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Abstract Sexually dimorphic development is responsible for some of the most remarkable phenotypic variation found in nature. Alternative splicing of the transcription factor gene doublesex (dsx) is a highly conserved developmental switch controlling the expression of sex-specific pathways. Here, we leverage sex-specific differences in butterfly wing color pattern to characterize the genetic basis of sexually dimorphic development. We use RNA-seq, immunolocalization, and motif binding site analysis to test specific predictions about the role of dsx in the development of structurally based ultraviolet (UV) wing patterns in Zerene cesonia (Southern Dogface). Unexpectedly, we discover a novel duplication of dsx that shows a sex-specific burst of expression associated with the sexually dimorphic UV coloration. The derived copy consists of a single exon that encodes a DNA binding but no protein-binding domain and has experienced rapid amino-acid divergence. We propose the novel dsx paralog may suppress UV scale differentiation in females, which is supported by an excess of Dsx-binding sites at cytoskeletal and chitin-related genes with sex-biased expression. These findings illustrate the molecular flexibility of the dsx gene in mediating the differentiation of secondary sexual characteristics. 

Abstract Comparisons of high-quality, reference butterfly, and moth genomes have been instrumental to advancing our understanding of how hybridization, and natural selection drive genomic change during the origin of new species and novel traits. Here, we present a genome assembly of the Southern Dogface butterfly, Zerene cesonia (Pieridae) whose brilliant wing colorations have been implicated in developmental plasticity, hybridization, sexual selection, and speciation. We assembled 266,407,278 bp of the Z. cesonia genome, which accounts for 98.3% of the estimated 271 Mb genome size. Using a hybrid approach involving Chicago libraries with Hi-Rise assembly and a diploid Meraculous assembly, the final haploid genome was assembled. In the final assembly, nearly all autosomes and the Z chromosome were assembled into single scaffolds. The largest 29 scaffolds accounted for 91.4% of the genome assembly, with the remaining ∼8% distributed among another 247 scaffolds and overall N50 of 9.2 Mb. Tissue-specific RNA-seq informed annotations identified 16,442 protein-coding genes, which included 93.2% of the arthropod Benchmarking Universal Single-Copy Orthologs (BUSCO). The Z. cesonia genome assembly had ∼9% identified as repetitive elements, with a transposable element landscape rich in helitrons. Similar to other Lepidoptera genomes, Z. cesonia showed a high conservation of chromosomal synteny. The Z. cesonia assembly provides a high-quality reference for studies of chromosomal arrangements in the Pierid family, as well as for population, phylo, and functional genomic studies of adaptation and speciation. 

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.