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.     

Does selection on horn length of males and females differ in protected and hunted populations of a weakly dimorphic ungulate?

Weaponry in ungulates may be costly to grow and maintain, and different selective pressures in males and females may lead to sex‐biased natural survival. Sexual differences in the relationship between weapon growth and survival may increase under anthropogenic selection through culling, for example because of trophy hunting. Selection on weaponry growth under different scenarios has been largely investigated in males of highly dimorphic ungulates, for which survival costs (either natural or hunting related) are thought to be greatest. Little is known, however, about the survival costs of weaponry in males and females of weakly dimorphic species. We collected information on horn length and age at death/shooting of 407 chamois Rupicapra rupicapra in a protected population and in two hunted populations with different hunting regimes, to explore sexual differences in the selection on early horn growth under contrasting selective pressures. We also investigated the variation of horn growth and body mass in yearling males (n = 688) and females (n = 539) culled in one of the hunted populations over 14 years. The relationship between horn growth and survival showed remarkable sexual differences under different evolutionary scenarios. Within the protected population, under natural selection, we found no significant trade‐off in either males or females. Under anthropogenic pressure, selection on early horn growth of culled individuals showed diametrically opposed sex‐biased patterns, depending on the culling regime and hunters’ preferences. Despite the selective bias between males and females in one of the hunted populations, we did not detect significant sex‐specific differences in the long‐term pattern of early growth. The relationship between early horn growth and natural survival in either sex might suggest stabilizing selection on horn size in chamois. Selection through culling can be strongly sex‐biased also in weakly dimorphic species, depending on hunters’ preferences and hunting regulations, and long‐term data are needed to reveal potential undesirable evolutionary consequences.     

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.     

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.     

DENSITY-DEPENDENT SEXUAL SELECTION IN THE FUNGUS BEETLE,BOLITOTHERUS CORNUTUS

The hypothesis that population density can affect sexual selection on male horn size was tested in a three-year study of a fungus beetle, Bolitotherus cornutus. Males of this species have horns that vary greatly in length. These horns are used in fights over females; longer-horned males win the majority of fights, regardless of population density. However, density does affect the relationship between horn length and access to females. In six populations of naturally and experimentally varying densities, longer-horned males gained a greater advantage in access to females in low-density populations than at high density. This increase in access to females causes an increase in the number of females inseminated by longer-horned males; thus, sexual selection for longer horns is stronger at lower densities.     

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.     

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.     

Environmental and evolutionary effects on horn growth of male bighorn sheep

The development of male secondary sexual characters such as antlers or horns has substantial biological and socio‐economic importance because in many species these traits affect male fitness positively through sexual selection and negatively through trophy hunting. Both environmental conditions and selective hunting can affect horn growth but their relative importance remains unexplored. We first examined how a large‐scale climate index, the Pacific Decadal Oscillation (PDO), local weather and population density influenced both absolute and relative annual horn growth from birth to three years of male bighorn sheep Ovis canadensis over 42 years. We then examined the relative influence of environmental conditions and evolution mainly driven by trophy hunting on male horn length at three years of age. Horn growth was positively influenced by low population density and warm spring temperature, suggesting that ongoing climate change should lead to larger horns. Seasonal values of PDO were highly correlated. Horn growth increased with PDO in spring or summer at low density, but was weak at high density regardless of PDO. The interaction between population density and PDO in spring or summer accounted for a similar proportion of the observed annual variation in horn growth (32% or 37%) as did the additive effects of spring temperature and density (34%). When environmental conditions deteriorated, males allocated relatively more resources to summer mass gain than to horn growth, suggesting a conservative strategy favoring maintenance of condition over allocation to secondary sexual characters. Population density explained 27% of the variation in horn length, while evolutionary effects explained 9% of the variance. Thus, our study underlines the importance of both evolution and phenotypic plasticity on the development of a secondary sexual trait.     

Sexual and male horn dimorphism in Copris ochus (Coleoptera: Scarabaeidae)

Copris ochus (Coleoptera: Scarabaeidae), an endangered species, is the largest dung beetle in Japan. In C. ochus, males have a long head horn, while females lack this long horn (sexual dimorphism). Very large males of C. ochus have disproportionately longer head horns than small males, suggesting male horn dimorphism, although the dimorphism has not been investigated quantitatively. To clarify sexual and male horn dimorphism in C. ochus quantitatively, we examined the scaling relationship between body size (prothorax width) and head horn length in 94 females and 76 males. These beetles were captured during July 1978 from a natural population on Mt. Aso in southwestern Japan using a light trap. Although the horn length of the females and males scaled with prothorax width, the scaling relationship differed between the sexes, i.e., the relationship was linear in females and nonlinear in males. Statistical tests for dimorphism in male horn length showed a significant discontinuous relationship, thus indicating distinct sexual and male dimorphism in head horns. Long- and short-horned C. ochus males may have different reproductive behaviors, as described in other horned dung 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.     

Contrasting patterns of sexually selected traits in Mediterranean and continental populations of European mouflon

The expression of sexually selected traits in highly dimorphic ungulates may be influenced by environmental quality. Variations in habitat conditions can impose different constraints on the allocation of energy resources to male life‐history traits, and possibly alter the female preferences for specific features. Here, we compared the horn growth patterns in male European mouflon Ovis aries musimon living in different habitats (Mediterranean vs. continental) but sharing a common genetic origin. We hypothesized that the expression of sexually selected traits such as horn development should be promoted in more favorable habitat conditions (i.e., Mediterranean). Using linear mixed models on data retrieved from individuals harvested under the same hunting regime, we found longer horns and greater individual variance in horn segment length in the Mediterranean population than in the continental one. Furthermore, Mediterranean rams showed no evidence of compensatory horn growth, as opposed to the continental rams. Unexpectedly, horn base circumference was greater in the continental habitat than in the Mediterranean one. The overall results suggest different patterns of investment in horns in the two populations, with seemingly stronger pressure and consequences of sexual selection on mouflon rams living in more favorable environments. Although the role of hunters' selectivity cannot be excluded a priori, our data suggest that the differences in the expression of sexually selected traits in our study populations may be influenced by environmental conditions. Because sexual selection can impose substantial fitness costs on individuals, further investigations on the trade‐offs between reproduction and survival would improve our understanding of the dynamics of mouflon populations living in different environmental conditions.     

Heterogeneity in male horn growth and longevity in a highly sexually dimorphic ungulate

In sexually dimorphic ungulates, sexual selection favoring rapid horn growth in males may be counterbalanced by a decrease in longevity if horns are costly to produce and maintain. Alternatively, if early horn growth varied with individual quality, it may be positively correlated with longevity. We studied Alpine ibex Capra ibex in the Gran Paradiso National Park, Italy, to test these alternatives by comparing early horn growth and longevity of 383 males that died from natural causes. After accounting for age at death, total horn length after age 5 was positively correlated with horn growth from two to four years. Individuals with the fastest horn growth as young adults also had the longest horns later in life. Annual horn growth increments between two and six years of age were independent of longevity for ibex whose age at death ranged from 8 to 16 years. Our results suggest that growing long horns does not constrain longevity. Of the variability in horn length, 22% could be explained by individual heterogeneity, suggesting persistent differences in phenotypic quality among males. Research on unhunted populations of sexually dimorphic ungulates documents how natural mortality varies according to horn or antler size, and can help reduce the impact of sport hunting on natural processes.     

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.     

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.     

Artificial selection,pre‐release diet,and gut symbiont inoculation effects on sterile male longevity for area‐wide fruit‐fly management

Longevity is an important life‐history trait for successful and cost‐effective application of the sterile insect technique. Furthermore, it has been shown that females of some species – e.g., Anastrepha ludens (Loew) (Diptera: Tephritidae) – preferentially copulate with ‘old’, sexually experienced males, rather than younger and inexperienced males. Long‐lived sterile males may therefore have greater opportunity to find and mate with wild females than short‐lived males, and be more effective in inducing sterility into wild populations. We explored the feasibility of increasing sterile male lifespan through selection of long‐lived strains and provision of pre‐release diets with added protein, and inoculated with bacterial symbionts recovered from cultures of the gut of wild Anastrepha obliqua (Macquart). Artificial selection for long‐lived A. ludens resulted in a sharp drop of fecundity levels for F1 females. Nevertheless, the cross of long‐lived males with laboratory females produced a female F1 progeny with fecundity levels comparable to those of females in the established colony. However, the male progeny of long‐lived males*laboratory females did not survive in higher proportions than laboratory males. Provision of sugar to A. obliqua adults resulted in increased survival in comparison to adults provided only with water, whereas the addition of protein to sugar‐only diets had no additional effect on longevity. Non‐irradiated males lived longer than irradiated males, and supplying a generic probiotic diet produced no noticeable effect in restoring irradiated male longevity of A. obliqua. We discuss the need to evaluate the time to reach sexual maturity and survival under stress for long‐lived strains, and the inclusion of low amounts of protein and specific beneficial bacteria in pre‐release diets to increase sterile male performance and longevity in the field.     

Horn length is not correlated with calling efforts in the horn‐headed cricket Loxoblemmus doenitzi (Orthoptera: Gryllidae)

Field cricket species are ideal model organisms for the study of sexual selection because cricket calling songs, used to attract mating partners, are pronouncedly sexually dimorphic. However, few studies have focused on other sexually dimorphic traits of field crickets. The horn‐headed cricket, Loxoblemmus doenitzi, exhibits exaggerated sexual dimorphism in head shape: males have flat heads with triangular horns, while females lack horns. This study examines the relationship between horn length, male calling efforts and diet quality. Horn length was not found to be significantly correlated with calling efforts. When diet was manipulated for late‐stage nymphs, calling efforts in the group with poor‐quality diet treatment was significantly lower than that of crickets in the group with high‐quality diet treatment. However, horn length was not affected by diet quality. The implication of these results in the context of the evolution of multiple signals and sexual dimorphism is discussed.     

ARTIFICIAL SELECTION ON HORN LENGTH-BODY SIZE ALLOMETRY IN THE HORNED BEETLE ONTHOPHAGUS ACUMINATUS (COLEOPTERA: SCARABAEIDAE)

Males of the horned beetle Onthophagus acuminatus Har. (Coleoptera: Scarabaeidae) exhibit horn length dimorphism due to a sigmoidal allometric relationship between horn length and body size: the steep slope of the allometry around the inflection of the sigmoid curve separates males into two groups; those larger than this inflection possess long horns, and those smaller than this inflection have short horns or lack horns. I examined the genetic basis of the allometric relationship between horn length and body size by selecting males that produced unusually long horns, and males that produced unusually short horns, for their respective body sizes. After seven generations of selection, lines selected for relatively long horns had significantly longer horn lengths for a given body size than lines selected for relatively short horns, indicating a heritable component to variation in the allometry. The sigmoidal shape of the allometry was not affected by this selection regime. Rather, selected lines differed in the position of the allometry along the body size axis. One consequence of lateral shifts in this allometric relationship was that the body size separating horned from hornless males (the point of inflection of the sigmoid curve) differed between selection lines: lines in which males were selected for relatively long horns began horn production at smaller body sizes than lines selected for relatively short horns. These results suggest that populations can evolve in response to selection on male horn length through modification of the growth relationship between horn length and body size.     

Reproductive competition promotes the evolution of female weaponry

Secondary sexual traits in females are a relatively rare phenomenon. Empirical studies have focused on the role of male mate choice in their evolution; however, recently it has been suggested that secondary sexual traits in females are more likely to be under selection via reproductive competition. We investigated female competition and the influence of female phenotype on fitness in Onthophagus sagittarius, a species of dung beetle that exhibits female-specific horns. We compared reproductive fitness when females were breeding in competition versus breeding alone and found that competition for breeding resources reduced fitness for all females, but that smaller individuals suffered a greater fitness reduction than larger individuals. When females were matched for body size, those with the longest horns gained higher reproductive fitness. The fitness function was positive and linear, favouring increased horn expression. Thus, we present evidence that female body size and horn size in O. sagittarius are under directional selection via competition for reproductive resources. Our study is a rare example of female contest competition selecting for female weaponry.     

Preliminary analysis of reproductive success in a large mammal with alternative mating tactics,the Northern chamois,Rupicapra rupicapra

In polygynous mating systems, reproductive skew depends on the ability of males to monopolize females, which in turn may promote the development of contrasting traits in the two sexes. Although dominant individuals normally enjoy a higher reproductive success (RS) than subordinates, the use of genetic markers has shown that behavioural observations of male mating success may not provide reliable clues of RS. We report the preliminary results of the first DNA‐based paternity analysis on the Northern chamois (Rupicapra rupicapra), a scarcely dimorphic mountain ungulate described as highly polygynous, in relation to mating tactic and age. Because of sampling difficulties, the success in parentage assignment was low, and the interpretation of results requires caution. Territorial males had a greater RS than nonterritorial ones but they were unable to monopolize mating events. Age had a weak effect on paternity outcome but only males ≥ 6 years showed siring success. Although future studies are needed to assess the opportunity for sexual selection in male chamois, the concurrence of limited sexual size dimorphism, compensatory growth, unbiased sex‐specific survival, RS of alternative mating tactics and, possibly, long breeding tenure, may hint at the adoption of a conservative mating strategy in this species.     

Whole‐genome resequencing uncovers molecular signatures of natural and sexual selection in wild bighorn sheep

The identification of genes influencing fitness is central to our understanding of the genetic basis of adaptation and how it shapes phenotypic variation in wild populations. Here, we used whole‐genome resequencing of wild Rocky Mountain bighorn sheep (Ovis canadensis) to >50‐fold coverage to identify 2.8 million single nucleotide polymorphisms (SNPs) and genomic regions bearing signatures of directional selection (i.e. selective sweeps). A comparison of SNP diversity between the X chromosome and the autosomes indicated that bighorn males had a dramatically reduced long‐term effective population size compared to females. This probably reflects a long history of intense sexual selection mediated by male–male competition for mates. Selective sweep scans based on heterozygosity and nucleotide diversity revealed evidence for a selective sweep shared across multiple populations at RXFP2, a gene that strongly affects horn size in domestic ungulates. The massive horns carried by bighorn rams appear to have evolved in part via strong positive selection at RXFP2. We identified evidence for selection within individual populations at genes affecting early body growth and cellular response to hypoxia; however, these must be interpreted more cautiously as genetic drift is strong within local populations and may have caused false positives. These results represent a rare example of strong genomic signatures of selection identified at genes with known function in wild populations of a nonmodel species. Our results also showcase the value of reference genome assemblies from agricultural or model species for studies of the genomic basis of adaptation in closely related wild taxa.