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In addition to companion animals and laboratory species, about 270 carnivore species play fundamental ecological roles in different ecosystems. However, almost 40% of carnivore species are now threatened or endangered in the wild because of human activities. While protection of natural habitats is critical, it is equally important to better understand carnivore reproduction, including a solid knowledge in sperm, oocyte, and embryo biology, to maintain sustainable populations in the wild and in conservation breeding centers. Characterizing gamete and embryo biology is also needed to develop cryopreservation and assisted reproductive technologies to enhance conservation efforts. The objective of this review is to provide the most recent knowledge in the biology of sperm cells, oocytes, and early embryos across all carnivore families. Overall, most data originate from populations maintained in breeding centers or zoos. Characterizations of sperm biology and cryopreservation are far more advanced than for oocytes and embryos. Currently, sperm biology is mainly studied in Canids, Felids, Ursids, and Mustelids, with more emphasis on structural than functional properties. Importantly, fundamental studies of gamete and embryo biology in domestic dogs, cats, and ferrets have paved the way for more precise characterizations in wild counterparts as well as the development of cryopreservation and assisted reproductive technologies. A striking feature of spermatozoa across a wide range of Canids and Felids is the presence of teratospermia (60% of abnormal sperm cells), which is related to the loss of genetic diversity in some populations. Although sperm structures differ across carnivore families, sperm biology remains difficult to compare because of the small amount of data in many species. Regarding oocyte biology and embryology, data are much scarcer than in sperm cells, with too few studies going beyond structural descriptions. More carnivore species and more individuals (especially from wild populations in addition to captive ones) must be studied to improve our understanding about comparative germplasm biology and develop adequate conservation breeding strategies including the use of cryobanking and assisted reproductive technologies.

To participate in fertilization and embryo development, oocytes stored within the mammalian female ovary must resume meiosis as they are arrested in meiotic prophase I. This ability to resume meiosis, known as meiotic competence, requires the tight regulation of cellular metabolism and chromatin configuration. Previously, we identified nuclear proteins associated with the transition from the pre-antral to the antral follicular stage, the time at which oocytes gain meiotic competence. In this study, the objective was to specifically investigate three candidate nuclear factors: bromodomain containing protein 2 (BRD2), nucleophosmin 1 (NPM1), and asparaginase-like 1 (ASRGL1). Although these three factors have been implicated with folliculogenesis or reproductive pathologies, their requirement during oocyte maturation is unproven in any system. Experiments were conducted using different stages of oocytes isolated from adult cat ovaries. The presence of candidate factors in developing oocytes was confirmed by immunostaining. While BRD2 and ASRGL1 protein increased between pre-antral and the antral stages, changes in NPM1 protein levels between stages were not observed. Using protein inhibition experiments, we found that most BRD2 or NPM1-inhibited oocytes were incapable of participating in fertilization or embryo development. Further exploration revealed that inhibition of BRD2 and NPM-1 in cumulus-oocyte-complexes prevented oocytes from maturing to the metaphase II stage. Rather, they remained at the germinal vesicle stage or arrested shortly after meiotic resumption. We therefore have identified novel factors playing critical roles in domestic cat oocyte meiotic competence. The identification of these factors will contribute to improvement of domestic cat assisted reproduction and could serve as biomarkers of meiotically competent oocytes in other species.

The development of highly differentiated sperm cells that are specialized for navigating to and fusing with an oocyte is essential for sexual reproduction. As a major part of differentiation, sperm undergo extensive post-meiotic maturation en route to the oocyte. This is regulated largely by soma-derived cues. In Caenorhabditis elegans, this process is called sperm activation, and it transforms immotile spermatids into migratory fertilization-competent cells. Here, we show that the negative regulator of sperm activation, SWM-1, is produced in an unexpected cell type: body wall muscle. SWM-1 is secreted into the body cavity and enters the gonad; there, it is present with its likely target, TRY-5, a spermiogenesis activator. We show that, in addition to SWM-1, the somatic gonad and body fluid can exchange other factors, suggesting that soma-germ line transfer could affect other reproductive processes. In addition, we show that SWM-1 may have a separate role in the sperm migratory environment, to which it is contributed by both males and hermaphrodites. These findings reveal that late stages in gamete differentiation can be regulated at the whole-organism level by broadly secreted factors. This article has an associated ‘The people behind the papers’ interview.

The development of highly differentiated sperm cells that are specialized for navigating to and fusing with an oocyte is essential for sexual reproduction. As a major part of differentiation, sperm undergo extensive post-meiotic maturation en route to the oocyte. This is regulated largely by soma-derived cues. In Caenorhabditis elegans , this process is called sperm activation, and it transforms immotile spermatids into migratory fertilization-competent cells. Here, we show that the negative regulator of sperm activation, SWM-1, is produced in an unexpected cell type: body wall muscle. SWM-1 is secreted into the body cavity and enters the gonad; there, it is present with its likely target, TRY-5, a spermiogenesis activator. We show that, in addition to SWM-1, the somatic gonad and body fluid can exchange other factors, suggesting that soma-germ line transfer could affect other reproductive processes. In addition, we show that SWM-1 may have a separate role in the sperm migratory environment, to which it is contributed by both males and hermaphrodites. These findings reveal that late stages in gamete differentiation can be regulated at the whole-organism level by broadly secreted factors. This article has an associated ‘The people behind the papers’ interview.

Competition among sperm to fertilize oocytes is a ubiquitous feature of sexual reproduction as well as a profoundly important aspect of sexual selection. However, little is known about the cellular mechanisms sperm use to gain competitive advantage or how these mechanisms are regulated genetically. In this study, we utilize a forward genetic screen in Caenorhabditis elegans to identify a gene, comp-1, whose function is specifically required in competitive contexts. We show that comp-1 functions in sperm to modulate their migration through and localization within the reproductive tract, thereby promoting their access to oocytes. Contrary to previously described models, comp-1 mutant sperm show no defects in size or velocity, thereby defining a novel pathway for preferential usage. Our results indicate not only that sperm functional traits can influence the outcome of sperm competition, but also that these traits can be modulated in a context-dependent manner depending on the presence of competing sperm.