Diversity in the Weapons of Sexual Selection: Horn Evolution in the Beetle Genus Onthophagus (Coleoptera: Scarabaeidae)

Abstract

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 world's 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.Key words. Adaptive radiation, beetle horns, character divergence, male competition, Onthophagus, phylogeny, sexual selection, weapons.Received October 18, 2004. Accepted January 23, 2005 The history of life has been accentuated by several spectacular evolutionary radiations (Darwin 1871;Simpson 1949;Rensch 1959), and character divergence within these radiations frequently involves the exaggerated structures of sexual selection (Darwin 1871; West Eberhard 1983; Andersson 1994). The Hawaiian radiation of drosophilid flies, for example, has resulted in more than 900 extant species that differ most conspicuously in the wing patterns and courtship displays of males (Carson 1979;Templeton 1979;Kaneshiro and Boake 1987;Hoy et al. 1988;Kaneshiro 1988;Kambysellis et al. 1995). Similarly, radiations of birds-of-paradise, pheasants, and African Great Lake cichlids all involve the ornaments and displays of males (Beebe 1953;Gilliard 1969;Dominey 1984;Diamond 1986;Turner 1994;Deutsch 1997;Prum 1997;Frith and Beehler 1998; van Oppen et al. 1998). In fact, for a great many animals, the exaggerated structures of sexual selection display an evolutionary lability far surpassing that of other, not sexually selected structures (Darwin 1871;Geist 1966Geist , 1978Gilliard 1969; West-Eberhard 1983; Andersson 1994).Diversification of the ornaments and displays of mate choice is understandable-even expected. Numerous studies suggest that female choice can drive rapid divergence among populations (Lande 1981; West Eberhard 1983;Kaneshiro and Boake 1987;Endler and Houde 1995; van Oppen et al. 1998; Boake 2000;Uy and Borgia 2000;Boughman 2001;Masta and Maddison 2002;Mendelson 2003;Coleman et al. 2004). Founder events, genetic drift, and minor...

Evolutionary trade-off between weapons and testes

“…Robust hypotheses exist for the phylogenetic relationships of 22 of the 25 species in Table 1 (16,32), and we conducted comparative analyses by using independent contrasts (33) on this reduced data set, obtaining 21 evolutionary contrasts. Regression of the evolutionary contrasts returned qualitatively similar patterns to our cross species analyses.…”

“…One pattern that has emerged from the within-species studies of Onthophagus spp. is that trade-offs are often more pronounced for morphological structures that are physically nearest to the developing horn (16,24). For example, in species with horns positioned at the rear of the head, the negative relationship between horn size and eye size is greater than that between horn size and either antennae or wing size (24).…”

“…The ancestral character state for this genus is thought to be one in which males were monomorphic for a single horn at the back or vertex of the head, but there have been repeated evolutionary gains of additional horns elsewhere on the head or on the thorax (16). Across the phylogeny of onthophagines in our data set, there were 14 separate increases in the number of horns, with horns added to the thorax in 8 lineages, and horns added to the head in 6 (Fig.…”

“…3). Male dimorphism in horn expression appears to have arisen once early in the history of this genus, but there is evidence for four subsequent losses and one evolutionary regain of male dimorphism, resulting in a mixture of monomorphic and dimorphic taxa (16,32) (Fig. 3).…”

“…Horns can comprise a significant proportion of male body size and can project from any of five locations on the head or thorax. Horns can be expressed in both sexes but in most species are expressed in males only (sexual dimorphism) or in just the largest males (male dimorphism) (16). Males use their horns to block the entrance to breeding tunnels containing females, and males with larger horns are competitively superior (17,18) and attain a higher reproductive success than their short-horned conspecifics (19).…”