Endocrine Control of Exaggerated Trait Growth in Rhinoceros Beetles.

Juvenile hormone (JH) is a key insect growth regulator frequently involved in modulating phenotypically plastic traits such as caste determination in eusocial species, wing polymorphisms in aphids, and mandible size in stag beetles. The jaw morphology of stag beetles is sexually-dimorphic and condition-dependent; males have larger jaws than females and those developing under optimum conditions are larger in overall body size and have disproportionately larger jaws than males raised under poor conditions. We have previously shown that large males have higher JH titers than small males during development, and ectopic application of fenoxycarb (JH analog) to small males can induce mandibular growth similar to that of larger males. What remains unknown is whether JH regulates condition-dependent trait growth in other insects with extreme sexually selected structures. In this study, we tested the hypothesis that JH mediates the condition-dependent expression of the elaborate horns of the Asian rhinoceros beetle, Trypoxylus dichotomus. The sexually dimorphic head horn of this beetle is sensitive to nutritional state during larval development. Like stag beetles, male rhinoceros beetles receiving copious food produce disproportionately large horns for their body size compared with males under restricted diets. We show that JH titers are correlated with body size during the late feeding and early prepupal periods, but this correlation disappears by the late prepupal period, the period of maximum horn growth. While ectopic application of fenoxycarb during the third larval instar significantly delayed pupation, it had no effect on adult horn size relative to body size. Fenoxycarb application to late prepupae also had at most a marginal effect on relative horn size. We discuss our results in context of other endocrine signals of condition-dependent trait exaggeration and suggest that different beetle lineages may have co-opted different physiological signaling mechanisms to achieve heightened nutrient-sensitive weapon growth.

Heightened condition-dependent growth of sexually selected weapons in the rhinoceros beetle, Trypoxylus dichotomus (Coleoptera: Scarabaeidae).

The exaggerated weapons and ornaments of sexual selection are condition-dependent traits that often grow to exaggerated proportions. The horns of male rhinoceros beetles are extremely sensitive to the larval nutritional environment and are used by rival males in combat over access to females. In contrast to horns, other parts of the body, such as wings, eyes, and legs, scale proportionally with body size, whereas others, such as males' external genitalia, are invariant with body size, regardless of nutrition. We document how body parts of the Asian rhinoceros beetle, Trypoxylus dichotomus, exhibit plasticity and constraint in response to nutritional condition. We discuss the implications of these results for the evolution of condition-dependent and condition-independent traits in animals.

No fecundity cost of female secondary sexual trait expression in the horned beetle Onthophagus sagittarius.

Typically males bear the products of sexual selection in the form of ornaments and/or weapons used to compete for and attract females. Secondary sexual traits in females have been thought of as the product of correlated responses to sexual selection on males. However, there is increasing phylogenetic evidence that female secondary sexual traits can arise independently of selection on males, and may be subject to sexual selection. Theoretical models of the evolution of female ornamentation via male mate choice have assumed that females suffer a cost of ornament expression via reduced fecundity, and hence female ornaments are less likely to evolve than male ornaments. In the dung beetle Onthophagus sagittarius, there has been an independent evolutionary origin of horns in females that are qualitatively different from the horns produced by males. We use this system as a model to examine the costs of horn expression for females within a life-history context. We identified a longevity cost of reproduction for females that was independent of horn expression. Large females lived longer, and after controlling for lifespan, had a higher lifetime fecundity, and invested more heavily in maternal provisioning than did small females. We found no evidence of a cost to females of investment in horns. Rather, the rate of increase in fecundity and horn expression with body size were equal, so that absolute horn size provides an accurate indicator of body size and maternal quality. The effects we observe were independent of female contest competition and/or male mate choice, which were excluded in our experimental protocol. However, we speculate on the potential functional contributions female horns might make to female fitness.

Insulin signaling and limb-patterning: candidate pathways for the origin and evolutionary diversification of beetle 'horns'.

Beetle 'horns' are rigid outgrowths of the insect cuticle used as weapons in contests for access to mates. Relative to their body size, beetle horns can be enormous. They protrude from any of five different regions of the head or thorax; they are curved, straight, branched or bladed; and their development is often coupled with the nutrient environment (male dimorphism) or with sex (sexual dimorphism). Here, we show that this extraordinary diversity of horns can be distilled down to four trajectories of morphological change--horn location, shape, allometry and dimorphism--and we illustrate how the developmental mechanisms regulating horn growth could generate each of these types of horn evolution. Specifically, we review two developmental pathways known to regulate growth of morphological structures in Drosophila and other insects: a limb-patterning pathway that specifies the location and shape of a structure, and the insulin pathway, which modulates trait growth in response to larval nutrition. We summarize preliminary evidence indicating that these pathways are associated with the development of beetle horns, and we show how subtle changes in the relative activities of these two pathways would be sufficient to generate most of the extant diversity of horn forms. Our objective is to intuitively connect genotype with phenotype, and to advocate an informed 'candidate gene' approach to studies of the developmental basis of evolution. We end by using this insight from development to offer a solution to the long-standing mystery of the scarabs: the observation by Darwin, Lameere, Arrow and others that this one family of beetles appeared to have a 'special tendency' towards the evolution of horns.

Hormonal control of male horn length dimorphism in Onthophagus taurus (Coleoptera: Scarabaeidae): a second critical period of sensitivity to juvenile hormone.

Male dung beetles (Onthophagus taurus) facultatively produce a pair of horns that extend from the base of the head: males larger than a threshold body size develop long horns, whereas males that do not achieve this size develop only rudimentary horns or no horns at all. Using topical applications of methoprene, we identified a sensitive period during the feeding stage of third (final) instar larvae when application of methoprene shifted the threshold body size for horn expression. Male larvae that received methoprene at this time delayed horn production until they attained a larger threshold body size than acetone-treated control larvae. This new sensitive period occurs earlier than a sensitive period previously reported for male horn regulation, and it coincides with a morph-specific pulse of ecdysteroid secretion described for this species. It appears that male horn expression is influenced by endocrine events at two different periods of larval development. We incorporate these results into an expanded model for the endocrine regulation of male horn expression.

Costs and the diversification of exaggerated animal structures.

Sexual selection can favor production of extravagant ornaments and weapons in the contest for access to the opposite sex. Existing explanations for the diversity of sexually selected structures focus on reproductive benefits conferred by particular ornament or weapon morphologies. Here, I show that costs of weapon production also may drive patterns of weapon evolution. In beetles, production of horns reduces the size of neighboring morphological structures (antennae, eyes, or wings, depending on the location of the horns), and these tradeoffs reveal unexpected functional associations between ecology and horn morphology. This study illustrates a critical but overlooked role of costs in sexual selection and has implications for understanding the evolution of animal morphology.

The development and evolution of exaggerated morphologies in insects.

We discuss a framework for studying the evolution of morphology in insects, based on the concepts of "phenotypic plasticity" and "reaction norms." We illustrate this approach with the evolution of some of the most extreme morphologies in insects: exaggerated, sexually selected male ornaments and weapons, and elaborate social insect soldier castes. Most of these traits scale with body size, and these scaling relationships are often nonlinear. We argue that scaling relationships are best viewed as reaction norms, and that the evolution of exaggerated morphological traits results from genetic changes in the slope and/or shape of these scaling relationships. After reviewing literature on sexually selected and caste-specific structures, we suggest two possible routes to the evolution of exaggerated trait dimensions: (a) the evolution of steeper scaling relationship slopes and (b) the evolution of sigmoid or discontinuous scaling relationship shapes. We discuss evolutionary implications of these two routes to exaggeration and suggest why so many of the most exaggerated insect structures scale nonlinearly with body size. Finally, we review literature on insect development to provide a comprehensive picture of how scaling relationships arise and to suggest how they may be modified through evolution.

The developmental basis for allometry in insects.

Within all species of animals, the size of each organ bears a specific relationship to overall body size. These patterns of organ size relative to total body size are called static allometry and have enchanted biologists for centuries, yet the mechanisms generating these patterns have attracted little experimental study. We review recent and older work on holometabolous insect development that sheds light on these mechanisms. In insects, static allometry can be divided into at least two processes: (1) the autonomous specification of organ identity, perhaps including the approximate size of the organ, and (2) the determination of the final size of organs based on total body size. We present three models to explain the second process: (1) all organs autonomously absorb nutrients and grow at organ-specific rates, (2) a centralized system measures a close correlate of total body size and distributes this information to all organs, and (3) autonomous organ growth is combined with feedback between growing organs to modulate final sizes. We provide evidence supporting models 2 and 3 and also suggest that hormones are the messengers of size information. Advances in our understanding of the mechanisms of allometry will come through the integrated study of whole tissues using techniques from development, genetics, endocrinology and population biology.

Hormonal control of male horn length dimorphism in the dung beetle Onthophagus taurus (Coleoptera: Scarabaeidae).

Male dung beetles (Onthophagus taurus) facultatively produce a pair of horns that extend from the base of the head: males growing larger than a threshold body size develop long horns, whereas males that do not achieve this size grow only rudimentary horns or no horns at all. Here we characterize the postembryonic development of these beetles, and begin to explore the hormonal regulation of horn growth. Using radioimmune assays to compare the ecdysteroid titers of horned males, hornless males, and females, we identify a small pulse of ecdysteroid which is present in both hornless males and females, but not in horned males. In addition, we identify a brief period near the end of the final (third) larval instar when topical applications of the juvenile hormone analog methoprene can switch the morphology of developing males. Small, normally hornless, males receiving methoprene during this sensitive period were induced to produce horns in 80% of the cases. We summarize this information in two models for the hormonal control of male dimorphism in horn length.

Competition among body parts in the development and evolution of insect morphology.

Changes in form during ontogeny and evolution depend in large measure on changes in the relative growth of the various parts of the body. The current consensus in developmental biology is that the final size of appendages and internal organs is regulated autonomously, within the structure itself. Size regulation of body parts typically requires no external control and is thought to be relatively insensitive to signals from the developmental environment. We show in two very different systems, butterfly wings and beetle horns, that experimentally induced changes in the allocation of developmental resources to one trait produces compensatory changes in the relative sizes of other traits. These findings illustrate that interaction among body parts in development is part of the mechanism of size regulation of those parts. Furthermore, in the case of beetle horns, we show that the tradeoff in size is manifest as a significant negative genetic correlation among the involved body parts and, therefore, constitutes a developmental source of genetic constraint on the evolution of body form.