Sexual selection,phenotypic variation,and allometry in genitalic and non‐genitalic traits in the sexually size‐dimorphic stick insect Micrarchus hystriculeus

The mobility hypothesis could explain the evolution of female‐biased size dimorphism if males with a smaller body size and longer legs have an advantage in scramble competition for mates. This hypothesis is tested by performing a selection analysis in the wild on Micrarchus hystriculeus (Westwood) (Phasmatodea), a sexually size dimorphic stick insect endemic to New Zealand. This analysis examined the form and strength of sexual selection on body size, leg lengths (front, mid and hind), and clasper size (a genitalic trait), and also quantified the degree of phenotypic variation and the allometric scaling pattern of these traits. By contrast to the mobility hypothesis, three lines of evidence were found to support significant stabilizing sexual selection on male hind leg length: a significant nonlinear selection gradient, negative static allometry, and a low degree of phenotypic variation. Hind leg length might be under stabilizing selection in males if having average‐sized legs facilitates female mounting or improves a male's ability to achieve the appropriate copulation position. As predicted, a negative allometric scaling pattern and low phenotypic variation of clasper size is suggestive of stabilizing selection and supports the ‘one‐size‐fits‐all’ hypothesis. Opposite to males, the mid and hind leg lengths of females showed positive static allometry. Relatively longer mid and hind leg lengths in larger females might benefit individuals via the better support of their larger abdomens. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 113 , 471–484.     

Experimental manipulation reveals a trade‐off between weapons and testes

Theory predicts a trade‐off between sexually selected weapons used to secure mates and post‐copulatory traits used to maximize fertilization success. However, individuals that have a greater capacity to acquire resources from the environment may invest more in both pre‐ and post‐copulatory traits, and trade‐offs may not be readily apparent. Here, we manipulate the phenotype of developing individuals to examine allocation trade‐offs between weapons and testes in Mictis profana (Hemiptera: Coreidae), a species where the hind legs are sexually selected weapons used in contests over access to females. We experimentally prevented males from developing weapons by inducing them to autotomize their hind legs before the final moult to adulthood. We compared trait expression in this group to males where autotomy was induced in the mid‐legs, which are presumably not under sexual selection to the same extent. We found males without weapons invested proportionally more in testes mass than those with their mid‐legs removed. Males that developed to adulthood without weapons did not differ from the mid‐leg removal group in other traits potentially under precopulatory sexual selection, other post‐copulatory traits or naturally selected traits. In addition, a sample of adult males from the same population in the wild revealed a positive correlation between investment in testes and weapons. Our study presents a critical contribution to a growing body of literature suggesting the allocation of resources to pre‐ and post‐copulatory sexual traits is influenced by a resource allocation trade‐off and that this trade‐off may only be revealed with experimental manipulation.     

Cryptic individual scaling relationships and the evolution of morphological scaling

Morphological scaling relationships between organ and body size—also known as allometries—describe the shape of a species, and the evolution of such scaling relationships is central to the generation of morphological diversity. Despite extensive modeling and empirical tests, however, the modes of selection that generate changes in scaling remain largely unknown. Here, we mathematically model the evolution of the group‐level scaling as an emergent property of individual‐level variation in the developmental mechanisms that regulate trait and body size. We show that these mechanisms generate a “cryptic individual scaling relationship” unique to each genotype in a population, which determines body and trait size expressed by each individual, depending on developmental nutrition. We find that populations may have identical population‐level allometries but very different underlying patterns of cryptic individual scaling relationships. Consequently, two populations with apparently the same morphological scaling relationship may respond very differently to the same form of selection. By focusing on the developmental mechanisms that regulate trait size and the patterns of cryptic individual scaling relationships they produce, our approach reveals the forms of selection that should be most effective in altering morphological scaling, and directs researcher attention on the actual, hitherto overlooked, targets of selection.     

The tale of the shrinking weapon: seasonal changes in nutrition affect weapon size and sexual dimorphism,but not contemporary evolution

Sexually selected traits are often highly variable in size within populations due to their close link with the physical condition of individuals. Nutrition has a large impact on physical condition, and thus, any seasonal changes in nutritional quality are predicted to alter the average size of sexually selected traits as well as the degree of sexual dimorphism in populations. However, although traits affected by mate choice are well studied, we have a surprising lack of knowledge of how natural variation in nutrition affects the expression of sexually selected weapons and sexual dimorphism. Further, few studies explicitly test for differences in the heritability and mean‐scaled evolvability of sexually selected traits across conditions. We studied Narnia femorata (Hemiptera: Coreidae), an insect where males use their hind legs as weapons and the femurs are enlarged, to understand the extent to which weapon expression, sexual dimorphism and evolvability change across the actual range of nutrition available in the wild. We found that insects raised on a poor diet (cactus without fruit) are nearly monomorphic, whereas those raised on a high‐quality diet (cactus with ripe fruit) are distinctly sexually dimorphic via the expression of large hind leg weapons in males. Contrary to our expectations, we found little evidence of a potential for evolutionary change for any trait measured. Thus, although we show weapons are highly condition dependent, and changes in weapon expression and dimorphism could alter evolutionary dynamics, our populations are unlikely to experience further evolutionary changes under current conditions.     

Intrasexual selection in Verreaux's sifaka (Propithecus verreauxi verreauxi)

Studies of sexual selection show that both female choice and male-male competition can influence the evolution and expression of male phenotypes. In this regard, it is important to determine the functional basis through which male traits influence variation in male reproductive success. In this study, we estimate the strength and type of sexual selection acting on adult males in a population of wild lemur, Verreaux's sifaka (Propithecus verreauxi verreauxi). The data used in this study were collected at Beza Mahafaly Special Reserve, southwest Madagascar. We conducted paternity analyses on 70 males in order to estimate the distribution of reproductive success in this population. Paternity data were combined with morphometric data in order to determine which morphological traits covary with male fitness. Five morphological traits were defined in this analysis: body size, canine size, torso shape, arm shape, and leg shape. We utilized phenotypic selection models in order to determine the strength and type of selection acting directly on each trait. Our results show that directional selection acts on leg shape (a trait that is functionally related to locomotor performance), stabilizing selection acts on body mass and torso shape, and negative correlational selection acts on body mass and leg shape. We draw from biomechanical and kinematic studies of sifaka locomotion to provide a functional context for how these traits influence male mating competition within an arboreal environment. Verreaux's sifaka and many other gregarious lemurs are sexually monomorphic in body mass and canine size, despite a high frequency and intensity of male-male aggressive competition. Our results provide some insight into this paradox: in our population, there is no directional selection acting on body mass or canine size in males. The total pattern of selection implicates that behaviors relating to locomotor performance are more important than behaviors relating to fighting ability during intrasexual contests.     

Diversity in the weapons of sexual selection: horn evolution in the beetle genus Onthophagus (Coleoptera: Scarabaeidae)

Both ornaments and weapons of sexual selection frequently exhibit prolific interspecific diversity of form. Yet, most studies of this diversity have focused on ornaments involved with female mate choice, rather than on the weapons of male competition. With few exceptions, the mechanisms of divergence in weapon morphology remain largely unexplored. Here, we characterize the evolutionary radiation of one type of weapon: beetle horns. We use partial sequences from four nuclear and three mitochondrial genes to develop a phylogenetic hypothesis for a worldwide sample of 48 species from the dung beetle genus Onthophagus (Coleoptera: Scarabaeidae). We then use these data to test for multiple evolutionary origins of horns and to characterize the evolutionary radiation of horns. Although our limited sampling of one of the world's most species-rich genera almost certainly underestimates the number of evolutionary events, our phylogeny reveals prolific evolutionary lability of these exaggerated sexually selected weapons (more than 25 separate gains and losses of five different horn types). We discuss these results in the context of the natural history of these beetles and explore ways that sexual selection and ecology may have interacted to generate this extraordinary diversity of weapon morphology.     

Tipping the scales: Evolution of the allometric slope independent of average trait size

The scaling of body parts is central to the expression of morphology across body sizes and to the generation of morphological diversity within and among species. Although patterns of scaling‐relationship evolution have been well documented for over one hundred years, little is known regarding how selection acts to generate these patterns. In part, this is because it is unclear the extent to which the elements of log‐linear scaling relationships—the intercept or mean trait size and the slope—can evolve independently. Here, using the wing–body size scaling relationship in Drosophila melanogaster as an empirical model, we use artificial selection to demonstrate that the slope of a morphological scaling relationship between an organ (the wing) and body size can evolve independently of mean organ or body size. We discuss our findings in the context of how selection likely operates on morphological scaling relationships in nature, the developmental basis for evolved changes in scaling, and the general approach of using individual‐based selection experiments to study the expression and evolution of morphological scaling.     

Spatiotemporal fluctuations in natural selection acting on the gall‐parasitic aphid Tetraneura sorini

The measurement of the selection gradient is crucial for understanding the magnitude of selection acting directly on a trait and predicting the evolutionary trajectory of that trait. This study evaluated the selection gradient acting on the morphology of the gall‐parasitic aphid Tetraneura sorini during the galling process and compared the strength among populations. Gall formers (first instars) frequently fight with conspecifics or heterospecifics for usurping incipient galls using their well‐developed hind legs. First instars that successfully acquired galls were found within galls, whereas those that failed were found dead on leaf surfaces. Selection gradients were estimated using logistic stepwise regression and partial least square (PLS) regression. Calculated selection differentials indicated that first instars that secured galls were larger in body size than failed individuals through all populations. However, selection gradients on weapon traits varied largely among populations or among years in the same population. We confirmed microevolutionary changes in the relationship between traits, which accorded with the expectation from changes in the selection gradients. When gall formers were transferred onto developing buds individually, individuals that successfully induced galls had smaller body size than failed individuals. Available evidence suggests that the selection gradient on body size becomes higher with an increasing proportion of T. sorini in the Tetraneura species community. Thus, we concluded that more intense fighting with conspecifics leads to stronger selective pressure on body size, but that selective pressure for each trait is variable depending on differences in the tactics and species composition among populations.     

Evolutionary allometry reveals a shift in selection pressure on male horn size

How selection pressures acting within species interact with developmental constraints to shape macro‐evolutionary patterns of species divergence is still poorly understood. In particular, whether or not sexual selection affects evolutionary allometry, the increase in trait size with body size across species, of secondary sexual characters, remains largely unknown. In this context, bovid horn size is an especially relevant trait to study because horns are present in both sexes, but the intensity of sexual selection acting on them is expected to vary both among species and between sexes. Using a unique data set of sex‐specific horn size and body mass including 91 species of bovids, we compared the evolutionary allometry between horn size and body mass between sexes while accounting for both the intensity of sexual selection and phylogenetic relationship among species. We found a nonlinear evolutionary allometry where the allometric slope decreased with increasing species body mass. This pattern, much more pronounced in males than in females, suggests either that horn size is limited by some constraints in the largest bovids or is no longer the direct target of sexual selection in very large species.     

Sperm competition and the coevolution of pre‐ and postcopulatory traits: Weapons evolve faster than testes among onthophagine dung beetles

Reproductive competition generates episodes of both pre‐ and postcopulatory sexual selection. Theoretical models of sperm competition predict that as the fitness gains from expenditure on the weapons of male combat increase, males should increase their expenditure on weapons and decrease their expenditure on traits that contribute to competitive fertilization success. Although traits subject to sexual selection are known to have accelerated evolutionary rates of phenotypic divergence, it is not known whether the competing demands of investment into pre‐ and postcopulatory traits affect their relative rates of evolutionary divergence. We use a comparative approach to estimate the rates of divergence in pre‐ and postcopulatory traits among onthophagine dung beetles. Weapons evolved faster than body size while testes mass and sperm length evolved more slowly than body size, suggesting that precopulatory competition is the stronger episode of sexual selection acting on these beetles. Although horns evolved faster than testes, evolutionary increases in horn length were not associated with evolutionary reductions in testes mass. Our data for onthophagines support the notion that in taxa where males are unable to monopolize paternity, expenditure on both weapons and testes should both be favored.     

Allometry and morphometrics of clypeal membrane size and shape in Nicrophorus (Coleoptera: Silphidae)

Contests between same‐sex opponents over resources necessary for reproduction, as well interactions used to discern mate quality, often involve exaggerated traits wherein large individuals have disproportionately larger traits. This positive allometric scaling of weapons or signals facilitates communication during social interactions by accentuating body size differences between individuals. Typically, males carry these exaggerated traits, as males must compete over limited female gametes. However, in Nicrophorus beetles both males and females engage in physical contests over the vertebrate carcasses they need to provision and raise offspring. Male and female Nicrophorus beetles have extended clypeal membranes directly above their mandibles, which could serve as signals. We investigated the scaling relationships between clypeal membrane size and shape and body size for five species of North American burying beetle to determine whether clypeal membranes contain exaggerated body size information. We found that clypeal membranes for both sexes of all species scaled positively with body size (slope > 1). Three of the five species also displayed sexual dimorphism in aspects of clypeal membrane size and shape allometry despite lack of dimorphism in body size. In two dimorphic species, small male clypeal membranes were statistically indistinguishable from the female form. We conclude that colored clypeal membranes in Nicrophorus beetles do contain exaggerated body size information. Observed patterns of dimorphism suggest that males sometimes experience stronger selection on marking size and shape, which might be explained by life history differences among species.     

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.     

Mating Behavior and Dual‐Purpose Armaments in a Camel Cricket

Sexual selection has often been dichotomized into intersexual and intrasexual components of selection, favoring ornaments and weapons, respectively. Here, we show that a weapon used in male–male combat is sometimes also used in a functionally similar manner for grasping females during mating. The hind legs of adult males of some species of Pristoceuthophilus camel crickets have strongly bent tibia and stout femora with two large conspicuous spines. Here, we show that (1) leg armature is positively allometric, (2) males use these leg modifications when fighting other males, (3) males sometimes use the same leg modifications in the same functional manner for grabbing and holding females for mating, (4) virgin females show more interest in males than do non‐virgin females, and (5) males are more likely to use their leg modifications to grab and hold females when paired with non‐virgin females than when paired with virgin females. We interpret these results as suggesting that males employ an alternative coercive mating strategy when paired with unreceptive females; alternative explanations are also discussed.     

Harder,better, faster,stronger: Weapon size is more sexually dimorphic than weapon biomechanical components in two freshwater anomuran species

Sexual selection influences the evolution of morphological traits that increase the likelihood of monopolizing scarce resources. When such traits are used during contests, they are termed weapons. Given that resources are typically linked to monopolizing mating partners, theory expects only males to bear weapons. In some species, however, females also bear weapons, although typically smaller than male weapons. Understanding why females bear smaller weapons can thus help us understand the selective pressures behind weapon evolution. However, most of our knowledge comes from studies on weapon size, while the biomechanics of weapons, such as the size of the muscles, efficiency, and shape are seldom studied. Our goal was to test if the theoretical expectations for weapon size sexual dimorphism also occur for weapon biomechanics using two aeglid crab species. Males of both species had larger claws which were also stronger than female claws. Male claws were also more efficient than females' claws (although we used only one species in this analysis). For weapon shape, though, only one species differed in the mean claw shape. Regarding scaling differences, in both species, male claws had higher size scaling than females, while only one species had a higher shape scaling. However, male weapons did not have higher scaling regarding strength and efficiency than females. Thus, males apparently allocate more resources in weapons than females, but once allocated, muscle and efficiency follow a similar developmental pathway in both sexes. Taken together, our results show that sexual dimorphism in weapons involves more than differences in size. Shape differences are especially intriguing because we cannot fully understand its causes. Yet, we highlight that such subtle differences can only be detected by measuring and analysing weapon shape and biomechanical components. Only then we might better understand how weapons are forged.     

Latitudinal variation and coevolutionary diversification of sexually dimorphic traits in the false blister beetle Oedemera sexualis

Sexual traits are subject to evolutionary forces that maximize reproductive benefits and minimize survival costs, both of which can depend on environmental conditions. Latitude explains substantial variation in environmental conditions. However, little is known about the relationship between sexual trait variation and latitude, although body size often correlates with latitude. We examined latitudinal variation in male and female sexual traits in 22 populations of the false blister beetle Oedemera sexualis in the Japanese Archipelago. Males possess massive hind legs that function as a female‐grasping apparatus, while females possess slender hind legs that are used to dislodge mounting males. Morphometric analyses revealed that male and female body size (elytron length), length and width of the hind femur and tibia, and allometric slopes of these four hind leg dimensions differed significantly among populations. Of these, three traits showed latitudinal variation, namely, male hind femur was stouter; female hind tibia was slenderer, and female body was smaller at lower latitudes than at higher latitudes. Hind leg sizes and shapes, as measured by principal component analysis of these four hind leg dimensions in each sex, covaried significantly between sexes, suggesting coevolutionary diversification in sexual traits. Covariation between sexes was weaker when variation in these traits with latitude was removed. These results suggest that coevolutionary diversification between male and female sexual traits is mediated by environmental conditions that vary with latitude.     

The effects of latitude,body size,and sexual selection on wing shape in a damselfly

Under natural selection, wing shape is expected to evolve to optimize flight performance. However, other selective factors besides flight performance may influence wing shape. One such factor could be sexual selection in wing sexual ornaments, which may lead to alternative variations in wing shape that are not necessarily related to flight performance. In the present study, we investigated wing shape variations in a calopterygid damselfly along a latitudinal gradient using geometric morphometrics. Both sexes show wing pigmentation, which is a known signal trait at intra‐ and interspecific levels. Wing shape differed between sexes and, within the same sex, the shape of the hind wing differed from the front wing. Latitude and body size explained a high percentage of the variation in wing shape for female front and hind wings, and male front wings. In male hind wings, wing pigmentation explained a high amount of the variation in wing shape. On the other hand, the variation in shape explained by pigmentation was very low in females. We suggest that the conservative morphology of front wings is maintained by natural selection operating on flight performance, whereas the sex‐specific differences in hind wings most likely could be explained by sexual selection. The observed sexual dimorphism in wing shape is likely a result of different sex‐specific behaviours. © 2011 The Linnean Society of London, Biological Journal of the Linnean Society, 2011, 102 , 263–274.     

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.     

Exaggerated allometric structures in relation to demographic and ecological parameters in Lucanus cervus (Coleoptera: Lucanidae)

Enlarged weapons and ornamental traits under sexual selection often show a positive allometric relationship with the overall body size. The present study explores the allometry of mandibles and their supporting structure, the head, in males of the European stag beetle, Lucanus cervus. This species shows a remarkable dimorphism in mandible shape and size that are used by males in intraspecific combats. Stag beetles were captured, measured, weighed, and released in the framework of a capture‐mark‐recapture study. The relationship of mandible length (ML) and head width in respect to the overall body size was described by a segmented regression model. A linear relationship was detected between ML and head width. The scaling relationships for both ML and head width identified the same switchpoint, highlighting the advantages of using combined results of weapons and their supporting structures in such analysis. These results led to a more consistent distinction of males in two morphologies: minor and major. The survival probability of individuals was dependent on the morphological class and was higher for minor males than for major. Elytron length and body mass of the individuals did not show any significant variation during the season. Differences in predatory pressure were detected between morphs by the collection and analysis of body fragments due to the predatory activity of corvids. Morphological differences and shift in demographic and ecological parameters between the two classes suggested that selection continues to favor intrasexual dimorphism in this species throughout a trade‐off mechanism between costs and benefits of carrying exaggerated traits. J. Morphol. 276:1193–1204, 2015. © 2015 Wiley Periodicals, Inc.     

Juvenile hormone regulates extreme mandible growth in male stag beetles

The morphological diversity of insects is one of the most striking phenomena in biology. Evolutionary modifications to the relative sizes of body parts, including the evolution of traits with exaggerated proportions, are responsible for a vast range of body forms. Remarkable examples of an insect trait with exaggerated proportions are the mandibular weapons of stag beetles. Male stag beetles possess extremely enlarged mandibles which they use in combat with rival males over females. As with other sexually selected traits, stag beetle mandibles vary widely in size among males, and this variable growth results from differential larval nutrition. However, the mechanisms responsible for coupling nutrition with growth of stag beetle mandibles (or indeed any insect structure) remain largely unknown. Here, we demonstrate that during the development of male stag beetles (Cyclommatus metallifer), juvenile hormone (JH) titers are correlated with the extreme growth of an exaggerated weapon of sexual selection. We then investigate the putative role of JH in the development of the nutritionally-dependent, phenotypically plastic mandibles, by increasing hemolymph titers of JH with application of the JH analog fenoxycarb during larval and prepupal developmental periods. Increased JH signaling during the early prepupal period increased the proportional size of body parts, and this was especially pronounced in male mandibles, enhancing the exaggerated size of this trait. The direction of this response is consistent with the measured JH titers during this same period. Combined, our results support a role for JH in the nutrition-dependent regulation of extreme mandible growth in this species. In addition, they illuminate mechanisms underlying the evolution of trait proportion, the most salient feature of the evolutionary diversification of the insects.     

Sexual dichromatism in wing pigmentation of New World dragonflies follows Rensch's rule

Many animal taxa that display sexual size dimorphism (SSD) exhibit a positive allometric relationship in which the degree of dimorphism increases with body size. This macroevolutionary pattern is known as Rensch's rule. Although sexual selection is hypothesized to be the main mechanism causing this pattern, body size is influenced by several selective forces, including natural and sexual selection. Therefore, by focusing exclusively on SSD one cannot ascertain which of these selective forces drives Rensch's rule. If sexual selection is indeed the main mechanism underlying Rensch's rule, we predict that other sexually selected traits, including coloration‐based ornaments, will also exhibit interspecific allometric scaling consistent with Rensch's rule. We tested this prediction using wing pigmentation of 89 species of dragonflies. Studies show that male wing pigmentation is generally under strong intra‐ and intersexual selection, so that sexual dichromatism in this trait should follow Rensch's rule. Conversely, the available evidence suggests that male body size is usually not sexually selected in dragonflies, so we do not expect SSD to follow Rensch's rule. First, we found that sexual dichromatism in wing pigmentation was consistent with Rensch's rule. The phylogenetic major axis regression slope was significantly greater than one. We also showed that the allometric slope for SSD was not different from unity, providing no support for Rensch's rule. Our results provide the first evidence that a trait which appears to be under strong sexual selection exhibits a pattern consistent with Rensch's rule.