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.     

Evolutionary dynamics of a sexual ornament in the house sparrow (Passer domesticus): the role of indirect selection within and between sexes

The relative contribution of sexual and natural selection to evolution of sexual ornaments has rarely been quantified under natural conditions. In this study we used a long-term dataset of house sparrows in which parents and offspring were matched genetically to estimate the within- and across-sex genetic basis for variation and covariation among morphological traits. By applying two-sex multivariate "animal models" to estimate genetic parameters, we estimated evolutionary changes in a male sexual ornament, badge size, from the contribution of direct and indirect selection on correlated traits within males and females, after accounting for overlapping generations and age-structure. Indirect natural selection on genetically correlated traits in males and females was the major force causing evolutionary change in the male ornament. Thus, natural selection on female morphology may cause indirect evolutionary changes in male ornaments. We observed however no directional phenotypic change in the ornament size of one-year-old males during the study period. On the other hand, changes were recorded in other morphological characters of both sexes. Our analyses of evolutionary dynamics in sexual characters require application of appropriate two-sex models to account for how selection on correlated traits in both sexes affects the evolutionary outcome of sexual selection.     

Timing of ornament growth, phenotypic variation, and size dimorphism in two promiscuous African whydahs (Ploceidae: Vidua)

Variation within populations is a prerequisite for the action of selection on morphological traits. Darwin assumed that there was much greater variation in sexual ornament size than in body size, but this may not be generally true of natural populations. I analyse field data on variation in body size and the length, area and mass of tail ornaments in paradise (Vidua paradisaea) and shaft-tailed whydahs (V. regia). Whydahs are promiscuous, brood parasitic African finches with elaborate tail ornaments in breeding males. The short, unadorned tails of male shaft-tailed whydahs, which carry a wire-like tail ornament, are non-significantly (1%) longer than female tails, but male paradise whydahs, which carry a large, broad ornament, have unadorned tails 10% longer than those of conspecific females. Fully grown ornament length, mass and area vary little more (CVs = 1.8-6.4%) than male or female body size traits (CVs = 1.7-6.1%). Instead, there is high variation in the timing of ornament development during prenuptial moult (CVs = 30.8–39.5% for paradise whydahs and 12.6–23.8% for shaft-tailed whydahs when corrected to a standard date). This temporal variation in development probably has greater significance for sexual selection in whydahs than maximum ornament size.     

I'm sexy and I glow it: female ornamentation in a nocturnal capital breeder

In many species, males rely on sexual ornaments to attract females. Females, by contrast, rarely produce ornaments. The glow-worm (Lampyris noctiluca) is an exception where wingless females glow to attract males that fly in search of females. However, little is known about the factors that promote the evolution of female ornaments in a sexual selection context. Here, we investigated if the female ornament of the glow-worm is a signal of fecundity used in male mate choice. In support of this, we found brightness to correlate with female fecundity, and males to prefer brighter dummy females. Thus, the glow emitted by females is a reliable sexual signal of female fecundity. It is likely that male preference for the fecundity-indicating ornament has evolved because of large variation among females in fecundity, and because nocturnal males cannot directly assess female size and fecundity. These results indicate that female ornamentation may evolve in capital breeders (i.e. those in which stored resources are invested in reproduction) when females vary significantly in fecundity and this variation cannot be assessed directly by males.     

No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius

Typically males bear the products of sexual selection in the form of ornaments and/or weapons used to compete for and attract females. Secondary sexual traits in females have been thought of as the product of correlated responses to sexual selection on males. However, there is increasing phylogenetic evidence that female secondary sexual traits can arise independently of selection on males, and may be subject to sexual selection. Theoretical models of the evolution of female ornamentation via male mate choice have assumed that females suffer a cost of ornament expression via reduced fecundity, and hence female ornaments are less likely to evolve than male ornaments. In the dung beetle Onthophagus sagittarius, there has been an independent evolutionary origin of horns in females that are qualitatively different from the horns produced by males. We use this system as a model to examine the costs of horn expression for females within a life-history context. We identified a longevity cost of reproduction for females that was independent of horn expression. Large females lived longer, and after controlling for lifespan, had a higher lifetime fecundity, and invested more heavily in maternal provisioning than did small females. We found no evidence of a cost to females of investment in horns. Rather, the rate of increase in fecundity and horn expression with body size were equal, so that absolute horn size provides an accurate indicator of body size and maternal quality. The effects we observe were independent of female contest competition and/or male mate choice, which were excluded in our experimental protocol. However, we speculate on the potential functional contributions female horns might make to female fitness.     

Sex-limited expression of ornamental feathers in birds

Extravagant secondary sexual characters show sexual size dimorphismin some species but are completely sex limited in others. Sexualornamentation has been hypothesized to benefit mainly malesthrough sexual selection, but the costs of secondary sexualcharacters initially would be experienced by both sexes. Theevolution of sexual size dimorphism of ornaments and, eventually, the complete sex-limited expression of these characters, willdepend on the effects of sexual and natural selection on thetwo sexes. A phylogenetic analysis controlling for similaritiesdue to common ancestry of 60 independent evolutionary originsof feather ornamentation in birds was used to investigate ecologicalfactors correlated with sexual size dimorphism and sex-limited expression of secondary sexual characters. When the size ofan ornament is large relative to body size, the trait willbe particularly costly for females, resulting in selectionfor increased sexual size dimorphism of the ornament. Indeed,sexual size dimorphism of ornaments was positively related to the relative size of male ornaments but was unrelated torelative size of female ornaments. Species with polygynousand lekking mating systems with little or no male parentalcare (in particular nest building and incubation) demonstratedsex-limited expression of ornaments as compared to monogamous species. Species with no food provisioning of offspring by themale showed a trend for increased sexual size dimorphism ofornaments. Therefore, large natural selection costs duringreproduction imposed by the expression of secondary sexualcharacters are related to the evolution of sexual size dimorphismof ornaments and eventually their complete loss from females.     

Plumage color as a composite trait: developmental and functional integration of sexual ornamentation

Most studies of condition-dependent sexual ornaments have treated such ornaments as single traits. However, sexual ornaments are often composites of several components, each produced by partially independent developmental pathways. Depending on environmental and individual condition, components of these ornaments may reflect different behavioral or physiological properties of an individual. One of the best-known, condition-dependent ornaments is carotenoid-based plumage coloration, which has at least four distinct components: pigment elaboration, patch area, pigment symmetry, and patch area symmetry. Here we examined fitness consequences of variation in individual components of carotenoid ornamentation in male house finches (Carpodacus mexicanus). Over 5 yr and several selection episodes, we studied variation in the plumage components in a large sample (n = 498) of males from a Montana population. The ornament components were partially independent of each other and had distinct fitness consequences. Selection for higher fecundity favored an increase in redness of coloration and a decrease in pigment asymmetry and patch area asymmetry but did not act on patch area itself. In contrast, viability selection favored larger and more symmetrical ornamental patches but did not act on pigment elaboration. Developmental and functional interrelationships among individual components of ornamentation strongly differed between house finch populations. Distinct patterns of selection on individual components of condition-dependent ornaments, combined with partially independent development of components, should favor the evolution of composite sexual traits whose components reliably reflect condition across a wide array of environments.     

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.     

Condition dependence of sexual ornament size and variation in the stalk-eyed fly Cyrtodiopsis dalmanni (Diptera: Diopsidae)

We used the stalk-eyed fly Cyrtodiopsis dalmanni to examine predictions made by condition-dependent handicap models of sexual selection. Condition was experimentally varied by manipulation of larval food availability. Cyrtodiopsis dalmanni is a highly dimorphic species exhibiting strong sexual selection, and the male sexual ornament (exaggerated eyespan) showed strong condition-dependent expression relative to the homologous trait in females and nonsexual traits. Male eyespan also showed a great increase in standardized variance under stress, unlike nonsexual traits. The inflated variance of the male ornament was primarily attributable to condition-dependent (but body-size-independent) increase in variance. Thus, evaluation of male eyespan allows females to gain additional information about male condition over and above that given by body size. These findings accord well with condition-dependent handicap models of sexual selection.     

No evidence of assortative mating on the basis of putative ornamental traits in Long‐tailed Finches Poephila acuticauda

When multiple ornaments are expressed in both sexes, they are generally assumed to be maintained by mutual sexual selection and have a function in mate choice. In the Long‐tailed Finch Poephila acuticauda both sexes exhibit multiple ornaments that vary in their expression in either size (pintail and throat patch) or colour (bill) between individuals and sexes. We assessed whether these ornaments are maintained by mutual sexual selection by exploring whether individuals in a wild population paired assortatively with respect to these ornamental traits, and the degree to which the expression of these ornamental traits was indicative of reproductive success. We found no evidence of assortative pairing with respect to variation in homologous ornaments or body condition in the two sexes. In addition, we found no effect of ornament expression on the reproductive success of either males or females. Our findings suggest that the expression of these apparently ornamental traits in both sexes of this species may play no current role in mutual mate selection or as indicator traits of reproductive performance. We are currently unable to identify any function for these very elaborate ornaments in either sex of this species and suggest that the typical assumption that all such traits have an ornamental function may need further examination.     

Experimental evidence that female ornamentation increases the acquisition of sperm and signals fecundity

Mate choice can lead to the evolution of sexual ornamentation. This idea rests on the assumption that individuals with more elaborate ornaments than competitors have higher reproductive success due to gaining greater control over mating decisions and resources provided by partners. Nevertheless, how the resources and quality of sexual partners that individuals gain access to are influenced by the ornamentation of rival individuals remains unclear. By experimentally concealing and subsequently revealing female ornaments to males, we confirm in the fowl, Gallus gallus, that female ornamentation influences male mating decisions. We further show, by manipulating the relative ornament size of females, that when females had larger ornaments than competitors they were more often preferred by males and obtained more sperm, especially from higher quality males, as measured by social status. Males may benefit by investing more sperm in females with larger ornaments as they were in better condition and produced heavier eggs. Female ornament size also decreased during incubation, providing a cue for males to avoid sexually unreceptive females. This study reveals how inter-sexual selection can lead to the evolution of female ornaments and highlights how the reproductive benefits gained from mate choice and bearing ornaments can be dependent upon social context.     

The allometric pattern of sexually size dimorphic feather ornaments and factors affecting allometry

The static allometry of secondary sexual characters is currently subject to debate. While some studies suggest an almost universal positive allometry for such traits, but isometry or negative allometry for nonornamental traits, other studies maintain that any kind of allometric pattern is possible. Therefore, we investigated the allometry of sexually size dimorphic feather ornaments in 67 species of birds. We also studied the allometry of female feathers homologous to male ornaments (female ornaments in the following) and ordinary nonsexual traits. Allometries were estimated as reduced major axis slopes of trait length on tarsus length. Ornamental feathers showed positive allometric slopes in both sexes, although that was not a peculiarity for ornamental feathers, because nonsexual tail feathers also showed positive allometry. Migration distance (in males) and relative size of the tail ornament (in females) tended to be negatively related to the allometric slope of tail feather ornaments, although these results were not conclusive. Finally, we found an association between mating system and allometry of tail feather ornaments, with species with more intense sexual selection showing a smaller degree of allometry of tail ornaments. This study is consistent with theoretical models that predict no specific kind of allometric pattern for sexual and nonsexual characters.     

Patterns of variation in ornaments of Crested Auklets Aethia cristatella

We investigated patterns of variation of feather and bill ornaments of Crested Auklets Aethia cristatella , a monogamous seabird, based on 963 individuals measured in the years 1990 to 1998. Three prominent ornaments were displayed: a forehead crest, composed of 11–31 curved feathers averaging about 40 mm in length, bilaterally symmetrical white auricular plumes on the sides of the head behind the eyes, averaging about 30 mm in length, and brightly coloured semi-circular rictal plates at the corners of the bill. As in other putative sexually selected traits, auklet ornaments were more variable across individuals than non-ornamental traits. Crest length and auricular plume length were positively correlated within individuals but not across years. Among the traits measured there was evidence for slight sexual dimorphism for the auricular plume and rictal plate ornaments and for culmen length and tarsus (males were slightly larger than females) but not for the crest ornament. Breeding adult females and males had greater crest and plume ornament expression than non-breeding adults. Paradoxically, females' crests and rictal plates were more variable than males' crests and rictal plates. Based on independent samples, the expression of feather ornaments and rictal plate varied among years between 1990 and 1998. Crested Auklet ornaments did not vary in concert with the ornaments of Whiskered Aethia pygmaea and Least Auklets Aethia pusilla during this period. Crested Auklet subadults had smaller ornaments than adults. Based on adults remeasured after an interval of one to seven years, the size of individuals' feather ornaments increased with age. We found no relationship between auricular plume length and asymmetry. Male auricular plumes and female crests were weakly correlated with body condition.     

Contrasting patterns of selection on the size and coloration of a female plumage ornament in common yellowthroats

Females often possess ornaments that appear smaller and duller than homologous traits in males. These ornaments may arise as nonfunctional by‐products of sexual selection in males and cause negative viability or fecundity selection in females in proportion to the cost of their production and maintenance. Alternatively, female ornaments may function as signals of quality that are maintained by sexual or social selection. In a 4‐year study of 83 female common yellowthroats (Geothlypis trichas) and their 222 young, we found strong viability and fecundity selection on the yellow bib, a carotenoid‐based plumage ornament that is a target of sexual selection in males. Females with larger bibs were older, larger and more fecund than females with smaller bibs. However, bib size positively covaried with bib total brightness and carotenoid chroma, aspects of bib coloration that were under negative viability and fecundity selection. Females with more colourful bibs laid fewer eggs in their first clutch, were more likely to suffer total brood loss due to predation and were less likely to return to the study area. Selection against bib coloration limits the value of bib size as a quality indicator in females and may constrain the elaboration of bib attributes in males.     

Multiple Ornaments in Male Northern Cardinals, Cardinalis cardinalis, as Indicators of Condition

Investigations of male ornaments in the context of sexual selection have tended to focus on single ornaments, although many species of birds possess multiple ornaments. Understanding the evolution of multiple ornaments requires knowledge of correlations among ornaments in the same individual and the extent to which ornament expression reflects individual condition and behavior. Variation in four male ornaments in socially monogamous, biparental northern cardinals (Cardinalis cardinalis) was related to body size, indices of condition, level of paternal care, and reproductive success. Redness of breast plumage positively predicted body size and negatively predicted nestling feeding rate. Bill color predicted current body condition, with birds with redder bills in better condition. Birds with smaller black face masks had greater reproductive success. These results are consistent with the hypothesis that different ornaments in male cardinals provide information on different aspects of condition and behavior.     

The sexual selection paradigm: have we overlooked other mechanisms in the evolution of male ornaments?

Extravagant male ornaments expressed during reproduction are almost invariably assumed to be sexually selected and evolve through competition for mating opportunities. Yet in species where male reproductive success depends on the defence of offspring, male ornaments could also evolve through social competition for offspring survival. However, in contrast to female ornaments, this possibility has received little attention in males. We show that a male ornament that is traditionally assumed to be sexually selected—the red nuptial coloration of the three-spined stickleback—is under stronger selection for offspring survival than for mating success. Males express most coloration during parenting, when they no longer attract females, and the colour correlates with nest retention and hatching success but not with attractiveness to females. This contradicts earlier assumptions and suggests that social selection for offspring survival rather than for sexual selection for mating success is the main mechanism maintaining the ornament in the population. These results suggest that we should consider other forms of social selection beyond sexual selection when seeking to explain the function and evolution of male ornaments. An incorrect assignment of selection pressures could hamper our understanding of evolution.     

Stabilizing sexual selection for female ornaments in a dance fly

Ornamental traits function by improving attractiveness and are generally presumed to experience directional selection for mating success. However, given the greater investment of females in offspring than males, female-specific ornaments can in theory signal fecundity yet be constrained by fecundity costs. Theoretical work predicts that such constraints can lead to stabilizing selection via male choice for intermediately ornamented females. Female dance flies Rhamphomyia longicauda (Diptera: Empididae) display two female-specific ornaments in mating swarms - inflatable abdominal sacs and pinnate tibial scales. We investigated the intensity and form of sexual selection on female traits including ornaments and found no evidence for directional sexual selection. Instead, we found marginally nonsignificant quadratic selection for all three measures of ornament expression. Canonical analysis confirmed that the strongest vectors of nonlinear selection were associated with ornamental traits, although the significance of the quadratic coefficients associated with these vectors depended on the statistical approach. Direct Mitchell-Olds and Shaw tests for the location of the maximum fitted fitness value for both raw morphological traits and canonical axes revealed only one marginally nonsignificant result for the multivariate axis loading most heavily on pinnate leg scales. Together, these results provide the first tentative support for stabilizing selection on female-specific ornaments.     

SEXUAL SELECTION,MULTIPLE MALE ORNAMENTS,AND AGE‐ AND CONDITION‐DEPENDENT SIGNALING IN THE COMMON YELLOWTHROAT

In many animals, sexual selection has resulted in complex signaling systems in which males advertise aspects of their phenotypic or genetic quality through elaborate ornamentation and display behaviors. Different ornaments might convey different information or be directed at different receivers, but they might also be redundant signals of quality that function reliably at different times (ages) or in different contexts. We explored sexual selection and age‐ and condition‐dependent signaling in the common yellowthroat (Geothlypis trichas), a sexually dichromatic warbler with two prominent plumage ornaments—a melanin‐based, black facial “mask” and carotenoid‐based, UV‐yellow “bib.” In a three‐year study, variance among males in the number of social (M_w) and extra‐pair (M_e) mates generated strong sexual selection on mask and bib attributes. Some traits (mask size, bib yellow brightness) were correlated with male age and did not experience selection beyond age‐related increases in M_w and M_e. Other traits showed age‐specific (bib size) or age‐reversed (ultraviolet brightness) patterns of selection that paralleled changes in the information‐content of each ornament. The components of male fitness generating selection in young versus old males were distinct, reflecting different sources of variation in male fertilization success. Age‐ and context‐dependent changes in the strength, direction, and target of selection may help explain the maintenance of multiple ornaments in this and other species.     

Ornament and body size variation and their measurement in natural populations

Measurement of intrapopulation variation in secondary sexual traits is a priority in the testing of sexual selection models. However, it is important to take care in the choice of materials and delimitation of populations. The use of museum skins to study variation in male tail ornaments may substantially underrepresent the real degree of intrapopulation variation. Data from live animals in specific areas provide more realistic estimates, and should be used whenever possible. I use as an example field data on male ornament length and body size in Vidua macroura (Aves: Ploceidae), a promiscuous, parasitic African finch with elongated tail plumes. Individual males differ in the timing and rate of ornament growth, and females are therefore faced with a large degree of phenotypic variation in male ornament size, even though genetic variation may not be great. By correcting for seasonal variation in the ornament lengths of males caught at different times, I show that mid-season coefficients of variation in ornament length of breeding males in two populations are as high as 18% and 55%. By contrast, tarsus, wing and unornamented tail lengths of the same males vary from 2 to 4%.     

On the function of female ornaments: male bluethroats prefer colourful females

Female ornaments in animals with conventional sex roles have traditionally been considered non-functional, being merely a genetically correlated response to selection for male ornamentation. Alternatively, female ornaments may be influenced by selection acting directly on the females, either through female–female competition or male choice. We tested the latter hypothesis in mate choice experiments with bluethroats (Luscinia s. svecica), a passerine bird in which females vary considerably in coloration of an ornamental throat patch. In outdoor aviaries placed in prime breeding habitat, males were allowed to choose between a colourful and a drab female. We found that males associated more with, and performed more sexual behaviours towards, colourful females. Female coloration was not age-related, but correlated significantly with body mass and tarsus length. Thus, we have demonstrated both a male preference for female ornamentation, and a relationship between ornament expression and female body size, which may be indicative of quality. Our results refute the correlated response hypothesis and support the hypothesis that female ornamentation is sexually selected.