Sexual Selection and the evolution of exaggerated morphologies in insects

The history of life has been accentuated by several spectacular evolutionary radiations, and character divergence within these radiations frequently involves the exaggerated structures of sexual selection.  The Hawaiian radiation of drosophilid flies, for example, has resulted in over 900 extant species that differ most conspicuously in the wing patterns and courtship displays of males.  Similarly, radiations of birds-of-paradise, pheasants, and African Great Lake cichlids all involve the ornaments and displays of males.  In general, the extreme structures of sexual selection display an evolutionary lability far surpassing that of other, non sexually-selected traits.

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. [Evolution of Animal Weapons Ann. Rev. Ecol. Syst. Evol. 2008]

In my laboratory, we address this discrepancy in many ways.  Students in this lab have begun to study the function and evolution of enlarged and spiny hindlegs in coreid bugs (Christine Miller), elongated elytral and pronotal claspers in tortoise beetles (Alex Trillo), and the enlarged horns of Japanese Horned Beetles (Ashley King), and we continue to explore the function of horns in a variety of species of scarabs.

Most of my efforts to date have focused on the evolutionary radiation of beetle horns.  In collaboration with Clifford Cunningham (Duke University), we have used partial sequences from seven genes to develop a phylogenetic hypothesis for a worldwide sample of 48 species from the dung beetle genus Onthophagus (Coleoptera: Scarabaeidae) (Emlen et al., 2005b [PDF]). [Figure][Figure][Figure]  We use these data to test for multiple evolutionary origins of horns, and to characterize the evolutionary radiation of horns.  Our phylogeny reveals prolific evolutionary lability of these exaggerated sexually selected weapons (over 25 separate gains and losses of five different horn types).  We consider these results in the context of the natural history of these beetles, and suggest ways that sexual selection and ecology may have interacted to generate this extraordinary diversity of weapon morphology.

Although this phylogeny has proven useful for reconstructing how horns have changed over time, and how the mechanisms regulating and modulating horn development have changed (e.g. Emlen et al. 2005a[PDF]), it has been less useful for examining the origins of beetle horns.  For this we needed to delve deeper into the history of the scarabs.  Using a recent phylogeny for the dung beetles [Philips, Pretorius & Scholtz 2004 “A phylogenetic analysis of dung beetles (Scarabaeinae: Scarabaeidae): unrolling an evolutionary history” Invertebrate Systematics 18: 53-88], Keith Philips (Western Kentucky University) and I tested the hypothesis that investment into the production of horns might have been most cost-effective when animals battled over restricted, and therefore economically-defendable substrates.  In the case of the dung beetles, we predicted that horns would be more likely to arise in lineages that fight over tunnels beneath dung (“tunnelers”) than in lineages that fought their battles above-ground (e.g. the “ball rollers”) – a prediction strongly supported by available data (Emlen & Philips 2006 [PDF]) (Figure).

Most recently, we have used phylogenies for the entire scarab superfamily (Browne & Scholtz 1998, 1999; Krell 2000; Smith et al. in press; see links below) to begin to reconstruct the earliest origins of horns [Figure].  In particular, insights from our studies of horn development have led us to propose that even the earliest of the scarabs may have had horns (Emlen et al. 2006[PDF]).  These Jurassic beetles almost certainly battled over burrows, either in hollowed-out plant stems or in the ground, and these ecological conditions may well have favored the evolution of enlarged cuticular weapons.  If true, this would mean that the tens of thousands of presently hornless species of scarab were secondarily hornless, and we are now using our comparative studies of horn development to test this startling hypothesis more directly.

Links to Scarab researchers and resources:
Scarab Workers World Directory
http://www-museum.unl.edu/research/entomology/workers/index2.htm
Clarke Scholtz (University of Pretoria)
http://www.up.ac.za/academic/zoology/New/chscholtz/index.html

Adrian Davis (University of Pretoria)
http://www.geocities.com/scarabgroup/Files/toPeople/AdrianDavis.html

Brett Ratcliffe (University of Nebraska)
http://www-museum.unl.edu/research/entomology/brettcra.htm

Mary Liz Jameson (University of Nebraska)
http://www-museum.unl.edu/research/entomology/workers/MJameson.htm

Andrew Smith (Canadian Museum of Nature)
http://www-museum.unl.edu/research/entomology/andrewsm.htm

Bruce Gill (Canadian Food Inspection Agency)
http://www.unl.edu/museum/research/entomology/workers/BGill.htm

Rob Knell (University of London)
http://alpha.qmul.ac.uk/~ugbt794/

T. Keith Philips (Western Kentucky University)
http://bioweb.wku.edu/faculty/Philips/

Leigh W. Simmons (University of Western Australia)
http://www.ceb.uwa.edu.au/

John Hunt (University of Exeter)
http://www.anu.edu.au/BoZo/hunt/

Joe Tomkins (University of Western Australia)

Janne Kotiaho  (University of Jyväskylä)
http://www.cc.jyu.fi/~jkotiaho/

Frank-Thorsten Krell (Natural History Museum, London)
http://www.nhm.ac.uk/research-curation/staff-directory/entomology/cv-3566.html

Yoshihito Hongo (Kyoto University)
http://ethol.zool.kyoto-u.ac.jp/Hongo/hongo.htm

Allen Moore (University of Exeter)
http://www.uec.ac.uk/biology/research/staff-research-interests/allen-moore.shtml

Tom Tregenza (University of Exeter)
http://www.uec.ac.uk/biology/research/staff-research-interests/tom-tregenza.shtml

Nina Wedell (University of Exeter)
http://www.uec.ac.uk/biology/research/staff-research-interests/nina-wedell.shtml