A single origin for nymphalid butterfly eyespots followed by widespread loss of associated gene expression

PLoS Genet. 2012;8(8):e1002893. doi: 10.1371/journal.pgen.1002893. Epub 2012 Aug 16.

Abstract

Understanding how novel complex traits originate involves investigating the time of origin of the trait, as well as the origin of its underlying gene regulatory network in a broad comparative phylogenetic framework. The eyespot of nymphalid butterflies has served as an example of a novel complex trait, as multiple genes are expressed during eyespot development. Yet the origins of eyespots remain unknown. Using a dataset of more than 400 images of butterflies with a known phylogeny and gene expression data for five eyespot-associated genes from over twenty species, we tested origin hypotheses for both eyespots and eyespot-associated genes. We show that eyespots evolved once within the family Nymphalidae, approximately 90 million years ago, concurrent with expression of at least three genes associated with early eyespot development. We also show multiple losses of expression of most genes from this early three-gene cluster, without corresponding losses of eyespots. We propose that complex traits, such as eyespots, may have originated via co-option of a large pre-existing complex gene regulatory network that was subsequently streamlined of genes not required to fulfill its novel developmental function.

Publication types

  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Animals
  • Biological Evolution
  • Butterflies / genetics*
  • Female
  • Gene Expression*
  • Gene Regulatory Networks
  • Genetic Association Studies
  • Genotype
  • Male
  • Multigene Family
  • Phenotype
  • Phylogeny
  • Pigmentation / genetics*
  • Wings, Animal / anatomy & histology
  • Wings, Animal / metabolism*

Grants and funding

This work was supported by a grant to AM from NSF (IOS 0818731). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.