Ashlee L. Child

ashleecc@aol.com

Abstract: Male dung beetles (Onthophagus) have a secondary sexual trait that is, a dimorphism of horns (Hunt & Simmons, 1998). These adult dung beetles can be separated into two distinct classes: Large, "major" males have head horns, while "minor" males have rudimentary horns or are hornless. The pronotal width and body weight relationship have a strong linear correlation within the range of sizes. Thus, the pronotal width is a good indicator of body size (Lee & Peng, 1981). Larvae growing larger than a genetically determined threshold size metamorphose into adults with long horns, and larvae not reaching this size metamorphose into adults lacking or with very short horns (Emlen, 1994a, 1996).

Horn lengths expressed by individual males do not replicate horn lengths of their father. Instead, horn lengths reflect nutritional circumstances during larval development. (Emlen, 1995). A hormonal switch that controls development is triggered by the amount of dung provided by its parents. Assistance by major males results in the construction of substantially heavier brood masses. Therefore, father-son resemblance may be generated through the level of paternal care provided (Hunt & Simmons, 1999). Variation in the expression of these ornaments often leads to a variation in reproductive success (Emlin, 1995).

Beetle horns have been shown to operate as a tool in intrasexual combat, and the existence of a "hornless" class suggests that these smaller males may engage in an alternate, less aggressive behavior. Studies of the horned beetles have shown that these two morphs have different types of reproductive behavior. Large, horned beetles are found guarding entrances of tunnels that contain females. Small, hornless males adopt a sneaking behavior by digging new tunnels that intercept the guarded tunnels, remaining undetected. These two male reproductive tactics are labeled "guarding" and "sneaking". "Alternative" male mating behavior may contribute to the maintenance of dimorphic variation in male horns (Emlen, 1997).

Introduction: Beetle horns are rigid extensions of the exoskeleton, which appeared during the evolution of beetles, and are exhibited in thousands of species. This splendid history is displayed by a vast variety of horn morphologies: long cylindrical rods, curved flat blades, distended mandibles, and sundry spines, knobs, or tubercles.

Notwithstanding these differences in morphology, all the horns are used essentially for the same purpose. Horns, generally expressed only in males, are used in male-to-male combat for access to resources used by females (Emlen, 2000).

The genus Onthophagus, characterized by prolific evolution of horns, contains over 2000 species. The males in most of these species develop some type of horn though they vary in shape and location. These horned beetles are not only sexually dimorphic but also exhibit dimorphic variation within males. Onthophagines display dimorphisms in the male body plan, which large "major" males develop enlarged horns on the head and/or pronotum and small "minor" males are hornless or have rudimentary horns. The lengths of these horns scale positively with male body size. Males that grow larger than a critical, or threshold body size produce fully developed horns; male that do not reach this body size are ‘minor’ males that have small to no horns (Emlen and Nijhout, 1999).

Horn Development: Five morphologically and behaviorally discernible stages have been identified in Onthophagine beetles. The first three stages are comprised of a feeding period (end of the third instars), followed by a 2-day purge (Stage IV).

Metamorphosis begins almost immediately after the larva runs out of food (regardless of the size or weight of the larva as long as they are in their final instar). Larvae reared on smaller food amount pupate sooner, and at a smaller body size, than larvae with larger food amounts (Emlen 2000, Hunt and Simmons 1997). During this time, larvae synthesize most of their adult structure including horns. O. taurus larvae, like many other Scarabaeids, develop within isolated brood masses – the parent females bury fixed amounts of dung. They cannot seek other nutrition but must develop completely using only the food available. Larvae that wait to initiate metamorphosis until all available food has been consumed will attain as large a body size as possible (Emlen and Nijhout, 1998).

The male horns first appear at the end of the final larval instar as a pair of invaginations of the larval epidermis in the occipital region of the head. It is only after the third larval stage, after larvae have completed all of their growth in body size and have begun to purge, that the beetle will become sensitive to the presence of juvenile hormone (JH). Exact levels of JH in O. taurus males have not been measured yet though it appears that larger animals have higher concentrations of JH during this critical period than smaller individuals. This is identified as the critical period for horn determination. High levels of JH appear to activate rapid cell proliferation causing future horned males. Low levels of JH initiate only minimal cell proliferation causing future hornless males.

Horn length cannot be determined until late in the larval development due that it is at the end of the feeding stage that larvae can evaluate their nutritional state (all growth in body size has completed). Somehow, Developing animals are able to incorporate information on their body size into the ‘decision’ of whether or not to grow horns. (Emlen, 2000).

Horn development is facultative, and depends on the attainment of a certain body size, which, in turn, is influenced by the nutrition obtained by males during development. The males’ developmental pathway is triggered by the amount of dung provided by his parents (Hung and Simmons, 1999).

Biparental Care: Parental care in dung-burying beetles is generally restricted to brood mass construction. In the majority of theses species, the female alone is capable of successfully provisioning larvae. Yet there are numerous studies indicating extensive levels on cooperation between males and females. Males have been observed helping move dung from the dung pad to the site of burial and oviposition (Hunt and Simmons, 1998).

When females breed alone (uniparental care), only females larger than average are adept for providing enough resources to rear a major son. Brood mass weight increases linearly with female size, however, brood mass number is not influenced by female size.

There is a significant effect on brood mass weight with assistance of major males though not with minor males. Brood masses produced with major males were 48% larger than expected given the size of female. Brood masses produced with minor males fell within the weight range expected for females provisioning alone (uniparental).

In experiments performed by Hunt and Simmons (Hunt and Simmons, 1999), they found the individual females breeding with major males produced heavier brood masses than those breeding with minor males or breeding alone. Paternal assistance increases the brood mass weight though it does not increase the overall brood mass number.

Paternal provisioning tactics are known to covary with male morphology. When O. taurus reaches a critical body size and invests in horns (<5 mm pronotum width) they invest in the production of horns and also switch parental provisioning tactics and assist females during brood mass construction. The level of care provided by major males did not increase with body size but represented an "all-or-none" tactic.

Offspring size upon emergence reflects the size of the brood ball, but not their parental sizes. Size is largely determined by the quantity of dung provided in the brood mass (Lee and Peng, 1981). Existence of a critical food quantity threshold separates the development of horned and hornless male phenotypes. Males confined to a food amount below a critical quantity failed to produce horns, but went from minimal to complete horn expression once food amounts larger than critical quantity were available to larvae (Moczek, 1998).

Paternal and maternal provisioning affects the body size and horn size of offspring produced. Food availability during larval development predictably determines adult morphology. An increased weight of brood ball results in the development of larger adult body sizes (Moczek, 1998). Nutritional conditions encountered by larva as it develops determine both final adult body size and length of horns. Thus, the additional dung provided by a major male increases the size of offspring (Hunt and Simmons, 2000).

Reproduction Tactics: Dimorphic variation in the Onthophagine species, two or more distinct male forms co-occurring in populations with intermediate forms scarce or lacking, implicates morphological specialization for alternative behavior (Emlen, 1997). As it turns out, the horned and hornless males do use entirely different behavioral tactics to encounter females and mate.

Females of both O. Taurus and O. acuminatus dig tunnels into the soil beneath a dung pad. After a tunnel of sufficient depth has been completed, the female will form a small cavity at the blind end. The females live in intricate tunnel systems, where they procure pieces of dung for themselves and their larvae. The dung pieces are formed into well-compacted, oval-shaped brood balls. At the top of each brood ball an egg chamber is formed, a single egg is deposited, and closed off with an excrement cap (Hunt and Simmons, 1998).

During the days following and all through egg laying, the females will mate repeatedly with males. Because the female is in the tunnel system during this time, access into a tunnel is a precondition for mating. Thus, male reproductive behavior will revolve around the processes of acquiring admittance to the females inside the tunnels (Moczek and Emlen, 2000).

Males employ two very different tactics to encounter and mate with females: 1) they attempt to control access to a female by guarding the entrance of her tunnel (this is called ‘guarding’, or 2) they attempt to bypass a guarding male (‘sneaking’).

Males who engage in guarding behavior remain inside a tunnel with a female and fight off any intruding males. Guarding males will block off tunnel entrances and periodically ‘patrol’ the length of a tunnel. A rival male could gain possession of a tunnel if he successfully evicted the resident male.

Sneaking males bypass the guarding male by either digging side tunnels that intercept the tunnels containing a female or by entering a guarded tunnel directly. Occasionally a guarding male will be away from the tunnel and the sneaking male can enter unchallenged. Once inside, a sneaking male will mate with a female and then leave. Even when a sneaking male succeeds in entering a tunnel undetected, they will exit immediately after mating (<10 min) (Emlen, 1997).

The question is, what male will take on which behavior? In competition with horned males, both males are aggressive and will compete in head-to-head combat. The fight will continue until one male is able to dislodge his opponent from the substrate and then pushing him out of the tunnel (resident male wins) or to push the resident male further into the tunnel until the diameter is enough for the stronger male to climb around the opponent and force him out of the tunnel (intruding male wins). Both horned males employ the guarding behavior.

Competition between two hornless males resembled the fighting between two horned males. Both take similar fighting positions engage in head-to-head pushes. In contrast to the horned male, once a defeated male is expelled from the tunnel, the hornless male will remain close to the tunnel entrance and repeatedly tries to reenter the tunnel (Moczek and Emlen, 2000).

Horned males did not exhibit any change in behavior when rivaled against a hornless male as compared to a horned male. In all cases a horned male will take on an aggressive fighting behavior. The hornless males behavior, however, changes and is more complex. If the hornless male was the resident male and a horned male intrudes, the hornless engaged in the head-to-head contact but in no cases won. Instead, the intruding horned male expelled the hornless male. The hornless male was observed repeatedly trying to enter the tunnel. The only ways a hornless male was able to mate with a female guarded by a horned male are 1) sneaking down the tunnel while the guarding male was absent, or 2) below-ground tunnels that intercept the main tunnel that contain the female (Moczek and Emlen 2000, Emlen 1997).

Horned males always used the fighting behavior independent of the morphology of the other male. They did not adopt the sneaking behavior but left the area of the main tunnel immediately.

Hornless males also fought for access to the main tunnel (possession of horns is not a prerequisite for the adoption of fighting behavior). Although, a hornless male was never able to defeat a horned male using the fighting behavior, it adopts a secondary sneaking behavior. This non-aggressive behavior does entail maneuvering in and out of tunnels quickly, which the horned male is not able to perform as well as the hornless male (Moczek and Emlen, 2000).

Moczek and Emlen suggest that the occurrence to two male morphologies reflects two discrete alternative reproductive tactics, each favoring opposite phenotypes (horn morphology).

Emlen, Douglas J. 1994. Environmental Control Of Horn Length Dimorphism In The Beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Proc. R. Soc. Lond. B 256, pp. 131-136

Emlen, Douglas J. 1996. Artificial Selection On Horn Length-Body Size Allometry In The Horned Beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Evolution. 50(3) pp. 1219-1229

Emlen, Douglas J. 1997. Alternative Reproductive Tactics And Male-Dimorphism In The Horned Beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Behav. Ecol. Sociobiol. 41: 335-341

Emlen, Douglas J. 1997. Diet Alters Male Horn Allometry In The Beetle Onthophagus acuminatus (Coleoptera: Scarabaeidae). Proc. R. Soc. Lond. B. 264, 567-574

Emlen, Douglas J. 2000. Integrating Development With Evolution: A Case Study With Beetle Horns. BioScience. Vol. 50 No. 5 pp. 403-418

Emlen, Douglas J. and Nijhout, H. Frederick. 1998. Hormonal Control Of Male Horn Length Dimorphism In The Dung Beetle Onthophagus taurus (Coleoptera: Scarabaeidae). Journal Of Insect Physiology. 45 (1999) 45-43

Hunt, J and Simmons, L.W. 1998. Patterns Of Parental Provisioning Covary With Male Morphology In A Horned Beetle (Onthophagus taurus) (Coleoptera: Scarabaeidae). Behav. Ecol. Sociobiol. 42: 447-451

Hunt, J and Simmons, L.W. 2000. Maternal And Paternal Effects On Offspring Phenotype In The Dung Beetle Onthophagus taurus. Evolution. 54(3), 2000, pp. 936- 941

Lee, J.M. and Peng, Y. 1981. Influence Of Adult Size Of Onthophagus gazella On Manure Pat Degradation, Nest Construction, And Progeny Size. Envir. Entomology. V. 10, pp. 626-630

Moczek, Armin Phillipp. 1998. Horn Polyphenism In The Beetle Onthophagus taurus: Larval Diet Quality And Plasticity In Parental Investment Determine Adult Body Size And Male Horn Morphology. Behavioral Ecology. Vol. 9 No. 6: 636-641

Moczek, Armin P. and Emlen, Douglas J. 2000. Male Horn Dimorphism In The Scarab Beetle, Onthophagus taurus: Do Alternative Reproductive Tactics Favor Alternative Phenotypes? Animal Behavior. 59, pp. 459-466