Project description:Color pattern mimicry in Heliconius butterflies is a classic case study of complex trait adaptation via selection on a few large effect genes. Association studies have linked color pattern variation to a handful of noncoding regions, yet the presumptive cis-regulatory elements (CREs) that control color patterning remain unknown. Here we combine chromatin assays, DNA sequence associations, and genome editing to functionally characterize 5 cis-regulatory elements of the color pattern gene optix We were surprised to find that the cis-regulatory architecture of optix is characterized by pleiotropy and regulatory fragility, where deletion of individual cis-regulatory elements has broad effects on both color pattern and wing vein development. Remarkably, we found orthologous cis-regulatory elements associate with wing pattern convergence of distantly related comimics, suggesting that parallel coevolution of ancestral elements facilitated pattern mimicry. Our results support a model of color pattern evolution in Heliconius where changes to ancient, multifunctional cis-regulatory elements underlie adaptive radiation.
Project description:Aposematic color pattern mimicry in Heliconius butterflies provides a well-known example of adaptation via selection on a few genes of large effect. To understand how selection at individual genes can drive the evolution of complex traits, we functionally characterized five novel enhancers of the color pattern gene, optix. In Heliconius erato we found that wing pattern enhancers are largely ancestral, pleiotropic, functionally interdependent, and introgressed between populations. Remarkably, many of these enhancers are also associated with regional pattern variation in the distantly related co-mimics Heliconius melpomene and Heliconius timareta. Our findings provide a case study of how parallel co-evolution of ancient, multifunctional regulatory elements can facilitate the rapid diversification of complex phenotypes, and provide a counterpoint to many widespread assumptions of cis-regulatory evolution.
Project description:Aposematic color pattern mimicry in Heliconius butterflies provides a well-known example of adaptation via selection on a few genes of large effect. To understand how selection at individual genes can drive the evolution of complex traits, we functionally characterized five novel enhancers of the color pattern gene, optix. In Heliconius erato we found that wing pattern enhancers are largely ancestral, pleiotropic, functionally interdependent, and introgressed between populations. Remarkably, many of these enhancers are also associated with regional pattern variation in the distantly related co-mimics Heliconius melpomene and Heliconius timareta. Our findings provide a case study of how parallel co-evolution of ancient, multifunctional regulatory elements can facilitate the rapid diversification of complex phenotypes, and provide a counterpoint to many widespread assumptions of cis-regulatory evolution.
Project description:Aposematic color pattern mimicry in Heliconius butterflies provides a well-known example of adaptation via selection on a few genes of large effect. To understand how selection at individual genes can drive the evolution of complex traits, we functionally characterized five novel enhancers of the color pattern gene, optix. In Heliconius erato we found that wing pattern enhancers are largely ancestral, pleiotropic, functionally interdependent, and introgressed between populations. Remarkably, many of these enhancers are also associated with regional pattern variation in the distantly related co-mimics Heliconius melpomene and Heliconius timareta. Our findings provide a case study of how parallel co-evolution of ancient, multifunctional regulatory elements can facilitate the rapid diversification of complex phenotypes, and provide a counterpoint to many widespread assumptions of cis-regulatory evolution.
Project description:Visual patterns in animals may serve different functions, such as attracting mates and deceiving predators. If a signal is used for multiple functions, the opportunity arises for conflict among the different functions, preventing optimization for any one visual signal. Here we investigate the hypothesis that spatial separation of different visual signal functions has occurred in Bicyclus butterflies. Using phylogenetic reconstructions of character evolution and comparisons of evolutionary rates, we found dorsal surface characters to evolve at higher rates than ventral characters. Dorsal characters also displayed sex-based differences in evolutionary rates more often than did ventral characters. Thus, dorsal characters corresponded to our predictions of mate signalling while ventral characters appear to play an important role in predator avoidance. Forewing characters also fit a model of mate signalling, and displayed higher rates of evolution than hindwing characters. Our results, as well as the behavioural and developmental data from previous studies of Bicyclus species, support the hypothesis that spatial separation of visual signal functions has occurred in Bicyclus butterflies. This study is the first to demonstrate, in a phylogenetic framework, that spatial separation of signals used for mate signalling and those used for predator avoidance is a viable strategy to accommodate multiple signal functions. This signalling strategy has important ramifications on the developmental evolution of wing pattern elements and diversification of butterfly species.
Project description:Neotropical Heliconius butterflies display a diversity of warningly colored wing patterns, which serve roles in both Müllerian mimicry and mate choice behavior. Wing pattern diversity in Heliconius is controlled by a small number of unlinked, Mendelian "switch" loci [1]. One of these, termed the K locus, switches between yellow and white color patterns, important mimicry signals as well as mating cues [2-4]. Furthermore, mate preference behavior is tightly linked to this locus [4]. K controls the distribution of white versus yellow scales on the wing, with a dominant white allele and a recessive yellow allele. Here, we combine fine-scale genetic mapping, genome-wide association studies, gene expression analyses, population and comparative genomics, and genome editing with CRISPR/Cas9 to characterize the molecular basis of the K locus in Heliconius and to infer its evolutionary history. We show that white versus yellow color variation in Heliconius cydno is due to alternate haplotypes at a putative cis-regulatory element (CRE) downstream of a tandem duplication of the homeodomain transcription factor aristaless. Aristaless1 (al1) and aristaless2 (al2) are differentially regulated between white and yellow wings throughout development with elevated expression of al1 in developing white wings, suggesting a role in repressing pigmentation. Consistent with this, knockout of al1 causes white wings to become yellow. The evolution of wing color in this group has been marked by retention of the ancestral yellow color in many lineages, a single origin of white coloration in H. cydno, and subsequent introgression of white color from H. cydno into H. melpomene.