A male-derived nonribosomal peptide pheromone controls female schistosome development.

Schistosomes cause morbidity and death throughout the developing world due to the massive numbers of eggs female worms deposit into the blood of their host. Studies dating back to the 1920s show that female schistosomes rely on constant physical contact with a male worm both to become and remain sexually mature; however, the molecular details governing this process remain elusive. Here, we uncover a nonribosomal peptide synthetase that is induced in male worms upon pairing with a female and find that it is essential for the ability of male worms to stimulate female development. We demonstrate that this enzyme generates ß-alanyl-tryptamine that is released by paired male worms. Furthermore, synthetic ß-alanyl-tryptamine can replace male worms to stimulate female sexual development and egg laying. These data reveal that peptide-based pheromone signaling controls female schistosome sexual maturation, suggesting avenues for therapeutic intervention and uncovering a role for nonribosomal peptides as metazoan signaling molecules.

A spatiotemporal molecular atlas of the ovulating mouse ovary.

Ovulation is essential for reproductive success, yet the underlying cellular and molecular mechanisms are far from clear. Here, we applied high-resolution spatiotemporal transcriptomics to map out cell type- and ovulation stage-specific molecular programs as function of time during follicle maturation and ovulation in mice. Our analysis revealed dynamic molecular transitions within granulosa cell types that occur in tight coordination with mesenchymal cell proliferation. We identified molecular markers for the emerging cumulus cell fate during the preantral-to-antral transition. We describe transcriptional programs that respond rapidly to ovulation stimulation and those associated with follicle rupture, highlighting the prominent roles of apoptotic and metabolic pathways during the final stages of follicle maturation. We further report stage-specific oocyte-cumulus cell interactions and diverging molecular differentiation in follicles approaching ovulation. Collectively, this study provides insights into the cellular and molecular processes that regulate mouse ovarian follicle maturation and ovulation with important implications for advancing therapeutic strategies in reproductive medicine.

Ecological perspectives on female and male reproductive success with competition in two Serapias species.

BACKGROUND AND AIMS: The deceptive strategies by which orchids are pollinated and how these are capable of attracting pollinators remain understudied with regard to their implications for plant fitness. Despite their ecological importance, limited investigations have been conducted on sexual deception and shelter mimicry in orchid species, making this a compelling avenue in orchid biology research. To expand the knowledge of these reproductive mechanisms, we studied the pollination of Serapias lingua and S. parviflora in co-occurring and isolated sites in the Balearic Islands (Spain), further accentuated by the presence of a hybrid, indicating shared pollinators. METHODS: We employed bagging and hand pollination experiments to examine the reproductive biology of the two species. Furthermore, we evaluated the influence of phenotypical and ecological factors on reproductive success, including biometric measurements, reproductive performance and neighbourhood diversity (co-flowering and pollinator communities). KEY RESULTS: Reproductive mechanisms between these two orchid species exhibit substantial disparities. Serapias lingua relies primarily on insect-mediated pollination, while S. parviflora demonstrates self-reproduction capacity. Although events of open pollination are rare, hybridization occurs predominantly when S. lingua is the pollen donor. Fruit set in S. parviflora was positively correlated with plant height, while in S. lingua it was negatively associated with flower size. The coexistence of the two species positively affected pollinium removal in S. parviflora, but did not exert an influence on reproductive traits in S. lingua. Overall, biometric parameters were diminished in isolated compared with co-occurring sites. At the community level, the increased diversity of co-flowering species in the vicinity exhibited an inhibitory effect on pollinium removal in S. parviflora. CONCLUSIONS: Under a context of pollinator loss or phenological mismatch between pollinator presence and flowering, the selfing capacity of S. parviflora would guarantee reproduction whereas S. lingua survival would be compromised. Furthers studies are needed to assess the effects of phenotypical and ecological factors on reproductive success of S. lingua in pollinator-decline scenarios.

As prey and pollinators, insects increase reproduction and allow for outcrossing in the carnivorous plant Dionaea muscipula.

PREMISE: Understanding the factors that limit reproductive success is a key component of plant biology. Carnivorous plants rely on insects as both nutrient sources and pollinators, providing a unique system for studying the effects of both resource and pollen limitation on plant reproduction. METHODS: We conducted a field experiment using wild-growing Dionaea muscipula J. Ellis (Droseraceae) in which we manipulated prey and pollen in a factorial design and measured flower production, number of fruits, and number of seeds. Because understanding reproduction requires knowledge of a plant species' reproductive and pollination biology, we also examined the pollination system, per-visit pollinator effectiveness, and pollen-ovule (P/O) ratio of D. muscipula. RESULTS: Plants that received supplemental prey produced more flowers than control plants. They also had a higher overall fitness estimate (number of flowers × fruit set (total fruits/total flowers) × seeds per fruit), although this benefit was significant only when prey supplementation occurred in the previous growing season. Neither pollen supplementation nor the interaction between pollen and prey supplementation significantly affected overall plant fitness. CONCLUSIONS: This study reinforces the reliance of D. muscipula on adequate prey capture for flower, fruit, and seed production and a mobile pollen vector for reproduction, indicating the importance of considering insects as part of an effective conservation management plan for this species.

A hundred-year-old mystery-the reproductive mode and larval morphology of the enigmatic frog genus Allophryne (Amphibia; Anura; Allophrynidae).

Frogs of the Allophrynidae are an enigmatic family from South America. To date, published information is lacking regarding this group's reproductive biology and larval morphology. Here, we provide the first detailed description of the reproductive mode, developmental mode, and tadpole morphology for Allophryne ruthveni. We developed a captive breeding and rearing protocol for this species and then conducted a series of observations to describe aspects of its reproductive biology. In captivity, this species exhibits aquatic oviposition, where single eggs are laid ungrouped within a simple jelly capsule and are scattered free in the water column before sinking to develop on benthic substrates. We did not observe parental care nor any parental interactions with eggs post-fertilization. Tadpoles are characterized by an oval body, anteroventral oral disc, a labial tooth row formula of 2(2)/3, and a dextral vent tube. The buccopharyngeal cavity is marked by the presence of two pairs of infralabial papilla and four lingual papillae. Cranial morphology is characterized by the presence of the commissura quadratoorbital. This species possesses an additional slip of the m. rectus cervicis and of the m. levator arcuum branchialium III. We discuss our results in comparison with glassfrogs (Centrolenidae).

Nonlinear compartmental modeling to monitor ovarian follicle population dynamics on the whole lifespan.

In this work, we introduce a compartmental model of ovarian follicle development all along lifespan, based on ordinary differential equations. The model predicts the changes in the follicle numbers in different maturation stages with aging. Ovarian follicles may either move forward to the next compartment (unidirectional migration) or degenerate and disappear (death). The migration from the first follicle compartment corresponds to the activation of quiescent follicles, which is responsible for the progressive exhaustion of the follicle reserve (ovarian aging) until cessation of reproductive activity. The model consists of a data-driven layer embedded into a more comprehensive, knowledge-driven layer encompassing the earliest events in follicle development. The data-driven layer is designed according to the most densely sampled experimental dataset available on follicle numbers in the mouse. Its salient feature is the nonlinear formulation of the activation rate, whose formulation includes a feedback term from growing follicles. The knowledge-based, coating layer accounts for cutting-edge studies on the initiation of follicle development around birth. Its salient feature is the co-existence of two follicle subpopulations of different embryonic origins. We then setup a complete estimation strategy, including the study of structural identifiability, the elaboration of a relevant optimization criterion combining different sources of data (the initial dataset on follicle numbers, together with data in conditions of perturbed activation, and data discriminating the subpopulations) with appropriate error models, and a model selection step. We finally illustrate the model potential for experimental design (suggestion of targeted new data acquisition) and in silico experiments.

Long-Term In Vitro Culture Alters Gene Expression Pattern of Genes Involved in Ontological Groups Representing Cellular Processes.

The oviduct provides an optimal environment for the final preparation, transport, and survival of gametes, the fertilization process, and early embryonic development. Most of the studies on reproduction are based on in vitro cell culture models because of the cell's accessibility. It creates opportunities to explore the complexity of directly linked processes between cells. Previous studies showed a significant expression of genes responsible for cell differentiation, maturation, and development during long-term porcine oviduct epithelial cells (POECs) in vitro culture. This study aimed at establishing the transcriptomic profile and comprehensive characteristics of porcine oviduct epithelial cell in vitro cultures, to compare changes in gene expression over time and deliver information about the expression pattern of genes highlighted in specific GO groups. The oviduct cells were collected after 7, 15, and 30 days of in vitro cultivation. The transcriptomic profile of gene expression was compared to the control group (cells collected after the first day). The expression of COL1A2 and LOX was enhanced, while FGFBP1, SERPINB2, and OVGP1 were downregulated at all selected intervals of cell culture in comparison to the 24-h control (p-value < 0.05). Adding new detailed information to the reproductive biology field about the diversified transcriptome profile in POECs may create new future possibilities in infertility treatments, including assisted reproductive technique (ART) programmes, and may be a valuable tool to investigate the potential role of oviduct cells in post-ovulation events.

Folliculectomy for the treatment of pre-ovulatory follicular stasis in three illegally captured West Coast green geckos (Naultinus tuberculatus) to enable wild rehabilitation.

CASE HISTORY: In 2023, the New Zealand Department of Conservation seized 63 endemic reptiles that were being held without a permit. This group included three adult female West Coast green geckos (Naultinus tuberculatus) that had been illegally removed from the wild 2 years earlier. They had been held in an outdoor enclosure with a pair of goldstripe geckos (Woodworthia chrysosiretica). CLINICAL FINDINGS: On physical examination, all three geckos had at least two soft palpable masses in the coelom. Repeated ultrasonographic examination over several months confirmed the diagnosis of pre-ovulatory follicular stasis (POFS) in each gecko, and in subsequent weeks, more ovarian follicles developed in each animal. LABORATORY FINDINGS: All three geckos were negative on culture of cloacal swabs for Salmonella spp., and negative on PCR assay of a cloacal flush for Cryptosporidium spp., despite other reptiles in the seized group showing positive results for multiple Salmonella spp., and one other gecko being positive for Cryptosporidium parvum, subtype IIcA5G3. TREATMENT AND OUTCOME: For all three geckos, para-midline ventral coeliotomy was performed under general anaesthesia, and folliculectomy of degenerate ovarian follicles was performed. Post-operative complications were seen in all three animals, which developed suture-line infections following disruption of normal skin shedding and entrapment of shed keratin in the surgical sites. A second surgery was undertaken to remove impacted keratin and caseous inflammatory material from the surgical wounds of all three animals and buried sutures were placed to close the coelomic wounds. The geckos were treated with 20 mg/kg ceftazidime IM every second day for 2 weeks post-operatively. Subsequent ecdysis (skin shedding) occurred without complication and the geckos were released back to the wild 10 months after admission. CLINICAL RELEVANCE: The recommended treatment for POFS in reptiles is ovariectomy, which is not appropriate for wild animals. The use of folliculectomy to resolve preovulatory follicular stasis should be considered for animals where retaining reproductive ability is essential.

Loss of Avian Intromittent Organs as a Sperm Competition Strategy: A Race to Be Last.

AbstractThe loss of the intromittent organ (IO) in the majority of birds remains unexplained. Here, I propose that IO loss results from sperm competition in the context of the unique avian sperm storage system. The first stage of fertilization is the movement of sperm through the vagina from the site of ejaculation to the sperm storage tubules (SSTs) at the uterovaginal junction. In a second stage, sperm are released from the SSTs and move through the uterus to the site of fertilization in the infundibulum. Last-male fertilization precedence can occur if sperm that arrive later at the uterovaginal junction occupy uterus-side SSTs, which then have a head start in the race to the infundibulum with each ovulation. Under such "last-in, first-out" conditions, there is strong sperm competition to arrive later at the SSTs. Consequently, the optimal male strategy would be placement of the ejaculate at the cloacal opening to allow any other sperm in the vagina to reach the SSTs first. Cloacal placement is effectively achieved by loss of the IO. The evolution of altricial development in Neoaves, the largest clade that lacks IOs, created conditions that favor IO loss. Specifically, the smaller clutch sizes and hatching asynchrony of altricial birds increase the intensity of sperm competition for fertilization of early eggs in the laying sequence and thus the selective advantage of later arrival at the SSTs. The rarity of IO loss among all animals suggests that the complex mechanism of avian fertilization creates unique conditions for sperm competition.

Advances in the study of microbiota in reproductive biology: A short review of recent research, following Leclaire et al. (2022).

Research on microbiota dynamics in humans (Gilbert et al., 2018), model organisms (Douglas, 2019), and free-ranging, wild animals (Grond et al., 2018) has taken off in the past decades, and even in nonmodel organisms, research has already shifted from initial characterization studies to those examining associations with behaviour and fitness (Bodawatta et al., 2022; Corl et al., 2020; Risely et al., 2018; Turjeman et al., 2020). The microbiota is known to change through pregnancy and parturition (Koren et al., 2012), and there is also evidence in humans that infertility may be associated with microbiota composition (Silva & Giacobini, 2019), but how the microbiota is related to reproductive fitness in free-ranging species is largely understudied or primarily focused on pathogen transmission (sexually transmitted infection) (Lombardo, 1998; Sheldon, 1993). In a From the Cover article in this issue of Molecular Ecology, Leclaire et al. (2022) begin to tease apart the relationship between the microbiota and reproductive fitness using the black-legged kittiwake (Rissa tridactyla) as their study species. Following characterization of the microbiota in multiple body sites of breeders and nonbreeders, they discovered that breeding and nonbreeding females had distinct microbiota, that higher performing female breeders had lower abundances of potentially pathogenic taxa, and that feathers of these birds were characterized by reduced microbiota diversity compared to low-performance breeders. Leclaire and her colleagues provide some of the first evidence of body-wide differences in microbiota composition in relation to breeding status. Their research further supports the relationship between the microbiota and host fitness, and additional studies focusing on this topic can continue to unravel intricacies in host-microbiota-reproductive strategy evolution (Comizzoli et al., 2021; Rowe et al., 2020). Here, I review the results of Leclaire et al. (2022) and provide a wider context for their research by reviewing other studies in the field, focusing on avian species.

Comparative floral development in male and female plants of Palmer amaranth (Amaranthus palmeri).

PREMISE: Characterizing the developmental processes in the transition from hermaphroditism to unisexuality is crucial for understanding floral evolution. Amaranthus palmeri, one of the most devastating weeds in the United States, is an emerging model system for studying a dioecious breeding system and understanding the biological traits of this invasive weed. The objectives of this study were to characterize phases of flower development in A. palmeri and compare organogenesis of flower development in female and male plants. METHODS: Flower buds from male and female plants were dissected for light microscopy. Segments of male and female inflorescences at different stages of development were cut longitudinally and visualized using scanning electron microscopy. RESULTS: Pistillate flowers have two to three styles, one ovary with one ovule, and five obtuse tepals. Staminate flowers have five stamens with five acute tepals. Floral development was classified into 10 stages. The distinction between the two flower types became apparent at stage four by the formation of stamen primordia in staminate flowers, which developed female and male reproductive organs initially, as contrasted to pistillate flowers, which produced carpel primordia only. In staminate flowers, the putative carpel primordia changed little in size and remained undeveloped. CONCLUSIONS: Timing of inappropriate organ termination varies across the two sexes in A. palmeri. Our study suggests that the evolution of A. palmeri from a cosexual ancestral state to complete dioecy is still in progress since males exhibited transient hermaphroditism and females produced strictly pistillate flowers.

Multi-omics perspective on studying reproductive biology in Daphnia sinensis.

Daphnia sinensis is a widespread freshwater microcrustacean. The assembled D. sinensis genome totaled 131.58 Mb with 92.23% of the assembly anchored onto 10 chromosomes. Based on the whole genome information, we further compared the transcriptomic and epigenomic characterization among parthenogenetic females, sexual females and males in D. sinensis. Transcriptomic analysis showed that the up-regulated genes in males were mainly grouped into the cuticle, sex differentiation and methyl farnesoate synthesis, which might play a pivotal role in steering development and reproduction processes. By comparison, the highly expressed genes in parthenogenetic females were mainly grouped into energy metabolism, mitosis, and DNA replication, which might contribute to maintaining rapid production of parthenogenetic females, and nutrient uptake for the growth of neonates. The whole-genome DNA methylation analysis showed that the methylation rate in parthenogenetic females was higher than that in sexual females and males, which might contribute to its rapid response to environment stress.

First evidence of multiple paternity in the blue shark (Prionace glauca).

Multiple paternity (MP) is defined as the behaviour in which females successfully mate with multiple males leading to offspring from different sires within the same litter. MP seems to be frequent and an evolutionary advantage in elasmobranchs. Here the authors report for the first time the occurrence of MP in the cosmopolitan blue shark Prionace glauca L. The evidence, gathered via microsatellite genotyping of pregnant females and their embryos, suggests that MP is very frequent in this species. Knowledge of MP in P. glauca should help describe more precisely its reproductive biology and contribute to the management of its populations.

Alternative reproductive tactics in goby fishes of the Caspian Sea.

Here we report on the reproductive morphology and histology of three Gobiidae species (the Caspian monkey goby, Neogobius pallasi; the Caspian goby, Neogobius caspius; and the round goby, Neogobius melanostomus) from the Iranian coastline of the Caspian Sea. Based on ageing, reproductive histology, and internal and external morphological measures, it appears that all three of these goby species have two types of reproductive males, a large courting, territorial, male type and a small cuckolding parasitic male type, a phenomenon known as alternative reproductive tactics (ART). Although ARTs have been reported previously for one of these species, the round goby, all reports stem from its invasive range; ARTs have never been reported before in any fish species in the Caspian Sea. In all three goby species there was a large, older male type, with a wide head, dark body colouration, and a large investment in accessory glands (AG), an organ important for female attraction and parental care. But there was also a small, light, younger male type, with a narrow head, longer urogenital papilla, and little investment in AGs. The Caspian goby were the largest of the three species, and in this species the smaller, lighter, presumably cuckolding male morph was quite rare (only about 5% of the reproductive male population). In contrast, many of the round goby and monkey goby males were the small, lighter parasitic type, making up nearly half the population of reproductive males (48% and 40%, respectively). Round goby and Caspian goby males had a prominent mesorchial gland, a fibrous sheath of pheromone-releasing connective tissue that attaches the testes to the dorsal body wall, but all the monkey goby specimens examined lacked this structure. Although ARTs are well documented across fish species and appear to be particularly common in gobies, our study provides the first evidence for ARTs in goby fishes from the Caspian Sea.

Inclusion and exclusion in the history of developmental biology.

Scientific disciplines embody commitments to particular questions and approaches, scopes and audiences; they exclude as well as include. Developmental biology is no exception, and it is useful to reflect on what it has kept in and left out since the field was founded after World War II. To that end, this article sketches a history of how developmental biology has been different from the comparative, human and even experimental embryologies that preceded it, as well as the embryology that was institutionalized in reproductive biology and medicine around the same time. Early developmental biology largely excluded evolution and the environment, but promised to embrace the entire living world and the whole life course. Developmental biologists have been overcoming those exclusions for some years, but might do more to deliver on the promises while cultivating closer relations, not least, to reproductive studies.

Progress in modern reproductive biology research in China†.

Reproductive biology is closely associated with human health and social progress. Modern reproductive biology research in China began in the 1930s. Advances in science, technology, government support, and international collaborations spawned the rapid growth of reproductive biology research in China. While the development of reproductive biology has provided both theoretical knowledge and applicable technologies, it has also generated new social and ethical concerns. This review summarizes and highlights the contributions of modern reproductive biology research in China, with a specific focus on aspects that are most related to human reproduction and health.

Catalyzing momentum in male contraceptive development†.

Globally, nearly half of all pregnancies are unplanned. Male contraceptives offer the potential to decrease unintended pregnancy and introduce contraceptive equity, but decades of research have yet to bring a novel product to market. New funding avenues from the philanthropic sector seek to stimulate research in male contraceptives through investments, grants, and support for trainees alongside other programs that encourage product development and ultimately commercialization. This Forum outlines the purpose of and funding opportunities provided by Male Contraceptive Initiative, a funding agency and non-profit focused on the advancement of non-hormonal, reversible contraceptive technologies for those who produce sperm.

Altmetric and bibliometric analysis of influential articles in reproductive biology, 1980-2019.

RESEARCH QUESTION: What are the most influential articles in reproductive biology journals from 1980 to 2019 according to Altmetric Attention Score (AAS), number of citations and Relative Citation Ratio (RCR)? DESIGN: Cross-sectional study of reproductive biology articles indexed in the National Institutes of Health Open Citation Collection from 1980 to 2019. Data were downloaded on 20 May 2021. The 100 articles with highest AAS, RCR and number of citations were analysed. RESULTS: Twenty-one reproductive biology journals were identified, including 120,069 articles published from 1980 to 2019. In total 227 reproductive biology classics were identified due to some overlap between the three lists. Compared with the 100 articles with the highest AAS (after excluding articles featured on both lists), the 100 top-cited articles were older (2014 versus 2001, mean difference [95% confidence interval] 13.5 [11.5, 15.5]), less likely to be open access (64% versus 85%), more likely to be reviews (42% versus 12%) and less likely to be observational studies (9% versus 51%) and randomized clinical trials (0% versus 5%). These same trends were observed in analyses comparing the 100 articles with highest AAS to the 100 articles with highest RCR. The most common topic was assisted reproduction, but prominent topics included infertility for top AAS articles, reproductive technology in animals for top-cited articles, and polycystic ovary syndrome for top RCR articles. CONCLUSIONS: Formerly, influential articles in reproductive biology journals were evaluated by absolute citation rates and subject to limitations of conventional bibliometric analysis. This is the first comprehensive study to use altmetrics and citation-based metrics to identify reproductive biology classics.

Nuclear Receptors in Ovarian Function.

The ovary undergoes cycles of hormone production that regulate physiological changes necessary for folliculogenesis, ovulation and luteinisation, ultimately contributing to female reproductive success. Crucial to these biological processes is stage-specific nuclear receptor signalling. While the transcriptional regulatory roles of steroid receptors in female fertility and especially ovarian functions have long been documented, non-steroid receptors also play an important part in regulating gene expression at various stages of ovarian development. The recent application of high-throughput genomic and transcriptomic technologies has begun to shed light on the molecular mechanisms underlying ovarian nuclear receptor actions and pointed to a complex interplay between highly specific transcription co-regulators as well as between nuclear receptors in mediating mutual as well as unique target genes. Interrelationships between nuclear receptors as well as the involvement of context-specific protein and non-protein co-regulators are likely keys to the precise and specific nuclear receptor action in the ovary. Leveraging such knowledge on the nuclear receptor network is especially valuable in the development of novel fertility treatments as well as female contraceptives.

New observations of the endangered giant freshwater whipray, Urogymnus polylepis, provide further evidence for its distribution and breeding in the north-east coast of India.

The present study reports observations of 13 giant freshwater whipray (Urogymnus polylepis) from commercial fish landings along the north-east coast of India and updates existing records based on field observations and local social media reports. The disc width of the landed specimens ranged from 120 to 223 cm and they weighed 95-300 kg. All 13 specimens observed were mature (nine females and four males) and three females were pregnant, with embryo numbers ranging between 4 and 15. Globally, U. polylepis is listed as 'Endangered', and greater protection measures are needed in India to assist in reversing current population declines.