Integrative Developmental Biology of insects

Mechanisms of phenotypic plasticity in beetle horns.

Horn expression is phenotypically ‘plastic’.  Horn length scales positively with overall body size, but body size is overwhelmingly influenced by the larval nutritional environment (Emlen 1994[PDF], 1997[PDF]).  Animals exposed to favorable nutrition grow large, and produce long horns, while genetically similar (e.g. sibling) animals encountering poor nutrition remain small, and these animals produce only very short horns [Figure].   

As a post-doc, and in collaboration with H. Frederik Nijhout (Duke University), I began to explore the development of horns (much of this work has since been extended by Armin Moczek [now at Indiana University], so see also his page).  We identified where and when developing horns grow, when this horn growth is sensitive to external (e.g. nutrition) and / or internal (overall growth, body size) conditions experienced by larvae, and how this interface between circumstance and patterns of growth is regulated (Emlen & Nijhout 1999[PDF]; Emlen & Nijhout 2001[PDF]; Moczek & Nijhout 2002; Emlen et al. 2005a[PDF] [Figure]).  Specifically, we have identified a sensitive ‘window’ of time near the end of the larval feeding period (Period I [Figure]) when animals appear to assess their body size relative to a genetically-mediated threshold size, and at least two of the hormones putatively involved in this size-assessment process (Juvenile Hormone and Ecdysone).  Animals larger than the threshold size produce horns; animals smaller than this size appear to be ‘reprogrammed’ by a morph-specific pulse of ecdysteroid [Figure], and dispense with horn production.

The horns themselves actually commence growth after the larvae have ceased feeding (Period II [Figure]), and these nascent structures have largely completed their growth by the time the larva molts into the pupa.  It is during this latter period (called the ‘gut purge’ and ‘prepupa’ period) that we think size-dependent scaling of all of the adult structures occurs. 

That large individuals produce larger eyes, wings, legs (and horns) than smaller individuals has been obvious to scientists for more than a century.  However, the developmental mechanisms generating this positive scaling among body parts have received relatively little attention (Stern & Emlen 1999[PDF]; Emlen & Nijhout 2000[PDF]; Emlen & Allen 2004[PDF]).  For Onthophagus taurus we now understand when this process occurs, and we have evidence that size information is communicated to imaginal cells at least in part by Juvenile Hormone (Emlen & Nijhout 2001; Emlen & Allen 2004).

We are currently investigating the relationship between nutrition, hormones, and gene expression in the control of cell proliferation in developing horns, and exploring a second possible mechanism of scaling/ allometry: insulin signaling.  We have predicted that nutrition-dependent phenotypic plasticity in trait size (including horn size, but also sizes of legs, eyes, wings, etc.) will involve the insulin-signaling pathway (Emlen & Allen 2004; Emlen et al. 2006[PDF]), as levels of both insulin and insulin-dependent growth factors are exquisitely sensitive to larval nutrition, and insulin-signaling regulates cell proliferation and organ growth.   We are now targeting most of our efforts on elements of this signaling pathway, and exploring whether and how nutrition and larval body size influence levels of expression of genes in this network in developing body parts, including horns. [Figure]

Links to relevant insect endocrinology/ physiology labs:

H. Frederik Nijhout  (Duke University)
http://www.biology.duke.edu/nijhout/

Wendy Smith (Northeastern University)
http://www.biology.neu.edu/faculty03/smith03.html

James Truman (University of Washington)
http://protist.biology.washington.edu/bio2/people/bio.html?parecID=378

Lynn Riddiford (University of Washington)
http://faculty.washington.edu/lmr/

Anthony Zera (University of Nebraska)
http://www.biosci.unl.edu/labs/zera/index.html

 
Illustration: Utako Kikutani        

Link to NSF Workshop Report on  “Integrative Developmental Biology”:

http://www.nsf.gov/publications/pub_summ.jsp?ods_key=nsf06034