Mechanoreceptor distribution in stag beetle jaws corresponds to the material stress in fights

Male stag beetles (Lucanidae) use their extremely elongated jaws to pinch their rivals forcefully in male–male battles. The morphology of these jaws has to be a compromise between robustness (to withstand the bite forces), length and weight. Cyclommatus metallifer stag beetles circumvent this trade-off by reducing their bite force when biting with their slender jaw tips. Here we describe the functional mechanism behind the force modulation behaviour. Scanning Electron Microscopy and micro CT imaging show large numbers of small sensors in the jaw cuticle. We find a strong correlation between the distribution of these sensors and that of the material stress in the same jaw region during biting. The jaw sensors are mechanoreceptors with a small protrusion that barely protrudes above the undulating jaw surface. The sensors stimulate dendrites that extend from the neuronal cell body through the entire thickness of the jaw exoskeleton towards the sensors at the external surface. They form a sensory field that functions in a feedback mechanism to control the bite muscle force. This negative feedback mechanism enabled the stag beetles to evolve massive bite muscles without risking overloading their valuable jaws.     

Impacts of diet quality on life‐history and reproductive traits in male and female armed beetle,Gnatocerus cornutus

1. The energy available for reproduction is usually limited by resource acquisition (i.e. condition). Because condition is known to be strongly affected by environmental factors, reproductive investments also vary across heterogeneous environments. 2. Although the condition dependence of reproductive investment is common to both sexes, reproductive traits may exhibit sexually different responses to environmental fluctuation due to sex‐specific life‐history strategies. However, few direct experimental studies have investigated the condition dependence of reproductive investments in both sexes. 3. We investigated the condition dependence of life‐history and reproductive traits of males and females in the beetle Gnatocerus cornutus Fabricus by manipulating larval and adult diet quality. We found that male and female life‐history traits exhibited similar responses to environmental fluctuations. 4. By contrast, the sexes exhibit different patterns of condition dependence in reproductive traits (i.e. the adult nutritional environment has a strong impact on the female lifetime reproductive success, whereas larval nutritional environment strongly affects the secondary sexual trait in males). 5. This difference in the plasticity of reproductive traits may lead to different selection pressures for each sex, even if both sexes develop and/or live in the same environment.     

Size-dependent precopulatory behavior as mate-securing tactic in the Japanese stag beetle, Prosopocoilus inclinatus (Coleoptera; Lucanidae)

Males of the Japanese stag beetle Prosopocoilus inclinatus show dimorphism in body size. Since females frequently resist male courtship behavior, males often fail to mate after encounters with females. The males of two morphs showed different precopulatory behavior. During encounters with females, small males acted more persistently against females resistance than large males by grasping the female more solidly and as a result, succeeded in copulation more frequently. This persistent precopulatory behavior could be regarded as an alternative mating tactic of small males that are inferior to large males in direct physical competition.     

Phylogenetic analysis of sexual dimorphism and eye-span allometry in stalk-eyed flies (Diopsidae)

Eye stalks and their scaling relationship with body size are important features in the mating system of many diopsid species, and sexual selection is a critical force influencing the evolution of this exaggerated morphology. Interspecific variation in eye span suggests there has been significant evolutionary change in this trait, but a robust phylogenetic hypothesis is required to determine its rate and direction of change. In this study, the pattern of morphological evolution of eye span is assessed in a phylogenetic framework with respect to its function in the sexual system of these flies. Specifically, we examine within the family Diopsidae the pattern of increase and decrease in sexual dimorphism, the morphological coevolution of eye span between males and females, and the evolutionary flexibility of eye-span allometry. Based on several different methods for reconstructing morphological change, results suggest a general pattern of evolutionary flexibility, particularly for eye-span allometry. Sexual dimorphism in eye span has evolved independently at least four times in the family and this trait also has undergone several reductions within the genus Diasemopsis. Despite most species being dimorphic, there is a strong phylogenetic correlation between males and females for mean eye span. The coevolution between the sexes for eye-span allometry, however, is significantly weaker. Overall, eye-span allometry exhibits significantly more change on the phylogeny than the other morphological traits. The evolutionary pattern in eye-span allometry is caused primarily by changes in eye-span variance. Therefore, this pattern is consistent with recent models that predict a strong relationship between sexual selection and the variance of ornamental traits and highlights the significance of eye-span allometry in intersexual and intrasexual signaling.     

Relationship between size and shape in the sexually dimorphic beetle Prosopocoilus inclinatus (Coleoptera: Lucanidae)

Male characters that are used for male−male combat are often developed and exaggerated, whereas female equivalent characters are vestigial or vanished. In order to assess whether the characters common to both sexes share the same phenotypic variability due to common genetic architecture, we compared males and females of the stag beetle Prosopocoilus inclinatus using recently developed geometric morphometric methods. Elliptic Fourier analysis was used to compare shape variation between male characters (including exaggerated mandibles) and developmentally homologous female characters. A significant positive correlation was found between the size or between the weight of different body parts in both sexes, but a conspicuous difference was detected in the frequency distribution of the weight of all the body parts. Elliptic Fourier analysis demonstrated that there was marked discontinuous variation in mandibles in males, whereas such a discontinuity was not clear in females. The shape of a character in males exhibited some similarity with that of other characters, but this was not found in females. In a character, growth trajectory of shape was significantly affected by both size and weight in males, whereas size and shape tended to vary independently in female characters. These results support the hypothesis that a large sexual dimorphism in variation in shape is due to alleles accumulating in tight linkage with a sex-determining gene.  © 2004 The Linnean Society of London, Biological Journal of the Linnean Society , 2004, 81 , 219–233     

The complex ecology of genitalia: Gonopodium length and allometry in the Trinidadian guppy

Male genitalia present an extraordinary pattern of rapid divergence in animals with internal fertilization, which is usually attributed to sexual selection. However, the effect of ecological factors on genitalia divergence could also be important, especially so in animals with nonretractable genitalia because of their stronger interaction with the surrounding environment in comparison with animals with retractable genitalia. Here, we examine the potential of a pervasive ecological factor (predation) to influence the length and allometry of the male genitalia in guppies. We sampled guppies from pairs of low‐predation (LP) and high‐predation (HP) populations in seven rivers in Trinidad, and measured their body and gonopodium length. A key finding was that HP adult males do not have consistently longer gonopodia than do LP adult males, as had been described in previous work. However, we did find such divergence for juvenile males: HP juveniles have longer gonopodia than do LP juveniles. We therefore suggest that an evolutionary trend toward the development of longer gonopodia in HP males (as seen in the juveniles) is erased after maturity owing to the higher mortality of mature males with longer gonopodia. Beyond these generalities, gonopodium length and gonopodium allometry were remarkably variable among populations even within a predation regime, thus indicating strong context dependence to their development/evolution. Our findings highlight the complex dynamics of genitalia evolution in Trinidadian guppies.     

Heritability of sperm length in the bumblebee Bombus terrestris

Sperm length is highly variable, both between and within species, but the evolutionary significance of this variation is poorly understood. Sexual selection on sperm length requires a significant additive genetic variance, but few studies have actually measured this. Here we present the first estimates of narrow sense heritability of sperm length in a social insect, the bumblebee Bombus terrestris. In spite of a balanced and straightforward rearing design of colonies, and the possibility to replicate measurements of sperm within single males nested within colonies, the analysis proved to be complex. Several appropriate statistical models were derived, each depending on different assumptions. The heritability estimates obtained ranged from h ² = 0.197 ± 0.091 to h ² = 0.429 ± 0.154. All our estimates were substantially lower than previous estimates of sperm length heritability in non-social insects and vertebrates.     

Temporal variation in body size and weapon allometry in the New Zealand giraffe weevil

1. Body size and exaggerated traits can show high phenotypic plasticity in response to environmental variation. Trait size can vary among generations but also fluctuate within a breeding season in response to resource availability. 2. This study documents patterns of temporal variation in body and weapon size, and in weapon allometry over 3 years for a wild population of New Zealand giraffe weevils [Lasiorhynchus barbicornis (Fabricius)], the males of which display an extremely elongated rostrum used as a weapon during contests for females. 3. It was predicted that body size and rostrum allometry would decrease during a breeding season, but in spite of significant annual and seasonal variation there was little evidence to support these predictions. Weapon allometry in males was more variable between years and over the breeding season than females, suggesting that male rostrum size may be more susceptible to environmental change than female rostrum size.     

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

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

Structure and function of the large pronotal horn of the sand‐living anthicid beetle Mecynotarsus tenuipes

Large insect horns function as antipredator armaments, digging implements and intraspecific combat weapons. The sand‐living anthicid beetle Mecynotarsus tenuipes possesses a large horn on the pronotum. Allometric relationships between body size and horn size did not show either a slope of more than 1 or sexual dimorphism, suggesting another function of the horn other than sexual selection via combat. Behavioral observation of individuals using a microvideo camera indicated that the horn is used to dig and move forward in loose sand. Only the horned M. tenuipes could dig into sand, in contrast to the hornless anthicid beetles Stricticollis valgipes and Clavicollis fugiens, which could not dig. When moving in sand, M. tenuipes joins its pronotal horn and head to form a conical shape, with which it pierces into the sand. Then, it opens its horn and head outward to create a space in the sand for forward motion. Although it can dig deeply into sand by repeating these behaviors sequentially, digging speed tends to slow with depth, probably because the weight of the substrate increases.     

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

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

Effects of multiple mating and male eye span on female reproductive output in the stalk-eyed fly, Cyrtodiopsis dalmanni

Females of the stalk-eyed fly, Cyrtodiopsis dalmanni, mate repeatedly during their lifetime and exhibit mating preferencefor males with large eye span. How these mating decisions affectfemale fitness is not fully understood. In this study, we examinedthe effects of multiple mating and male eye span on short-termreproductive output in this species. Experiments that manipulatedthe number of copulations and partners a female received suggested that obtaining a sufficient sperm supply is an important benefitassociated with multiple mating. The average percentage offertile eggs laid by females increased as a function of matingfrequency and ranged from 40% for females mated once, to 80%for females mated continuously. In addition, a high proportionof copulations in this species appeared to be unsuccessful. One-third of all females mated once laid less than 10% fertileeggs. There was no significant difference in reproductive performancebetween females mated to multiple partners and females matedto a single partner. There was also no indication that femalesreceived any short-term reproductive benefits from mating withmales with large eye span. In fact, females mated to males with short eye span laid a higher percentage of fertile eggs thanfemales mated to large eye span males.     

The role of doublesex in the evolution of exaggerated horns in the Japanese rhinoceros beetle

Male‐specific exaggerated horns are an evolutionary novelty and have diverged rapidly via intrasexual selection. Here, we investigated the function of the conserved sex‐determination gene doublesex (dsx) in the Japanese rhinoceros beetle (Trypoxylus dichotomus) using RNA interference (RNAi). Our results show that the sex‐specific T. dichotomus dsx isoforms have an antagonistic function for head horn formation and only the male isoform has a role for thoracic horn formation. These results indicate that the novel sex‐specific regulation of dsx during horn morphogenesis might have been the key evolutionary developmental event at the transition from sexually monomorphic to sexually dimorphic horns.     

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.     

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

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

Horn polyphenism and related head shape variation in a single-horned dung beetle: Onthophagus (Palaeonthophagus) fracticornis (Coleoptera: Scarabaeidae)

Horns of Onthophagus beetles are typical examples of phenotypically plastic traits: they are expressed as a function of environmental (nutritional) stimuli, and their reaction norm (i.e. the full set of horn lengths expressed as a response to different degrees of nutritional states) can be either linear or threshold-dependent. Horned males of Onthophagus ( Palaeonthophagus ) fracticornis (Preyssler, 1790) bear a single triangular cephalic protrusion of vertex carina, which has received phylogenetic support as the most primitive horn shape in the genus. Inter- and intra-sexual patterns of horn expression were studied in O. fracticornis by means of static allometries while associated variations in head shape were assessed using geometric morphometric techniques. The relation between log-transformed measurements of body size and vertex carina supported an isometric scaling in females. On the contrary, a sigmoidal model described better the horn length-body size allometry in males, with a switch point between alternative morphs at a pronotum width of 3.88 mm. Sigmoidal static allometries of horns in Onthophagus populations arise from a threshold-dependent developmental process of horn growth. This process underlies the expression of both plesiomorphic and apomorphic horn shapes in the genus. Given that the single-horn model has been identified as primitive, we propose that such a developmental process giving rise to it may be evolutionarily ancient as well. Horn expression was accompanied by a deformation of the head which makes minor and major morphs appear even more different. Therefore, in this species both horn and head shape expression contribute to male dimorphism.     

Basicranial axis length v. skull length in analysis of carnivore skull shape

Skull length is the measurement most commonly used as a standard against which other aspects of cranial morphology are compared to derive an index of relative size or proportions. However, skull length is composed of two different functional components, facial skull and cerebral skull, which vary independently and have different scaling relationships with body size. An analysis of carnivore skull shape with measurements standardized against basicranium length produced very different results than an analysis using skull length as the standard. For example, expressions of relative size of cranial measurements were reduced by 13% in mustelids and increased by 20% in canids, reflecting removal of jaw length (short in mustelids and long in canids) from the comparative standard (basicranial axis length). Cranial measurements scale with higher allometric exponents against basicranial axis length than against skull length.