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.     

Radio-telemetric monitoring of dispersing stag beetles: implications for conservation

Migratory movements of the endangered stag beetles Lucanus cervus (18 males, 38 females) were monitored radio-telemetrically for three reproductive periods (2003–2005). The aim of the study was to estimate the migratory range of free-ranging individuals as a measure of connectivity among neighbouring populations for future conservation measures. Miniature transmitters of c . 350 mg (battery life: 10–15 days) were attached externally to the pronotum. Transmitter/beetle mass ratio was 12.8% on average (7.1–28.0%). Male dispersal behaviour consisted of frequent flights directed to sites with reproductive females and rarely of on-ground movement. Total displacement distance recorded was up to 2065 m, the maximum distance of a single flight being 1720 m. Flights always began at elevated structures such as trees and shrubs and took place in an air temperature range of 11–27°C. Within this range, temperature did not influence flight distance. Female dispersal behaviour consisted mostly of a single flight, followed by mating and consequent ground movements towards oviposition sites. Total displacement distance recorded was up to 762.6 m, the maximum distance of a single flight being 701 m. Climatic constraints of flights were the same as in males. Modelling the dispersal behaviour suggests that about 1% of males are capable of maintaining gene flux among nest sites within a radius of about 3 km. However, the colonization of new nest sites depends on the dispersal ability of females and amounts to less than 1 km. Thus, isolated populations (distance to the next population greater than 3 km) have an increased probability of local extinction.     

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.     

Energetic constraints, size gradients, and size limits in benthic marine invertebrates

Populations of marine benthic organisms occupy habitats witha range of physical and biological characteristics. In the intertidalzone, energetic costs increase with temperature and aerial exposure,and prey intake increases with immersion time, generating sizegradients with small individuals often found at upper limitsof distribution. Wave action can have similar effects, limitingfeeding time or success, although certain species benefit fromwave dislodgment of their prey; this also results in gradientsof size and morphology. The difference between energy intakeand metabolic (and/or behavioral) costs can be used to determinean energetic optimal size for individuals in such populations.Comparisons of the energetic optimal size to the maximum predictedsize based on mechanical constraints, and the ensuing mortalityschedule, provides a mechanism to study and explain organismsize gradients in intertidal and subtidal habitats. For specieswhere the energetic optimal size is well below the maximum sizethat could persist under a certain set of wave/flow conditions,it is probable that energetic constraints dominate. When theopposite is true, populations of small individuals can dominatehabitats with strong dislodgment or damage probability. Whenthe maximum size of individuals is far below either energeticoptima or mechanical limits, other sources of mortality (e.g.,predation) may favor energy allocation to early reproductionrather than to continued growth. Predictions based on optimalsize models have been tested for a variety of intertidal andsubtidal invertebrates including sea anemones, corals, and octocorals.This paper provides a review of the optimal size concept, andemploys a combination of the optimal energetic size model andlife history modeling approach to explore energy allocationto growth or reproduction as the optimal size is approached.     

Internal and external constraints in the evolution of morphological allometries in a butterfly

Much diversity in animal morphology results from variation in the relative size of morphological traits. The scaling relationships, or allometries, that describe relative trait size can vary greatly in both intercept and slope among species or other animal groups. Yet within such groups, individuals typically exhibit low variation in relative trait size. This pattern of high intra- and low intergroup variation may result from natural selection for particular allometries, from developmental constraints restricting differential growth among traits, or both. Here we explore the relative roles of short-term developmental constraints and natural selection in the evolution of the intercept of the allometry between the forewing and hindwing of a butterfly. First, despite a strong genetic correlation between these two traits, we show that artificial selection perpendicular to the forewing-hindwing scaling relationship results in rapid evolution of the allometry intercept. This demonstrates an absence of developmental constraints limiting intercept evolution for this scaling relationship. Mating experiments in a natural environment revealed strong stabilizing selection favoring males with the wild-type allometry intercept over those with derived intercepts. Our results demonstrate that evolution of this component of the forewing-hindwing allometry is not limited by developmental constraints in the short term and that natural selection on allometry intercepts can be powerful.     

Thermoregulation in endothermic dung beetles (Coleoptera: Scarabaeidae): effect of body size and ecophysiological constraints in flight

We explore the physiological constraints of body temperature as related to body mass and ambient temperature during flight in endothermic dung beetles showing a mass-related breakpoint where species show strong vs. weak endothermy. We found two different strategies in the dung beetles prior to flight; larger beetles (>1.9 g) elevate and maintain their body temperature (T(b)) at levels well above ambient temperature (T(a)) whereas smaller beetles' (<1.9 g) T(b) tends to conform with T(a). Physiological constraints analysis revealed a constant maximum tolerated temperature (in flight) of 42 degrees C and a minimum temperature for flight of around 25 degrees C. These, with body mass, may play a role in thermal niche partitioning and geographical distribution patterns.     

Patterns of species assemblages and geographical distributions associated with mandible size differences in coastal tiger beetles in Japan

Nine species of tiger beetle (Cicindelidae) occur in coastal habitats in Japan, with two to four species co-occurring at each locality. To examine the patterns of coexistence and geographical distribution, the mandible size of co-occurring species at 17 localities in Japan was examined, based on the assumption that competition for food is an important factor in determining these patterns. The interspecific overlap of mandible length was absent or very low in localities with two or three species, whereas it was more or less evident in localities with four species. For four large coastal species, the geographical distributions of two species with similar mandible lengths are either allopatric or parapatric, whereas those of two species with different mandible lengths largely overlap. These results strongly suggest that size-assortment in mandible length is important in determining species assemblage and distribution in coastal tiger beetles in Japan.An erratum to this article can be found at     

Evolutionary and plastic variation in larval growth and digestion reveal the complex underpinnings of size and age at maturation in dung beetles

Age and size at maturity are key life‐history components, yet the proximate underpinnings that mediate intra‐ and interspecific variation in life history remain poorly understood. We studied the proximate underpinnings of species differences and nutritionally plastic variation in adult size and development time in four species of dung beetles. Specifically, we investigated how variation in insect growth mediates adult size variation, tested whether fast juvenile growth trades‐off with developmental stability in adult morphology and quantified plastic responses of digestive systems to variation in food quality. Contrary to the common size–development time trade‐off, the largest species exhibited by far the shortest development time. Correspondingly, species diverged strongly in the shape of growth trajectories. Nutritionally plastic adjustments to growth were qualitatively similar between species but differed in magnitude. Although we expected rapid growth to induce developmental costs, neither instantaneous growth rates nor the duration of larval growth were related to developmental stability in the adult. This renders the putative costs of rapid growth enigmatic. We further found that larvae that encounter a challenging diet develop a larger midgut and digest more slowly than animals reared on a more nutritious diet. These data are consistent with the hypothesis that larvae invest into a more effective digestive system when exposed to low‐quality nutrition, but suggest that species may diverge readily in their reliance on these mechanisms. More generally, our data highlight the complex, and often hidden, relationships between immature growth and age and size at maturation even in ecologically similar species.     

Diversification process of stag beetles belonging to the genus Platycerus Geoffroy (Coleoptera: Lucanidae) in Japan based on nuclear and mitochondrial genes

Molecular phylogenies of the genus Platycerus in Japan were characterized based on the nuclear 28S ribosomal RNA and mitochondrial cytochrome oxidase subunit I (COI) genes. These analyses, combined with our previous morphological information, revealed a detailed diversification process of Platycerus in Japan, as well as estimates of their divergence times. Japanese species were monophyletic and were inferred to have diverged to the acuticollis species group and all other species ca 1.69 Mya. The acuticollis species group then appeared to split into P. viridicuprus and a group including P. takakuwai, P. albisomni and P. acuticollis ca 1.26 Mya. Other specific divergences have occurred primarily since ca 0.33 Mya. Comparing the molecular trees and the morphological tree, we also found introgression of the COI gene in some species. Genetic divergence of Platycerus has occurred intensely in southwestern Japan.     

Local ecological divergence of two closely related stag beetles based on genetic,morphological, and environmental analyses

The process of phenotypic adaptation to the environments is widely recognized. However, comprehensive studies integrating phylogenetic, phenotypic, and ecological approaches to assess this process are scarce. Our study aims to assess whether local adaptation may explain intraspecific differentiation by quantifying multidimensional differences among populations in closely related lucanid species, Platycerus delicatulus and Platycerus kawadai, which are endemic saproxylic beetles in Japan. First, we determined intraspecific analysis units based on nuclear and mitochondrial gene analyses of Platycerus delicatulus and Platycerus kawadai under sympatric and allopatric conditions. Then, we compared differences in morphology and environmental niche between populations (analysis units) within species. We examined the relationship between morphology and environmental niche via geographic distance. P. kawadai was subdivided into the “No introgression” and “Introgression” populations based on mitochondrial COI gene – nuclear ITS region discordance. P. delicatulus was subdivided into “Allopatric” and “Sympatric” populations. Body length differed significantly among the populations of each species. For P. delicatulus, character displacement was suggested. For P. kawadai, the morphological difference was likely caused by geographic distance or genetic divergence rather than environmental differences. The finding showed that the observed mitochondrial–nuclear discordance is likely due to historical mitochondrial introgression following a range of expansion. Our results show that morphological variation among populations of P. delicatulus and P. kawadai reflects an ecological adaptation process based on interspecific interactions, geographic distance, or genetic divergence. Our results will deepen understanding of ecological specialization processes across the distribution and adaptation of species in natural systems.     

Host-plant specificity limits the geographic distribution of thistle feeding ladybird beetles

The relationships between two phytophagous ladybird beetle species, Epilachna pustulosa K^ono and E. niponica Lewis (Coleoptera, Coccinellidae), and their main host plants, thistles (Cirsium spp., Asteraceae) were investigated in Oshima Peninsula, southern Hokkaido, northern Japan. Epilachna pustulosa was found feeding on Cirsium kamtschaticum in the northernmost part of the peninsula, whereas E. niponica was confined to the Ohno Plain and adjacent areas in the southernmost part, and occurred mainly on C. alpicola. No thistle feeding epilachnines were found in the middle part of the peninsula despite the abundance of another thistle species, C. grayanum. Both beetle species showed lower adult preference and reduced growth performance on C. grayanum compared to their respective host plants under laboratory conditions. We concluded that the distribution of thistle feeding epilachnines in Oshima Peninsula was principally determined by the availability of appropriate host plants.     

Social cognition on the Internet: testing constraints on social network size

The social brain hypothesis (an explanation for the evolution of brain size in primates) predicts that humans typically cannot maintain more than 150 relationships at any one time. The constraint is partly cognitive (ultimately determined by some aspect of brain volume) and partly one of time. Friendships (but not necessarily kin relationships) are maintained by investing time in them, and failure to do so results in an inexorable deterioration in the quality of a relationship. The Internet, and in particular the rise of social networking sites (SNSs), raises the possibility that digital media might allow us to circumvent some or all of these constraints. This allows us to test the importance of these constraints in limiting human sociality. Although the recency of SNSs means that there have been relatively few studies, those that are available suggest that, in general, the ability to broadcast to many individuals at once, and the possibilities this provides in terms of continuously updating our understanding of network members' behaviour and thoughts, do not allow larger networks to be maintained. This may be because only relatively weak quality relationships can be maintained without face-to-face interaction.     

Symbiosis constraints: Strong mycobiont control limits nutrient response in lichens

Symbioses such as lichens are potentially threatened by drastic environmental changes. We used the lichen Peltigera aphthosa—a symbiosis between a fungus (mycobiont), a green alga (Coccomyxa sp.), and N₂‐fixing cyanobacteria (Nostoc sp.)—as a model organism to assess the effects of environmental perturbations in nitrogen (N) or phosphorus (P). Growth, carbon (C) and N stable isotopes, CNP concentrations, and specific markers were analyzed in whole thalli and the partners after 4 months of daily nutrient additions in the field. Thallus N was 40% higher in N‐fertilized thalli, amino acid concentrations were twice as high, while fungal chitin but not ergosterol was lower. Nitrogen also resulted in a thicker algal layer and density, and a higher δ¹³C abundance in all three partners. Photosynthesis was not affected by either N or P. Thallus growth increased with light dose independent of fertilization regime. We conclude that faster algal growth compared to fungal lead to increased competition for light and CO₂ among the Coccomyxa cells, and for C between alga and fungus, resulting in neither photosynthesis nor thallus growth responded to N fertilization. This suggests that the symbiotic lifestyle of lichens may prevent them from utilizing nutrient abundance to increase C assimilation and growth.     

The rarity and overexploitation paradox: stag beetle collections in Japan

For some wildlife commodities, rare species are especially sought after. The tendency for rare commodities to be of higher value can fuel their exploitation and as numbers dwindle, the demand can increase. Consequently, this can precipitate these rare species into an overexploitation vortex where they become increasingly rare, valued and exploited until eventual extinction. We focus here on the hobby of collecting stag beetles, to ascertain if the market value of these items is driven by rarity and if, consequently, these species are vulnerable to this overexploitation vortex. Stag beetle collections fuel a large and lucrative market in Japan, involving more than 700 species from all over the world, with over 15 million specimens imported a year. Some particularly valued species fetch more than US$5,000 a piece. We assessed the importance of species rarity as an acquisition criterion in this market using two methods: an Internet online questionnaire responded to by 509 participants and through examining the quantities imported in Japan and prices paid by collectors. We discovered that species rarity is one of the main choice criteria for acquisition by collectors: rare stag beetles are valued more than the common species and, consequently, stag beetles are vulnerable to the anthropogenic Allee effect in this market. Because of the sheer size of the market and the pervasive nature of this rarity paradox, the attraction to rarity equates to a potential extinction threat for many rare stag beetles species.