Mystery of the scarabs resolved? Starting to put the pieces together….

The fantastic shapes of beetles with horns have awed biologists for centuries (Drury 1770; Fischer 1823; Burmeister 1847; Bates 1863; Darwin 1871; Paulian 1935; Beebe 1944; Arrow 1951).  Thousands of scarab species bear horns (Arrow 1951; Enrodi 1985).  The extreme sizes of these structures (Figure), and their concentration within one taxonomic family of beetles, has led naturalists since Darwin to reflect on the special nature of the Scarabs, noting both that sexual selection appears to have acted especially effectively in these beetles (Darwin, 1871, p. 377), and that they appeared to have a ‘special tendency’ to the acquisition of horns (Arrow, 1951, p. 94).  What was it about the scarabs that predisposed so many lineages towards the evolution of these exaggerated weapons?   Recent advances in our understanding of how insects develop, and in particular, of how beetle horns develop, are providing fresh new tools for addressing this and other long-standing questions of animal diversity and morphological evolution.

No scarab systematist that we are aware of has reconstructed the ancestor of the scarabs as a beetle with horns; there simply are too many hornless species, and the major clades with horns are too widely dispersed within this multitude of hornless taxa (Figure).  This clear pattern led Arrow to conclude in his treatise ‘The Horned Beetles’ (1951) that “it is certain that these horns have had no common origin” (p. 94).  Recently, our studies of horn development have caused us to revisit this longstanding ‘mystery of the scarabs,’ and this developmental perspective has led us to a very different conclusion. 

Most scarab horns are dimorphic (review: Emlen & Nijhout 2000 [PDF]).  Dimorphic mechanisms enable the complete suppression of horn growth in subsets of individuals (e.g. small males, females), and breakdowns in these mechanisms can lead to sudden reappearances of horns either in the lab (e.g. experiments perturbing hormone levels during the period of horn growth; Emlen & Nijhout 1999[PDF]; Moczek & Nijhout 2002) or in nature (e.g. ‘gynandromorph’ females with full expression of ‘male’ horns; Lachaume 1983; Dechambre 1987; Ratcliffe 1989).

Because these developmental ‘switch’ or threshold mechanisms can lead to sudden reversals in the expression (or suppression) of complex morphological traits, they are predicted to facilitate rapid and repeated evolution of these structures (West-Eberhard 2003).  Within the beetle genus Onthophagus, threshold mechanisms of dimorphism appear to have contributed to a mosaic pattern of horn evolution (multiple gains and losses of horns; Emlen et al. 2005a[PDF]), and we have begun to suspect that these same mechanisms might explain patterns of horn evolution within the scarabs as a whole.  All of the principle clades of horned scarabs contain species with pronounced male- and sexual dimorphism, suggesting that the origin of these regulatory processes may predate the divergence of these lineages – i.e. both horns and horn dimorphism may have been present in the common ancestor to all of the scarabs.  If true, this would mean that the developmental capacity to suppress horn growth may be a shared feature of all scarabs; it would also mean that the tens of thousands of extant hornless scarab species were secondarily hornless.

Several observations – all reflecting a developmental perspective – suggest that this may in fact be the case.  First, most of the “hornless” families and subfamilies of scarabs contain at least a few species with either rudimentary horns (e.g. Plecomidae, Passalidae, Ochodaidae, Orphninae), or with fully-developed horns (e.g. Melolonthinae, Cetoniinae, Rutelinae).  The locations, shapes and patterns of expression (dimorphism) of these horns are often similar to the horns of other scarabs.  Second, the pupal stages of many scarabs have thoracic ‘horns’, and these are often present in individuals (e.g. females) or species that lack this horn as adults.  Pupal ‘horns’ may serve a current function as support structures protecting animals during the vulnerable metamorphic molt (Main 1922; Halffter & Matthews 1966; Edmonds & Hallfter 1978), but they may also represent developmental carry-overs from a horn that was present in the adult stages of an ancestor (Ballerio 1999; A. Moczek & T. Cruickshank, personal communication).  Third, even within completely hornless species – in one case a species within a completely hornless subfamily, the Ceratocanthidae, which have been a distinct clade for at least 65 million years -- mutant adult individuals occasionally appear with fully developed horns, and these horns also resemble the horns of other scarabs (Figure; Ziani 1995; Ballerio 1999; A. Ballerio, personal communication [http://www.unl.edu/museum/research/entomology/workers/ABallerio.htm]).  We interpret all of these as evidence for the existence of a mechanism for horn development in these scarab families – a mechanism that is apparently suppressed in most individuals of most of species.  Consideration of this developmental potential for horn growth leads to a very different reconstruction for the ancestor state of the earliest scarabs, and we now suspect that these Jurassic beetles may have had both horns, and horn dimorphism. 

What was the ‘special tendency’ of the scarabs that predisposed so many lineages towards the evolution of horns?  We suggest that it was a shared and inherited developmental capacity both for the production of horns, and for the facultative suppression of horn growth.  The first scarabs are thought to have excavated burrows either into the stems of cycads (Lameere 1904) or into the soil (Scholtz & Chown 1995).  Contests over restricted (defendable) substrates are an almost universal feature of extant horned beetle species (e.g. Eberhard 1978; Eberhard 1987; Rasmussen 1994; Emlen 2000[PDF]; Iguchi 2001; Hongo 2003), and the first scarab horns may have aided animals in battles within the confines of these early burrows.  We further suggest that the mechanisms of dimorphism facilitated rapid gains, losses, and re-gains of horns in the history of these beetles, and contributed to the patterns observed by Darwin, Lameere, Arrow and others: multiple, disparate lineages of scarabs that appear to have independently evolved horns.

There are several ways to begin to test this hypothesis.  For example, we predict that mutant individuals with horns (teratologies) will be found in additional lineages of hornless scarabs, and that fossils of early scarabs will be found with horns.  But the most compelling tests are likely to come from studies of horn development.  Comparative studies of development have helped resolve several long-standing controversies involving the deep past (e.g. the origin of insect wings [Shubin et al. 1997] and wing polyphenism [Abouheif & Wray 2002]), in part because they bring an entirely new and informative suite of characters to these analyses.  In this case, we will compare the endocrine mechanisms generating dimorphism, and the ‘downstream’ pathways involved with horn growth (limb patterning, insulin), in three widely divergent clades of scarabs representing what are traditionally considered to be three independent evolutionary origins of horns (scarabaeinae, dynastinae, lucanidae), to search for signatures of a shared past embedded within the details of their respective developmental mechanisms. 

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