Hybridization in the Anthropocene - how pollution and climate change disrupt mate selection in freshwater fish.

Chemical pollutants and/or climate change have the potential to break down reproductive barriers between species and facilitate hybridization. Hybrid zones may arise in response to environmental gradients and secondary contact between formerly allopatric populations, or due to the introduction of non-native species. In freshwater ecosystems, field observations indicate that changes in water quality and chemistry, due to pollution and climate change, are correlated with an increased frequency of hybridization. Physical and chemical disturbances of water quality can alter the sensory environment, thereby affecting chemical and visual communication among fish. Moreover, multiple chemical compounds (e.g. pharmaceuticals, metals, pesticides, and industrial contaminants) may impair fish physiology, potentially affecting phenotypic traits relevant for mate selection (e.g. pheromone production, courtship, and coloration). Although warming waters have led to documented range shifts, and chemical pollution is ubiquitous in freshwater ecosystems, few studies have tested hypotheses about how these stressors may facilitate hybridization and what this means for biodiversity and species conservation. Through a systematic literature review across disciplines (i.e. ecotoxicology and evolutionary biology), we evaluate the biological interactions, toxic mechanisms, and roles of physical and chemical environmental stressors (i.e. chemical pollution and climate change) in disrupting mate preferences and inducing interspecific hybridization in freshwater fish. Our study indicates that climate change-driven changes in water quality and chemical pollution may impact visual and chemical communication crucial for mate choice and thus could facilitate hybridization among fishes in freshwater ecosystems. To inform future studies and conservation management, we emphasize the importance of further research to identify the chemical and physical stressors affecting mate choice, understand the mechanisms behind these interactions, determine the concentrations at which they occur, and assess their impact on individuals, populations, species, and biological diversity in the Anthropocene.

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.

A social learning primacy trend in mate-copying: an experiment in Drosophila melanogaster.

Social learning is learning from the observation of how others interact with the environment. However, in nature, individuals often need to process serial social information and may favour either the most recent information (recency bias), constantly updating knowledge to match the environment, or the information that appeared first in the series (primacy bias), which may slow down adjustment to environmental change. Mate-copying is a widespread form of social learning in a mate choice context related to conformity in mate choice, and where a naive individual develops a preference for a given mate (or mate phenotype) seen being chosen by conspecifics. Mate-copying is documented in most vertebrate taxa and in the fruit fly Drosophila melanogaster. Here, we tested experimentally whether female fruit flies show a primacy or a recency bias by presenting pictures of a female copulating with one of two contrastingly coloured male phenotypes. We found that after two sequential contradictory demonstrations, females show a tendency to prefer males of the phenotype preferred in the first demonstration, suggesting that mate-copying in D. melanogaster is not based on the most recently observed mating and may be influenced by a form of primacy bias.

Asymmetric mate preference and reproductive interference mediate climate-induced changes in mate availability in a small mammal hybrid zone.

Range expansion and contraction are among the most common biotic responses to changing environmental conditions, yet much is to be learned about the mechanisms that underlie range-edge population dynamics, especially when those areas are points of secondary contact between closely related species. Here, we present field-measured parentage data that document the reproductive outcomes of changes in mate availability at a secondary contact zone between two species of woodrat in the genus Neotoma. Changes in mate availability resulted from drought-driven differential survival between the species and their hybrids. As the availability of conspecific mates declined, rates of hybridization increased, leading to the accumulation of admixed individuals in the zone of contact. Patterns of reproductive success in the wild appear to be the result of a combination of both pre-mating isolation and post-zygotic selection resulting from genomic incompatibilities between the parental lineages. Evidence of asymmetric mate preference between the parental lineages came from both skewed reproductive output in the field and laboratory preference trials. Moreover, partial genomic incompatibility was evident from the near-zero reproductive success of F1 males and because nearly all surviving hybrids had one pure parent. Nonetheless, high reproductive success of F1 females and backcrossing in both parental directions allow for introgression between the parental species. These findings reveal how climate change may alter evolutionary outcomes for species at the edge of their ranges through an interplay of behavioral, demographic, and genetic mechanisms.

Beyond Simple vs Complex: Exploring the Nuanced and Unexpected Effects of Spatial Environmental Complexity on Mating Patterns and Female Fecundity.

The features of the physical environment set the stage upon which sexual selection operates, and consequently can have a significant impact on variation in realized individual fitness, and influence a population's evolutionary trajectory. This phenomenon has been explored empirically in several studies using fruit flies (Drosophila melanogaster) which have found that changing the spatial complexity of the mating environment influenced male-female interaction dynamics, (re)mating rates and realized female fecundities. However, these studies did not explore mating patterns, which can dramatically alter the genetic composition of the next generation, and frequently only compared a single, small "simple" environment to a single larger "complex" environment. While these studies have shown that broadly changing the characteristics of the environment can have big effects on reproductive dynamics, the plasticity of this outcome to more subtle changes has not been extensively explored. Our study set out to compare patterns of mating and courtship between large- and small-bodied males and females, and female fecundities in both a simple environment and two distinctly different spatially-complex environments. We found that realized offspring production patterns differed dramatically between all three environments, indicating that the effects of increasing spatial complexity on mating outcomes are sensitive to the specific type of environmental complexity. Furthermore, we observed female fecundities were higher for flies in both complex environments compared those in the simple environment, supporting its role as a mediator of sexual conflict. Together, these results show that the union of gametes within a population can be greatly influenced by the specific spatial features of the environment and that while some outcomes of increased environmental complexity are likely generalizable, other phenomena like mating patterns and courtship rates may vary from one complex environment to another.

Sexual conflict and sexual networks in bed bugs: the fitness cost of traumatic insemination, female avoidance and male mate choice.

Sexual conflict is prevalent among animals and is primarily caused by the fact that the optimal mating rates are often higher in males than in females. While there is a growing appreciation that females can also gain from multiple matings, we still know relatively little about which sex controls the observed mating rates and how close it is to the optimal female mating rates. To address this issue, we tracked female bed bugs (Cimex lectularius) inseminated daily versus weekly and found that weekly inseminated females lived longer and produced over 50% more offspring. In a follow-up experiment employing a social network framework, we placed 24 bed bugs into a semi-naturalistic arena and recorded all sexual interactions. While recently inseminated females did not avoid males more often, they were more frequently rejected by males. Finally, we tracked avoidance behaviour in a single cohort of female bed bugs as they received six successive daily inseminations. Avoidance rates increased and insemination durations decreased with increasing number of prior inseminations. Overall, our results indicate high costs of polyandry. Although females possess some plastic avoidance strategies, the observed rates of insemination fall closer to the male rather than female optimum.

Fake news? The impact of information mismatch on mating behaviour.

Multiple cues are often used for mate choice in complex environments, potentially entailing mismatches in the information conveyed by different sources. We address the consequences of this information mismatch for receivers using the spider mite Tetranychus urticae, in which virgin females are highly valuable mates compared to mated females, given first male sperm precedence. Accordingly, males are known to prefer virgins and distinguish them using cues from the females themselves and that they leave on the substrate. Whereas cues from females are highly reliable, those left on the substrate may not reflect the real female mating status if females move and/or mate. Here, we tested the consequences of such mismatch by exposing males to mated or virgin females on patches previously impregnated with cues deposited by females of either mating status. Male mating attempts were solely affected by substrate cues while female acceptance and the number of mating events were independently affected by both cues. Copulation duration, in contrast, depended mainly on the mating status of the female, with the number of copulations and the total time spent mating being intermediate in environments with mismatched information. We also show that males incur mating costs, reflected in reduced survival in environments with virgin cues. These results suggest that substrate cues left by females are instrumental for males to find their mates. However, in environments with mismatched information, males may pay survival costs without the associated benefit of mating with virgins, or they may lose opportunities to mate with virgins by responding to substrate cues from mated females. The benefit of using multiple cues will then hinge upon the frequency of information mismatch, which itself should vary with the dynamics of populations.

Synthesis of sexual selection: a systematic map of meta-analyses with bibliometric analysis.

Sexual selection has been a popular subject within evolutionary biology because of its central role in explaining odd and counterintuitive traits observed in nature. Consequently, the literature associated with this field of study became vast. Meta-analytical studies attempting to draw inferences from this literature have now accumulated, varying in scope and quality, thus calling for a synthesis of these syntheses. We conducted a systematic literature search to create a systematic map with a report appraisal of meta-analyses on topics associated with sexual selection, aiming to identify the conceptual and methodological gaps in this secondary literature. We also conducted bibliometric analyses to explore whether these gaps are associated with the gender and origin of the authors of these meta-analyses. We included 152 meta-analytical studies in our systematic map. We found that most meta-analyses focused on males and on certain animal groups (e.g. birds), indicating severe sex and taxonomic biases. The topics in these studies varied greatly, from proximate (e.g. relationship of ornaments with other traits) to ultimate questions (e.g. formal estimates of sexual selection strength), although the former were more common. We also observed several common methodological issues in these studies, such as lack of detailed information regarding searches, screening, and analyses, which ultimately impairs the reliability of many of these meta-analyses. In addition, most of the meta-analyses' authors were men affiliated to institutions from developed countries, pointing to both gender and geographical authorship biases. Most importantly, we found that certain authorship aspects were associated with conceptual and methodological issues in meta-analytical studies. Many of our findings might simply reflect patterns in the current state of the primary literature and academia, suggesting that our study can serve as an indicator of issues within the field of sexual selection at large. Based on our findings, we provide both conceptual and analytical recommendations to improve future studies in the field of sexual selection.

Cost of mate choice: Changing patterns of global age disparity in marriage and their consequences to women's health including maternal mortality and menopause.

BACKGROUND: Consistent across cultures and throughout time is the male preference for younger females. Given its prevalence, the mate choice theory proposes that age-disparate relationships may have contributed to the evolution of maternal mortality and menopause. OBJECTIVES: The objective is to document evidence for age disparity in marriage from past and present populations and evaluate their relevance to maternal mortality and menopause. DESIGN: Cross-sectional data were collected from various regions and time points, ranging from the Roman era to the current decade. METHODS: To analyze both the age disparity in marriage and age at marriage, data were collected from Ancestry.ca for Quebec, Massachusetts, India, South Africa, and England and Wales. Additional data were taken from the United Nations as a more recent and comprehensive source. To analyze the relationships between age disparity in marriage and different social factors, data on gross domestic product, maternal mortality rates, fertility, primary school enrollment, child marriage rates, and percentage of women in the total labor force were collected from the World Health Organization, World Bank, and United Nations International Children's Emergency Fund. RESULTS: The results showed that males were significantly older than females at first marriage in all populations and time frames sampled, supporting the assumption underlying the mate choice theory. Maternal mortality rates were strongly associated with age-disparate relationships, increasing by 275 per 100,000 live births for each additional year in the age disparity. CONCLUSION: The results from this study provide support for the assumption underlying the mate choice theory of maternal mortality and menopause.

Changing patterns of global age disparity in marriage provide support for the mate choice theory of menopause, raising the possibility of a gradual shift in delayed reproduction and delayed menopause. Living things have inherent capacity to survive and reproduce until they die, with one exception: humans. Women go through menopause while men remain fertile. Among the many explanations offered for the origin of menopause, grandmother hypothesis is the leading one. Being too old to reproduce, it is argued, grandmothers stop reproducing and make up for the loss of fitness through helping (grand mothering) their grand offspring. There are two problems with this theory: first, grand mothering and menopause need not be connected, and second, grandmothers cannot be simultaneously too old to reproduce and not too old to be able to gather resources to make up for their loss of fitness. We proposed a mate choice theory of menopause which posits that human mating system is non-random, that is, males have preference for younger females, depriving older females from reproduction and allowing deleterious fertility mutations to accumulate giving rise to menopause. Male preference for younger females is consistent across cultures and dominates all social relations affecting mate choice including monogamy, serial monogamy, widowers remarrying, polygamy, harem, and others. In this study, we wanted to test if male preference for younger females has been widespread through time. We collected data on age disparity in marriage from past and present populations, from Roman era to the current decade, and evaluated their relevance to the origin of maternal mortality and menopause. The results showed that males were significantly older than females at first marriage in all populations and time frames sampled, supporting the assumption underlying the mate choice theory of menopause. Maternal mortality rates were strongly associated with age­disparate relationships, increasing by 275 per 100,000 live births for each additional year in the age disparity. Through repeated cycles of widowers marring younger women, maternal mortality would have functioned as a reinforcer of the origin of menopause.

Visual Attention to Evolutionarily Relevant Information by Heterosexual Men and Women While Viewing Mock Online Dating Profiles.

The way people create social connections and access information has been altered greatly by technology in recent decades. Online browsing of visual profiles has become a common means for seeking potential partners for both short- and long-term relationships. Little is known, however, about how people prioritize mate quality information while viewing online profiles. Using eye-tracking methods and self-report, this study investigated how people evaluated profile-based facial attractiveness and text-based financial resources information, represented by income and occupation. Heterosexual male and female participants, aged between 18 and 27 years, viewed opposite-sex profiles while their eye-movements were recorded using a remote eye-tracking camera. In line with current theory, resources information had little effect on men's overall attention to women's faces, whereas women's overall attention to men's faces varied depending on the level of income and occupation. Women evaluated men's faces more when income and occupation were low, regardless of attractiveness. Unexpectedly, however, men marginally increased their attention toward unattractive women who showed a high-level of income and more esteemed occupation. Men self-reported a higher interest in women for a short-term relationship and women self-reported a higher interest in men for a long-term relationship. This work provides a foundation to further examine how people browse profile-based information and to investigate the mate selection process, with real-world implications for online dating app users, profile design, and content.

Mate choice in the brain: species differ in how male traits 'turn on' gene expression in female brains.

Mate choice plays a fundamental role in speciation, yet we know little about the molecular mechanisms that underpin this crucial decision-making process. Stickleback fish differentially adapted to limnetic and benthic habitats are reproductively isolated and females of each species use different male traits to evaluate prospective partners and reject heterospecific males. Here, we integrate behavioural data from a mate choice experiment with gene expression profiles from the brains of females actively deciding whether to mate. We find substantial gene expression variation between limnetic and benthic females, regardless of behavioural context, suggesting general divergence in constitutive gene expression patterns, corresponding to their genetic differentiation. Intriguingly, female gene co-expression modules covary with male display traits but in opposing directions for sympatric populations of the two species, suggesting male displays elicit a dynamic neurogenomic response that reflects known differences in female preferences. Furthermore, we confirm the role of numerous candidate genes previously implicated in female mate choice in other species, suggesting evolutionary tinkering with these conserved molecular processes to generate divergent mate preferences. Taken together, our study adds important new insights to our understanding of the molecular processes underlying female decision-making critical for generating sexual isolation and speciation.

The role of male quality in sequential mate choice: pregnancy replacement in small mammals?

Females mainly increase their reproductive success by improving the quality of their mates and need to be discriminative in their mate choices. Here, we investigate whether female mammals can trade up sire quality in sequential mate choice during already progressed pregnancies. A male-induced pregnancy termination (functional 'Bruce effect') could thus have an adaptive function in mate choice as a functional part of a pregnancy replacement. We used bank voles (Myodes glareolus) as a model system and exchanged the breeding male in the early second trimester of a potential pregnancy. Male quality was determined using urine marking values. Females were offered a sequence of either high- then low-quality male (HL) or a low- then high-quality male (LH). The majority of females bred with high-quality males independent of their position in the sequence, which may indicate a pregnancy replacement in LH but not in HL. The body size of the second male, which could have been related to the coercion of females by males into remating, did not explain late pregnancies. Thus, pregnancy replacement, often discussed as a counterstrategy to infanticide, may constitute adaptive mate choice in female mammals, and female choice may induce pregnancy replacement in mammals.

Testing Sexual Strategy Theory in Norway.

Choosing a romantic partner for a long-term relationship is one of the most significant decisions one makes during our lifetime. We have inherited an evolved framework from our ancestors that contains traits, as well as preferences for these traits, to solve this task. We use this framework consciously or unconsciously to choose prospective romantic partners. Following this reasoning, sexual strategy theory (SST) has been proposed for predicting which traits women and men prefer in a romantic partner for a long-term relationship. These predictions were empirically tested in the current work based on a sample of 1193 Norwegian adolescents who responded to an online questionnaire. We implemented the study hypotheses, derived from SST, in three statistical models, which were tested using structural equation modeling. In brief, our results revealed that women only valued resources more than men when we controlled for materialistic traits. This finding contrasts with SST's prediction that women would value resources more than men, independently of other variables. As for the second prediction that men value physical attractiveness more than women, this pattern existed universally and was independent of, for instance, how egalitarian they were. We thus conclude that SST was only partially supported and that variables that may reflect societal circumstances (e.g., wealth, gender, equality) should be considered when examining the mate choice behavior of women and men. The theoretical and practical implications of the study are also discussed.

Wolbachia affect female mate preference and offspring fitness in a parasitoid wasp.

BACKGROUND: Wolbachia are widespread intracellular bacteria in insects that often have high rates of spread due to their impact on insect reproduction. These bacteria may also affect the mating behavior of their host with impacts on the fitness of host progeny. In this study, we investigated the impact of Wolbachia on a preference for mating with young or old males in the parasitoid wasp Habrobracon hebetor. RESULTS: Our results showed that uninfected females from a tetracycline-treated line preferred to mate with young males, whereas Wolbachia-infected females had no preference. Time to mating was relatively shorter in the infected lines. Regardless of Wolbachia infection status, progeny resulting from matings with young males showed higher fitness than those from crosses with old males, and infected females crossed with infected young males showed the highest performance. CONCLUSION: These results suggest an impact of Wolbachia on female mate preference and offspring fitness although it is unclear how this phenomenon increases Wolbachia transmission of infected wasps. © 2024 Society of Chemical Industry.

Female Mate Choice in Wild Kenyan Blue Monkeys (Cercopithecus mitis).

Female mate choice may drive sexual selection, but discerning whether female behaviors reflect free expression of choice or responses to constraints can be difficult. We investigated the efficacy of female choice in wild blue monkeys using 10 years of behavior and paternity data (N = 178 male-female dyads). Although blue monkeys live modally in one-male polygynous groups, where male-biased intersexual power is expected, females can access multiple potential mates during seasonal male influxes and occasional intergroup encounters. Additionally, extra-group males sire offspring. We examined female resistance rates to male-initiated sexual interactions, and unsolicited proceptive behavior that females directed to males (corrected for male availability). Females seldom resisted male solicitation, but initiated sexual interactions more than males. Females generally preferred residents. Those who preferred non-residents tended to have residents with longer tenures, but neither female parity nor rank influenced the tendency to prefer non-residents vs. residents. The male most solicited by a particular female fathered that female's infant 82% of the time; odds of siring were 26 times higher for most vs. nonpreferred males. Female preference predicted paternity even more strongly among non-resident males, with odds of siring 33 times higher for most vs. nonpreferred non-residents. Neither female rank nor parity influenced her likelihood of having her preferred partner as sire. Paternity by preferred males did not affect infant survival. While we cannot fully discount the effect of male-male competition on paternity, these results suggest that blue monkey females can exercise choice successfully, even in a polygynous mating system.

Measuring the Efficiency of Purging by non-random Mating in Human Populations.

Human populations harbor a high concentration of deleterious genetic variants. Here, we tested the hypothesis that non-random mating practices affect the distribution of these variants, through exposure in the homozygous state, leading to their purging from the population gene pool. To do so, we produced whole-genome sequencing data for two pairs of Asian populations exhibiting different alliance rules and rates of inbreeding, but with similar effective population sizes. The results show that populations with higher rates of inbred matings do not purge deleterious variants more efficiently. Purging therefore has a low efficiency in human populations, and different mating practices lead to a similar mutational load.

Females adopt sexual catalepsy to facilitate mating.

Theory predicts that males and females of dioecious species typically engage in an evolutionary sexual conflict over the frequency and choice of mating partner. Female sexual cannibalism, a particularly dramatic illustration of this conflict, is widespread in certain animal taxa including spiders. Nevertheless, females of some funnel weaving spiders that are generally aggressive to conspecifics enter a cataleptic state after male courtship, ensuring the males can mate without risk of attack. In this study, we demonstrated that the physical posture and duration, metabolites, and central neurotransmitters of females of Aterigena aculeata in sexual catalepsy closely resemble females in thanatosis but are distinct from those in anesthesia, indicating that the courted females feign death to eliminate the risk of potentially aggressive responses and thereby allow preferred males to mate. Unlike the taxonomically widespread thanatosis, which generally represents a deceptive visual signal that acts against the interest of the receivers, sexual catalepsy of females in the funnel weaving spiders may deliver a sexual-receptive signal to the courting males and thereby benefit both the signal senders and receivers. Therefore, sexual catalepsy in A. aculeata may not reflect a conflict but rather a confluence of interest between the sexes.

How music-induced emotions affect sexual attraction: evolutionary implications.

More than a century ago, Darwin proposed a putative role for music in sexual attraction (i.e., sex appeal), a hypothesis that has recently gained traction in the field of music psychology. In his writings, Darwin particularly emphasized the charming aspects of music. Across a broad range of cultures, music has a profound impact on humans' feelings, thoughts and behavior. Human mate choice is determined by the interplay of several factors. A number of studies have shown that music and musicality (i.e., the ability to produce and enjoy music) exert a positive influence on the evaluation of potential sexual partners. Here, we critically review the latest empirical literature on how and why music and musicality affect sexual attraction by considering the role of music-induced emotion and arousal in listeners as well as other socio-biological mechanisms. Following a short overview of current theories about the origins of musicality, we present studies that examine the impact of music and musicality on sexual attraction in different social settings. We differentiate between emotion-based influences related to the subjective experience of music as sound and effects associated with perceived musical ability or creativity in a potential partner. By integrating studies using various behavioral methods, we link current research strands that investigate how music influences sexual attraction and suggest promising avenues for future research.

The quantitative genetic basis of variation in sexual versus non-sexual butterfly wing colouration: autosomal, Z-linked, and maternal effects.

Viability indicator traits are expected to be integrated extensively across the genome yet sex-limited to ensure that any benefits are sexually concordant. Understanding how such expectations are accommodated requires elucidating the quantitative genetic architecture of candidate traits in and across the sexes. Here we applied an animal modelling approach to partition the autosomal, allosomal, and direct maternal bases of variation in sexual versus non-sexual dorsal wing colouration in the butterfly Eurema hecabe. The sexual colour trait-coherently scattered ultraviolet that is under strong directional selection due to female choice-is brighter and more expansive in males, and overlays non-sexual pigmentary yellow markings that otherwise dominate both wing surfaces in each sex. Our modelling estimated high and sexually equivalent autosomal variances for ultraviolet reflectance (furnishing h2 ~ 0.58 overall and ~0.75 in males), accompanied by smaller but generally significant Z-linked and maternal components. By contrast, variation in non-sexual yellow was largely attributed to Z-linked sources. Intersexual genetic correlations based upon the major source of variation in each trait were high and not different from 1.0, implying regulation by a pool of genes common to each sex. An expansive autosomal basis for ultraviolet is consistent with its hypothesized role as a genome-wide viability indicator and ensures that both sons and daughters will inherit their father's attractiveness.

Sexual selection and speciation in the Anthropocene.

Anthropogenic change threatens global biodiversity by causing severe ecological disturbance and extinction. Here, we consider the effects of anthropogenic change on one process that generates biodiversity. Sexual selection (a potent evolutionary force and driver of speciation) is highly sensitive to the environment and, thus, vulnerable to anthropogenic ecological change. Anthropogenic alterations to sexual display and mate preference can make it harder to distinguish between conspecific and heterospecific mates or can weaken divergence via sexual selection, leading to higher rates of hybridization and biodiversity loss. Occasionally, anthropogenically altered sexual selection can abet diversification, but this appears less likely than biodiversity loss. In our rapidly changing world, a full understanding of sexual selection and speciation requires a global change perspective.