On the origin and evolutionary diversification of beetle horns

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   Fig. 1.

   Evolution of horn allometry. Horn length–body size scaling relationships shown for the head horns of nine Australian species of Onthophagus, representing a well supported monophyletic clade within the phylogeny of Emlen et al. (29).

   
   
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   Fig. 2.

   Development of beetle horns. Life cycle shown for the dung beetle Onthophagus taurus. After hatching, beetles pass through three larval instars before molting first into a pupa and then into an adult. Black arrows indicate feeding periods; gray arrows indicate nonfeeding periods. Arrow thickness approximates overall animal body size, and gaps between arrows indicate molting events. The final (third) larval instar can be divided into a feeding period and a nonfeeding prepupal period. Drawings inside the arrows illustrate egg, first through third larval instars, prepupa, pupa, and adult. Horn development can be divided into two stages: a period of horn growth when horn cell proliferation occurs, and a period of horn remodeling. The top box shows horn growth. Front view of thoracic (green) and head (blue) horn discs are shown, along with two profile views of the prepupal head and thorax during this stage. The side box shows horn remodeling. The drawings illustrate the profile of a large male just after pupation and the head and thorax of the same male at two later stages during the pupal period. The head horns are remodeled slightly, to form a pair of curved and slender adult horns. The pupal thoracic horn is removed completely, and is not present in adults. Close-up profiles of prepupa and pupa are adapted from figure 2 of ref. 48.

   
   
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   Fig. 3.

   Nutrition-dependent phenotypic plasticity and allometry in insects. (a) Female (left) and male (right) Proagoderus (Onthophagus) lanista, showing among-individual variation in body size and, in males, horn size. (b) Scaling relationships (allometries) for four morphological traits in the beetle O. acuminatus. Individuals reared with access to large food amounts (high nutrition) (open symbols) emerged at larger adult body sizes than full-sibling individuals reared with smaller food amounts (low nutrition) (closed symbols). Traits differed in how sensitive (plastic) their growth was to this variation in nutrition. Male horns were the most sensitive, and horn lengths were >10-fold longer in the largest individuals than they were in the smallest individuals (females of this species do not produce enlarged horns, and the height of the corresponding head region is indicated by the gray squares). Leg and wing development was also sensitive to nutrition, but legs were less plastic than wings or horns. Male genitalia were almost entirely insensitive to nutrition, and the size of the aedeagus was largely body size invariant. Horns, legs, and genitalia are plotted on the same scale to illustrate the relative plasticity (horns, legs) or canalization (male genitalia, female horns) of their development. Wings were much larger and are shown on their own scale. In all cases, the degree of plasticity/canalization (black arrows) is reflected in the steepness of the trait size–body size allometries. (c) Model for one developmental mechanism of allometry in insects. Larval nutritional state is reflected in circulating levels of insulins (and growth factors; data not shown), which modulate the rate of growth of each of the trait imaginal discs. Traits whose disc cells are sensitive to these signals exhibit greater nutrition-dependent phenotypic plasticity and steeper allometry slopes than other traits whose disc cells are less sensitive to these signals.

   
   
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   Fig. 4.

   Development of a branched beetle horn. Horn disc from a late-stage prepupa of a male rhinoceros beetle (Trypoxylus [Allomyrina] dichotoma, Dynastinae) showing the folded tubes of epidermis (a) that, once unfolded, will comprise the branched adult horn (b). Four distinct axes of proximal–distal outgrowth are visible in this disc (blue arrows, inset) corresponding to each of the distal branch tips of the final horn. All branches are already formed by the time the animal pupates (a and c), suggesting that the evolution of a branched horn shape in this lineage resulted primarily from genetic modifications to the patterning processes that control cell proliferation (horn growth). However, the grooves between horn branches are more pronounced in the adult than in the pupa (b and c show the same individual), suggesting that some remodeling of horn shape also occurs during the pupal period.