Insulin signaling and limb-patterning: candidate pathways for the origin and evolutionary diversification of beetle ‘horns’

Abstract

Beetle 'horns' are rigid outgrowths of the insect cuticle used as weapons in contests for access to mates. Relative to their body size, beetle horns can be enormous. They protrude from any of five different regions of the head or thorax; they are curved, straight, branched or bladed; and their development is often coupled with the nutrient environment (male dimorphism) or with sex (sexual dimorphism). Here, we show that this extraordinary diversity of horns can be distilled down to four trajectories of morphological change -horn location, shape, allometry and dimorphism -and we illustrate how the developmental mechanisms regulating horn growth could generate each of these types of horn evolution. Specifically, we review two developmental pathways known to regulate growth of morphological structures in Drosophila and other insects: a limb-patterning pathway that specifies the location and shape of a structure, and the insulin pathway, which modulates trait growth in response to larval nutrition. We summarize preliminary evidence indicating that these pathways are associated with the development of beetle horns, and we show how subtle changes in the relative activities of these two pathways would be sufficient to generate most of the extant diversity of horn forms. Our objective is to intuitively connect genotype with phenotype, and to advocate an informed 'candidate gene' approach to studies of the developmental basis of evolution. We end by using this insight from development to offer a solution to the longstanding mystery of the scarabs: the observation by Darwin, Lameere, Arrow and others that this one family of beetles appeared to have a 'special tendency' towards the evolution of horns.

Evolutionary Endocrinology: The Developing Synthesis between Endocrinology and Evolutionary Genetics

“…Considerable discussion and empirical work is in progress on alterations in the signaling pathways described above in the context of the evolution of body size or size of organs (e.g., beetle horns) within and between species (De Jong & Bochdanovits 2003, Emlen et al 2006, Shingleton et al 2005.…”

Many ways to be small: different environmental regulators of size generate distinct scaling relationships inDrosophila melanogaster

“…Consequently, the last 100 years have seen an ever-increasing accumulation of data concerning the scaling relationship of myriad morphological traits, and upon which insights into the evolution of morphology have been based (Huxley 1924;Gould 1966;Brown et al 2000). More recent efforts have concentrated on the genetic and developmental basis of scaling relationships, to better understand the proximate mechanisms upon which selection has acted to create morphological diversity (Emlen & Allen 2003;Emlen et al 2006;Shingleton et al 2007Shingleton et al , 2008.…”

A developmental staging series for the lizard genus Anolis: A new system for the integration of evolution, development, and ecology

“…This has led to significant advances in our understanding of the molecular bases of morphological evolution. However, as the field of ''evolutionary developmental biology'' has grown as a discipline, few have addressed the inextricable bonds between organismal development, population-based historical processes, and the external environment (with several notable exceptions, e.g., Colosimo et al, 2004;Beldade et al, 2005;Emlen et al, 2006;Hoekstra, 2006). This omission is in a large part based on the historic reliance of developmental biologists on the study of relatively few, evolutionarily distant ''model'' organisms that have been readily amenable to embryological and/or genetic manipulation, particularly within the vertebrate lineage; mainly mice, chickens, frogs, and zebrafish.…”