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The evolution of sexual secondary characteristics necessitates regulatory factors that confer sexual identity to differentiating tissues and cells. InColias eurythemebutterflies, males exhibit two specialized wing scale types—ultraviolet-iridescent (UVI) and spatulate scales—which are absent in females and likely integral to male courtship behavior. This study investigates the regulatory mechanisms and single-nucleus transcriptomics underlying these two sexually dimorphic cell types during wing development. We show thatDoublesex(Dsx) expression is itself dimorphic and required to repress the UVI cell state in females, while unexpectedly, UVI activation in males is independent fromDsx. In the melanic marginal band,Dsxis required in each sex to enforce the presence of spatulate scales in males, and their absence in females. Single-nucleus RNAseq reveals that UVI and spatulate scale cell precursors each show distinctive gene expression profiles at 40% of pupal development, with marker genes that include regulators of transcription, cell signaling, cytoskeletal patterning, and chitin secretion. Both male-specific cell types share a low expression of theBric-a-brac(Bab) transcription factor, a key repressor of the UVI fate. Bab ChIP-seq profiling suggests that Bab binds thecis-regulatory regions of gene markers associated to UVI fate, including potential effector genes involved in the regulation of cytoskeletal processes and chitin secretion, and loci showing signatures of recent selective sweeps in a UVI-polymorphic population. These findings open new avenues for exploring wing patterning and scale development, shedding light on the mechanisms driving the specification of sex-specific cell states and the differentiation of specialized cell ultrastructures. 

Supergenes can evolve when recombination-suppressing mechanisms like inversions promote co-inheritance of alleles at two or more polymorphic loci that affect a complex trait. Theory shows that such genetic architectures can be favoured under balancing selection or local adaptation in the face of gene flow, but they can also bring costs associated with reduced opportunities for recombination. These costs may in turn be offset by rare ‘gene flux’ between inverted and ancestral haplotypes, with a range of possible outcomes. We aimed to shed light on these processes by investigating the ‘BC supergene’, a large genomic region comprising multiple rearrangements associated with three distinct wing colour morphs inDanaus chrysippus, a butterfly known as the African monarch, African queen and plain tiger. Using whole-genome resequencing data from 174 individuals, we first confirm the effects of BC on wing colour pattern: background melanism is associated with SNPs in the promoter region ofyellow, within an inverted subregion of the supergene, while forewing tip pattern is most likely associated with copy-number variation in a separate subregion of the supergene. We then show that haplotype diversity within the supergene is surprisingly extensive: there are at least six divergent haplotype groups that experience suppressed recombination with respect to each other. Despite high divergence between these haplotype groups, we identify an unexpectedly large number of natural recombinant haplotypes. Several of the inferred crossovers occurred between adjacent inversion ‘modules’, while others occurred within inversions. Furthermore, we show that new haplotype groups have arisen through recombination between two pre-existing ones. Specifically, an allele for dark colouration in the promoter ofyellowhas recombined into distinct haplotype backgrounds on at least two separate occasions. Overall, our findings paint a picture of dynamic evolution of supergene haplotypes, fuelled by incomplete recombination suppression. 

The hexagonal cells built by honey bees and social wasps are an example of adaptive architecture; hexagons minimize material use, while maximizing storage space and structural stability. Hexagon building evolved independently in the bees and wasps, but in some species of both groups, the hexagonal cells are size dimorphic—small worker cells and large reproductive cells—which forces the builders to join differently sized hexagons together. This inherent tiling problem creates a unique opportunity to investigate how similar architectural challenges are solved across independent evolutionary origins. We investigated how 5 honey bee and 5 wasp species solved this problem by extracting per-cell metrics from 22,745 cells. Here, we show that all species used the same building techniques: intermediate-sized cells and pairs of non-hexagonal cells, which increase in frequency with increasing size dimorphism. We then derive a simple geometric model that explains and predicts the observed pairing of non-hexagonal cells and their rate of occurrence. Our results show that despite different building materials, comb configurations, and 179 million years of independent evolution, honey bees and social wasps have converged on the same solutions for the same architectural problems, thereby revealing fundamental building properties and evolutionary convergence in construction behavior. 

Evolutionary innovations underlie the rise of diversity and complexity—the 2 long-term trends in the history of life. How does natural selection redesign multiple interacting parts to achieve a new emergent function? We investigated the evolution of a biomechanical innovation, the latch-spring mechanism of trap-jaw ants, to address 2 outstanding evolutionary problems: how form and function change in a system during the evolution of new complex traits, and whether such innovations and the diversity they beget are repeatable in time and space. Using a new phylogenetic reconstruction of 470 species, and X-ray microtomography and high-speed videography of representative taxa, we found the trap-jaw mechanism evolved independently 7 to 10 times in a single ant genus ( Strumigenys ), resulting in the repeated evolution of diverse forms on different continents. The trap mechanism facilitates a 6 to 7 order of magnitude greater mandible acceleration relative to simpler ancestors, currently the fastest recorded acceleration of a resettable animal movement. We found that most morphological diversification occurred after evolution of latch-spring mechanisms, which evolved via minor realignments of mouthpart structures. This finding, whereby incremental changes in form lead to a change of function, followed by large morphological reorganization around the new function, provides a model for understanding the evolution of complex biomechanical traits, as well as insights into why such innovations often happen repeatedly.