SEXUAL SELECTION IN THE BARN SWALLOW HIRUNDO RUSTICA. III. FEMALE TAIL ORNAMENTS

Male secondary sexual characters are often expressed in females, and the maintenance of the character in females can be due to either direct selection on females favoring the maintenance of the trait, or a correlated response to selection in males. Here I report on determinants of and phenotypic selection on tail length of female barn swallows Hirundo rustica. The homologous trait in males is under strong directional sexual selection. Female tail length was positively associated with several reproductive parameters including total seasonal reproductive success, even when controlling for year and age effects. A change in female tail length from one year to another was often associated with a change in the reproductive parameters correlated with absolute tail length. There was little evidence for an association between female tail length and the duration of the incubation period (only females incubate) and absolute and relative female provisioning rates of offspring, and subsequent size of offspring. Tail length of female barn swallows was positively correlated with that of their mates. Female tail length was a heritable trait as determined from regression of the tail trait of offspring on that of their mother and their father, and there was a positive genetic correlation between the tail trait in males and females. In conclusion, female tail length reliably reflects female reproductive potential, and the trait appears to be under directional selection, which may result in an evolutionary response to selection because of the heritability of the tail trait.     

RECONSTRUCTING THE EVOLUTION OF SEXUAL DICHROMATISM: CURRENT COLOR DIVERSITY DOES NOT REFLECT PAST RATES OF MALE AND FEMALE CHANGE

Males of sexually dimorphic species often appear more divergent among taxa than do females, so it is often assumed that evolutionary changes have occurred primarily in males. Yet, sexual dimorphisms can result from historical changes in either or both of the sexes, and few previous studies have investigated such patterns using phylogenetic methods. Here, we describe the evolution of male and female plumage colors in the grackles and allies (Icteridae), a songbird clade with a broad range in levels of sexual dichromatism. Using a model of avian perceptual color space, we calculated color distances within and among taxa on a molecular phylogeny. Our results show that female plumage colors have changed more dramatically than male colors in the evolutionary past, yet male colors are significantly more divergent among species today. Historical increases in dichromatism have involved changes in both sexes, whereas decreases in dichromatism have nearly always involved females evolving rapidly to look like males. Dichromatism is also associated with mating system in this group, with monogamous taxa tending to exhibit relatively low levels of sexual dichromatism. Our findings suggest that, despite appearances, female plumage evolution plays a more prominent role in sexual dichromatism than is generally assumed.     

MULTIPLE GENETIC LINKAGES BETWEEN FEMALE PREFERENCE AND MALE SIGNAL IN RAPIDLY SPECIATING HAWAIIAN CRICKETS

Diverging sexual communication systems can lead to the evolution of new species that no longer recognize each other as potential mates. The coevolution of male and female components of sexual communication is facilitated by physical linkage between genes underlying signals and preferences. By crossing two closely related Hawaiian crickets (Laupala kohalensis and Laupala paranigra) with vastly different song pulse rates and female preferences, and assessing segregation of songs and preferences among second generation backcrosses, we show a strong genetic correlation between song and preference variation. Furthermore, multiple, but not all, quantitative trait loci underlying song variation also predict female preferences. This physical linkage or pleiotropy may have facilitated the striking diversification of pulse rates observed among Laupala species in conjunction with one of the most rapid species radiations so far recorded.     

SEXUAL SELECTION IN A WOLF SPIDER: MALE DRUMMING ACTIVITY,BODY SIZE,AND VIABILITY

Females are often believed to actively choose highly ornamented males (males with extravagant morphological signals or intense sexual display), and ornaments should be honest signals of male viability. However, this belief is relying only on some pieces of empirical evidence from birds. Our study reports active female choice on sexual display that indicates male viability in spiders. We established trials in which we studied female choice in relation to male courtship drumming activity and body size. Females chose the most actively drumming males as mating partners, but the body size of the males did not seem to be selected. Male drumming activity turned out to be a good predictor of male viability, whereas male viability was independent of male body mass. Our results suggest that by actively choosing mates according to male drumming performance, but independently of male body mass, females are preferring viable males as mates. Because Hygrolycosa rubrofasciata males do not provide obvious direct benefits to their offspring, females may gain some indirect benefits; offspring may have higher chance of survival, or the offspring may inherit the attractiveness of their father.     

A PHYLOGENETIC PERSPECTIVE ON THE EVOLUTION OF SEXUAL DICHROMATISM IN TANAGERS (THRAUPIDAE): THE ROLE OF FEMALE VERSUS MALE PLUMAGE

The evolution of sexual dichromatism in tanagers (family Thraupidae) was studied from a phylogenetic perspective using a molecular-based phylogeny. Mapping patterns of sexual dimorphism in plumage onto the phylogeny reveals that changes in female plumage occur more frequently than changes in male plumage. Possible explanations for this pattern include sexual selection acting on female plumage and natural selection for background matching. The results of this study and other recent phylogenetic and comparative studies suggest that factors affecting female plumage are important in shaping patterns of sexual dimorphism.     

SEXUAL SELECTION AND MALE CHARACTERISTICS IN THE BLUEHEAD WRASSE,THALASSOMA BIFASCIATUM: MATING SITE ACQUISITION,MATING SITE DEFENSE,AND FEMALE CHOICE

Through a series of replacement experiments with the bluehead wrasse, Thalassoma bifasciatum, we have identified male morphological characteristics that appear to be under phenotypic sexual selection. We were particularly interested in whether the various sources of sexual selection (male-male competition for unoccupied mating sites, defense of mating sites against small males, and female choice of males) were (1) independently associated with different phenotypic characteristics; (2) jointly affected the same characteristic in the same way; or (3) jointly affected the same characteristic in an antagonistic fashion. We replaced the resident large, brightly colored Terminal Phase (TP) males on a reef with the same number of TP males from other reefs. When transplanted, these males contest with each other to take over mating sites. The transplanted group of males were then scored for three components of fitness: (1) the quality of the site obtained through competition with other large males; (2) the male's ability to defend arriving females from small intruding males; and (3) changes in female visits to the site once the new male takes over. The first and second components are part of intrasexual selection; the third represents intersexual selection. We measured the opportunity for selection by partitioning variance in mating success, and measured the direct effects of sexual selection by estimating the covariance between morphology and fitness components. Opportunities for selection: Because females generally remain faithful to particular mating sites, most (54%) of the explainable variation in male mating success is due to the acquisition of a particular mating territory, which is the outcome of competition among TP males. There was less variation in mating success due to shifts in site use by females and defense of females against the intrusions of smaller males, but all components were significant. Effects of selection: Success in male–male competition among TP males, estimated by the quality of the territory acquired, was positively associated with body length and the relative length of the pectoral fin. Success in territorial defense against small males was primarily related to body length, with lesser contributions from body depth and the area of a white band on the flank. Contribution to fitness through female choice of males was positively associated with white band area. In the two instances where a character was associated with two fitness components, the direction of selection was the same. While body length was positively associated with winning intrasexual contests, it was not correlated to any behavioral measures of aggression. Similarly, the white band associated with attractiveness was not correlated with any aspect of courtship or aggression. Parasite load was uncorrelated with other morphological characters, and did not appear to affect any aspect of sexual selection. There was no evidence for stabilizing selection or significant additional contributions from second-order effects to the fitness surfaces. Fitness functions calculated using cubic splines were generally linear except for body length, which appeared sigmoid in its effect on site acquisition ability; this same feature tended to plateau in its effect on site defense. Analyses of the interactions of selection gradients with reef or experiment indicated that the effect of particular male characters on estimates of fitness was generally homogeneous in both time and space.     

DIRECT AND INDIRECT SEXUAL SELECTION AND QUANTITATIVE GENETICS OF MALE TRAITS IN GUPPIES (POECILIA RETICULATA)

Abstract.— The ornamentation and displays on which sexual attractiveness and thus mating success are based may be complex and comprise several traits. Predicting the outcome of sexual selection on such complex phenotypes requires an understanding of both the direct operation of selection on each trait and the indirect consequences of selection operating directly on genetically correlated traits. Here we report the results of a quantitative genetic analysis of the ornamentation, sexual attractiveness, and mating success of male guppies (Poecilia reticulata). We analyze male ornamentation both from the point of view of single ornamental traits (e.g., the area of each color) and of composite measures of the way the entire pattern is likely to be perceived by females (e.g., the mean and contrast in chroma). We demonstrate that there is substantial additive genetic variation in almost all measures of male ornamentation and that much of this variation may be Y linked. Attractiveness and mating success are positively correlated at the phenotypic and genetic level. Orange area and chroma, the area of a male's tail, and the color contrast of his pattern overall are positively correlated with attractiveness and/or mating success at the phenotypic and genetic levels. Using attractiveness and mating success as measures of fitness, we estimate gradients of linear directional sexual selection operating on each male trait and use equations of multivariate evolutionary change to predict the response of male ornamentation to this sexual selection. From these analyses, we predict that indirect selection may have important effects on the evolution of male guppy color patterns.     

REDUCED GENETIC VARIANCE AMONG HIGH FITNESS INDIVIDUALS: INFERRING STABILIZING SELECTION ON MALE SEXUAL DISPLAYS IN DROSOPHILA SERRATA

Directional selection is prevalent in nature, yet phenotypes tend to remain relatively constant, suggesting a limit to trait evolution. However, the genetic basis of this limit is unresolved. Given widespread pleiotropy, opposing selection on a trait may arise from the effects of the underlying alleles on other traits under selection, generating net stabilizing selection on trait genetic variance. These pleiotropic costs of trait exaggeration may arise through any number of other traits, making them hard to detect in phenotypic analyses. Stabilizing selection can be inferred, however, if genetic variance is greater among low‐ compared to high‐fitness individuals. We extend a recently suggested approach to provide a direct test of a difference in genetic variance for a suite of cuticular hydrocarbons (CHCs) in Drosophila serrata. Despite strong directional sexual selection on these traits, genetic variance differed between high‐ and low‐fitness individuals and was greater among the low‐fitness males for seven of eight CHCs, significantly more than expected by chance. Univariate tests of a difference in genetic variance were nonsignificant but likely have low power. Our results suggest that further CHC exaggeration in D. serrata in response to sexual selection is limited by pleiotropic costs mediated through other traits.     

SEQUENTIAL FEMALE ASSESSMENT DRIVES COMPLEX SEXUAL SELECTION ON BOWER SHAPE IN A CICHLID FISH

In many animals, sexual selection on male traits results from female mate choice decisions made during a sequence of courtship behaviors. We use a bower‐building cichlid fish, Nyassachromis cf. microcephalus, to show how applying standard selection analysis to data on sequential female assessment provides new insights into sexual selection by mate choice. We first show that the cumulative selection differentials confirm previous results suggesting female choice favors males holding large volcano‐shaped sand bowers. The sequential assessment analysis reveals these cumulative differentials are the result of selection acting on different bower dimensions during the courtship sequence; females choose to follow males courting from tall bowers, but choose to engage in premating circling with males holding bowers with large diameter platforms. The approach we present extends standard selection analysis by partitioning the variances of increasingly accurate estimates of male reproductive fitness and is applicable to systems in which sequential female assessment drives sexual selection on male traits.     

GENETIC CORRELATION BETWEEN A FEMALE MATING PREFERENCE AND THE PREFERRED MALE CHARACTER IN SEAWEED FLIES (COELOPA FRIGIDA)

The mating preferences of female seaweed flies Coelopa frigida were determined by observing their acceptance or rejection of males of known size. The inversion karyotype of both males and females was also determined. Females exhibited a preference to mate with large males, and evidence is presented that a genetic correlation exists between the female preference and the preferred trait. Females carrying the inversion karyotype associated with large male size showed a strong preference for large males; females carrying the inversion associated with small male size also exhibited a preference for large males, but it was significantly less strong. This finding suggests that a Fisherian process may be operating.     

INTRALOCUS SEXUAL CONFLICT AND ENVIRONMENTAL STRESS

Intralocus sexual conflict (IaSC) occurs when selection at a given locus favors different alleles in males and females, placing a fundamental constraint on adaptation. However, the relative impact of IaSC on adaptation may become reduced in stressful environments that expose conditionally deleterious mutations to selection. The genetic correlation for fitness between males and females (r_MF) provides a quantification of IaSC across the genome. We compared IaSC at a benign (29°C) and a stressful (36°C) temperature by estimating r_MFs in two natural populations of the seed beetle Callosobruchus maculatus using isofemale lines. In one population, we found substantial IaSC under benign conditions signified by a negative r_MF (?0.51) and, as predicted, a significant reduction of IaSC under stress signified by a reversed and positive r_MF (0.21). The other population displayed low IaSC at both temperatures (r_MF: 0.38; 0.40). In both populations, isofemale lines harboring alleles beneficial to males but detrimental to females at benign conditions tended to show overall low fitness under stress. These results offer support for low IaSC under stress and suggest that environmentally sensitive and conditionally deleterious alleles that are sexually selected in males mediate changes in IaSC. We discuss implications for adaptive evolution in sexually reproducing populations.     

MALE MATE CHOICE AND THE EVOLUTION OF FEMALE PLUMAGE COLORATION IN THE HOUSE FINCH

The house finch (Carpodacus mexicanus) is a sexually dichromatic passerine in which males display colorful plumage and females are generally drab brown. Some females, however, have a subdued version of the same pattern of ornamental coloration seen in males. In previous research, I found that female house finches use male coloration as an important criterion when choosing mates and that the plumage brightness of males is a reliable indicator of male nest attentiveness. Male house finches invest substantially in the care of young and, like females, stand to gain by choosing high-quality mates. I therefore hypothesized that a female's plumage brightness might be correlated with her quality and be the basis for male mate choice. In laboratory mate choice experiments, male house finches showed a significant preference for the most brightly plumaged females presented. Observations of a wild population of house finches, however, suggest that female age is the primary criterion in male choice and that female plumage coloration is a secondary criterion. In addition, yearling females tended to have more brightly colored plumage than older females, and there was no relationship between female plumage coloration and overwinter survival, reproductive success, or condition. These observations fail to support the idea that female plumage coloration is an indicator of individual quality. Male mate choice for brightly plumaged females may have evolved as a correlated response to selection on females to choose brightly colored males.     

POPULATION DIVERGENCE IN SEXUAL ORNAMENTS: THE WHITE FOREHEAD PATCH OF NORWEGIAN PIED FLYCATCHERS IS SMALL AND UNSEXY

Models of sexual selection suggest that populations may easily diverge in male secondary sexual characters. Studies of a Spanish population of the pied flycatcher, Ficedula hypoleuca, and a Swedish population of the closely related collared flycatcher, F. albicollis, have indicated that the white forehead patch of males is a sexually selected trait. We studied the white forehead patch of male pied flycatchers (n = 487) in a Norwegian population over seven years. Males with large forehead patches were in general more brightly colored, but patch height was not correlated to body mass, body size, or parasite loads. Conditions during the nestling period did not seem to influence patch height as an adult. Patch height increased slightly from the first to the second year as adults, but then remained relatively constant at higher ages. Patch height was not related to survival. Year-to-year changes showed that males who increased in patch height also increased in body mass, suggesting that expression of the forehead patch may be partly condition dependent. However, changes in body mass explained only a small proportion of the variance in patch height between males. Thus, patch height would not be a good indicator of male quality. Furthermore, patch size was also not related to male ability to feed nestlings, indicating that females would not obtain direct benefits by choosing males with large patches. However, patch height could be a Fisher trait, but this requires heritability and there was no significant father-son resemblance in patch height. Comparisons of the males visited by each female during the mate sampling period indicated that chosen males did not have larger forehead patches than rejected males. Experimental manipulation of patch height did not affect male mating success. These results indicate that females do not use patch size as a mate choice cue. Finally, patch height did not predict the outcome of male contests for nestboxes, suggesting that the forehead patch is not an intrasexually selected cue of status. Norwegian pied flycatchers have smaller forehead patches than both Spanish pied flycatchers and Swedish collared flycatchers. We suggest that this pattern may be explained by the lack of sexual selection on the forehead patch in the Norwegian population as compared to the other populations, where the patch is apparently sexually selected. We discuss possible reasons for these population divergences, such as female choice on an alternative secondary sexual character (general plumage color) and speciation among Ficedula flycatchers.     

FEMALE PROMISCUITY IS POSITIVELY ASSOCIATED WITH NEUTRAL AND SELECTED GENETIC DIVERSITY IN PASSERINE BIRDS

Passerine birds show large interspecific variation in extrapair paternity rates. There is accumulating evidence that such promiscuous behavior is driven by indirect, genetic benefits to females. Sexual selection theory distinguishes between two types of genetic benefits, additive and nonadditive effects, mediated by preferences for good and compatible genes, respectively. Good genes preferences should imply directional selection and mating skew among males, and thus reduced genetic diversity in the population. In contrast, compatible genes preferences should give balancing selection that retains genetic diversity. Here, we test how well these predictions fit with patterns of variation in genetic diversity and promiscuity levels among passerine birds. We found that more promiscuous species had higher nucleotide diversity at autosomal introns, but not at Z‐chromosome introns. We also found that major histocompatibility complex (MHC) class IIB alleles had higher sequence diversity, and therefore should recognize a broader spectrum of pathogens, in more promiscuous species. Our results suggest that female promiscuity targets a multitude of autosomal genes for their nonadditive, compatibility benefits. Also, as immunity genes seem to be of particular importance, we hypothesize that interspecific variation in female promiscuity among passerine birds has arisen in response to the strength of pathogen‐mediated selection.     

FEMALE AND MALE GENETIC EFFECTS ON OFFSPRING PATERNITY: ADDITIVE GENETIC (CO)VARIANCES IN FEMALE EXTRA‐PAIR REPRODUCTION AND MALE PATERNITY SUCCESS IN SONG SPARROWS (MELOSPIZA MELODIA)

Ongoing evolution of polyandry, and consequent extra‐pair reproduction in socially monogamous systems, is hypothesized to be facilitated by indirect selection stemming from cross‐sex genetic covariances with components of male fitness. Specifically, polyandry is hypothesized to create positive genetic covariance with male paternity success due to inevitable assortative reproduction, driving ongoing coevolution. However, it remains unclear whether such covariances could or do emerge within complex polyandrous systems. First, we illustrate that genetic covariances between female extra‐pair reproduction and male within‐pair paternity success might be constrained in socially monogamous systems where female and male additive genetic effects can have opposing impacts on the paternity of jointly reared offspring. Second, we demonstrate nonzero additive genetic variance in female liability for extra‐pair reproduction and male liability for within‐pair paternity success, modeled as direct and associative genetic effects on offspring paternity, respectively, in free‐living song sparrows (Melospiza melodia). The posterior mean additive genetic covariance between these liabilities was slightly positive, but the credible interval was wide and overlapped zero. Therefore, although substantial total additive genetic variance exists, the hypothesis that ongoing evolution of female extra‐pair reproduction is facilitated by genetic covariance with male within‐pair paternity success cannot yet be definitively supported or rejected either conceptually or empirically.     

PROMISCUITY,SEXUAL SELECTION,AND GENETIC DIVERSITY: A REPLY TO SPURGIN

We recently reported a positive association between female promiscuity and genetic diversity across passerine birds, and launched the hypothesis that female promiscuity acts as a balancing selection, pressure maintaining genetic diversity in populations (Gohli et al. 2013 ). Spurgin ( 2013 ) questions both our analyses and interpretations. While we agree that the hypothesis needs more comprehensive empirical testing, we find his specific points of criticism unjustified. In a more general perspective, we call for a more explicit recognition of female mating preferences as mechanisms of selection in population genetics theory.     

GOOD GENES DRIVE FEMALE CHOICE FOR MATING PARTNERS IN THE LEK-BREEDING EUROPEAN TREEFROG

Investigating the mechanisms underlying female mate choice is important for sexual-selection theory, but also for population-genetic studies, because distinctive breeding strategies affect differently the dynamics of gene diversity within populations. Using field-monitoring, genetic-assignment, and laboratory-rearing methods, we investigated chorus attendance, mating success and offspring fitness in a population of lek-breeding tree-frogs ( Hyla arborea ) to test whether female choice is driven by good genes or complementary genes. Chorus attendance explained ∼50% of the variance in male mating success, but did not correlate with offspring fitness. By contrast, offspring body mass and growth rate correlated with male attractiveness, measured as the number of matings obtained per night of calling. Genetic similarity between mating partners did not depart from random, and did not affect offspring fitness. We conclude that females are able to choose good partners under natural settings and obtain benefits from the good genes, rather than compatible genes, their offspring inherit. This heritability of fitness is likely to reduce effective population sizes below values previously estimated.     

FEMALE-FEMALE COMPETITION IN KATYDIDS: SEXUAL SELECTION FOR INCREASED SENSITIVITY TO A MALE SIGNAL?

In contrast to studies of sex-specific weaponry and other sexually selected traits, there has been no examination of Darwin's (1871, p. 418) suggestion that elaborations or enlargements of “the organs of sense” function to enhance mating success. In certain katydids the size of thoracic spiracles, which are a main input into the hearing system, determines auditory sensitivity of females. Here we present evidence that sexual dimorphism in the spiracle size of a pollen katydid, Kawanaphila nartee, is a result of sexual selection on females competing to locate nuptial-gift giving males. In field experiments in which female K. nartee were attracted to a calling male, we show a pairing advantage to females with larger auditory spiracles. The spiracle-size advantage was not a correlated result of a larger body size or mass of winners. Finally, there was no spiracle-size advantage or body-mass advantage for mating females in a later stage of competition when experimental females struggled for access to a silent male. We suggest that research on the detection of displays has lagged behind work on the displays themselves; the focus has been on the species specificity of signal perception rather than on the fitness consequences of variation in the ability to detect cues from mates or predators.     

TRAIT COMPENSATION AND SEX‐SPECIFIC AGING OF PERFORMANCE IN MALE AND FEMALE PROFESSIONAL BASKETBALL PLAYERS

Phenotypic traits are often influenced by dynamic resource allocation trade‐offs which, when occurring over the course of individual lifespan, may manifest as trait aging. Although aging is studied for a variety of traits that are closely tied to reproduction or reproductive effort, the aging of multiple traits related to fitness in other ways are less well understood. We took advantage of almost 30 years of data on human whole‐organism performance in the National Basketball Association (USA) to examine trends of aging in performance traits associated with scoring. Given that patterns of aging differ between sexes in other animal species, we also analyzed a smaller dataset on players in the Women's National Basketball Association to test for potential sex differences in the aging of comparable traits. We tested the hypothesis that age‐related changes in a specific aspect of overall performance can be compensated for by elevated expression of another, related aspect. Our analyses suggest that the aging of performance traits used in basketball is generally characterized by senescence in males, whereas age‐related changes in basketball performance are less evident in females. Our data also indicate a different rate of senescence of different performance traits associated with scoring over a male's lifetime.