Wingless and aristaless2 define a developmental ground plan for moth and butterfly wing pattern evolution

Abstract

Butterfly wing patterns have long been a favorite system for studying the evolutionary radiation of complex morphologies. One of the key characteristics of the system is that wing patterns are based on a highly conserved ground plan of pattern homologies. In fact, the evolution of lepidopteran wing patterns is proposed to have occurred through the repeated gain, loss, and modification of only a handful of serially repeated elements. In this study, we examine the evolution and development of stripe wing pattern elements. We show that expression of the developmental morphogen wingless (wg) is associated with early determination of the major basal (B), discal (DI and DII), and marginal (EI) stripe patterns in a broad sampling of Lepidoptera, suggesting homology of these pattern elements across moths and butterflies. We describe for the first time a novel Lepidoptera-specific homeobox gene, aristaless2 (al2), which precedes wg expression during the early determination of DII stripe patterns. We show that al2 was derived from a tandem duplication of the aristaless gene, whereupon it underwent a rapid coding and cis-regulatory divergence relative to its more conserved paralog aristaless1 (al1), which retained an ancestral expression pattern. The al2 stripe expression domain evolutionarily preceded the appearance of the DII pattern elements in multiple lineages, leading us to speculate that al2 represented preexisting positional information that may have facilitated DII evolution via a developmental drive mechanism. In contrast to butterfly eyespot patterns, which are often cited as a key example of developmental co-option of preexisting developmental genes, this study provides an example where the origin of a major color pattern element is associated with the evolution of a novel lepidopteran homeobox gene. © 2010 The Author. Published by Oxford University Press on behalf of the Society for Molecular Biology and Evolution. All rights reserved.