Size-assortative mating and sexual size dimorphism are predictable from simple mechanics of mate-grasping behavior

Background  

A major challenge in evolutionary biology is to understand the typically complex interactions between diverse counter-balancing factors of Darwinian selection for size assortative mating and sexual size dimorphism. It appears that rarely a simple mechanism could provide a major explanation of these phenomena. Mechanics of behaviors can predict animal morphology, such like adaptations to locomotion in animals from various of taxa, but its potential to predict size-assortative mating and its evolutionary consequences has been less explored. Mate-grasping by males, using specialized adaptive morphologies of their forelegs, midlegs or even antennae wrapped around female body at specific locations, is a general mating strategy of many animals, but the contribution of the mechanics of this wide-spread behavior to the evolution of mating behavior and sexual size dimorphism has been largely ignored.     

A comparison of heterosexual and homosexual mating preferences in personal advertisements

Human heterosexual mating preferences have been shown to conform to predictions drawn from evolutionary theory, with men and women adopting broadly distinct strategies. Attempts to reconcile sexual selection theory with homosexual behavior have been less consistent, however, and have largely focussed on addressing two alternative perspectives: (i) that gay men and lesbians display phenotypic traits in common with opposite sex heterosexual individuals or (ii) that homosexual individuals display sex-typical, or exaggerated sex-typical phenotypes. Testing these hypotheses is complicated by sampling issues involved in the study of human sexual orientation, since obtaining standardized and comparable samples of heterosexual and non-heterosexual mating preferences is a prerequisite to analysis. Here we present a comparison of homosexual and heterosexual mating strategies in men and women using a sample of 1733 personal (‘lonely hearts’) adverts gathered from a single source. We used principal components analysis in order to expose underlying structure of the advertisements, and identify three components involving relative emphasis placed on resources, physical attractiveness and personality when offering or seeking mate characteristics. While homosexual individuals are shown to resemble their own-sex heterosexual counterparts in terms of emphasis placed on partner physical attractiveness relative to partner personality, no clear pattern emerges in other aspects of advertisement strategy. Nevertheless, there we find no evidence in support of the hypothesis that homosexual men and women are intrinsically opposite-sex typical in terms of mate preferences.     

“Women Are Better Than Men”–Public Beliefs on Gender Differences and Other Aspects in Multitasking

Reports in public media suggest the existence of a stereotype that women are better at multitasking than men. The present online survey aimed at supporting this incidental observation by empirical data. For this, 488 participants from various ethnic backgrounds (US, UK, Germany, the Netherlands, Turkey, and others) filled out a self-developed online-questionnaire. Results showed that overall more than 50% of the participants believed in gender differences in multitasking abilities. Of those who believed in gender differences, a majority of 80% believed that women were better at multitasking. The main reasons for this were believed to be an evolutionary advantage and more multitasking practice in women, mainly due to managing children and household and/or family and job. Findings were consistent across the different countries, thus supporting the existence of a widespread gender stereotype that women are better at multitasking than men. Further questionnaire results provided information about the participants’ self-rated own multitasking abilities, and how they conceived multitasking activities such as childcare, phoning while driving, and office work.     

Environmentally realistic exposure to the herbicide atrazine alters some sexually selected traits in male guppies

Male mating signals, including ornaments and courtship displays, and other sexually selected traits, like male-male aggression, are largely controlled by sex hormones. Environmental pollutants, notably endocrine disrupting compounds, can interfere with the proper functioning of hormones, thereby impacting the expression of hormonally regulated traits. Atrazine, one of the most widely used herbicides, can alter sex hormone levels in exposed animals. I tested the effects of environmentally relevant atrazine exposures on mating signals and behaviors in male guppies, a sexually dimorphic freshwater fish. Prolonged atrazine exposure reduced the expression of two honest signals: the area of orange spots (ornaments) and the number of courtship displays performed. Atrazine exposure also reduced aggression towards competing males in the context of mate competition. In the wild, exposure levels vary among individuals because of differential distribution of the pollutants across habitats; hence, differently impacted males often compete for the same mates. Disrupted mating signals can reduce reproductive success as females avoid mating with perceptibly suboptimal males. Less aggressive males are at a competitive disadvantage and lose access to females. This study highlights the effects of atrazine on ecologically relevant mating signals and behaviors in exposed wildlife. Altered reproductive traits have important implications for population dynamics, evolutionary patterns, and conservation of wildlife species.     

New‐age ideas about age‐old sex: separating meiosis from mating could solve a century‐old conundrum

Ever since Darwin first addressed it, sexual reproduction reigns as the ‘queen’ of evolutionary questions. Multiple theories tried to explain how this apparently costly and cumbersome method has become the universal mode of eukaryote reproduction. Most theories stress the adaptive advantages of sex by generating variation, they fail however to explain the ubiquitous persistence of sexual reproduction also where adaptation is not an issue. I argue that the obstacle for comprehending the role of sex stems from the conceptual entanglement of two distinct processes – gamete production by meiosis and gamete fusion by mating (mixis). Meiosis is an ancient, highly rigid and evolutionary conserved process identical and ubiquitous in all eukaryotes. Mating, by contrast, shows tremendous evolutionary variability even in closely related clades and exhibits wonderful ecological adaptability. To appreciate the respective roles of these two processes, which are normally linked and alternating, we require cases where one takes place without the other. Such cases are rather common. The heteromorphic sex chromosomes Y and W, that do not undergo meiotic recombination are an evolutionary test case for demonstrating the role of meiosis. Substantial recent genomic evidence highlights the accelerated rates of change and attrition these chromosomes undergo in comparison to those of recombining autosomes. I thus propose that the most basic role of meiosis is conserving integrity of the genome. A reciprocal case of meiosis without bi‐parental mating, is presented by self‐fertilization, which is fairly common in flowering plants, as well as most types of apomixis. I argue that deconstructing sex into these two distinct processes – meiosis and mating – will greatly facilitate their analysis and promote our understanding of sexual reproduction.     

Assortative mating and the evolution of desirability covariation

Mate choice lies close to differential reproduction, the engine of evolution. Patterns of mate choice consequently have power to direct the course of evolution. Here we provide evidence suggesting one pattern of human mate choice—the tendency for mates to be similar in overall desirability—caused the evolution of a structure of correlations that we call the d factor. We use agent-based models to demonstrate that assortative mating causes the evolution of a positive manifold of desirability, d, such that an individual who is desirable as a mate along any one dimension tends to be desirable across all other dimensions. Further, we use a large cross-cultural sample with n = 14,478 from 45 countries around the world to show that this d-factor emerges in human samples, is a cross-cultural universal, and is patterned in a way consistent with an evolutionary history of assortative mating. Our results suggest that assortative mating can explain the evolution of a broad structure of human trait covariation.     

The unexpected mating system of the androdioecious barnacle Chelonibia testudinaria (Linnaeus 1758)

Androdioecy was first described by Darwin in his seminal work on barnacle diversity; he identified males and hermaphrodites in the same reproductive population. Today, we realize that many androdioecious plants and animals share astonishing similarities, particularly with regard to their evolutionary history and mating system. Notably, these species were ancestrally dioecious, and their mating system has the following characteristics: hermaphrodites self‐fertilize frequently, males are more successful in large mating groups, and males have a mating advantage. A male mating advantage makes androdioecy more likely to persist over evolutionary times. Androdioecious barnacles, however, appear to persist as an outlier with a different evolutionary trajectory: they originate from hermaphroditic species. Although sexual systems of androdioecious barnacles are known, no information on the mating system of androdioecious barnacles is available. This study assessed the mating system of the androdioecious barnacle Chelonibia testudinaria. In contrast to other androdioecious species, C. testudinaria does not self‐fertilize, males do not have a mating advantage over hermaphrodites, and the average mating group is quite small, averaging only three individuals. Mating success is increased by proximity to the mate and penis length. Taken together, the mating system of C. testudinaria is unusual in comparison with other androdioecious plants and animals, and the lack of a male mating advantage suggests that the mating system alone does not provide an explanation for the maintenance of androdioecy in this species. Instead, we propose that sex‐specific life history equalizes male and hermaphroditic overall fitness.     

The tempo and mode of three-dimensional morphological evolution in male reproductive structures

Various evolutionary forces may shape the evolution of traits that influence the mating decisions of males and females. Phenotypic traits that males and females use to judge the species identify of potential mates should evolve in a punctuated fashion, changing significantly at the time of speciation but changing little between speciation events. In contrast, traits experiencing sexual selection or sexually antagonistic interactions are generally expected to change continuously over time because of the directional selection pressures imposed on one sex by the actions of the other. To test these hypotheses, we used spherical harmonic representations of the shapes of male mating structures in reconstructions of the evolutionary tempo of these structures across the history of the Enallagma damselfly clade. Our analyses show that the evolution of these structures is completely consistent with a punctuated model of evolutionary change and a constant evolutionary rate throughout the clade's history. In addition, no interpopulation variation in shape was detected across the range of one species. These results indicate that male mating structures in this genus are used primarily for identifying the species of potential mates and experience little or no selection from intraspecific sexual selection or sexual antagonism. The implications of these results for speciation are discussed.     

Variations in sexual behavior among capuchin monkeys function for conspecific mate recognition: a phylogenetic analysis and a new hypothesis for female proceptivity in tufted capuchins

Researchers of capuchin monkeys have noted stereotyped body postures, facial expressions, and vocalizations that accompany copulations in this genus. Notable variations in these sexual behaviors are observed across capuchin species. Although several hypotheses exist to explain variation in the duration and vigor of sexual behaviors across species, there is no proposed explanation for variation in the forms of these behaviors. I hypothesized that the forms of sexual behaviors function as recognition signals of conspecific mates. Such signals are adaptive when F1 hybrids exhibit reduced fitness compared with nonhybrid offspring. Recent evidence from nonprimate taxa supports the existence of species recognition signals during mating. Using newly observed sexual behaviors for Cebus albifrons and a recent phylogeny of capuchins, I found significant support for a key prediction of the conspecific mate recognition hypothesis: evolutionary changes in sexual behaviors were associated with speciation. Given the resultant best model for evolution of sexual behaviors, I reconstructed the ancestral pattern of sexual behaviors for extant capuchin species (genera Cebus and Sapajus). This reconstruction suggests that the extreme female proceptivity of tufted capuchin monkeys may function to increase female reproductive choices in the context of sperm-limited males (genus Sapajus).     

Sexually antagonistic coevolution in a mating system: combining experimental and comparative approaches to address evolutionary processes

We combined experimental and comparative techniques to study the evolution of mating behaviors within in a clade of 15 water striders (Gerris spp.). Superfluous multiple mating is costly to females in this group, and consequently there is overt conflict between the sexes over mating. Two alternative hypotheses that could generate interspecific variation in mating behaviors are tested: interspecific variation in optimal female mating rate versus sexually antagonistic coevolution of persistence and resistance traits. These potentially coevolving traits include male grasping and female antigrasping structures that further the interests of one sex over the other during premating struggles. Both processes are known to play a role in observed behavioral variation within species. We used two large sets of experiments to quantify behavioral differences among species, as well as their response to an environmentally (sex-ratio) induced change in optimal female mating rate. Our analysis revealed a large degree of continuous interspecific variation in all 20 quantified behavioral variables. Nevertheless, species shared the same set of behaviors, and each responded in a qualitatively similar fashion to sex-ratio alterations. A remarkably large proportion (> 50%) of all interspecific variation in the magnitude of behaviors, including their response to sex ratio, could be captured by a single multivariate axis. These data suggest tight coevolution of behaviors within a shared mating system. The pattern of correlated evolution was best accounted for by antagonistic coevolution in the relative abilities of each sex to control the outcome of premating struggles. In species where males have a relative advantage, mating activity is high, and the opposite is found in species where females have gained a relative advantage. Our analyses also suggested that evolution has been unconstrained by history, with no consistent evolutionary tendency toward or away from male or female relative advantage.     

Effects of exogenous testosterone and mating context on men's preferences for female facial femininity

Correlational research suggests that men show greater attraction to feminine female faces when their testosterone (T) levels are high. Men's preferences for feminine faces also seem to vary as a function of relationship context (short versus long-term). However, the relationship between T and preferences for female facial femininity has yet to be tested experimentally. In the current paper, we report the results of two experiments examining the causal role of T in modulating preferences for facial femininity across both short and long-term mating contexts. Results of Experiment 1 (within-subject design, n = 24) showed that participants significantly preferred feminized versus masculinized versions of women's faces. Further, participants showed a stronger preference for feminine faces in the short versus the long-term context after they received T, but not after they received placebo. Post-hoc analyses suggested that this effect was driven by a lower preference for feminine faces in the long-term context when on T relative to placebo, and this effect was found exclusively for men who received placebo on the first day of testing, and T on the second day of testing (i.e., Order x Drug x Mating context interaction). In Experiment 2 (between-subject design, n = 93), men demonstrated a significant preference for feminized female faces in the short versus the long-term context after T, but not after placebo administration. Collectively, these findings provide the first causal evidence that T modulates men's preferences for facial femininity as a function of mating context.     

Macroevolutionary evidence suggests trait‐dependent coevolution between behavior and life‐history

Species with fast life‐histories typically prioritize current over future reproductive events, compared to species with slow life‐histories. These species therefore require greater energetic input into reproduction, and also likely have less time to realize their reproductive potential. Hence, behaviors that increase access to both resources and mating opportunities, at a cost of increased mortality risk, could coevolve with the pace of life‐history. However, whether this prediction holds across species, remains untested under standardized conditions. Here, we test how risky behaviors, which facilitate access to resources and mating opportunities (i.e., activity, boldness, and aggression), along with metabolic rate, coevolve with the pace of life‐history across 20 species of killifish that present remarkable divergences in the pace of life‐history. We found a positive association between the pace of life‐history and aggression, but interestingly not with other behavioral traits or metabolic rate. Aggression is linked to interference competition, and in killifishes is often employed to secure mates, while activity and boldness are more relevant for exploiting energetic resources. Our results suggest that the trade‐off between current and future reproduction plays a more prominent role in shaping mating behavior, while behaviors related to energy acquisition may be influenced by ecological factors.     

Why does the magnitude of genotype‐by‐environment interaction vary?

Genotype‐by‐environment interaction (G × E), that is, genetic variation in phenotypic plasticity, is a central concept in ecology and evolutionary biology. G×E has wide‐ranging implications for trait development and for understanding how organisms will respond to environmental change. Although G × E has been extensively documented, its presence and magnitude vary dramatically across populations and traits. Despite this, we still know little about why G × E is so evident in some traits and populations, but minimal or absent in others. To encourage synthetic research in this area, we review diverse hypotheses for the underlying biological causes of variation in G × E. We extract common themes from these hypotheses to develop a more synthetic understanding of variation in G × E and suggest some important next steps.     

Mortality costs of sexual selection and parental care in natural populations of birds

Abstract Is the cost of reproduction different between males and females? On the one hand, males typically compete intensely for mates, thus sexual selection theory predicts higher cost of reproduction for males in species with intense male‐male competition. On the other hand, care provisioning such as incubating the eggs and raising young may also be costly, thus parental care theory predicts higher mortality for the care‐giving sex, which is often the female. We tested both hypotheses of reproductive costs using phylogenetic comparative analyses of sex‐specific adult mortality rates of 194 bird species across 41 families. First, we show that evolutionary increases in male‐male competition were associated with male‐biased mortalities. This relationship is consistent between two measures of mating competition: social mating system and testis size. Second, as predicted by the parental cost hypothesis, females have significantly higher adult mortalities (mean ± SE, 0.364 ± 0.01) than males (0.328 ± 0.01). However, the mortality cost of parental care was only detectable in males, when the influence of mating competition was statistically controlled. Taken together, our results challenge the traditional explanation of female‐biased avian mortalities, because evolutionary changes in female care were unrelated to changes in mortality bias. The interspecific variation in avian mortality bias, as we show here, is driven by males, specifically via the costs of both mating competition and parental care. We also discuss alternative hypotheses for why most birds exhibit female‐biased mortalities, whereas in mammals male‐biased mortalities predominate.     

The clock gene,period, influences migratory flight and reproduction of the oriental armyworm,Mythimna separata (Walker)

The oriental armyworm, Mythimna separata, is a major long-distance migratory insect pest of grain crops in China and other Asian countries. Migratory flights and reproductive behavior usually occur at night, regulated by a circadian rhythm. However, knowledge about the linkages between adult flight, reproduction, and clock genes is still incomplete. To fill this important gap in our knowledge, a clock gene (designated Msper) was identified and phylogenetic analysis indicated that the encoded protein (MsPER) was highly similar to PER proteins from other insect species. Quantitative RT-PCR assays demonstrated that significantly different spatiotemporal and circadian rhythmic accumulations of mRNA encoding MsPER occurred during development under steady 14 h : 10 h light : dark conditions. The highest mRNA accumulation occurred in adult antennae and the lowest in larvae. Msper was expressed rhythmically in adult antennae, relatively less in photophase and more entering scotophase. Injecting small interference RNA (siRNA) into adult heads effectively knocked down Msper mRNA levels within 72 h. Most siRNA-injected adults reduced their evening flight activity significantly and did not exhibit a normal evening peak of flight activity. They also failed to mate and lay eggs within 72 h. Adult mating behavior was restored to control levels by 72 h post injection. We infer that Msper is a prominent clock gene that acts in regulating adult migratory flight and mating behaviors of M. separata. Because of its influence on migration and mating, Msper may be a valuable gene to target for effective management of this migratory insect.     

Effects of Female‐Female Aggression in a Sexual/Unisexual Species Complex

The maintenance of sexual reproduction is still a largely unresolved question in evolutionary biology, and one of the most puzzling aspects of this is the coexistence of sexual and asexual females. This often leads to widespread niche overlap, posing an interesting challenge to competitive exclusion theory. In this study, we investigate how the aggressive behaviors between females in a sexual/unisexual mating complex of mollies (Poecilia latipinna and P. formosa) differ, and the effects these behaviors have on both the performer and receiver of aggressive acts. We exposed females to five treatments: (1) alone (control); (2) a large and small sexual female; (3) a large sexual female and a small unisexual female; (4) a small sexual female and a large unisexual female; and (5) a large and small unisexual female. We found that P. formosa females were on average more aggressive over time when compared to their sexual hosts, P. latipinna. The females of P. formosa, however, incurred a higher cost of being aggressive. Large, aggressor females of this species had a lower body fat content than their conspecific recipients. By contrast, P. latipinna females showed no differentiation between aggressors and recipients. Here, we combine life history methodology and behavioral observations to show that female competition can in fact be quantitatively measured and that these aggressive behaviors are costly to perform. The adaptive value of this interspecies aggression is not yet completely understood, but sexual competition, access to resources, and position within the shoal are all possible functions.     

A Continuum of Behavioral Plasticity in Urban and Desert Black Widows

Behavioral plasticity marks an individual's ability to modulate behavior across functional contexts. Behavioral syndromes, on the other hand, appear as consistent individual variation in behavior that is both repeatable for individuals within a functional context (e.g., consistent voracity toward prey) and correlated across contexts (e.g., high voracity toward prey and high levels of boldness toward enemies). Thus, adaptive plasticity and syndromes represent two extremes of a behavioral plasticity continuum upon which most behavioral phenotypes fall. We tested for both adaptive plasticity and behavioral syndromes in the western black widow spider, Latrodectus hesperus. We measured behavior in three contexts: startle, startle + prey, and startle + mate, and found (1) classic behaviorally plastic responses to predation risk, (2) high repeatability of behavior within contexts, and (3) evidence of a correlation between startle + prey and startle + mate contexts, indicative of a behavioral syndrome. As relative behavioral plasticity may vary across populations, we also compared urban and desert populations to test whether spiders from these habitats exhibit different behaviors and/or behavioral syndromes. While we found that urban males used in mating trials courted urban females significantly more than desert females, we found no other differences in the behavior of urban and desert black widows. Thus, black widows, regardless of habitat, are characterized by both context‐specific behavioral plasticity and across‐context correlations, presenting a phenotypic complexity that is likely exhibited, to varying degrees, by most organisms.     

Mate value and self-esteem: evidence from eight cultural groups

This paper explores self-perceived mate value (SPMV), and its association with self-esteem, in eight cultures. 1066 participants, from 8 cultural groups in 7 countries, rated themselves on 24 SPMVs and completed a measure of self-esteem. Consistent with evolutionary theory, women were more likely to emphasise their caring and passionate romantic nature. In line with previous cross-cultural research, characteristics indicating passion and romance and social attractiveness were stressed more by respondents from individualistic cultures, and those higher on self-expression (rather than survival) values; characteristics indicative of maturity and confidence were more likely to be mentioned by those from Traditional, rather than Secular, cultures. Contrary to gender role theory, societal equality had only limited interactions with sex and SPMV, with honesty of greater significance for male self-esteem in societies with unequal gender roles. These results point to the importance of cultural and environmental factors in influencing self-perceived mate qualities, and are discussed in relation to broader debates about the impact of gender role equality on sex differences in personality and mating strategies.     

Sexual selection on bushcricket genitalia operates in a mosaic pattern

In most species with internal fertilization, male genitalia evolve faster than other morphological structures. This holds true for genital titillators, which are used exclusively during mating in several bushcricket subfamilies. Several theories have been proposed for the sexual selection forces driving the evolution of internal genitalia, especially sperm competition, sexually antagonistic coevolution (SAC), and cryptic female choice (CFC). However, it is unclear whether the evolution of genitalia can be described with a single hypothesis or a combination of them. The study of species‐specific genitalia action could contribute to the controversial debate about the underlying selective evolutionary forces. We studied female mating behaviors in response to experimentally modified titillators in a phylogenetically nested set of four bushcricket species: Roeseliana roeselii, Pholidoptera littoralis littoralis, Tettigonia viridissima (of the subfamily Tettigoniinae), and Letana inflata (Phaneropterinae). Bushcricket titillators have several potential functions; they stimulate females and suppress female resistance, ensure proper ampulla or spermatophore attachment, and facilitate male fixation. In R. roeselii, titillators stimulate females to accept copulations, supporting sexual selection by CFC. Conversely, titillator modification had no observable effect on the female's behavior in T. viridissima. The titillators of Ph. l. littoralis mechanically support the mating position and the spermatophore transfer, pointing to sexual selection by SAC. Mixed support was found in L. inflata, where manipulation resulted in increased female resistance (evidence for CFC) and mating failures by reduced spermatophore transfer success (evidence for SAC). Sexual selection is highly species‐specific with a mosaic support for either cryptic female choice or sexually antagonistic coevolution or a combination of both in the four species.