Abstract
BackgroundHeliconius butterfly wing pattern diversity offers a unique opportunity to investigate how natural genetic variation can drive the evolution of complex adaptive phenotypes. Positional cloning and candidate gene studies have identified a handful of regulatory and pigmentation genes implicated in Heliconius wing pattern variation, but little is known about the greater developmental networks within which these genes interact to pattern a wing. Here we took a large-scale transcriptomic approach to identify the network of genes involved in Heliconius wing pattern development and variation. This included applying over 140 transcriptome microarrays to assay gene expression in dissected wing pattern elements across a range of developmental stages and wing pattern morphs of Heliconius erato.ResultsWe identified a number of putative early prepattern genes with color-pattern related expression domains. We also identified 51 genes differentially expressed in association with natural color pattern variation. Of these, the previously identified color pattern “switch gene” optix was recovered as the first transcript to show color-specific differential expression. Most differentially expressed genes were transcribed late in pupal development and have roles in cuticle formation or pigment synthesis. These include previously undescribed transporter genes associated with ommochrome pigmentation. Furthermore, we observed upregulation of melanin-repressing genes such as ebony and Dat1 in non-melanic patterns.ConclusionsThis study identifies many new genes implicated in butterfly wing pattern development and provides a glimpse into the number and types of genes affected by variation in genes that drive color pattern evolution.
Highlights
Heliconius butterfly wing pattern diversity offers a unique opportunity to investigate how natural genetic variation can drive the evolution of complex adaptive phenotypes
Ommochrome- and melanin-stage arrays were more intermixed in their expression similarities, with the hybrid forewing melanin phenotype clustering more closely with the hybrid ommochrome phenotype rather than with the rest of the melanin samples
Additional studies focusing on ommochrome and melanin candidate genes [57,58,59,60,61] increased the total of number of wing-pattern related genes to around 20 and provided some insight into the identity of potential downstream genes involved in pattern realization
Summary
Heliconius butterfly wing pattern diversity offers a unique opportunity to investigate how natural genetic variation can drive the evolution of complex adaptive phenotypes. We initiate investigation into the gene networks underlying the development and variation of adaptive wing patterns in Heliconius butterflies This genus has long been a popular system for studying the genetics underlying phenotypic diversification [13,14,15]. The species Heliconius erato and Heliconius melpomene are remarkable in their intraspecific color pattern variation, as they converge on over 20 mimetic wing patterns in various regions of the neotropics [16,17,18]. These phenotype-rich and highly convergent species provide an opportunity to study how complex variation in developmental patterning networks can arise within species and diversify under natural selection
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