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1. Novel Doublesex Duplication Associated with Sexually Dimorphic Development of Dogface Butterfly Wings

   https://doi.org/10.1093/molbev/msab228  

   Rodriguez-Caro, Fernando; Fenner, Jennifer; Bhardwaj, Shivam; Cole, Jared; Benson, Caleb; Colombara, Alexandra M; Papa, Riccardo; Brown, Matthew W; Martin, Arnaud; Range, Ryan C; et al (July 2021, Molecular Biology and Evolution)

   True, John (Ed.)

   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. 

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2. A learning experience elicits sex‐dependent neurogenomic responses in Bicyclus anynana butterflies

   https://doi.org/10.1111/mec.16920  

   Ernst, David A.; Agcaoili, Gabrielle A.; Merrill, Abbigail N.; Westerman, Erica L. (March 2023, Molecular Ecology)

   Abstract Sexually dimorphic behaviour is pervasive across animals, with males and females exhibiting different mate selection, parental care, foraging, dispersal, and territorial strategies. However, the genetic underpinnings of sexually dimorphic behaviours are poorly understood. Here we investigate gene networks and expression patterns associated with sexually dimorphic imprinting‐like learning in the butterflyBicyclus anynana. In this species, both males and females learn visual preferences, but learn preferences for different traits and use different signals as salient, unconditioned cues. To identify genes and gene networks associated with this behaviour, we examined gene expression profiles of the brains and eyes of male and female butterflies immediately post training and compared them to the same tissues of naïve individuals. We found more differentially expressed genes and a greater number of associated gene networks in the eyes, indicating a role of the peripheral nervous system in visual imprinting‐like learning. Females had higher chemoreceptor expression levels than males, supporting the hypothesized sexual dimorphic use of chemical cues during the learning process. In addition, genes that influenceB. anynanawing patterns (sexual ornaments), such asinvected,spalt, andapterous, were also differentially expressed in the brain and eye, suggesting that these genes may influence both sexual ornaments and the preferences for these ornaments. Our results indicate dynamic and sex‐specific responses to social scenario in both the peripheral and central nervous systems and highlight the potential role of wing patterning genes in mate preference and learning across the Lepidoptera. 

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3. Sex-linked gene traffic underlies the acquisition of sexually dimorphic UV color vision in Heliconius butterflies

   https://doi.org/10.1073/pnas.2301411120  

   Chakraborty, Mahul; Lara, Angelica Guadalupe; Dang, Andrew; McCulloch, Kyle J.; Rainbow, Dylan; Carter, David; Ngo, Luna Thanh; Solares, Edwin; Said, Iskander; Corbett-Detig, Russell B.; et al (August 2023, Proceedings of the National Academy of Sciences)

   The acquisition of novel sexually dimorphic traits poses an evolutionary puzzle: How do new traits arise and become sex-limited? Recently acquired color vision, sexually dimorphic in animals like primates and butterflies, presents a compelling model for understanding how traits become sex-biased. For example, someHeliconiusbutterflies uniquely possess UV (ultraviolet) color vision, which correlates with the expression of two differentially tuned UV-sensitive rhodopsins, UVRh1 and UVRh2. To discover how such traits become sexually dimorphic, we studiedHeliconius charithonia, which exhibits female-specific UVRh1 expression. We demonstrate that females, but not males, discriminate different UV wavelengths. Through whole-genome shotgun sequencing and assembly of theH. charithoniagenome, we discovered thatUVRh1is present on the W chromosome, making it obligately female-specific. By knocking outUVRh1, we show that UVRh1 protein expression is absent in mutant female eye tissue, as in wild-type male eyes. A PCR survey ofUVRh1sex-linkage across the genus shows that species with female-specific UVRh1 expression lackUVRh1gDNA in males. Thus, acquisition of sex linkage is sufficient to achieve female-specific expression ofUVRh1, though this does not preclude other mechanisms, likecis-regulatory evolution from also contributing. Moreover, both this event, and mutations leading to differential UV opsin sensitivity, occurred early in the history ofHeliconius. These results suggest a path for acquiring sexual dimorphism distinct from existing mechanistic models. We propose a model where gene traffic to heterosomes (the W or the Y) genetically partitions a trait by sex before a phenotype shifts (spectral tuning of UV sensitivity). 

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4. Ontogenetic Change in Male Expression of Testosterone-Responsive Genes Contributes to the Emergence of Sex-Biased Gene Expression in Anolis sagrei

   https://doi.org/10.3389/fphys.2022.886973  

   Hale, Matthew D.; Robinson, Christopher D.; Cox, Christian L.; Cox, Robert M. (June 2022, Frontiers in Physiology)

   Sex differences in gene expression tend to increase with age across a variety of species, often coincident with the development of sexual dimorphism and maturational changes in hormone levels. However, because most transcriptome-wide characterizations of sexual divergence are framed as comparisons of sex-biased gene expression across ages, it can be difficult to determine the extent to which age-biased gene expression within each sex contributes to the emergence of sex-biased gene expression. Using RNAseq in the liver of the sexually dimorphic brown anole lizard ( Anolis sagrei ), we found that a pronounced increase in sex-biased gene expression with age was associated with a much greater degree of age-biased gene expression in males than in females. This pattern suggests that developmental changes in males, such as maturational increases in circulating testosterone, contribute disproportionately to the ontogenetic emergence of sex-biased gene expression. To test this hypothesis, we used four different experimental contrasts to independently characterize sets of genes whose expression differed as a function of castration and/or treatment with exogenous testosterone. We found that genes that were significantly male-biased in expression or upregulated as males matured tended to be upregulated by testosterone, whereas genes that were female-biased or downregulated as males matured tended to be downregulated by testosterone. Moreover, the first two principal components describing multivariate gene expression indicated that exogenous testosterone reversed many of the feminizing effects of castration on the liver transcriptome of maturing males. Collectively, our results suggest that developmental changes that occur in males contribute disproportionately to the emergence of sex-biased gene expression in the Anolis liver, and that many of these changes are orchestrated by androgens such as testosterone. 

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5. A Conserved Somatic Sex Determination Cascade Instructs Trait‐Specific Sexual Dimorphism in Horned Dung Beetles

   https://doi.org/10.1111/ede.70004  

   Mitchell, London C; Moczek, Armin P; Nadolski, Erica M (March 2025, Evolution & Development)

   ABSTRACT Sex‐specific trait expression represents a striking dimension of morphological variation within and across species. The mechanisms instructing sex‐specific organ development have been well studied in a small number of insect model systems, suggesting striking conservation in some parts of the somatic sex determination pathway while hinting at possible evolutionary lability in others. However, further resolution of this phenomenon necessitates additional taxon sampling, particularly in groups in which sexual dimorphisms have undergone significant elaboration and diversification. Here, we functionally investigate the somatic sex determination pathway in the gazelle dung beetleDigitonthophagus gazella, an emerging model system in the study of the development and evolution of sexual dimorphisms. We find that RNA interference (RNAi) targetingtransformer (tra)caused chromosomal females to develop morphological traits largely indistinguishable from those normally only observed in males, and thattra^RNAiis sufficient to induce splicing of the normally male‐specific isoform ofdoublesexin chromosomal females, while leaving males unaffected. Further,intersex^RNAiwas found to phenocopy previously described RNAi phenotypes ofdoublesexin female but not male beetles. These findings match predictions derived from models of the sex determination cascade as developed largely through studies inDrosophila melanogaster. In contrast, efforts to targettransformer2via RNAi resulted in high juvenile mortality but did not appear to affectdoublesexsplicing, whereas RNAi targetingSex‐lethaland two putative orthologs ofhermaphroditeyielded no obvious phenotypic modifications in either males or females, raising the possibility that the function of a subset of sex determination genes may be derived in select Diptera and thus nonrepresentative of their roles in other holometabolous orders. Our results help illuminate how the differential evolutionary lability of the somatic sex determination pathway has contributed to the extraordinary morphological diversification of sex‐specific trait expression found in nature. 

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