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.     

Mechanical limits to maximum weapon size in a giant rhinoceros beetle

The horns of giant rhinoceros beetles are a classic example of the elaborate morphologies that can result from sexual selection. Theory predicts that sexual traits will evolve to be increasingly exaggerated until survival costs balance the reproductive benefits of further trait elaboration. In Trypoxylus dichotomus, long horns confer a competitive advantage to males, yet previous studies have found that they do not incur survival costs. It is therefore unlikely that horn size is limited by the theoretical cost–benefit equilibrium. However, males sometimes fight vigorously enough to break their horns, so mechanical limits may set an upper bound on horn size. Here, I tested this mechanical limit hypothesis by measuring safety factors across the full range of horn sizes. Safety factors were calculated as the ratio between the force required to break a horn and the maximum force exerted on a horn during a typical fight. I found that safety factors decrease with increasing horn length, indicating that the risk of breakage is indeed highest for the longest horns. Structural failure of oversized horns may therefore oppose the continued exaggeration of horn length driven by male–male competition and set a mechanical limit on the maximum size of rhinoceros beetle horns.     

Live fast, die young: trade-offs between fitness components and sexually antagonistic selection on weaponry in Soay sheep

Males are predicted to compete for reproductive opportunities, with sexual selection driving the evolution of large body size and weaponry through the advantage they confer for access to females. Few studies have explored potential trade-offs of investment in secondary sexual traits between different components of fitness or tested for sexually antagonistic selection pressures. These factors may provide explanations for observed polymorphisms in both form and quality of secondary sexual traits. We report here an analysis of selection on horn phenotype in a feral population of Soay sheep (Ovis aries) on the island of Hirta, St. Kilda, Scotland. Soay sheep display a phenotypic polymorphism for horn type with males growing either normal or reduced (scurred) horns, and females growing either normal, scurred, or no (polled) horns; further variation in size exists within horn morphs. We show that horn phenotype and the size of the trait displayed is subject to different selection pressures in males and females, generating sexually antagonistic selection. Furthermore, there was evidence of a trade-off between breeding success and longevity in normal-horned males, with both the normal horn type and larger horn size being associated with greater annual breeding success but reduced longevity. Therefore, selection through lifetime breeding success was not found to act upon horn phenotype in males. In females, a negative association of annual breeding success within the normal-horned phenotype did not result in a significant difference in lifetime fitness when compared to scurred individuals, as no significant difference in longevity was found. However, increased horn size within this group was negatively associated with breeding success and longevity. Females without horns (polled) suffered reduced longevity and thus reduced lifetime breeding success relative the other horn morphs. Our results therefore suggest that trade-offs between different components of fitness and antagonistic selection between the sexes may maintain genetic variation for secondary sexual traits within a population.     

Linear and threshold-dependent expression of secondary sexual traits in the same individual: insights from a horned beetle (Coleoptera: Scarabaeidae)

Elaborate horns or horn‐like structures in male scarab beetles commonly scale with body size either (a) in a linear fashion with horn size increasing relatively faster than body size or (b) in a threshold‐dependent, sigmoid fashion; that is, males smaller than a certain critical body size develop no or only rudimentary horns, whereas males larger than the threshold size express fully developed horns. The development of linear vs. sigmoid scaling relationships is thought to require fundamentally different regulatory mechanisms. Here we show that such disparate regulatory mechanisms may co‐occur in the same individual. Large males of the south‐east Asian Onthophagus (Proagoderus) watanabei (Ochi & Kon) (Scarabaeidae, Onthophagini) develop a pair of long, curved head horns as well as a single thoracic horn. We show that unlike paired head horns in a large number of Onthophagus species, in O. watanabei the relationship between head horns and body size is best explained by a linear model. Large males develop disproportionately longer horns than small males, but the difference in relative horn sizes across the range of body sizes is small compared to other Onthophagus species. However, the scaling relationship between the thoracic horn and body size is best explained by a strongly sigmoid model. Only males above a certain body size threshold express a thoracic horn and males smaller than this threshold express no horn at all. We found a significant positive correlation between head and thoracic horn length residuals, contrary to what would be expected if a resource allocation tradeoff during larval development would influence the length of both horn types. Our results suggest that the scaling relationship between body size and horn length, and the developmental regulation underlying these scaling relationships, may be quite different for different horns, even though these horns may develop in the same individual. We discuss our results in the context of the developmental biology of secondary sexual traits in beetles. © 2004 The Linnean Society of London, Biological Journal of the Linnean Society, 2004, 83 , 473–480.     

Male and female secondary sexual traits show different patterns of quantitative genetic and environmental variation in the horned beetle Onthophagus sagittarius

The expression of secondary sexual traits in females has often been attributed to a correlated response to selection on male traits. In rare cases, females have secondary sexual traits that are not homologous structures to secondary sexual traits in males and are thus less likely to have evolved in females because of correlated selection. In this study, we used the dung beetle Onthophagus sagittarius, a species with sex‐specific horns, to examine the environmental and quantitative genetic control of horn expression in males and females. Offspring subjected to different brood mass manipulations (dung addition/removal) were found to differ significantly in body size. Brood mass manipulation also had a significant effect on the length of male horns; however, female horn length was found to be relatively impervious to the treatment, showing stronger patterns of additive genetic variance than males. We found no correlations between horn expression in males and females. We therefore conclude that the horns of O. sagittarius females are unlikely to result from genetic correlations between males and females. Rather, our data suggest that they may be under independent genetic control.     

Sexually dimorphic male horns and their use in agonistic behaviors in the horn-headed cricket <Emphasis Type="Italic">Loxoblemmus doenitzi</Emphasis> (Orthoptera: Gryllidae)

Sexual dimorphism, the difference between the sexes in secondary sexual characters, is in general driven by processes of sexual selection. The horn-headed cricket, Loxoblemmus doenitzi, exhibits sexual dimorphism in head shape. Males have flat heads and triangular horns on both sides of their heads, whereas females have rounded heads and no horns. We hypothesized that male horns have evolved due to intra-sexual selection, in which males use these horns as weapons in aggressive interactions. We tested two predictions of this hypothesis by conducting agonistic trials with field-caught males of L. doenitzi: (1) the horns should be used in agonistic interactions between males, and (2) the asymmetry in horn size or horn use may determine contest outcome. Horn length was significantly correlated with thorax length and hind femur length. During agonistic interactions, males aggressively used their horns by beating the opponent’s horns with their own or by poking the opponent’s body. However, logistic regression analysis revealed that neither horn length nor horn use were significant factors for contest outcome. Instead, body size was significant for determining contest outcome. We discuss possible scenarios for evolution of male horns in L. doenitzi.     

Allometric plasticity in a polyphenic beetle

Abstract 1. Environmental conditions, such as variation in nutrition, commonly contribute to morphological variation among individuals by affecting body size and the expression of certain morphological traits; however the scaling relationship between a morphological trait and body size over a range of body sizes is generally assumed not to change in response to environmental fluctuation (allometric plasticity), but instead to be constant and diagnostic for a particular trait and species or population. The work reported here examined diet‐induced allometric plasticity in the polyphenic beetle Onthophagus taurus Schreber (1759) (Coleoptera: Scarabaeidae). 2. Male O. taurus vary in body size depending on larval nutrition. Only males above a critical body size threshold express fully developed horns; males smaller than this threshold develop only rudimentary horns or no horns at all. 3. Field populations that naturally utilise two different resources for feeding larvae (horse dung vs. cow manure) exhibited significant differences in the average scaling relationship between body size and male horn length over the same range of body sizes. Males collected from cow manure populations expressed consistently longer horns for a given body size than males collected from horse dung populations. 4. Males reared in the laboratory on horse dung or cow manure also exhibited significant differences in the average scaling relationship between body size and horn length. Differences between laboratory populations reared on horse dung or cow manure were of the same kind and magnitude as differences between field populations that utilise these different resources naturally. 5. These findings suggest that between‐population differences in scaling relationships between horn length and body size can be the product of differences in the quality of resources available to developing larvae. Results are discussed in the context of onthophagine mating systems and recent insights in the developmental and endocrine control of horn polyphenisms.     

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.     

Fluctuating asymmetry in red junglefowl

Fluctuating asymmetry, the random deviation from perfect bilateral symmetry, has recently attracted considerable attention. Levels of asymmetry have been shown to correlate with measures of individual quality. We measured asymmetry in a variety of ornamental and non-ornamental traits in red junglefowl, Gallus gallus and examined the patterns of asymmetry among different traits within an individual. All ornamental traits had significantly higher levels of fluctuating asymmetry than did non-ornamental traits. However, inter-trait correlations of asymmetry were low for both ornamental and non-ornamental traits. We then correlated measures of asymmetry with several potential indicators of male quality, including comb size, body size, and body condition. We found little evidence that asymmetry in any measured trait reflected male quality. We measured asymmetry in ornamental traits at several stages of development and found no relationship between male condition and changes in asymmetry over time. Our results indicate that it is necessary to employ caution when choosing traits to be measured in studies of fluctuating asymmetry and that a relationship between asymmetry and individual quality cannot be assumed.     

A negative association between horn length and survival in a weakly dimorphic ungulate

While all models of sexual selection assume that the development and expression of enlarged secondary sexual traits are costly, males with larger ornaments or weapons generally show greater survival or longevity. These studies have mostly been performed in species with high sexual size dimorphism, subject to intense sexual selection. Here, we examined the relationships between horn growth and several survival metrics in the weakly dimorphic Pyrenean chamois (Rupicapra pyrenaica). In this unhunted population living at high density, males and females were able to grow long horns without any apparent costs in terms of longevity. However, we found a negative relationship between horn growth and survival during prime age in males. This association reduces the potential evolutionary consequences of trophy hunting in male chamois. We also found that females with long horns tended to have lower survival at old ages. Our results illustrate the contrasting conclusions that may be drawn when different survival metrics are used in analyses. The ability to detect trade‐off between the expression of male secondary sexual traits and survival may depend more on environmental conditions experienced by the population than on the strength of sexual selection.     

No evidence for condition-dependent expression of male genitalia in the dung beetle Onthophagus taurus

We examine the condition-dependence of male genitalia in the dung beetle Onthophagus taurus by manipulating the quality of dung provided for larval growth and development. We show that the influence of larval nutrition differed considerably across three different trait classes (sexual, nonsexual and genital). The size of all nonsexual traits varied with dung quality but their allometric slopes remained unchanged. Relative horn length and allometry, but not absolute horn length, showed a high degree of plasticity with differences in dung quality. In contrast, both absolute size and allometry of genitalia were largely unresponsive to changes in dung quality. Male genitalia exhibited intermediate levels of phenotypic variation and lower allometric slopes than both horns and nonsexual traits. Thus, our findings provide little support for good genes hypotheses of genital evolution. We use our findings to discuss a developmental mechanism and selection pressures that may prevent the condition-dependent expression of genitalia.     

Proximate determination of male horn dimorphism in the beetle Onthophagus taurus (Coleoptera: Scarabaeidae)

The existence of discrete phenotypic variation within one sex poses interesting questions regarding how such intrasexual polymorphisms are produced and modified during the course of evolution. Approaching these kinds of questions requires insights into the genetic architecture underlying a polymorphism and an understanding of the proximate mechanisms determining phenotype expression. Here we explore the genetic underpinnings and proximate factors influencing the expression of beetle horns – a dramatic sexually selected trait exhibiting intramale dimorphism in many species. Two relatively discrete male morphs are present in natural populations of the dung beetle Onthophagus taurus (Scarabaeidae, Onthophagini). Males exceeding a critical body size develop a pair of long, curved horns on their heads, while those smaller than this critical body size remain essentially hornless. We present results from laboratory breeding experiments designed to assess the relative importance of inherited and environmental factors as determinants of male morphology. Using father–son regressions, our findings demonstrate that horn length and body size of male progeny are not predicted from paternal morphology. Instead, natural variation in an environmental factor, the amount of food available to larvae, determined both the body sizes exhibited by males as adults and the presence or absence of horns. The nonlinear scaling relationship between the body size and horn length of males bred in the laboratory did not differ from the pattern of variation present in natural populations, suggesting that nutritional conditions account for variation in male morphology in natural populations as well. We discuss our results by extending ideas proposed to explain the evolution of conditional expression of alternative phenotypes in physically heterogeneous environments toward incorporating facultative expression of secondary sexual traits. We use this synthesis to begin characterizing the potential origin and subsequent evolution of facultative horn expression in onthophagine beetles.     

Horn growth patterns in Alpine chamois

The analysis of horn growth may provide important information about the allocation of metabolic resources to secondary sexual traits. Depending on the selective advantages offered by horn size during intra- and inter-specific interactions, ungulates may show different investment in horn development, and growth variations within species may be influenced by several parameters, such as sex, age, or resource availability. We investigated the horn growth patterns in two hunted populations of Alpine chamois (Rupicapra r. rupicapra) in the Central Italian Alps. We tested the role of individual heterogeneity on the growth pattern and explored the variation in annulus length as a function of different factors (sex, age, hunting location, cohort). We then investigated the mechanisms underlying horn growth trajectories to test for the occurrence of compensatory or recovery growth and their potential differences between sexes and populations. Annulus length varied as a function of sex, age of individuals and, marginally, hunting location; no effect of cohort or individual heterogeneity was detected. Male and female chamois showed compensatory horn growth within the first 5½ years of life, though the partial convergence of horn trajectories in chamois suggests that this mechanisms would best be described as ‘recovery growth’. Compensation rates were greater in males than in females, while only compensatory growth rates up to 2½ years of age were different in the two populations. Besides confirming the sex- and age-dependent pattern of horn development, our study suggests that the mechanism of recovery growth supports the hypothesis of horn size as a weakly selected sexual trait in male and female chamois. Furthermore, the greater compensation rates in horn growth shown by male chamois possibly suggest selective effects of hunting on age at first reproduction, while different compensation rates between populations may suggest the occurrence of some plasticity in resource allocation to sexual traits in relation to different environments.     

Trade-off between horns and other functional traits in two <Emphasis Type="Italic">Onthophagus</Emphasis> species (Scarabaeidae,Coleoptera)

Beetle horns are extraordinarily diversified secondary sexual structures used for mate choice and male–male combat. Due to an interaction of nutritional, hormonal and genetic factors, their polyphenic development is metabolically expensive and occurs in the virtually closed system of the pre-pupal stage, after the developing larva has stopped feeding. Previous studies showed the occurrence of resource competition resulting in a trade-off between horns and other morphological structures. These studies also revealed functional associations between autoecology and horns, as a function of their physical location (i.e. head versus pronotum), and suggested that constraints imposed by trade-offs on adult morphology may have profound evolutionary consequences, such as ecological and reproductive isolation. In this study, we compared trade-off patterns between horns and other functional traits (eyes, antennae, legs, head, epipharynges and genitalia) in two congeneric species bearing horns located in the same anatomical area, but with different morphologies. Specifically, we considered Onthophagus taurus, characterised by a pair of long, lunated cephalic horns, and Onthophagus fracticornis, expressing a single cephalic horn. We demonstrated that, even when horns are located in the same physical position on the insect’s body, differences in horn morphology can bring about differences in how functional traits respond to horn investment. These differences are interpretable in the light of the hierarchy of functions carried out by these structures and their component parts in each species.     

Sprint speed is not reduced by exaggerated male weapons in a flower beetle Dicronocephalus wallichii

Exaggerated sexually selected traits are assumed to decrease the mobility of bearers. However, previous empirical studies have often failed to support this assumption, possibly because locomotor performance represents the integration of numerous morphological, physiological and behavioural traits. Males of a flower beetle Dicronocephalus wallichii Pouillaude 1914 (Coleoptera: Scarabaeidae: Cetoniinae) possess elongated forelegs and a pair of exaggerated horns, which are used as dual weapons in male–male competition for mates. We investigated whether these two sexual traits impede the maximum sprint speed on bamboo branches with different angles and thicknesses under laboratory conditions. Our results suggested that no negative relationship exists between relative foreleg length or horn length and sprint speed. Elongated forelegs and horns may entail negligible locomotor costs. Males with longer horns and forelegs were found to have longer midlegs and hindlegs independent of body size. Thus, elongated midlegs and hindlegs in males may enhance balance, stabilize running on bamboo branches and compensate for the locomotor costs of bearing exaggerated weapons. Furthermore, a positive relationship was found between horn length and sprint speed on a horizontal branch. Males with longer horns probably have more energy and/or invest more heavily in appendage musculature. As is known in other animals, male horns of D. wallichii may act as honest indicators of body condition.     

The intensity of sexual selection predicts weapon size in male bovids

As a classical example of a sexually selected trait, the horns of male bovids offer a prime opportunity to identify predictors of the intensity of sexual selection. Here I use the comparative method to quantify sexual and natural selection pressures behind interspecific variation in horn length. I show that male horn length depends on factors proposed to affect the mean mate number per mating male, correlating positively with group size and negatively with male territoriality. This suggests that whereas group size increases the opportunity for sexual selection, territoriality reduces it because territorial males are unable to follow and monopolize female groups as effectively as males in nonterritorial species. Sexual body size dimorphism also correlates positively with group size and negatively with territoriality, corroborating these factors as predictors of the intensity of sexual selection on males. Female horn length was unaffected by the factors related to mating system, suggesting that this trait is mainly under natural selection. Using female horn length as a proxy for forces of natural selection revealed a negative effect on male horn length. Thus where natural selection favors female horns, possibly as effective weapons against predators, a similar selection pressure on males might prevent them from evolving too elaborate horns through sexual selection. There was no correlation found between horn length and latitude, thus providing no support for the hypothesis that horns have a thermoregulatory function.     

Diet alters male horn allometry in the beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae)

Darwin considered the horns of male beetles to be among the most striking examples of sexual selection. As with antlers in deer or elk, beetle horns scale positively with male body size, with the result that large males have disproportionately longer horns than small males. It is generally assumed that such scaling relationships (''static allometries'') are insensitive to short-term changes in the environment, and for this reason they are regularly used as diagnostic attributes of populations or species. Here I report breeding experiments on horned beetles that demonstrate that the scaling relationship between male horn length and body size changes when larval nutrition changes. Males reared on a low-quality diet had longer horn lengths at any given body size than sibling males reared on a high-quality diet. Such ''allometry plasticity'' may explain seasonal changes observed in this same scaling relationship in a natural population. These experiments demonstrate that scaling relationships of sexually selected traits can respond facultatively to variation in the environment, thereby revealing a new mechanism by which males regulate the production of exaggerated secondary sexual traits.     

Plasticity of size and allometry in multiple sexually selected traits in an armed beetle <Emphasis Type="Italic">Gnatocerus cornutus</Emphasis>

Male-male competition frequently results in the evolution of sexually selected traits used as weapons and ornaments. The expression of these traits often depends on male condition, i.e., condition dependence. Although males often have multiple sexually selected traits, to date many studies have focused on the morphological analysis of one sexual trait whilst ignoring the others. We here report phenotypic plasticity for multiple sexual traits, by manipulating larval diet quality and density, in the broad-horned flour beetle Gnatocerus cornutus. The male beetles possess enlarged mandibles, developed genae and a pair of small horns, but females lack these completely. Larval density significantly affected overall body size but not relative investment in each sexual trait. In contrast, diet quality had no effect on body size but had a significant effect on relative investment in the mandibles and genae. These results indicate that the allometric intercepts of the mandible and genae alter in response to diet quality, i.e., allometric plasticity. However, diet quality had no effect on the growth of the horn. Thus, multiple sexual traits exhibited differences in plasticity as a result of larval nutrient condition in G. cornutus males.     

Age-dependent genetic effects on a secondary sexual trait in male Alpine ibex, Capra ibex

Secondary sexual traits, such as horns in ungulates, may be good indicators of genetic quality because they are costly to develop. Genetic effects on such traits may be revealed by examining correlations between multilocus heterozygosity (MLH) and trait value. Correlations between MLH and fitness traits, termed heterozygosity-fitness correlations (HFC), may reflect inbreeding depression or associative overdominance of neutral microsatellite loci with loci directly affecting fitness traits. We investigated HFCs for horn growth, body mass and faecal counts of nematode eggs in wild Alpine ibex (Capra ibex). We also tested if individual inbreeding coefficients (f') estimated from microsatellite data were more strongly correlated with fitness traits than MLH. MLH was more strongly associated with trait variation than f'. We found HFC for horn growth but not for body mass or faecal counts of nematode eggs. The effect of MLH on horn growth was age-specific. The slope of the correlation between MLH and yearly horn growth changed from negative to positive as males aged, in accordance with the mutation accumulation theory of the evolution of senescence. Our results suggest that the horns of ibex males are an honest signal of genetic quality.     

Compensatory Growth Limits Opportunities for Artificial Selection in Alpine Chamois

ABSTRACT In ungulates, big males with large weapons typically outcompete other males over access to estrous females. In many species, rapid early growth leads to large adult mass and weapon size. We compared males in one hunted and one protected population of Alpine chamois (Rupicapra rupicapra) to examine the relationship between horn length and body mass. We assessed whether early development and hunter selectivity affected age-specific patterns of body and horn size and whether sport hunting could be an artificial selection pressure favoring smaller horns. Adult horn length was mostly independent of body mass. For adult males, the coefficient of variation of horn length (0.06) was <50% of that for body mass (0.16), suggesting that horn length presents a lower potential for selection and may be less important for male mating success than is body mass. Surprisingly, early development did not affect adult mass because of apparent compensatory growth. We found few differences in body and horn size between hunted and protected populations, suggesting the absence of strong effects of hunting on male phenotype. If horn length has a limited role in male reproductive success, hunter selectivity for males with longer horns is unlikely to lead to an artificial selective pressure on horn size. These results imply that the potential evolutionary effects of selective hunting depend on how the characteristics selected by hunters affect individual reproductive success.