Sexual selection, stabilizing selection and fluctuating asymmetry in two populations of pupfish (Cyprinodon pecosensis)

Fluctuating asymmetry of morphological traits is thought to reflect the capacity of a genotype to produce an integrated, functional phenotype. I tested three predictions. (1) In a polygynous breeding system, under intense sexual selection on males, breeding males should show greater symmetry in bilaterally symmetrical traits than non-breeding males or females. (2) If these traits are under stabilizing selection, highly symmetrical individuals also should be modal phenotypes, thus near the mean value for that trait, whereas individuals with increased asymmetry should represent marginal phenotypes, near the extremes of the distribution for that trait. (3) Differences in the intensity of sexual selection should be reflected in differences in the degree of fluctuating asymmetry between sexes among populations. I examined the relationship between male breeding status and the degree of fluctuating asymmetry of four bilaterally symmetrical- traits, preorbital and preopercular pores and pectoral and pelvic fin rays, in two populations of Pecos pupfish which differed in the intensity of sexual selection. These traits do not function in male-male competition or female choice, thus are not directly affected by sexual selection. In Mirror Lake breeding males, as a group, were most symmetrical for all four traits, while non-breeding males and females showed higher levels of fluctuating asymmetry. Similarly, symmetrical individuals also represented modal phenotypes for four traits (breeding males), and for three traits (non-breeding males and females). These patterns were not seen in the Lake Francis population, where breeding males were as asymmetrical as non-breeding males and females, and the degree of fluctuating symmetry did not differ between modal and marginal phenotypes for any of the four traits. When ecological conditions favour intense sexual selection, either through female choice, male-male competition, or both, breeding males represent the most fit phenotypes. Thus sexual selection reinforces the effects of stabilizing selection on characters that do not function as secondary sexual traits. However, when sexual selection is relaxed, differences between sexes disappear.     

Facial attractiveness,developmental stability,and fluctuating asymmetry

Despite robust cross-cultural reliability of human facial attractiveness ratings, research on facial attractiveness has only superficially addressed the connection between facial attractiveness and the history of sexual selection in Homo sapiens. There are reasons to believe that developmental stability and phenotypic quality are related. Recent studies of nonhuman animals indicate that developmental stability, measured as fluctuating asymmetry in generally bilateral symmetrical traits, is predictive of performance in sexual selection: Relatively symmetrical males are advantaged under sexual selection. This pattern is suggested by our study of facial attractiveness and fluctuating asymmetry in seven bilateral body traits in a student population. Overall, facial attractiveness negatively correlated with fluctuating asymmetry; the relation for men, but not for women, was statistically reliable. Possible confounding factors were controlled for in the analysis.     

Fluctuating asymmetry and sexual selection

Fluctuating asymmetry occurs when an individual is unable to undergo identical development on both sides of a bilaterally symmetrical trait. Fluctuating asymmetry measures the sensitivity of development to a wide array of genetic and environmental stresses. We propose that fluctuating asymmetry is used in many signalling contexts for assessment of an individual's ability to cope with its environment. We hypothesize that fluctuating asymmetry is used in sexual selection, both in fighting and mate choice, and in competition for access to resources. Evidence is reviewed showing that the patterns of fluctuating asymmetry in secondary sexual characters differ from those seen in other morphological traits. Secondary sexual characters show much higher levels of fluctuating asymmetry. Also, there is often a negative relationship between fluctuating asymmetry and the absolute size of ornaments, whereas the relationship is typically U-shaped in other morphological traits. The common negative relationship between fluctuating asymmetry and ornament size suggests that many ornaments reliably reflect individual quality.     

Patterns of fluctuating asymmetry in sexual ornaments predict female choice

Extravagant secondary sexual characters are assumed to have arisen and be maintained by sexual selection. While traits like horns, antlers and spurs can be ascribed to intrasexual competition, other traits such as extravagant feather ornaments, displays and pheromones have to be ascribed to mate choice. A number of studies have tested whether females exert selection on the size of male ornaments, but only some of these have recorded female preferences for the most extravagantly ornamented males. Here I demonstrate that female choice can be directly predicted from the relationship between the degree of fluctuating asymmetry and the size of a secondary sexual character. Fluctuating asymmetry is an epigenetic measure of the ability of individuals to cope with stress, and it occurs when an individual is unable to undergo identical development of an otherwise bilaterally symmetric trait on both sides of its body. There is a negative relationship between the degree of fluctuating asymmetry and the absolute size of an ornament in those bird species with a female preference for the largest male sex trait, while there is a flat or U-shaped relationship among species without a female preference. These results suggest that females prefer exaggerated secondary sexual characters if they reliably demonstrate the ability of males to cope with genetic and environmental stress. Some species may demonstrate a flat or U-shaped relationship between the degree of fluctuating asymmetry and the absolute size of an ornament because (i) the genetic variance in viability signalled by the secondary sex trait has been depleted; (ii) the secondary sex trait is not particularly costly and therefore does not demonstrate condition dependence; or because (iii) the sex traits can be considered arbitrary traits rather than characters reflecting good genes.     

Parasites differentially increase the degree of fluctuating asymmetry in secondary sexual characters

The degree of fluctuating asymmetry has been demonstrated to reflect the ability of individuals to cope with different kinds of environmental stress (Parsons 1990). Parasites and diseases are one kind of environmental stress which most individuals encounter during their lifetime. Parasites have also been suggested to play an important role in sexual selection and the development of ornaments, since the full expression of ornaments may reflect the ability of hosts to cope with the debilitating effects of parasites. Here I report for the first time that a parasite, the haematophagous tropical fowl mite Ornithonyssus bursa (Macronyssidae, Gamasida), directly affects the degree of fluctuating asymmetry in a secondary sexual character of its host, the elongated tail of the swallow Hirundo rustica (Aves: Hirundinidae). I experimentally manipulated the mite load of swallow nests during one season by either increasing or reducing the number of mites, or keeping nests as controls. The degree of fluctuating asymmetry was measured in the subsequent year after the swallows had grown new tail ornaments under the altered parasite regime. The degree of fluctuating asymmetry was larger at increasing levels of parasites for male tail length, but not for the length of the shortest tail feather or wing length or for tail and wing length in females. These results suggest that the degree of fluctuating asymmetry in tail ornaments, but not in other feather traits, reliably reveals the level of parasite infestation. This has important implications for the ability of conspecifics to use the size and the expression of ornaments in assessment of phenotypic quality and thus in sexual selection.     

Condition-dependent asymmetry is fluctuating asymmetry

Asymmetry has been demonstrated to play a role in signalling systems such as sexual selection and pollination, with receivers showing a preference for symmetrical signals. Large signals often have the smallest degree of asymmetry, a finding that is consistent with signal asymmetry being condition-dependent. The kind of asymmetry displayed by signals was supposed or shown to be fluctuating asymmetry, and signals revealing individual differences in the ability to stabilize developmental processes, despite a hostile developmental environment, was supposed to be the basis for the preference for symmetric signals. Recently, it has been suggested that condition-dependent signals display antisymmetry rather than fluctuating asymmetry, based on analyses of the relationship between asymmetry and mean length of the left and the right character in a few published graphs of absolute asymmetry of signals. Here I demonstrate on the basis of a much larger number of data sets, including those previously published, that the previous results are biased because of the methods used for the analyses, and that characters with condition-dependent asymmetry show fluctuating asymmetry rather than antisymmetry. In particular, frequency distributions of signed left-minus-right character values display leptokurtosis, as predicted if asymmetry distributions reflected individual differences in developmental precision, rather than platykurtosis. Platykurtosis is predicted if the traits are antisymmetric. The preponderance of leptokurtic distributions is consistent with recent modelling showing that inherent differences in the ability of individuals to control developmental processes invariably leads to leptokurtic distributions of signed left-minus-right character values.     

The Developmental Instability—Sexual Selection Hypothesis: A General Evaluation and Case Study

Developmental instability results from small, random perturbations to developmental processes of individual traits. Phenotypic outcomes of developmental instability include fluctuating asymmetry (FA, subtle deviations from perfect bilateral symmetry) and phenodeviance (minor morphological abnormalities). A great deal of research over the past 18 years has focused on the role of developmental instability in sexual selection. A driving force behind this research has been the developmental instability-sexual selection hypothesis, which posits that symmetry and lack of phenodeviance in secondary sexual traits are assessed by mates and rivals because they provide a reliable cue of individual genetic quality. The present article tests this hypothesis by evaluating its five main predictions using published results: expressions of developmental instability in secondary sexual traits should be (1) negatively correlated with mating success; (2) directly assessed by mates and sexual rivals; (3) heritable; (4) condition-dependent; and (5) negatively correlated with ornament size. The first two predictions receive considerable, though not ubiquitous, support from a range of animal species. However, FA in secondary sexual traits is generally not significantly heritable, indicating that FA is unlikely to reveal genetic quality that can be transmitted to offspring. Similarly, there is little evidence to support the predictions that FA is condition dependent, and that it is negatively phenotypically or genetically correlated with sexual trait size. Based on an evaluation of the evidence overall, it is concluded that this hypothesis is unlikely to be viable; it appears unlikely that mate choice for symmetry evolves by “good genes” sexual selection. Hypotheses that do not require asymmetry and phenodeviance to reveal heritable genetic quality may explain observed links between FA/phenodeviance and mating success. Results of a case study of Drosophila bipectinata are summarized, which reinforce this general conclusion. It is suggested that nonadditive genetic variation arising from an interaction between trait-specific developmental genes and genetic background may drive sexual selection for reducing developmental instability in some cases. Levels of developmental instability variation in a population may need to surpass a critical threshold for sexual selection to operate, possibly explaining some of the pronounced heterogeneity in the effect of developmental instability on sexual selection reported in the literature.     

Jamaican Symmetry Project: long-term study of fluctuating asymmetry in rural Jamaican children.

Fluctuating asymmetry, small deviations from perfect bilateral symmetry, is negatively correlated with health and positively correlated with sexual selection in human adults, but the accumulation, persistence, and fitness implications of asymmetries during childhood are largely unknown. Here, we introduce the Jamaican Symmetry Project, a long-term study of fluctuating asymmetry and its physical and behavioral correlates in rural Jamaican children. The project is based on an initial sample of 285 children (156 boys and 129 girls), aged 5 to 11 years. We describe the design of the project and the methodology of measuring 10 paired morphometric traits. All traits except hand width showed fluctuating asymmetry. Fluctuating asymmetries of the legs tended to be related and were less than half as great as fluctuating asymmetries of the arms and ears. Therefore the legs may show high developmental stability resulting from selection for mechanical efficiency. A fluctuating asymmetry composite score revealed that boys have significantly lower fluctuating asymmetry than girls and that this effect resides mainly in the elbows. There were significant positive relationships between composite fluctuating asymmetry and age, height, and weight, but multiple regression analyses showed that age was negatively related to fluctuating asymmetry, whereas body size was positively correlated. These findings are compared with results from recent English studies.     

Patterns of fluctuating asymmetry in flowers: Implications for sexual selection in plants

Characters in animals used in signalling and subjected to strong directional selection often demonstrate (i) an elevated level of fluctuating asymmetry (small random deviations from bilateral symmetry) and (ii) a negative relationship between the degree of individual fluctuating asymmetry and the size of a given character. We tested these two predictions in plants since flowers are subjected to strong directional selection and are involved in signalling to pollinators, whereas leaves are supposed not to be directly involved in signalling. The overall level of fluctuating asymmetry in a number of plant species with bilaterally or radially symmetric flowers was not generally higher in floral traits than in leaves. The level of fluctuating asymmetry in plants was sometimes significantly consistent within individuals. The absolute degree of individual fluctuating asymmetry in floral traits was generally negatively related to the size of the trait, while there was a positive relationship for leaves. The degree of individual fluctuating asymmetry in floral traits was marginally negatively related to the degree of individual fluctuating asymmetry in leaf traits. These patterns of fluctuating asymmetry in plants suggest that (i) the degree of asymmetry in flowers signals different aspects of quality than does the degree of asymmetry in leaves, and that (ii) fluctuating asymmetry in flowers often reflects the phenotypic quality of individual plants.     

Developmental stability,sexual selection and speciation

Fluctuating asymmetry occurs when an individual is unable to undergo identical development of an otherwise bilaterally symmetric trait on both sides of its body. Since both sides of a bilaterally symmetric trait are the result of the actions of a single genome, fluctuating asymmetry represents an epigenetic measure of the sensitivity of development to stress. Different morphological traits may show a direct relationship between their functional importance and their degree of developmental canalization. This may explain why some characters show high degrees of fluctuating asymmetry, and why these characters more often become exaggerated secondary sexual ornaments. The degree of fluctuating asymmetry is generally larger in small marginal populations living in novel environments, and this will particularly lead to relatively large degrees of asymmetry in the least developmentally canalized traits. More stringent selection against heterozygotes in marginal populations may further break down developmental stability and linkage groups which would lead to increased genetic variance. Females may prefer to mate with males having large, but relatively symmetric morphological characters, because it is more difficult to make large traits (a good genes argument), a large trait is more easily perceived (a sensory bias preference), and because symmetry signals ability to cope with stress (a good genes argument). The low degree of developmental stability and the large amount of genetic variance in secondary sexual characters in small, marginal populations could set the scene for rapid development of divergence and speciation in marginal populations.     

Evolution of animal genitalia: morphological correlates of fitness components in a water strider

Rapid divergence of male genitalia is one of the most general evolutionary trends in animals with internal fertilization, but the mechanisms of genital evolution are poorly understood. The current study represents the first comprehensive attempt to test the main hypotheses that have been suggested to account for genital evolution (the lock-and-key, sexual selection and pleiotropy hypotheses) with intraspecific data. We measure multivariate phenotypic selection in a water strider species, by relating five different components of fitness (mating frequency, fecundity, egg hatching rate, offspring survival rate and offspring growth rate) to a suite of genital and non-genital morphological traits (in total 48). Body size had a series of direct effects in both sexes. Large size in females was positively related to both fecundity and egg hatching rate. There was positive sexual selection for large size in males (mating frequency), which to some extent was offset by a reduced number of eggs laid by females mated to large males. Male genitalic morphology influenced male mating frequency, but the detected directional selection on genitalia was due to indirect selection on phenotypically correlated non-intromittent traits. Further, we found no assortative mating between male intromittent genitalia and female morphology. Neither did we find any indications of male genitalia conveying information of male genetic quality. Several new insights can be gained from our study. Most importantly, our results are in stark disagreement with the long standing lock-and-key hypothesis of genital evolution, as well as with certain models of sexual selection. Our results are, however, in agreement with other models of sexual selection as well as with the pleiotropy hypothesis of genital evolution. Fluctuating asymmetry of bilaterally symmetrical traits, genital as well as non-genital, had few effects on fitness. Females with low fluctuating asymmetry in leg length produced offspring with a higher survival rate, a pattern most proba bly caused by direct phenotypic maternal effects. We also discuss the relevance of our results to sexual conflict over mating, and the evolution of sexual traits by coevolutionary arms races between the sexes.     

Phenotypic variation and fluctuating asymmetry in sexually dimorphic feather ornaments in relation to sex and mating system

Secondary sexual characters have been hypothesized to demonstrate increased phenotypic variation between and within individuals as compared to ordinary morphological traits. We tested whether this was the case by studying phenotypic variation, expressed as the coefficient of variation (CV), and developmental instability, measured as fluctuating asymmetry (FA), in ornamental and non-ornamental traits of 70 bird species with feather ornamentation while controlling for similarity among species due to common descent. Secondary sexual characters differed from ordinary morphological traits by showing large phenotypic CV and FA. This difference can be explained by the different mode of selection operating on each kind of trait: a history of intense directional (ornaments) and stabilizing selection (non-ornaments). Phenotypic variation is reduced in the sex with more intense sexual selection (males), but does not differ among species with different mating systems. The strength of stabilizing selection arising from natural selection is associated with decreased CV (wing CV is smaller than tarsus or tail CVs). We found evidence of FA being reduced in ornamental feathers strongly affected by aerodynamics (tail feathers) compared to other ornaments, but only in females. In conclusion, CV and FA were not related, suggesting mat phenotypic plasticity and developmental instability are independent components of phenotypic variation.     

Ectoparasitism in mothers causes higher positional fluctuating asymmetry in their sons: implications for sexual selection

Random deviations from perfect bilateral symmetry, fluctuating asymmetry, arise from developmental instability. I tested experimentally whether parasitism in female Drosophila nigrospiracula increases fluctuating asymmetry in male offspring. I also developed a novel measure for estimating developmental instability in a meristic trait called positional fluctuating asymmetry, which is based on the difference in the position of thoracic bristles between the right and left sternopleuron. I expected this measure to be a more sensitive indicator of developmental instability than the traditional numerical fluctuating asymmetry, because the latter is based on the difference in the actual presence or absence of bristles. Female flies burdened with hematophagous mites, Macrocheles subbadius (Macrochelidae), produced sons with significantly higher positional fluctuating asymmetry than did females carrying no mites. This effect, which may have resulted from impaired provisioning of oocytes by infested females, was dose dependent and magnified in the progeny of younger (18-20 d) versus older (30-32 d) females. This apparent magnification resulted from a slight but not significant increase in asymmetry of offspring of the older and unparasitized females. In contrast, the same mite loads had no effect on offspring numerical fluctuating asymmetry. If low-positional fluctuating asymmetry males enjoy a mating advantage, then with appropriate genetic variability, sexual selection could drive the evolution of host resistance in host populations. However, variability in neither kind of asymmetry influenced male mating success in nature. Thus, although male positional fluctuating asymmetry is causally associated with parasitism via maternal effects, asymmetry-based sexual selection is unlikely to influence the evolution of mite resistance in D. nigrospiracula. The value of the sensitivity afforded by positional fluctuating asymmetry is discussed in the context of sexual selection and conservation biology.     

Environmental origins of sexually selected variation and a critique of the fluctuating asymmetry-sexual selection hypothesis

Identifying sources of phenotypic variability in secondary sexual traits is critical for understanding their signaling properties, role in sexual selection, and for predicting their evolutionary dynamics. The present study tests for the effects of genotype, developmental temperature, and their interaction, on size and fluctuating asymmetry of the male sex comb, a secondary sexual character, in Drosophila bipectinata Duda. Both the size and symmetry of elements of the sex comb have been shown previously to be under sexual selection in a natural population in northeastern Australia. Two independent reciprocal crosses were conducted at 25 degrees and 29 degrees C between genetic lines extracted from this population that differed in the size of the first (TC1) and third (TC3) comb segments. These temperatures are within the documented range experienced by the species in nature. Additive and dominance genetic effects were detected for TC1, whereas additive genetic, and Y-chromosomal effects were detected for TC3. TC2 and TC3 decreased sharply with increasing temperature, by 10% and 22%, respectively. In contrast, positional fluctuating asymmetry (PFA) significantly increased with temperature, by up to 38%. The results (1) document an important source of environmental variance in a sexual ornament expected to reduce trait heritability in field populations, and thus act to attenuate response to sexual selection, (2) suggest that variation in ornament size reflects differences in male condition; and (3) support the general hypothesis that asymmetry in a sexual ornament is indicative of developmental instability arising from environmental stress. The "environmental heterogeneity" (EH) hypothesis is proposed, and supportive evidence for it presented, to explain negative size-FA correlations in natural populations. Data and theory challenge the use of negative size-FA correlations observed in nature to support the FA-sexual selection hypothesis, which posits that such correlations are driven by differences in genetic quality among individuals.     

Parasites increase fluctuating asymmetry of maleDrosophila nigrospiracula: Implications for sexual selection

Fluctuating asymmetry (minor deviations from perfect bilateral symmetry) is manifested by individuals less able to buffer environmental stress during development. I utilized a system of two naturally-occurring parasites ofDrosophila nigrospiracula to test whether parasitic infection during host development yields elevated degrees of fluctuating asymmetry in two morphological traits of males. This hypothesis has important implications for sexual selection, as it may explain why asymmetric males are often found to be sexually disadvantaged. In my system, nematodes infect larvae and therefore are more likely to disrupt development than mites which only parasitize adult flies. As predicted, nematode-infected maleD. nigrospiracula had a higher degree of bristle asymmetry than did mite-infested and control (carrying neither parasite) males. There was also a significant relation between nematode number and degree of asymmetry. There was a significant negative relation between nematode load and size of adult males, implicating a causal link between nutritional stress during host development and fluctuating asymmetry. Patterns of wing length asymmetry were inconsistent with those of bristle asymmetry. Nematode-infected males did not differ in wing length asymmetry relative to mite-infested and control males, nor was there a significant relation between nematode number and wing asymmetry. This inconsistency in expression of asymmetry may reflect different intensities of selection operating on each morphological trait.     

The evolution of human sexuality

The study of human sexuality from the darwinian perspective is in an explosive phase. Recent research is diverse; for instance, the dynamics of heterosexual relationships, the role of honest advertisement in attractiveness, the role of fluctuating asymmetry in sexual competition, and sexual conflict over fertilization, seen in sperm competition adaptations of men and possible cryptic sire-choice adaptation of women. Also, recent research reveals that the sexual selection that designed human secondary sexual traits was functional rather than strictly fisherian.     

Bilateral symmetry and sexual selection: a meta-analysis

A considerable body of primary research has accumulated over the last 10 yr testing the relationship between developmental instability in the form of fluctuating asymmetry and performance of individuals in mating success itself or sexual attractiveness. This research comprises 146 samples from 65 studies of 42 species of four major taxa. We present the results of a meta-analysis of these studies, which demonstrates that there is indeed an overall significant, moderate negative relationship: for studies, the overall mean Pearson's r or effect size = -.42, P <.0005; for species, the overall mean r = -.34, .01 < P < .025. Based on calculated fail-safe numbers, the effect-size estimates are highly robust against any publication or reporting bias that may exist. There is considerable evidence that the magnitude of the negative correlation between fluctuating asymmetry and success related to sexual selection is greater for males than for females, when a secondary sexual trait rather than an ordinary trait is studied, with experimentation compared with observation, and for traits not involved with mobility compared with traits affecting mobility. There is also limited evidence that higher taxa may differ in effect size and that intensity of sexual selection negatively correlates with effect size.     

Within-individual changes in developmental stability affect flight performance

Developmental stability, as measured by fluctuating asymmetry,has been purported to be an indicator of individual quality,and low asymmetry can be selected for by sexual selection processes.However, low asymmetry can also arise due to biomechanical constraintsoperating on trait design, as it is predicted that asymmetrywill decrease mechanical efficiency. Specifically, it has beenpredicted that wing length asymmetry will be negatively relatedto avian flight performance. To date, empirical investigationshave only studied the influence of increasing asymmetry beyondnaturally occurring average values. I examined the influenceof within-individual changes in primary feather developmentalstability on flight performance in European starlings by studyingasymmetry and flight before and after wing molt. Individualsthat exhibited a decrease in wing asymmetry through molt experiencedincreased aerodynamic performance in terms of both angle oftakeoff and level flapping-flight speed. Birds that increasedwing asymmetry suffered a decrease in flight performance. Takeoffspeed and the ability to negotiate an aerial obstacle coursewere unaffected by asymmetry. My data provide empirical supportfor the predicted influence of wing asymmetry on flight, eventhough the changes in asymmetry were very small (mean = 0.47%of trait size) and further indicate the importance of biomechanicalconsiderations in any study of developmental stability     

Response of fluctuating and directional asymmetry to selection on wing shape in Drosophila melanogaster

We tested whether directional selection on an index-based wing character in Drosophila melanogaster affected developmental stability and patterns of directional asymmetry. We selected for both an increase (up selection) and a decrease (down selection) of the index value on the left wing and compared patterns of fluctuating and directional asymmetry in the selection index and other wing traits across selection lines. Changes in fluctuating asymmetry across selection lines were predominantly small, but we observed a tendency for fluctuating asymmetry to decrease in the up-selected lines in both replicates. Because changes in fluctuating asymmetry depended on the direction of selection, and were not related to changes in trait size, these results fail to support existing hypotheses linking directional selection and developmental stability. Selection also produced a pattern of directional asymmetry that was similar in all selected lines whatever the direction of selection. This result may be interpreted as a release of genetic variance in directional asymmetry under selection.     

What does sexual trait FA tell us about stress?

There is widespread acceptance that fluctuating asymmetry (FA) increases under environmental and genetic stress. Fluctuating asymmetry in sexual traits is thought to be particularly sensitive to stress and to reflect genetic and phenotypic quality. Recent experimental studies show that the relationship between FA and stress is inconsistent, and there is little evidence that sexual traits are especially responsive to stress.