Fluctuating asymmetry in a secondary sexual trait: no associations with individual fitness, environmental stress or inbreeding, and no heritability

It has been suggested that fluctuating asymmetry (FA) in secondary sexual traits may be a useful indicator of either individual quality or environmental stress. We tested this concept using a series of analyses of FA in male antler size in a wild red deer (Cervus elaphus) population, using four measures of size repeated across successive years on the same individuals. We found no consistent evidence of correlations between traits in levels of FA, nor of any associations between known environmental or developmental conditions. None of the four measures of FA showed a significant heritability (average h2 = 0.041), nor was there any evidence of inbreeding depression. For three of the four traits, fluctuating asymmetry did not predict either annual or lifetime breeding success. However there were significant associations between breeding success and FA in antler length. Given the series of null results in our other tests, it seems likely that this was a direct mechanistic effect rather than because measures of FA were indicative of individual quality or condition.     

Hand asymmetry does not relate to key life history traits in post-menopausal contemporary Finnish women

Associations between fluctuating asymmetry (FA, a putative marker of developmental instability, DI) and life history traits have received a great deal of attention in the non-human literature. However, the patterns found are very heterogeneous and generalizations are difficult to make. In humans, only a few studies have related FA to life histories and fitness. In this paper we study such relationships using hand FA and several key life history traits in 209 post-menopausal Finnish women born between 1946 and 1958. Asymmetry measurements were based on scans of the hands and the life histories of these women were collected using questionnaires. No significant associations were detected and trends were opposite to expectations. We did find evidence for directional asymmetry, as traits in the right hand were larger on average. This may be due to handedness, questioning the usefulness of hand FA as a measure of DI. We conclude that future studies in humans should carefully examine the usefulness of traits as measures of DI.     

Quantifying the strength and form of sexual selection on men's traits

Although recent research has increasingly focused on human sexual selection, fundamental questions remain concerning the relative influence of individual traits on success in competition for mates and the mechanisms, form, and direction of these sexual selective pressures. Here, we explore sexual selection on men's traits by ascertaining men's dominance and attractiveness from male and female acquaintances. On a large American university campus, 63 men from two social fraternities provided anthropometric measurements, facial photographs, voice recordings, and reported mating success (number of sexual partners). These men also assessed each other's dominance, and 72 women from two socially affiliated sororities assessed the men's attractiveness. We measured facial masculinity from inter-landmark distances and vocal masculinity from acoustic parameters. We additionally obtained facial and vocal attractiveness and dominance ratings from unfamiliar observers. Results indicate that dominance and the traits associated with it predict men's mating success, but attractiveness and the traits associated with it do not. These findings point to the salience of contest competition on men's mating success in this population.     

Short-term exposure to a synthetic estrogen disrupts mating dynamics in a pipefish

Sexual selection is responsible for the evolution of some of the most elaborate traits occurring in nature, many of which play a vital role in competition over access to mates and individual reproductive fitness. Because expression of these traits is typically regulated by sex-steroids there is a significant potential for their expression to be affected by the presence of certain pollutants, such as endocrine disrupting compounds. Endocrine disruptors have been shown to alter primary sexual traits and impact reproduction, but few studies have investigated how these compounds affect secondary sexual trait expression and how that may, in turn, impact mating dynamics. In this study we examine how short-term exposure to a synthetic estrogen impacts secondary sexual trait expression and mating dynamics in the Gulf pipefish, a species displaying sex-role reversal. Our results show that only 10 days of exposure to 17α-ethinylestradiol results in adult male pipefish developing female-like secondary sexual traits. While these males are capable of reproduction, females discriminate against exposed males in mate choice trials. In natural populations, this type of discrimination would reduce male mating opportunities, thus potentially reducing their long-term reproductive success. Importantly, the effects of these compounds on mating dynamics and mating opportunity would not be observed using the current standard methods of assessing environmental contamination. However, disrupting these processes could have profound effects on the viability of exposed populations.     

Sexual selection on morphological and physiological traits and fluctuating asymmetry in the yellow dung fly

Previous univariate studies of the yellow dung fly (Scathophaga stercoraria) have demonstrated strong sexual selection, in terms of mating success, on male size (estimated as hind tibia length). To identify specific target(s) of selection on body size and possible conflicting selection pressures on particular body parts, two multivariate field studies of sexual selection were conducted. In one study using point samples from three populations, we assessed several morphological traits, including genital traits and measures of fluctuating asymmetry (FA) of all paired traits. There was sexual selection for large male size in general, confirming previous, univariate studies. With the possible exception of thorax width, which was selected in the opposite direction, no main target of selection was identified, as most morphological traits were highly correlated. There was no detectable sexual selection on the male external genital structures assessed. In a second study using multiple samples from one population, we included physiological measures of energy reserves (lipids, glucose and glycogen) known to affect mating success, in addition to trait size and FA of wings and legs. Inclusion of physiological traits is rare in phenomenological studies of selection. This study again confirmed the mating advantage of large males, and additionally showed independent positive influences of lipid and glucose but not glycogen levels. FA in paired traits generally did not affect male mating success, but was negatively correlated with energy reserves. Our study suggests that inclusion of physiological measures and genital traits in phenomenological studies of selection would be fruitful in other species.     

Men's revealed preference for their mates' ages

Both young and old men say that they are sexually attracted to young, fertile women, but older men tend to marry older women, including those who are peri- and post-menopausal. We assessed men's freely revealed preference for their mates' age using an unusual marriage phenomenon in South Korea: the practice in which men purchase their brides from developing countries. Presumably, the men's mate choice, at least regarding the brides' age, is unrestricted by women. We analyzed all first marriages reported in 2010–2014 in South Korea and compared men who married Korean brides (N = 1,088,457) with those who purchased their brides (N = 45,528); the age range of grooms and brides was 15–59. While the former exhibited the typical pattern where older men married older women, the latter, whether young or old, always married young, fertile women. This finding is consistent with men's stated preference for young, fertile women in mating and suggests that the typical pattern is generated by women's limiting role in mating.     

Fluctuating asymmetry in certain morphological traits in laboratory populations of Drosophila ananassae.

Fluctuating asymmetry (FA, subtle random deviations from perfect bilateral symmetry) is often used as a measure of developmental instability (DI), which results from perturbations in developmental pathways caused by genetic or environmental stressors. During the present study, we estimated FA in 5 morphological traits, viz. wing length (WL), wing to thorax ratio (W:T), sternopleural bristle number (SBN), sex-comb tooth number (SCTN), and ovariole number (ON) in 18 laboratory populations of Drosophila ananassae. FA levels of measured traits differed significantly among populations except for SBN (in males and females) and W:T ratio (in females). Positional fluctuating asymmetry (PFA), a sensitive measure of DI, also varied significantly among the populations for SBN in females and SCTN in males. Interestingly, both males and females were similar for nonsexual traits. However, when FA across all traits (sexual and nonsexual) was combined into a single composite index (CFA), significant differences were found for both populations and sexes. Males showed higher CFA values than females, suggesting that males are more prone to developmental perturbations. The magnitude of FA differed significantly among traits, being lowest for nonsexual traits (SBN, WL, W:T ratio) and highest for sexual traits (SCTN and ON). The trait size of sexual traits (SCTN and ON) was positively correlated with their asymmetry. The possible reasons for variation in FA both among traits and among populations, and the usefulness of FA as an indicator of developmental stress and phenotypic quality in D. ananassae are discussed.     

Adult obesity: Panel study from native Amazonians

This paper examines three morphological indicators measuring obesity among a native Amazonian population of foragers-farmers in Bolivia (Tsimane’) and estimates the associations between them and standard covariates of obesity (e.g., socioeconomic status [SES]). We collected annual data from 350 non-pregnant women and 385 men ≥20 years of age from all 311 households in 13 villages during five consecutive years (2002–2006). We used three indicators to measure obesity: body-mass index (BMI), waist circumference (WC), and body fat using bioelectrical impedance analysis (BF-BIA). We ran separate individual random-effect panel multiple regressions for women and men with wealth, acculturation, health, and household food availability as key covariates, and controlled for village and year fixed effects and village × year interaction effects. Although BMI increases by a statistically significant annual growth rate of 0.64% among women and 0.37% among men over the five years, the increase does not yield significant biological meanings. Neither do we find consistent and biologically meaningful covariates associated with adult obesity.     

Fluctuating asymmetry and sexual selection in the Mediterranean fruitfly (Diptera, Tephritidae)

Sexual selection is known to operate at medfly leks with a few males gaining a high proportion of matings. However, specific male characteristics subject to sexual selection have not been identified. Here we report laboratory studies indicating that directional sexual selection operates on the level of fluctuating asymmetry (FA) in the superior frontal orbital setae (sex setae), with symmetrical males gaining more matings. Studies relating mating success with FA in a male trait have generally been taken as evidence of the operation of indirect sexual selection. For a male trait to acts as a reliable indicator of fitness, FA in the male trait should be negatively associated with trait size and females should mate with the males with the most exaggerated form of the trait. However no association was found between seta FA and mean seta length. In addition sexual selection did not appear to operate on mean trait size, although males with an intermediate sex seta to wing length ratio did achieve higher mating success, indicating that stabilizing sexual selection operates on this relative dimension. It is suggested that differences in male competitive ability may provide an alternative explanation of how such associations between mating success and FA in male characteristics can arise.     

Symmetry of the face in old age reflects childhood social status

The association of socioeconomic status (SES) with a range of lifecourse outcomes is robust, but the causes of these associations are not well understood. Research on the developmental origins of health and disease has led to the hypothesis that early developmental disturbance might permanently affect the lifecourse, accounting for some of the burden of chronic diseases such as coronary heart disease. Here we assessed developmental disturbance using bodily and facial symmetry and examined its association with socioeconomic status (SES) in childhood, and attained status at midlife. Symmetry was measured at ages 83 (facial symmetry) and 87 (bodily symmetry) in a sample of 292 individuals from the Lothian Birth Cohort 1921 (LBC1921). Structural equation models indicated that poorer SES during early development was significantly associated with lower facial symmetry (standardized path coefficient ?.25, p = .03). By contrast, midlife SES was not significantly associated with symmetry. The relationship was stronger in men (?.44, p = .03) than in women (?.12, p = .37), and the effect sizes were significantly different in magnitude (p = .004). These findings suggest that SES in early life (but not later in life) is associated with developmental disturbances. Facial symmetry appears to provide an effective record of early perturbations, whereas bodily symmetry seems relatively imperturbable. As bodily and facial symmetries were sensitive to different influences, they should not be treated as interchangeable. However, markers of childhood disturbance remain many decades later, suggesting that early development may account in part for associations between SES and health through the lifecourse. Future research should clarify which elements of the environment cause these perturbations.     

Lack of support for relation between woman's masculinity preference,estradiol level and mating context

It has been proposed that women's preferences for male facial sexual dimorphism are positively correlated with conception probability and differ between short- and long-term mating contexts. In this study, we tested this assumption by analyzing relationships between estradiol levels to the women's preferences of male faces that were manipulated to vary in masculinity. Estradiol was measured in daily saliva samples throughout the entire menstrual cycle collected by Polish women with regular menstrual cycles. In our analyses, we included the three most commonly used definitions of the fertile window in the literature. After computing the overall masculinity preference of each participant and measuring hormone levels, we found that i) the timing of ovulation varied greatly among women (between − 11 and − 17 days from the onset of the next menses, counting backwards), ii) there was no relationship between daily, measured during the day of the test (N = 83) or average for the cycle (N = 115) estradiol levels and masculinity preferences, iii) there were no differences in masculinity preferences between women in low- and high-conception probability phases of the cycle, and iv) there were no differences in masculinity preferences between short- and long-term mating contexts. Our results do not support the idea that women's preferences for a potential sexual partner's facial masculinity fluctuate throughout the cycle.     

Fitness costs and benefits of personality disorder traits

Extreme personality traits in humans often have detrimental life consequences, so they have long been supposed to be diseases. However, many other species display personality variants that are maintained due to their fitness advantages; in this case, they are construed as strategies. To examine the fitness costs and benefits of pathological personality traits in humans, we measured features of the A (socially odd, distrustful), B (incentive-seeking, selfish) and C (fearful, inhibited) clusters with the Personality Diagnostic Questionnaire-4 + (PDQ-4 +) in a sample of 738 outpatients. Fitness relevant parameters like mating success, reproductive output, self preservation, and access to status were assessed with the Life Outcome Questionnaire. No fitness advantages were found for high-A subjects. In contrast, high-B subjects tripled low-B subjects with regard to mating success and had 39% more offspring. Further, high-C subjects outperformed low-C subjects in attaining status and avoiding risks. These findings help explain the commonness of some extreme personality traits in humans, and suggest that they should be seen as evolutionary strategies rather than as diseases.     

Human vocal behavior within competitive and courtship contexts and its relation to mating success

Beyond the linguistic content of their speech, speakers of both sexes convey diverse biological and psychosocial information through their voices, which are important when assessing potential mates and competitors. However, studies investigating the relationships between mating success and acoustic inter-individual differences are scarce. In this study, we investigated such relationships in both sexes in courtship and competitive interactions—as they correspond to the two different types of sexual selection—using an experimental design based on a simulated dating game. We assessed which type of sexual selection best predicted mating success, here defined as the self-reported number of sexual partners within the past year. Our results show that only acoustic inter-individual differences in the courtship context for both men and women predicted their mating success. Men displaying faster articulation rate and louder voices reported significantly more sexual partners; in contrast, men displaying higher intonation reported a greater negative effect of roughness and breathiness on their mating success. Women who displayed relatively less breathy voices and shorter speech duration reported significantly fewer sexual partners. These novel findings are discussed in light of the mate choice context and the relative contribution of both types of sexual selection shaping acoustic features of speech.     

A latent variable model of developmental instability in relation to men's sexual behaviour

A single trait's fluctuating asymmetry (FA) is expected to be a poor measure of developmental instability. Hence, studies that examine associations between FA and outcomes expected to covary with developmental instability often have little power in detecting meaningful relationships. One way of increasing the power of detecting relationships between developmental instability and outcomes is through the use of multiple traits' FA. The way multiple traits have typically been used is in trait aggregates. Here, we illustrate another way of examining relationships with developmental instability using multiple traits' FA: through structural equation modelling. Covariances between measures of FA and an outcome variable are interpreted within the context of an explicit model of associations between variables, which is tested for fit and the parameters specified within the model are estimated. We used nine traits' FA as markers of a latent variable of men's developmental instability, which was associated with the number of sexual partners. The results indicate a sizeable correlation between developmental instability and men's sexual history, despite small correlations between individual traits' FA and sexual history.     

Evolutionary history shapes the association between developmental instability and population‐level genetic variation in three‐spined sticklebacks

Developmental instability (DI) is the sensitivity of a developing trait to random noise and can be measured by degrees of directionally random asymmetry [fluctuating asymmetry (FA)]. FA has been shown to increase with loss of genetic variation and inbreeding as measures of genetic stress, but associations vary among studies. Directional selection and evolutionary change of traits have been hypothesized to increase the average levels of FA of these traits and to increase the association strength between FA and population‐level genetic variation. We test these two hypotheses in three‐spined stickleback (Gasterosteus aculeatus L.) populations that recently colonized the freshwater habitat. Some traits, like lateral bone plates, length of the pelvic spine, frontal gill rakers and eye size, evolved in response to selection regimes during colonization. Other traits, like distal gill rakers and number of pelvic fin rays, did not show such phenotypic shifts. Contrary to a priori predictions, average FA did not systematically increase in traits that were under presumed directional selection, and the increases observed in a few traits were likely to be attributable to other factors. However, traits under directional selection did show a weak but significantly stronger negative association between FA and selectively neutral genetic variation at the population level compared with the traits that did not show an evolutionary change during colonization. These results support our second prediction, providing evidence that selection history can shape associations between DI and population‐level genetic variation at neutral markers, which potentially reflect genetic stress. We argue that this might explain at least some of the observed heterogeneities in the patterns of asymmetry.     

Variation in testosterone levels and male reproductive effort: Insight from a polygynous human population

Recent evidence suggests that, in humans, variations in testosterone (T) levels between men reflect their differential allocation in mating versus parenting efforts. However, most studies have been conducted in urbanized, monogamous populations, making generalizations from them questionable. This study addresses the question of whether indicators of male reproductive effort are associated with variations in salivary T levels in a polygynous population of agriculturists in rural Senegal. We first show that pair-bonding and/or transition to fatherhood is associated with T profiles: married fathers (N = 53) have lower morning and afternoon T levels than unmarried non-fathers (N = 28). Second, among fathers, individual differences in parenting effort, as well as variations in mating effort, predict morning T levels. Indeed, men highly investing in parental care show lower morning T levels. Moreover, among men under 50, polygynous men show higher morning T levels than monogamous men. Taken together with previous results in monogamous settings, these findings suggest that the endocrine regulation of reproductive effort is probably a general feature of human populations.     

Sexual selection on morphological and physiological traits and fluctuating asymmetry in the black scavenger fly Sepsis cynipsea

Previous univariate studies of the fly Sepsis cynipsea (Diptera: Sepsidae) have demonstrated spatiotemporally variable and consequently overall weak sexual selection favouring large male size, which is nevertheless stronger on average than fecundity selection favouring larger females. To identify specific target(s) of selection on body size and additional traits possibly affecting mating success, two multivariate field studies of sexual selection were conducted. In one study using seasonal replicates from three populations, we assessed 15 morphological traits. No clear targets of sexual selection on male size could be detected, perhaps because spatiotemporal variation in selection was again strong. In particular, there was no (current) selection on male abdomen length or fore coxa length, the only traits for which S. cynipsea males are not smaller than females. Interestingly, copulating males had a consistently shorter fore femur base, a secondary sexual trait, and a wider clasper (hypopygium) gap, an external genital trait. In a second study using daily and seasonal replicates from one population, we included physiological measures of energy reserves (lipids, glucose, glycogen), in addition to hind tibia length and fluctuating asymmetry (FA) of all pairs of legs. This study again confirmed the mating advantage of large males, and additionally suggests independent positive influences of lipids (the long-term energy stores), with effects of glucose and glycogen (the short-term energy stores) tending to be negative. FA of paired traits was not associated with male mating success. Our study suggests that inclusion of physiological measures and genital traits in phenomenological studies of selection, which is rare, would be fruitful in other species.     

Individual asymmetry as a predictor of fitness in the bat Carollia perspicillata

The measurement of fitness in wild populations is a challenging task, and a number of proxies have been proposed with different degrees of success. Developmental instability/stability (DI) is an organismal property associated with variance in bilateral asymmetry (fluctuating asymmetry—FA) and a correlated effect on fitness. This study provides evidence to corroborate the hypothesis that asymmetry partly reflects DI and is correlated with a reduction in fitness measured by survival and reproduction in bats. We studied two colonies of the bat Carollia perspicillata in southeastern Brazil over 5 years, marking and recapturing individuals. Gaussian mixture models for signed Forearm Asymmetry (ForA) distribution indicated that ~20% of asymmetry variation was due to DI heterogeneity among individuals. ForA, body condition (Scaled Mass Index—SMI) and Forearm Length (ForL) were used as predictors of survival probability in Cormack‐Jolly‐Seber models. Asymmetry was negatively associated with survival, whereas SMI and ForL were positively associated. The male C. perspicillata defend sites within the roost that are favoured by female harems, but there are mating opportunities for bachelor males, leading to both territorial disputes and sperm competition. As predicted by sexual selection, ForA was negatively associated with relative Testicle Length, a measure of reproductive potential. In females, ForA was negatively associated with the probability of two pregnancies (as opposed to one) in a given breeding season. The effect magnitudes and directions of associations suggest that asymmetry, even though not perfectly reflecting DI variation, is a useful predictor for fitness components in C. perspicillata.     

Facial attractiveness and fertility in populations with low levels of modern birth control

Evolutionary models of human mate choice generally assume that physical attractiveness has evolved through sexual selection, i.e., it has been associated with higher mating opportunities and subsequent reproductive success across our evolutionary history. Here we investigate whether facial attractiveness is related to fertility in order to understand the extent to which selection can operate on attractive traits in modern populations. We used data from two populations where the prevalence of modern birth control methods is low and thus unlikely to disconnect mating opportunities from reproductive success: men and women from contemporary rural Senegal and men from the West Point Military Academy in the USA who graduated in 1950. We found that facial attractiveness negatively predicts age-specific reproduction in both sexes in Senegal and is independent from lifetime reproductive success in men from the USA. Overall, the results suggest that facial attractiveness is not under positive selection and raise questions about methodological approaches currently used to assess attractiveness.     

Age specific mating incidence and reproductive behavior of the ladybird beetle,Anegleis cardoni (Weise) (Coleoptera: Coccinellidae)

Age specific mating incidence, mating behavior, mate recognition cues and effect of sexual status on mating of ladybird beetle, Anegleis cardoni (Weise) (Coleoptera: Coccinellidae) were studied in detail. The mating duration was very short (14.40 ± 0.72 min) in comparison to other ladybirds. Courtship was male dominated and was displayed in steps, viz. approach, watch, examine, sharp turns, mount, attempt and mate. Sharp turns is an additional behavior observed during courtship in this ladybird, and is characterized by sharp turning movements towards the mate, and is undertaken by both males and females. Active mating of A. cardoni involved multiple strokes of the aedeagus. Mating duration and the number of strokes were higher in unmated males than in mated ones. Results reveal that physical cues probably play a role in the initiation of courtship, while chemical signals are probably involved in the continuation of courtship, culminating in intromission. The removal of male antennae and obscurity of elytral patterns significantly decreased mating success, whereas female antennal ablation and obscuring of the pronotum did not affect mate recognition.