule. In other species, it has been shown that not only germ cell apoptosis, but also Sertoli cell apoptosis, including decreased proliferative activity, spermatophagy or autophagy, are involved in testicular regression. Furthermore, the most recent studies indicate that there are multiple patterns of seminiferous epithelium regression in seasonally breeding animals, which may not only be used by different species, but also by the same ones to reproduce in the best conditions, ensuring their survival. In conclusion, at this time, it is not possible to consider the existence of a paradigmatic cellular mechanism in the involution of the seminiferous epithelium applicable to all male mammals with seasonal reproduction, rather the existence of several mechanisms which participate to a greater or lesser extent in each of the species that have been studied to date. Full article
(This article belongs to the Special Issue New Insights in Testicular Biology of Seasonal Breeders)
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