A simulation study of the genetic regulatory hierarchy for butterfly eyespot focus determination

Abstract

The color patterns on the wings of butterflies have been an important model system in evolutionary developmental biology. Two types of models have been used to study these patterns. The first type of model employs computational techniques and generalized mechanisms of pattern formation to make predictions about how color patterns will vary as parameters of the model are changed. These generalized mechanisms include diffusion gradient, reaction-diffusion, lateral inhibition, and threshold responses. The second type of model uses known genetic interactions from Drosophila melanogaster and patterns of candidate gene expression in one of several butterfly species (most often Junonia (Precis) coenia or Bicyclus anynana) to propose specific genetic regulatory hierarchies that appear to be involved in color pattern formation. This study combines these two approaches using computational techniques to test proposed genetic regulatory hierarchies for the determination of butterfly eyespot foci (also known as border ocelli foci). Two computer programs, STELLA 8.1 and Delphi 2.0, were used to simulate the determination of eyespot foci. Both programs revealed weaknesses in a genetic model previously proposed for eyespot focus determination. On the basis of these simulations, we propose two revised models for eyespot focus determination and identify components of the genetic regulatory hierarchy that are particularly sensitive to changes in model parameter values. These components may play a key role in the evolution of butterfly eyespots. Simulations like these may be useful tools for the study of other evolutionary developmental model systems and reveal similar sensitive components of the relevant genetic regulatory hierarchies.

A simulation study of mutations in the genetic regulatory hierarchy for butterfly eyespot focus determination

“…The experimental basis and general structure of our computer simulation of the developing butterfly wing are described in detail elsewhere (Evans and Marcus, 2006). Briefly, we implemented a set of gene expression threshold equations in a PASCAL application written within the Delphi 2.0 (1996) programming environment in order to place the alternative models for the genetic regulatory hierarchy within a spatial modeling environment.…”

“…This computational approach revealed that a previously proposed hypothesis for the genetic regulatory network underlying eyespot development (Marcus, 2005) was flawed, but revealed two alternative networks that were capable of producing all of the gene expression patterns known from wild-type pre-pupal butterfly eyespots ( Fig. 1; Evans and Marcus, 2006).…”

“…A recent computational model tested genetic regulatory hierarchies hypothesized to underlie the formation of butterfly eyespot foci (Evans and Marcus, 2006). The computational model demonstrated that one proposed hierarchy was incapable of reproducing the known patterns of gene expression associated with eyespot focus determination in wild-type butterflies, but that two slightly modified alternative hierarchies were capable of reproducing all of the known gene expressions patterns.…”

“…Color patterns are suitable for study because they are highly variable, consist of clearly defined subunits, exist in two dimensions, and are structurally simple (Beldade and Brakefield, 2002;Nijhout, 1991), and at least some patterns are clearly associated with fitness benefits associated with natural or sexual selection (Hill and Vaca, 2004;Kingsolver, 1995;Robertson and Monteiro, 2005;Stevens, 2005). Recently, we implemented a model for color pattern development that combined gene expression data from developing wings with computational algorithms that until that point had only been used to model generalized mechanisms of pattern development in butterflies (Evans and Marcus, 2006). This computational approach revealed that a previously proposed hypothesis for the genetic regulatory network underlying eyespot development (Marcus, 2005) was flawed, but revealed two alternative networks that were capable of producing all of the gene expression patterns known from wild-type pre-pupal butterfly eyespots ( Fig.…”

“…We expanded the computational model first presented in Evans and Marcus (2006) to incorporate the changes associated with these mutant phenotypes. This computational approach to modeling pattern formation in these mutants allows us to make predictions about patterns of gene expression, which with few exceptions (Brakefield, et al, 1996;Weatherbee, et al, 1999) are largely unstudied in butterfly mutants.…”