Heritability of male mandible length in the stag beetle Cyclommatus metallifer

Numerous coleopteran species express male‐specific “weapon traits” that often show size variations among males, even within a single population. Many empirical studies have demonstrated that environmental conditions during development affect absolute weapon size. However, relatively few studies in horned beetles support the hypothesis that the relationship between weapon size and body size, also referred to as a “scaling relationship” or “static allometry”, is largely determined by genetic factors. In this study, the heritability of absolute mandible length and static allometry between mandible length and body size were estimated in the stag beetle Cyclommatus metallifer. While no significant heritable variation was observed in absolute mandible length, high heritability (h² = 0.57 ± 0.25) was detected in the static allometry between mandible length and body size. This is the first report on the genetic effect on male mandible size in Lucanidae, suggesting that absolute mandible size is largely determined by environmental conditions while the static allometry between weapon size and body size is primarily determined by genetic factors.     

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.     

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.     

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.     

Size variation and mating success in the stag beetle, Lucanus cervus

Abstract.  The stag beetle, Lucanus cervus , is Britain's largest beetle, with a patchy distribution in southern England. The literature suggests that it displays exceptional size variation, particularly in the males, but no analysis of size inequality has ever been conducted. In the present study, stag beetle adults are measured and allometric relationships derived between various parameters and total body length. Most of the specimens found each year are fragments and head width can be used as a good predictor of total body length in each sex. Body size differs between years and between localities and male beetles show a greater degree of size inequality than females. However, L. cervus does not show greater inequality in size than many other beetle species and populations of males are composed of a relatively large number of small individuals. These males are not at a disadvantage in mating because it is the ratio of male : female size that determines mating success. Very large males are less successful in mating and it is suggested that lack of mating success may act as an additional constraint on mandible size in this species. Size variation is most likely caused by variation in larval food resources, coupled with variation in local climatic conditions.     

Resource Holding Potential and the Outcome of Aggressive Interactions between Paired Male <Emphasis Type="Italic">Aegus chelifer chelifer</Emphasis> (Coleoptera: Lucanidae) Stag Beetles

Interactions between male stag beetles usually involve aggressive behavior using their long mandibles as weapons to compete with rival males over females. Considerable variation exists within populations in male body size, and may affect their behavior and the outcome of male-male contests. We investigated the aggressive interactions between male Aegus chelifer chelifer, a small tropical stag beetle species. Morphological traits in relation to aggressiveness and the outcome of fights were examined in laboratory-reared beetles. The fight-engagement ratios of major and minor morph males were not significantly different and analyses revealed that the size of body parts had more effect on the fighting success than the weapon part (mandibles). The probability of winning a contest was higher in males with a larger head width (HW), and so HW was considered as the resource holding potential (RHP). No effects of the trait size on the initiation of fights or aggressive intensity was found. Relationships between the fight duration and RHP were not significantly consistent with any assessment strategies, but were close to the mutual assessment model.     

Variation in the ontogenetic allometry of horn length in bovids along a body mass continuum

Allometric relationships describe the proportional covariation between morphological, physiological, or life‐history traits and the size of the organisms. Evolutionary allometries estimated among species are expected to result from species differences in ontogenetic allometry, but it remains uncertain whether ontogenetic allometric parameters and particularly the ontogenetic slope can evolve. In bovids, the nonlinear evolutionary allometry between horn length and body mass in males suggests systematic changes in ontogenetic allometry with increasing species body mass. To test this hypothesis, we estimated ontogenetic allometry between horn length and body mass in males and females of 19 bovid species ranging from ca. 5 to 700 kg. Ontogenetic allometry changed systematically with species body mass from steep ontogenetic allometries over a short period of horn growth in small species to shallow allometry with the growth period of horns matching the period of body mass increase in the largest species. Intermediate species displayed steep allometry over long period of horn growth. Females tended to display shallower ontogenetic allometry with longer horn growth compared to males, but these differences were weak and highly variable. These findings show that ontogenetic allometric slope evolved across species possibly as a response to size‐related changes in the selection pressures acting on horn length and body mass.     

SEX‐SPECIFIC PATTERNS OF MORPHOLOGICAL DIVERSIFICATION: EVOLUTION OF REACTION NORMS AND STATIC ALLOMETRIES IN NERIID FLIES

The consequences of sex‐specific selection for patterns of diversification remain poorly known. Because male secondary sexual traits are typically costly to express, and both costs and benefits are likely to depend on ambient environment and individual condition, such traits may be expected to diversify via changes in reaction norms as well as the scaling of trait size with body size (static allometry). We investigated morphological diversification within two species of Australian neriid flies (Telostylinus angusticollis, Telostylinus lineolatus) by rearing larvae from several populations on larval diets varying sixfold in nutrient concentration. Mean body size varied among populations of T. angusticollis, but body size reaction norms did not vary within either species. However, we detected diversification of reaction norms for body shape in males and females within both species. Moreover, unlike females, males also diversified in static allometry slope and reaction norms for static allometry slope of sexual and nonsexual traits. Our findings reveal qualitative sex differences in patterns of morphological diversification, whereby shape–size relationships diversify extensively in males, but remain conserved in females despite extensive evolution of trait means. Our results highlight the importance of incorporating plasticity and allometry in studies of adaptation and diversification.     

Allometry for sexual size dimorphism: testing two hypotheses for Rensch's rule in the water strider Aquarius remigis

Within any given clade, male size and female size typically covary, but male size often varies more than female size. This generates a pattern of allometry for sexual size dimorphism (SSD) known as Rensch's rule. I use allometry for SSD among populations of the water strider Aquarius remigis (Hemiptera, Gerridae) to test the hypothesis that Rensch's rule evolves in response to sexual selection on male secondary sexual traits and an alternative hypothesis that it is caused by greater phenotypic plasticity of body size in males. Comparisons of three populations reared under two temperature regimes are combined with an analysis of allometry for genital and somatic components of body size among 25 field populations. Contrary to the sexual-selection hypothesis, genital length, the target of sexual selection, shows the lowest allometric slope of all the assayed traits. Instead, the results support a novel interpretation of the differential-plasticity hypothesis: that the traits most closely associated with reproductive fitness (abdomen length in females and genital length in males) are "adaptively canalized." While this hypothesis is unlikely to explain Rensch's rule among species or higher clades, it may explain widespread patterns of intraspecific variation in SSD recently documented for many insect species.     

It's all relative: allometry and variation in the baculum (os penis) of the harp seal, Pagophilus groenlandicus (Carnivora: Phocidae)

We compared allometry and variation in the baculum (os penis), mandible, and humerus of the harp seal, Pagophilus groenlandicus. This species is presumed to have a promiscuous mating system in which choice of mate by females during intromission with different males is likely. The baculum is large and grows throughout life so may be an honest indicator of males' quality (size) or viability (age). We predicted that bacular size would exhibit stronger allometry relative to body size than mandibles or humeri. The baculum is less functionally (mechanically) constrained than mandibles or humeri so we also predicted it would be more variable, though less variable than sexually selected traits which do not function as honest indicators. Our sample (N=67 seals) represented broad ranges of size and age (0–35 yr) so we compared variation using residuals from allometric regressions of skeletal measurements on body length. Bacular size was isometric to body length until ∼ 137 cm (when some seals enter puberty) in body length then was highly positively allometric; mandibular and humeral size were negatively allometric to body length throughout growth. Bacula were more variable than mandibles or humeri. Bacular size in large specimens (>137 cm in body length) was related strongly to body length and weakly to age. We interpret bacular size to be an uncheatable honest indicator of male quality and viability. High bacular variation conforms with theoretical predictions of females' asymmetrical choice of mate and choice of extremes, and may reflect corresponding anatomical variation among females. Some bacular variation may also result incidentally from positive allometry coupled with lifelong bacular growth, which can amplify early differences between reproductive and somatic growth, enabled by weak selection on bacular form in relation to function.     

Genital and body allometry in two species of noctuid moths (Lepidoptera: Noctuidae)

One‐size‐fits‐all and related hypotheses predict that static allometry slopes for male genitalia will be consistently lower than 1.0 and lower than the slopes for most other body parts (somatic traits). We examined the allometry of genitalic and somatic morphological traits in males and females of two species of noctuid moths, Spodoptera exigua (Hübner, [1808]) and Helicoverpa armigera (Hübner, [1808]). The relationship between genitalic traits and body size was generally strongly negative‐allometric in males but with no significant differences from 1.00 in females of the two species examined. However, in females, the slope of genital traits was also lower than the slopes for somatic traits. The relationship between somatic traits and the body size indicator was approximately isometric in most cases in males, except in four traits in S. exigua, in which the slopes showed slight negative allometry, and the hind tibia in H. armigera, in which the slope had positive allometry. However, in females, some somatic traits showed isometric and some other showed negative allometry in both species. The coefficients of variation (CV) for all structures in the males were low, not exceeding 10%. Genitalic traits showed significantly lower CV than somatic traits in males. In females, somatic traits showed lower CV than genitalic traits but with no significant difference in the H. armigera. Our observations of strongly negative allometry for genitalic traits in males are consistent with stabilizing selection on genital size and we suggest that male performance in interactions with females is the source of selection on male genital allometry. The difference in the degree of phenotypic variation between genitalic and somatic traits in the two studied species is attributed to the different developmental‐genetic architectures of these traits. Female genitalia showed a similar trend to the males, although the difference between genital and somatic traits was not significant in females. This finding suggests that selection is acting differently on male and female genitalia. Positive allometry of hind tibia in H. armigera may be a result of secondary sexual 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.     

Sexual dimorphism and allometry in two seed beetles (Coleoptera: Bruchidae)

Male Callosobruchus chinensis (Coleoptera: Bruchidae) have elaborated, pectinate antennae, which are absent from conspecific females and both sexes of a congener, Callosobruchus maculatus. To begin to unravel the mechanisms producing this striking dimorphism, we examined which morphological traits best explain body size variation in bruchid beetles and quantified sexual dimorphism of antenna size through allometric analyses. Using principal component analyses, we found that elytron length and pronotum width were significantly correlated with the first principal component, which was interpreted as explaining variation in body size. Regressions of log‐transformed body size measures on log‐transformed antenna length revealed that males of both species had longer antennae than conspecific females for any given body size, although most of this effect was attributable to higher intercepts, rather than increased allometry, in males. Comparisons among heterospecific males revealed that C. maculatus males have noticeably longer antennae than C. chinensis males at large body sizes. Callosobruchus chinensis males, thus, appear to have increased the receptive area of their antennae by adding to the width of, rather than further elongating, their antennae. Finally, we found evidence for positive allometry between log‐transformed antenna length and log‐transformed antenna width in C. chinensis males. We discuss our results in the context of evidence supporting the presence of an additional, and potentially unique, sex pheromone in C. chinensis females.     

Phylogeny of Japanese stag beetles (Coleoptera: Lucanidae) inferred from 16S mtrRNA gene sequences, with reference to the evolution of sexual dimorphism of mandibles

As a first step in reconstructing the phylogeny of world stag beetles (Coleoptera: Lucanidae), phylogenetic relationships among the major members of Japanese stag beetles were explored by analyzing a sequence of 1030 nucleotides from the mitochondrial 16S ribosomal RNA (16S rRNA) gene. A total of 20 species and three additional subspecies representing 13 genera were examined to provide basic information on the phylogeny of world Lucanidae. The resultant phylogenetic tree indicates that the family Lucanidae is monophyletic, and contains two major lineages: one consists of the genera Platycerus, Aesalus, Ceruchus, and Nicagus, and the other includes Dorcus, Rhaetulus, Prosopocoilus, Aegus, Neolucanus, Prismognathus, Lucanus, Figulus, and Nigidius. Generic members of the latter lineage are further divided into the following four sublineages: i) Figulus and Nigidius; ii) Prismognathus and Lucanus; iii) Aegus and Neolucanus; and iv) Dorcus, Rhaetulus, and Prosopocoilus. These molecular phylogenetic relationships are used as a basis for a preliminary exploration of the evolution of sexual dimorphism in the shape of the mandible. The results of this investigation suggest that strong sexual dimorphism with well-developed mandibles in males evolved independently at least twice, once in the genus Aegus and once in the ancestor of the Lucanus-Prismognathus and Dorcus-Rhaetulus-Prosopocoilus clades. Alternatively, it is possible that sexual dimorphism of mandibles has undergone secondary loss in the genera Figulus and Nigidius.     

Exaggerated Trait Allometry,Compensation and Trade-Offs in the New Zealand Giraffe Weevil (Lasiorhynchus barbicornis)

Sexual selection has driven the evolution of exaggerated traits among diverse animal taxa. The production of exaggerated traits can come at a cost to other traits through trade-offs when resources allocated to trait development are limited. Alternatively some traits can be selected for in parallel to support or compensate for the cost of bearing the exaggerated trait. Male giraffe weevils (Lasiorhynchus barbicornis) display an extremely elongated rostrum used as a weapon during contests for mates. Here we characterise the scaling relationship between rostrum and body size and show that males have a steep positive allometry, but that the slope is non-linear due to a relative reduction in rostrum length for the largest males, suggesting a limitation in resource allocation or a diminishing requirement for large males to invest increasingly into larger rostra. We also measured testes, wings, antennae, fore- and hind-tibia size and found no evidence of a trade-off between these traits and rostrum length when comparing phenotypic correlations. However, the relative length of wings, antennae, fore- and hind-tibia all increased with relative rostrum length suggesting these traits may be under correlational selection. Increased investment in wing and leg length is therefore likely to compensate for the costs of flying with, and wielding the exaggerated rostrum of larger male giraffe weevils. These results provide a first step in identifying the potential for trait compensation and trades-offs, but are phenotypic correlations only and should be interpreted with care in the absence of breeding experiments.     

The allometry between secondary sexual traits and body size is nonlinear among cervids

Allometric relationships between sexually selected traits and body size have been extensively studied in recent decades. While sexually selected traits generally display positive allometry, a few recent reports have suggested that allometric relationships are not always linear. In male cervids, having both long antlers and large size provides benefits in terms of increased mating success. However, such attributes are costly to grow and maintain, and these costs might constrain antler length from increasing at the same rate as body mass in larger species if the quantity of energy that males can extract from their environment is limiting. We tested for possible nonlinearity in the relationship between antler size and body mass (on a log–log scale) among 31 cervids and found clear deviation from linearity in the allometry of antler length. Antler length increased linearly until a male body mass threshold at approximately 110 kg. Beyond this threshold, antler length did not change with increasing mass. We discuss this evidence of nonlinear allometry in the light of life-history theory and stress the importance of testing for nonlinearity when studying allometric relationships.     

Mandible allometry in extant and fossil Balaenopteridae (Cetacea: Mammalia): the largest vertebrate skeletal element and its role in rorqual lunge feeding

Rorqual whales (crown Balaenopteridae) are unique among aquatic vertebrates in their ability to lunge feed. During a single lunge, rorquals rapidly engulf a large volume of prey‐laden water at high speed, which they then filter to capture suspended prey. Engulfment biomechanics are mostly governed by the coordinated opening and closing of the mandibles at large gape angles, which differentially exposes the floor of the oral cavity to oncoming flow. The mouth area in rorquals is delimited by unfused bony mandibles that form kinetic linkages to each other and with the skull. The relative scale and morphology of these skeletal elements have profound consequences for the energetic efficiency of foraging in these gigantic predators. Here, we performed a morphometric study of rorqual mandibles using a data set derived from a survey of museum specimens. Across adult specimens of extant balaenopterids, mandibles range in size from ～1–6 m in length, and at their upper limit they represent the single largest osteological element of any vertebrate, living or extinct. Our analyses determined that rorqual mandibles exhibit positive allometry, whereby the relative size of these mandibles becomes greater with increasing body size. These robust scaling relationships allowed us to predict mandible length for fragmentary remains (e.g. incomplete and/or fossil specimens), as we demonstrated for two partial mandibles from the latest Miocene of California, USA, and for mandibles from previously described fossil balaenopterids. Furthermore, we showed the allometry of mandible length to body size in extant mysticetes, which hints at fundamental developmental constraints in mysticetes despite their ecomorphological differences in feeding styles. Lastly, we outlined how our findings can be used to test hypotheses about the antiquity and evolution of lunge feeding. © 2012 The Linnean Society of London     

Sexual selection and the allometry of earwig forceps

Summary Positive intraspecific allometry, the tendency for large individuals to have relatively larger morphological traits, is thought to be more likely for secondary sexual traits than naturally selected traits. This is because secondary sexual traits are often used to signal individual quality and positive allometry should arise where the costs and/or benefits of signalling are size dependent. Here we examine the allometric relationships between forceps length, a sexually selected trait and elytra length, a naturally selected trait, in 42 species of earwig. Both forceps and elytra showed positive allometry. However, the degree of allometry was greater for forceps as predicted. If allometry arises due to sexual selection we would predict a greater degree of allometry in species with more exaggerated secondary sexual traits. Across species, the degree of forcep allometry did increase with forcep exaggeration. The relevance of positive allometry to reliable signalling is discussed.     

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.     

Phenetic relationships among four Apodemus species (Rodentia, Muridae) inferred from skull variation

Phenetic relationships among four Apodemus species (A. agrarius, A. epimelas, A. flavicollis and A. sylvaticus) inferred from skull (mandible and cranium) variation were explored using landmark-based geometric morphometrics. Analysis of size variation revealed that mandibles and crania of A. epimelas were the largest, followed by those of A. flavicollis, while A. agrarius and A. sylvaticus had the smallest ones. Phenetic relationships inferred from mandible shape variation better reflected phylogenetic relationships among the analyzed Apodemus species than those inferred from cranial differences. Concerning cranial shape variation, the most differentiated species was A. epimelas, whose ecology clearly differs from the other three species. Thus, differentiation of the mandible provided a pattern fully concordant with the phylogeny, while the cranium differentiation was in agreement with ecology expectations. The most evident shape changes of mandible and cranium involved the angular process and facial region, respectively. We also found that allometry had a significant influence on shape variation and that size-dependent shape variation differed among the analyzed species. Moreover, mandible and cranium are differently influenced by allometric changes. Different phenetic relationships inferred from mandible and cranium shape variation imply that phylogeny, ecology, together with factors related to size differences are all involved in the observed morphological divergence among the analyzed Apodemus species.