Mating Partners Research Articles

Impaired pheromone detection and abnormal sexual behavior in female mice deficient for ancV1R.

Ancient vomeronasal receptor type-1 (ancV1R), a putative vomeronasal receptor, is highly conserved across a wide range of vertebrates and is expressed in the majority of vomeronasal sensory neurons, co-expressing with canonical vomeronasal receptors, V1Rs and V2Rs. The pseudogenization of ancV1R is closely associated with vomeronasal organ (VNO) degeneration, indicating its critical role in pheromone sensing. However, the specific role of ancV1R remains unknown. In this study, to elucidate the function of ancV1R, we conducted phenotypic analyses of ancV1R-deficient female mice. Behavioral analyses showed that ancV1R-deficient females exhibited rejective responses toward male sexual behavior and displayed no preference for male urine. Physiological analyses demonstrate that the loss-of-function mutation of ancV1R reduced VNO response to various pheromone cues, including male urine, the sexual enhancing pheromone exocrine gland-secreting peptide 1 (ESP1), and β-estradiol 3-sulfate. Pre-exposure to ESP1 did not overcome the rejection behavior caused by ancV1R deficiency. Analysis of neural activity in the vomeronasal system revealed increased responses in the medial amygdala and posteromedial cortical amygdala of mutant females upon contact with males but not in response to male urine alone. Additionally, upon male contacts, ancV1R-deficient females exhibited increased neural activity in the lateral septum, a stress-associated brain region, along with elevated stress hormone levels. Such effects were not observed in females exposed solely to male urine. These findings suggest that, in females, ancV1R facilitates VNO responses to pheromone stimuli and plays a crucial role in perceiving males as mating partners. The absence of ancV1R results in failure of male perception, leading to abnormal sexual behaviors and stress responses upon male contact.

The significance of social interactions in synchronized swarming flight in a termite.

In social insects, individuals of working caste coordinate their actions to manage various collective tasks. Such collective behaviours exist not only in workers but also in winged reproductives (alates). During certain seasons, newly emerged alates fly from the nest to disperse and find mating partners in a synchronized manner. This 'swarming' behaviour is one of the collective behaviours that involve the greatest number of individuals in social insects. However, such synchronization is considered to be caused by the response to specific environmental cues rather than behavioural coordination among colony members. Here, we show that a termite Reticulitermes kanmonensis shows synchronized dispersal flight among alates within the same colony even under the constant temperature environment. Under the semi-field environment with fluctuating temperatures, alates within the same colony synchronized their dispersal flight under higher temperatures, while flight was suppressed under lower temperatures. We observed that termites synchronized their dispersal flights even under constant temperature conditions in the laboratory (20℃), indicating that environmental cues are not always necessary for synchronization. In either case, higher synchronization happened with a larger number of alates. These results suggest that social factors interplay with environmental cues to enable the synchronized swarming flight of social insects.

Function and evolution of Ir52 receptors in mate detection in Drosophila

Identifying a suitable mating partner is an ancient and critical biological problem. How a fruit fly distinguishes a fly of the same species from flies of innumerable related species remains unclear. We analyze the Ir52 receptors, expressed in taste neurons on the fly legs and encoded by a cluster of genes. We find that the cluster shows dynamic evolution, rapidly expanding and contracting over evolutionary time. We develop a novel invivo expression system and find that Ir52 receptors respond differently to pheromone extracts of different fly species. The receptors are activated by some compounds and inhibited by others, with different receptors showing distinct response profiles. Circuit mapping shows that Ir52 neurons are pre-synaptic to sexually dimorphic neurons that overlap with neurons acting in courtship behavior. Our results support a model in which Ir52 receptors detect information about the species of a potential mating partner.

Fight, retreat, repeat: The male-male agonistic behavior in the wood-feeding cockroach, Panesthia angustipennis spadica (Dictyoptera: Blattodea: Blaberidae).

Competition is one of the most critical factors affecting animal behaviors. Aggressive interactions are central to acquiring resources or mating partners. Agonistic behavior is more common among males than females. Although laboratory observations of these behaviors give detailed descriptions under controlled conditions, field observations without human intervention are required because those supply information that provides insights into their function. In this paper, we report on the field observation and auxiliary laboratory experiments of male-male agonistic behavior of a wood-feeding cockroach, Panesthia angustipennis, and discuss its strategy. In the field, a male pushed the opponent with the horn on the pronotum out of a gap between two logs, under which a female was. After pushing, the male repeatedly returned to a place close to the female, even if it did not subdue the opponent entirely. It suggests that the male-male agonistic behavior in P. angustipennis has both attack and avoidance. The bout was repeated as the ejected male reapproached the male. In contrast, the inferior male often escaped in the laboratory recording after field observation. Keeping the fighting experience for several days may contribute to the males avoiding a "losing battle." This study significantly enhances our understanding of the mating strategy of P. angustipennis through male-male agonistic behavior and provides possibilities for its cognitive aspects from the fighting experience.

Assortativity in sympatric speciation and species classification

We investigate the role of assortative mating in speciation using the sympatric model of Derrida and Higgs. The model explores the idea that genetic differences create incompatibilities between individuals, preventing mating if the number of such differences is too large. Speciation, however, only happens in this mating system if the number of genes is large. Here we show that speciation with small genome sizes can occur if assortative mating is introduced. In our model individuals are represented by three chromosomes: one responsible for reproductive compatibility, one for coding the trait on which assortativity will operate, and a neutral chromosome. Reproduction is possible if individuals are genetically similar with respect to the first chromosome, but among these compatible mating partners, the one with the most similar trait coded by the second chromosome is selected. We show that this type of assortativity facilitates speciation, which can happen with a small number of genes in the first chromosome. Species, classified according to reproductive isolation, dictated by the first chromosome, can display different traits values, as measured by the second and the third chromosomes. Therefore, species can also be identified based on similarity of the neutral trait, which works as a proxy for reproductive isolation.

A behavioral syndrome of competitiveness in a non-social rodent

Animals compete for limited resources such as food, mating partners, and territory. The outcome of this intraspecific competition should be determined by individual variation in behavioral traits, such as aggressiveness and dominance status. Consistent among-individual differences in behavior likely contribute to competitiveness and predispose individuals to acquire specific dominance ranks during parts of their adult life. Nevertheless, how dominance rank is correlated with animal personality traits remains largely unclear. In a first step towards better understanding these functional links, we studied trait integration into behavioral syndromes, using 26 captive male bank voles (Myodes glareolus). We repeatedly assessed boldness in an emergence test, exploration in an open-field test, aggressiveness in staged dyadic encounters, and the among-individual correlations between these behaviors. We further related these personality traits to dominance rank, from quantifying urine marking value (UMV), as marking in bank voles is related to dominance rank. We found repeatable variations in boldness, exploration, aggressiveness, and UMV, which were correlated at the among-individual level. Aggressiveness tended to be negatively correlated with body condition, a proxy for fitness. Thus, key personality traits and social rank are functionally integrated into a behavioral syndrome of intraspecific competitiveness. By joining social and non-social aspects of personality, our findings contribute to the ecological validation of personality traits and suggest how they contribute to higher-order component traits, such as dominance which directly affect fitness components.

Mosquitoes integrate visual and acoustic cues to mediate conspecific interactions in swarms

Male mosquitoes form aerial aggregations, known as swarms, to attract females and maximize their chances of finding a mate. Within these swarms, individuals must be able to recognize potential mates and navigate the social environment to successfully intercept a mating partner. Prior research has almost exclusively focused on the role of acoustic cues in mediating the male mosquito's ability to recognize and pursue females. However, the role of other sensory modalities in this behavior has not been explored. Moreover, how males avoid collisions with one another in the swarm while pursuing females remains poorly understood. In this study, we combined free-flight and tethered-flight simulator experiments to demonstrate that swarming Anopheles coluzzii mosquitoes integrate visual and acoustic information to track conspecifics and avoid collisions. Our tethered experiments revealed that acoustic stimuli gated mosquito steering responses to visual objects simulating nearby mosquitoes, especially in males that exhibited a strong response toward visual objects in the presence of female flight tones. Additionally, we observed that visual cues alone could trigger changes in mosquitoes' wingbeat amplitude and frequency. These findings were corroborated by our free-flight experiments, which revealed that Anopheles coluzzii modulate their thrust-based flight responses to nearby conspecifics in a similar manner to tethered animals, potentially allowing for collision avoidance within swarms. Together, these results demonstrate that both males and females integrate multiple sensory inputs to mediate swarming behavior, and for males, the change in flight kinematics in response to multimodal cues might allow them to simultaneously track females while avoiding collisions.

Wasted Efforts Impair Random Search Efficiency and Reduce Choosiness in Mate-Pairing Termites.

AbstractRandom search theories predict that animals employ movement patterns that optimize encounter rates with target resources. However, animals are not always able to achieve the best search strategy. Energy depletion, for example, limits searchers' movement activities, forcing them to adjust their behaviors before and after encounters. Here, we investigate the cost of mate search in a termite, Reticulitermes speratus, and reveal that the costs associated with mate finding reduce the selectivity of mating partners. After a dispersal flight, termites search for a mating partner with limited reserved energy. We found that their movement activity and diffusiveness progressively declined over extended mate search. Our data-based simulations qualitatively confirmed that the reduced movement diffusiveness decreased the searching efficiency. Also, prolonged search periods reduced survival rate and the number of offspring. Thus, mate search has two different negative effects on termites. Finally, we found that termites with an extended mate search reduced the selectivity of mating partners, where males immediately paired with any encountering females. Thus, termites dramatically changed their mate search behavior depending on their internal states. Our finding highlights that accounting for the searchers' internal states is essential to fill the gap between random search theories and empirical behavioral observations.

Mutations and Differential Transcription of Mating-Type and Pheromone Receptor Genes in Hirsutella sinensis and the Natural Cordyceps sinensis Insect-Fungi Complex.

Sexual reproduction in ascomycetes is controlled by the mating-type (MAT) locus. (Pseudo)homothallic reproduction has been hypothesized on the basis of genetic data from Hirsutella sinensis (Genotype #1 of Ophiocordyceps sinensis). However, the differential occurrence and differential transcription of mating-type genes in the MAT1-1 and MAT1-2 idiomorphs were found in the genome and transcriptome assemblies of H. sinensis, and the introns of the MAT1-2-1 transcript were alternatively spliced with an unspliced intron I that contains stop codons. These findings reveal that O. sinensis reproduction is controlled at the genetic, transcriptional, and coupled transcriptional-translational levels. This study revealed that mutant mating proteins could potentially have various secondary structures. Differential occurrence and transcription of the a-/α-pheromone receptor genes were also found in H. sinensis. The data were inconsistent with self-fertilization under (pseudo)homothallism but suggest the self-sterility of H. sinensis and the requirement of mating partners to achieve O. sinensis sexual outcrossing under heterothallism or hybridization. Although consistent occurrence and transcription of the mating-type genes of both the MAT1-1 and MAT1-2 idiomorphs have been reported in natural and cultivated Cordyceps sinensis insect-fungi complexes, the mutant MAT1-1-1 and α-pheromone receptor transcripts in natural C. sinensis result in N-terminal or middle-truncated proteins with significantly altered overall hydrophobicity and secondary structures of the proteins, suggesting heterogeneous fungal source(s) of the proteins and hybridization reproduction because of the co-occurrence of multiple genomically independent genotypes of O. sinensis and >90 fungal species in natural C. sinensis.

Natural variation in sexual traits and gene expression between selfing and outcrossing Arabidopsis lyrata suggests sexual selection at work.

Flowering plants show significant diversity in sexual strategies, profoundly impacting the evolution of sexual traits and associated genes. Sexual selection is one of the primary evolutionary forces driving sexual trait variation, particularly evident during pollen-pistil interactions, where pollen grains compete for fertilization and females select mating partners. Multiple mating may intensify competition among pollen donors for siring, while in contrast, self-fertilization reduces sire-sire competition, relaxing the sexual selection pressure. Traits involved in male-male competition and female choice are well described, and molecular mechanisms underlying pollen development and pollen-pistil interactions have been extensively studied in the model species Arabidopsis thaliana. However, whether these molecular mechanisms are involved in sexual selection in nature remains unclear. To address this gap, we measured intrinsic pollen performance and its interaction with female choice, and investigated the associated gene expression patterns in a selfing and an outcrossing population of Arabidopsis lyrata. We found that pollen germination and pollen tube growth were significantly higher in outcrossers than selfers, and this difference was accompanied by changes in expression of genes involved in vesicle transport and cytoskeleton. Outcrosser mother plants showed a negative impact on pollen tube growth compared to selfer mother plants, together with a difference of expression for genes involved in auxin and stress response, suggesting a potential mechanism for female choice through molecular crosstalk at the post-pollination stage. Our study provides insight on the impact of sexual selection on the evolution of sexual gene expression in plants.

Sex-specific discrimination of familiar and unfamiliar mates in the Tokay gecko

Social animals need to keep track of other individuals in their group to be able to adjust their behaviour accordingly and facilitate group cohesion. This recognition ability varies across species and is influenced by cognitive capacities such as learning and memory. In reptiles, particularly Squamates (lizards, snakes, and worm lizards), chemical communication is pivotal for territoriality, reproduction, and other social interactions. However, the cognitive processes underlying these social interactions remain understudied. In our study, we examined the ability of male and female Tokay geckos (Gekko gecko) to chemically differentiate familiar and unfamiliar mating partners. Our findings suggest that both sexes can make this distinction, with males responding more to the odour of a familiar mate, and females responding more to unfamiliar mates. The lizards maintained their discriminatory abilities for two to three weeks but not up to six weeks after separation. This research highlights the efficacy of using odours as social stimuli for investigating social cognition in lizards, a promising avenue to better understand social cognition in these animals.

Lie to me to lay with me: Females deceive males via terminal investment.

Historically, males have frequently been portrayed as the manipulative and deceptive gender, while females are often seen as adopting a coy and passive role. In this context, it is proposed that males use a terminal investment strategy, misleading females about their true poor condition, while females passively opt to mate with these deceptive males. However, we hypothesize that females in suboptimal condition may also engage in a terminal investment strategy by mimicking or enhancing their attractiveness to match that of females in better conditions. We studied this hypothesis in Tenebrio molitor, by subjecting females to three varying doses of lipopolysaccharides of Escherichia coli (LPS; 0.25, 0.5, or 1 mg ml-1), or three doses of the pro-oxidant Paraquat (PQ; 20, 40 or 80 mM), and subsequently assessing their survival and attractiveness to males. The LPS treatments and 20 mM of PQ had no significant effect on the survival or attractiveness of the females. However, females treated with 40 or 80 mM PQ survived fewer days compared to the control group. Those injected with 40 mM were more attractive than their control counterparts, while those treated with 80 mM were less attractive. Since the identical doses of LPS, which induce terminal investment in males, had no effect on females, we suggest sexual dimorphism in terminal investment. Furthermore, similar to males, if the stressor reaches a sufficiently high level, the signal becomes honest. These findings highlight how the quantity of stressors influences support for the terminal investment strategy in both males and females. Notably, this study challenges prevailing notions regarding gender roles in sexual selection, indicating that females, not just males, conceal their poor condition to attract mating partners.

Genetic Links between Reproductive Traits and Amino Acid Pairwise Distances of Swine Leukocyte Antigen Alleles among Mating Partners in Microminipigs.

Previously, we found that a greater dissimilarity in swine leukocyte antigen (SLA) class I and class II alleles between mating partners resulted in increased farrowing rates in a highly inbred population of Microminipigs (MMPs). In this follow-up study, we have analyzed the effects of dissimilarity in SLA alleles between mating partners for seven different reproductive traits, including litter size and the number of stillborn and live or dead weaned piglets. We determined the relationships among reproductive traits within each mating event and the amino acid distances of SLA alleles as markers of diversity between mating partners. Our results indicate that mating partners with greater amino acid pairwise genetic distances in the SLA-1 class I gene or DQB1 class II gene alleles were associated with significantly larger litter sizes and higher numbers of live piglets at birth and weaning. Also, partners with greater pairwise distances in the SLA-2 class I gene alleles exhibited fewer pre-weaning deaths. These findings suggest that the dissimilarity in SLA class I and class II alleles between mating partners may affect not only farrowing rates but also other key reproductive traits such as litter size and improved piglet survival rates. Consequently, SLA alleles could serve as valuable genetic markers for selecting mating partners in breeding programs and for conducting epistatic studies on various reproductive traits in MMPs.

Love bites: males of lizards prefer to mate with conspecifics, but do not disdain parthenogens

Abstract Parthenogenesis has been discovered in a great number of reptiles, indicating that parthenogens can outcompete bisexual species and hybridize with them. This raises intriguing questions: how do parthenogenetic species coexist with gonochoristic relatives, and what outcome does this coexistence produce? To answer these two questions, we studied relationships between male rock lizards, Darevskia valentini, and parthenogenetic Darevskia armeniaca. We compared social and sexual reactions of males to females of their own species and parthenogenetic D. armeniaca and vice versa. We found that females of both species basked together with males and demonstrated mostly submissive behaviour. Females of D. valentini were less aggressive towards males in the mixed-species population than in the single-species population, suggesting female competition for males. The proportion of successful and unsuccessful mating attempts with females of bisexual and unisexual species was equal, and we found no significant differences in male reactions to bisexual and unisexual females in sympatry. The proportion of females bearing mating scars on their venters and the number of these scars per female were greater in the bisexual species. This indicates that females of the bisexual species were more attractive than parthenogenetic females as mating partners to males. We found no triploid hybrids among the offspring of parthenogenetic females that mated with males in the mixed population. Our findings suggest that parthenogenetic species might outcompete bisexual species by mating with males and integrating into the social system.

Sexually antagonistic coevolution of the male nuptial gift and female feeding behaviour in decorated crickets.

The evolution of nuptial gifts has traditionally been considered a harmonious affair, providing benefits to both mating partners. There is growing evidence, however, that receiving a nuptial gift can be actively detrimental to the female. In decorated crickets (Gryllodes sigillatus), males produce a gelatinous spermatophylax that enhances sperm transfer but provides little nutritional benefit and hinders female post-copulatory mate choice. Here, we examine the sexually antagonistic coevolution of the spermatophylax and the female feeding response to this gift in G. sigillatus maintained in experimental populations with either a male-biased or female-biased adult sex ratio. After 25 generations, males evolving in male-biased populations produced heavier spermatophylaxes with a more manipulative combination of free amino acids than those evolving in female-biased populations. Moreover, when the spermatophylax originated from the same selection regime, females evolving in male-biased populations always had shorter feeding durations than those evolving in female-biased populations, indicating the evolution of greater resistance. Across populations, female feeding duration increased with the mass and manipulative combination of free amino acids in the spermatophylax, suggesting sexually antagonistic coevolution. Collectively, our work demonstrates a key role for interlocus sexual conflict and sexually antagonistic coevolution in the mating system of G. sigillatus.

The role of promiscuous molecular recognition in the evolution of RNase-based self-incompatibility in plants

How do biological networks evolve and expand? We study these questions in the context of the plant collaborative-non-self recognition self-incompatibility system. Self-incompatibility evolved to avoid self-fertilization among hermaphroditic plants. It relies on specific molecular recognition between highly diverse proteins of two families: female and male determinants, such that the combination of genes an individual possesses determines its mating partners. Though highly polymorphic, previous models struggled to pinpoint the evolutionary trajectories by which new specificities evolved. Here, we construct a novel theoretical framework, that crucially affords interaction promiscuity and multiple distinct partners per protein, as is seen in empirical findings disregarded by previous models. We demonstrate spontaneous self-organization of the population into distinct “classes” with full between-class compatibility and a dynamic long-term balance between class emergence and decay. Our work highlights the importance of molecular recognition promiscuity to network evolvability. Promiscuity was found in additional systems suggesting that our framework could be more broadly applicable.

Sperm competition favours intermediate sperm size in a hermaphrodite1.

Sperm competition is a potent mechanism of postcopulatory sexual selection that has been found to shape reproductive morphologies and behaviours in promiscuous animals. Especially sperm size has been argued to evolve in response to sperm competition through its effect on sperm longevity, sperm motility, the ability to displace competing sperm, and ultimately fertilization success. Additionally, sperm size has been observed to co-evolve with female reproductive morphology. Theoretical work predicts that sperm competition may select for longer sperm but may also favour shorter sperm if sperm size trades-off with number. In this study, we studied the relationship between sperm size and postmating success in the free-living flatworm, Macrostomum lignano. Specifically, we used inbred isolines of M. lignano that varied in sperm size to investigate how sperm size translated into the ability of worms to transfer and deposit sperm in a mating partner. Our results revealed a hump-shaped relationship with individuals producing sperm of intermediate size having the highest sperm competitiveness. This finding broadens our understanding of the evolution of sperm morphology by providing empirical support for stabilizing selection on sperm size under sperm competition.

Experiments with a set of cooperative enrichment devices used by groups of Indo-Pacific bottlenose dolphins

Dolphins in the wild cooperate to find food, gain and maintain access to mating partners, look after their young ones, or for the sheer joy of play. Under human care, environmental enrichments provide mental and physical stimulation and opportunities for the dolphins to practice their natural abilities. In this review, I focus on a set of enrichment devices we designed for cooperative problem-solving. They allowed the dolphins to utilize and improve their cognitive skills, leading to improved socialization within the group. While the devices provided appropriate challenges to the dolphins, they also allowed the investigation of the impact of demographic and social factors on the cooperative actions. We found that age and relatedness had no impact on cooperation; in turn, cooperation increased with group size. In addition, during the use of these cognitive enrichments, partner preference and intersexual differences were revealed in cooperative actions. The novel multi-partner devices were not only used by dolphin pairs but also by dolphin trios and quartets, providing evidence for group-level cooperation. In addition, a novel food-sharing device was used prosocially by dolphin pairs. Finally, the introduction of these cognitive enrichments leads to measurable short- and long-term welfare improvement. Thus, the use of these cognitive enrichments paired with systematic data collection bridged science with welfare. Future studies will investigate intersexual differences in independent groups, the emergence and function of cooperative interactions, and the socio-dynamics using cognitive enrichments.

Is promiscuity the key? Multiple paternity in the garden dormouse (Eliomys quercinus)

Many mammals have a promiscuous mating system with multiple sired litters. Promiscuity can increase the genetic variability, reduce the risk of inbreeding, and increase the effective population size, and is therefore crucial for preventing genetic loss and maintaining adaptability. This is particularly true for small and threatened populations. The garden dormouse (Eliomys quercinus) is a threatened species, which exhibited a drastic decline over the last 20–30 years. The aim of this study was therefore to investigate the mating system of the garden dormouse in mountain forest habitat by parentage analyses using 5 polymorphic microsatellite markers combined with morphometric data and information about the nesting behavior. Genetic parentage analyses revealed that 64% (9 of 14) of the litters were sired by at least two males, suggesting that garden dormice have a promiscuous mating system. The genetic findings were further supported by indirect indicators of promiscuity, such as testes, that were nearly four times larger than predicted for a rodent of its body mass and only slight male biased sexual size dimorphism. The finding of a promiscuous mating system in garden dormice should be taken into account in future conservation efforts. Due to its habitat preferences and limited dispersal potential garden dormice are vulnerable to forest fragmentation. The connection of suitable habitats facilitates dispersal and promotes access to potential mating partners, which could be especially important for populations colonizing new habitats. Access to potential mates may also reduce inbreeding, loss of genetic variability which is crucial for populations viability and survival.

Localized Expression of Olfactory Receptor Genes in the Olfactory Organ of Common Minke Whales.

Baleen whales (Mysticeti) possess the necessary anatomical structures and genetic elements for olfaction. Nevertheless, the olfactory receptor gene (OR) repertoire has undergone substantial degeneration in the cetacean lineage following the divergence of the Artiodactyla and Cetacea. The functionality of highly degenerated mysticete ORs within their olfactory epithelium remains unknown. In this study, we extracted total RNA from the nasal mucosae of common minke whales (Balaenoptera acutorostrata) to investigate ORs' localized expression. All three sections of the mucosae examined in the nasal chamber displayed comparable histological structure. However, the posterior portion of the frontoturbinal region exhibited notably high OR expression. Neither the olfactory bulb nor the external skin exhibited the expression of these genes. Although this species possesses four intact non-class-2 ORs, all the ORs expressed in the nasal mucosae belong to class-2, implying the loss of aversion to specific odorants. These anatomical and genomic analyses suggest that ORs are still responsible for olfaction within the nasal region of baleen whales, enabling them to detect desirable scents such as prey and potential mating partners.