Douglas J. Emlen

Male horn dimorphism in the scarab beetle, Onthophagus taurus: do alternative reproductive tactics favour alternative phenotypes?

In a variety of organisms morphological variation is discrete rather than continuous. Discrete variation within a sex has attracted particular interest as it is thought to reflect the existence of alternative adaptations to a heterogeneous selection environment. The beetle Onthophagus taurus shows a dimorphism for male horns: males that exceed a critical body size develop a pair of long, curved horns on their heads, while smaller males remain hornless. In this study we report on the alternative reproductive tactics used by males with these two morphologies, and present experimental and behavioural data suggesting that these alternative tactics selectively favour discretely different male phenotypes. Horned males aggressively defended tunnel entrances containing breeding females. Fights involved the use of horns, and males with longer horns were more likely to win fights. In contrast, hornless males employed nonaggressive sneaking behaviours when faced with competitively superior males. Sneaking behaviours appeared to require high degrees of manoeuvrability inside tunnels to access and mate with females despite the presence of a guarding male. Comparisons of running performances of males with identical body sizes but different horn lengths suggest that the possession of horns reduces male agility inside tunnels. Thus, horn possession confers a clear advantage to males using fighting behaviours to access females, whereas hornlessness may be favoured in males that rely primarily on sneaking behaviours. Combined, the two alternative reproductive tactics used by male O. taurus appear to favour opposite horn phenotypes, which may explain the paucity of intermediate morphologies in natural populations of O. taurus. Copyright 2000 The Association for the Study of Animal Behaviour.

Alternative reproductive tactics and male-dimorphism in the horned beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae)

Abstract Adult dung beetles (Onthophagus acuminatus) exhibit continuous variation in body size resulting from differential nutritional conditions experienced during larval development. Males of this species have a pair of horns that protrude from the base of the head, and the lengths of these horns are bimodally distributed in natural populations. Males growing larger than a threshold body size develop long horns, and males that do not achieve this size grow only rudimentary horns or no horns at all. Previous studies of other horned beetle species have shown that horned and hornless males often have different types of reproductive behavior. Here I describe the mating behaviors of the two male morphs of O. acuminatus during encounters with females. Females excavate tunnels beneath dung, where they feed, mate and provision eggs. Large, horned males were found to guard entrances to tunnels containing females. These males fought with all other males that attempted to enter these tunnels. In contrast, small, hornless males encountered females by sneaking into tunnels guarded by other males. In many instances, this was accomplished by digging new tunnels that intercepted the guarded tunnels below ground. Side-tunneling behavior allowed sneaking males to enter tunnels beneath the guarding male, and mate with females undetected. Both overall body size and relative horn length significantly affected the outcome of fights over tunnel ownership. These results suggest that alternative reproductive tactics may favor divergence in male horn morphology, with long horns favored in males large enough to guard tunnels, and hornlessness favored in smaller males that adopt the “sneaking” behavioral alternative.

Environmental control of horn length dimorphism in the beetle Onthophagus acuminatus (Coleoptera:Scarabaeidae)

Impressive examples of male ornamentation occur in horned beetles. Many beetle species are characterized by substantial amounts of phenotypic variation in horn length, and in some species this variation is biomodally distributed so that males may be separated into two groups on the basis of horn length. Two discrete male morphs are present in natural populations of Onthophagus acuminatus (Coleoptera: Scarabaeidae), a dung beetle common to lowland tropical forests of Panama. Large males possess a pair of frontal horns, which in small males are greatly reduced in length or are lacking. This paper presents results from experiments designed to assess the relative importance of genetic and environmental factors as determinants of male horn morphology. Experimental manipulation of food quantity, a factor known to influence body size, showed that male horn length variation in O. acuminatus was influenced primarily by environmental factors. Horn lengths of male progeny were a function of individual differences in body size (the manipulated variable) and not of the horn lengths of their fathers, in both experimental and control populations. These results support recent theories on sexual selection which predict that male ornaments will evolve to be reliable indicators of male quality. The utility of incorporating studies of developmental mechanism into analyses of morphological evolution is discussed.

A Mechanism of Extreme Growth and Reliable Signaling in Sexually Selected Ornaments and Weapons

Truthful Embellishments Exaggerated ornaments such as beetle horns, deer antlers, and extreme tail lengths in birds are typically assumed to be subject to sexual selection because they signal the quality of an individuals breeding status—but how? Emlen et al. (p. 860, published online 26 July) present a general mechanistic model for the evolution of exaggerated traits, proposing that sensitivity to the insulin response pathway can explain variation among individuals. The exaggerated size of such ornaments and their increased variability between individuals are a result of sexual selection for traits that are honest signals of the fitness of the individual. Rhinoceros beetle horns, a sexually selected weapon, are more sensitive to nutrition and reliably indicate male quality. Many male animals wield ornaments or weapons of exaggerated proportions. We propose that increased cellular sensitivity to signaling through the insulin/insulin-like growth factor (IGF) pathway may be responsible for the extreme growth of these structures. We document how rhinoceros beetle horns, a sexually selected weapon, are more sensitive to nutrition and more responsive to perturbation of the insulin/IGF pathway than other body structures. We then illustrate how enhanced sensitivity to insulin/IGF signaling in a growing ornament or weapon would cause heightened condition sensitivity and increased variability in expression among individuals—critical properties of reliable signals of male quality. The possibility that reliable signaling arises as a by-product of the growth mechanism may explain why trait exaggeration has evolved so many different times in the context of sexual selection.

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.

Evolutionary trade-off between weapons and testes.

It has long been recognized that male mating competition is responsible for the evolution of weaponry for mate acquisition. However, when females mate with more than one male, competition between males can continue after mating in the form of sperm competition. Theory predicts that males should increase their investment in sperm production as sperm competition is increased, but it assumes that males face a trade-off between sperm production and other life-history traits such as mate acquisition. Here, we use a genus of horned beetle, Onthophagus, to examine the trade-off between investment in testes required for fertilizations and investment in weapons used to obtain matings. In a within-species study, we prevented males from developing horns and found that these males grew larger and invested relatively more in testes growth than did males allowed to grow horns. Among species, there was no general relationship between the relative sizes of horns and testes. However, the allometric slope of horn size on body size was negatively associated with the allometric slope of testes size on body size. We suggest that this reflects meaningful evolutionary changes in the developmental mechanisms regulating trait growth, specifically in the degree of nutrition-dependent phenotypic plasticity versus canalization of traits. Finally, we show how this resource allocation trade-off has influenced the evolutionary diversification of weapons, revealing a rich interplay between developmental trade-offs and both pre- and postmating mechanisms of sexual competition.

DIVERSITY IN THE WEAPONS OF SEXUAL SELECTION: HORN EVOLUTION IN THE BEETLE GENUS ONTHOPHAGUS (COLEOPTERA: SCARABAEIDAE)

Abstract 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 worlds 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.

ARTIFICIAL SELECTION ON HORN LENGTH-BODY SIZE ALLOMETRY IN THE HORNED BEETLE ONTHOPHAGUS ACUMINATUS (COLEOPTERA: SCARABAEIDAE)

Males of the horned beetle Onthophagus acuminatus Har. (Coleoptera: Scarabaeidae) exhibit horn length dimorphism due to a sigmoidal allometric relationship between horn length and body size: the steep slope of the allometry around the inflection of the sigmoid curve separates males into two groups; those larger than this inflection possess long horns, and those smaller than this inflection have short horns or lack horns. I examined the genetic basis of the allometric relationship between horn length and body size by selecting males that produced unusually long horns, and males that produced unusually short horns, for their respective body sizes. After seven generations of selection, lines selected for relatively long horns had significantly longer horn lengths for a given body size than lines selected for relatively short horns, indicating a heritable component to variation in the allometry. The sigmoidal shape of the allometry was not affected by this selection regime. Rather, selected lines differed in the position of the allometry along the body size axis. One consequence of lateral shifts in this allometric relationship was that the body size separating horned from hornless males (the point of inflection of the sigmoid curve) differed between selection lines: lines in which males were selected for relatively long horns began horn production at smaller body sizes than lines selected for relatively short horns. These results suggest that populations can evolve in response to selection on male horn length through modification of the growth relationship between horn length and body size.

On the origin and evolutionary diversification of beetle horns

Many scarab beetles produce rigid projections from the body called horns. The exaggerated sizes of these structures and the staggering diversity of their forms have impressed biologists for centuries. Recent comparative studies using DNA sequence-based phylogenies have begun to reconstruct the historical patterns of beetle horn evolution. At the same time, developmental genetic experiments have begun to elucidate how beetle horns grow and how horn growth is modulated in response to environmental variables, such as nutrition. We bring together these two perspectives to show that they converge on very similar conclusions regarding beetle evolution. Horns do not appear to be difficult structures to gain or lose, and they can diverge both dramatically and rapidly in form. Although much of this work is still preliminary, we use available information to propose a conceptual developmental model for the major trajectories of beetle horn evolution. We illustrate putative mechanisms underlying the evolutionary origin of horns and the evolution of horn location, shape, allometry, and dimorphism.

Evolution of Sexual Dimorphism and Male Dimorphism in the Expression of Beetle Horns: Phylogenetic Evidence for Modularity, Evolutionary Lability, and Constraint

Beetle horns are enlarged outgrowths of the head or thorax that are used as weapons in contests over access to mates. Horn development is typically confined to males (sexual dimorphism) and often only to the largest males (male dimorphism). Both types of dimorphism result from endocrine threshold mechanisms that coordinate cell proliferation near the end of the larval period. Here, we map the presence/absence of each type of dimorphism onto a recent phylogeny for the genus Onthophagus (Coleoptera: Scarabaeidae) to explore how horn development has changed over time. Our results provide empirical support for several recent predictions regarding the evolutionary lability of developmental thresholds, including uncoupled evolution of alternative phenotypes and repeated fixation of phenotypes. We also report striking evidence of a possible developmental constraint. We show that male dimorphism and sexual dimorphism map together on the phylogeny; whenever small males have horns, females also have horns (and vice versa). We raise the possibility that correlated evolution of these two phenomena results from a shared element in their endocrine regulatory mechanisms rather than a history of common selection pressures. These results illustrate the type of insight that can be gained only from the integration of developmental and evolutionary perspectives.