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1. Frequencies of house fly proto-Y chromosomes across populations are predicted by temperature heterogeneity within populations

   https://doi.org/10.1093/jhered/esae056  

   Foy, Patrick D; Loetzerich, Sara R; Boxler, David; Burgess, Edwin R; Trout_Fryxell, R T; Gerry, Alec C; Hinkle, Nancy C; Machtinger, Erika T; Olds, Cassandra; Tarone, Aaron M; et al (October 2024, Journal of Heredity)

   Wilson, Melissa (Ed.)

   Sex chromosomes often differ between closely related species and can even be polymorphic within populations. Species with multifactorial sex determination segregate for multiple different sex-determining loci within populations, making them uniquely informative of the selection pressures that drive the evolution of sex chromosomes. The house fly (Musca domestica) is a model species for studying multifactorial sex determination because male-determining genes have been identified on all six of the chromosomes, which means that any chromosome can be a “proto-Y.” Natural populations of house flies also segregate for a recently derived female-determining locus, meaning house flies also have a proto-W chromosome. The different proto-Y chromosomes are distributed along latitudinal clines on multiple continents, their distributions can be explained by seasonality in temperature, and they have temperature-dependent effects on physiological and behavioral traits. It is not clear, however, how the clinal distributions interact with the effect of seasonality on the frequencies of house fly proto-Y and proto-W chromosomes across populations. To address this question, we measured the frequencies of house fly proto-Y and proto-W chromosomes across nine populations in the United States of America. We confirmed the clinal distribution along the eastern coast of North America, but it is limited to the eastern coast. In contrast, the annual mean daily temperature range predicts proto-Y chromosome frequencies across the entire continent. Our results therefore suggest that temperature heterogeneity can explain the distributions of house fly proto-Y chromosomes in a way that does not depend on the cline. 

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2. Polygenic response of sex chromosomes to sexual antagonism

   https://doi.org/10.1093/evolut/qpad231  

   Muralidhar, Pavitra; Coop, Graham (December 2023, Evolution)

   Charlesworth, Deborah; Connallon, Tim (Ed.)

   Abstract Sexual antagonism occurs when males and females differ in their phenotypic fitness optima but are constrained in their evolution to these optima because of their shared genome. The sex chromosomes, which have distinct evolutionary “interests” relative to the autosomes, are theorized to play an important role in sexually antagonistic conflict. However, the evolutionary responses of sex chromosomes and autosomes have usually been considered independently, that is, via contrasting the response of a gene located on either an X chromosome or an autosome. Here, we study the coevolutionary response of the X chromosome and autosomes to sexually antagonistic selection acting on a polygenic phenotype. We model a phenotype initially under stabilizing selection around a single optimum, followed by a sudden divergence of the male and female optima. We find that, in the absence of dosage compensation, the X chromosome promotes evolution toward the female optimum, inducing coevolutionary male-biased responses on the autosomes. Dosage compensation obscures the female-biased interests of the X, causing it to contribute equally to male and female phenotypic change. We further demonstrate that fluctuations in an adaptive landscape can generate prolonged intragenomic conflict and accentuate the differential responses of the X and autosomes to this conflict. 

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3. A conserved trans regulatory loop involving an odorant binding protein controls male mating behavior in flies

   https://doi.org/10.1101/2021.06.22.447776  

   Delclos, Pablo J; Adhikari, Kiran; Hassan, Oluwatomi; Oderhowho, Alexander A; Sriskantharajah, Vyshnika; Trinh, Tammie; Meisel, Richard P (January 2021, bioRxiv)

   A major goal in evolutionary biology is to understand how natural variation is maintained in sexually selected and sexually dimorphic traits. Hypotheses to explain genetic variation in sexually selected traits include context-dependent fitness effects, epistatic interactions, and pleiotropic constraints. The house fly, Musca domestica, is a promising system to investigate how these factors affect polymorphism in sexually selected traits. Two common Y chromosomes (YM and IIIM) segregate as stable polymorphisms in natural house fly populations, appear to be locally adapted to different thermal habitats, and differentially affect male mating success. Here, we perform a meta-analysis of RNA-seq data which identifies genes encoding odorant binding proteins (in the Obp56h family) as differentially expressed between the heads of males carrying YM and IIIM Differential expression of Obp56h has been associated with variation in male mating behavior in Drosophila melanogaster. We find differences in male mating behavior between house flies carrying the Y chromosomes that are consistent with the relationship between male mating behavior and expression of Obp56h in D. melanogaster. We also find that male mating behaviors in house fly are affected by temperature, and the same temperature differentials further affect the expression of Obp56h genes. However, we show that temperature-dependent effects cannot explain the maintenance of genetic variation for male mating behavior in house fly. Using a network analysis and allele-specific expression measurements, we find evidence that the house fly IIIM chromosome is a trans regulator of Obp56h gene expression. Moreover, we find that Obp56h disproportionately affects the expression of genes on the D. melanogaster chromosome that is homologous to the house fly IIIM chromosome. This provides evidence for a conserved trans regulatory loop involving Obp56h expression that affects male mating behavior in flies. The complex regulatory architecture controlling Obp56h expression suggests that variation in male mating behavior could be maintained by epistasis or pleiotropic constraints. 

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4. Social antagonism facilitates supergene expansion in ants

   https://doi.org/10.1016/j.cub.2023.10.049  

   Scarparo, Giulia; Palanchon, Marie; Brelsford, Alan; Purcell, Jessica (December 2023, Current Biology)

   Antagonistic selection has long been considered a major driver of the formation and expansion of sex chromosomes. For example, sexually antagonistic variation on an autosome can select for suppressed recombination between that autosome and the sex chromosome, leading to a neo-sex chromosome. Autosomal supergenes, chromosomal regions containing tightly linked variants affecting the same complex trait, share similarities with sex chromosomes, raising the possibility that sex chromosome evolution models can explain the evolution of genome structure and recombination in other contexts. We tested this premise in a Formica ant species wherein we identified four supergene haplotypes on chromosome 3 underlying colony social organization and sex ratio. We discovered a novel rearranged supergene variant (9r) on chromosome 9 underlying queen miniaturization. The 9r is in strong linkage disequilibrium with one chromosome 3 haplotype (P2) found in multi-queen (polygyne) colonies. We suggest that queen miniaturization is strongly disfavored in the single queen (monogyne) background, and thus socially antagonistic. As such, divergent selection experienced by ants living in alternative social ‘environments’ (monogyne and polygyne) may have contributed to the emergence of a genetic polymorphism on chromosome 9 and associated queen-size dimorphism. Consequently, an ancestral polygyne-associated haplotype may have expanded to include the polymorphism on chromosome 9, resulting in a larger region of suppressed recombination spanning two chromosomes. This process is analogous to the formation of neo-sex chromosomes and consistent with models of expanding regions of suppressed recombination. We propose that miniaturized queens, 16-20% smaller than queens without 9r, could be incipient intraspecific social parasites. 

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5. Chromosome-specific drift under stabilizing selection generates polygenic barriers to sex chromosome turnover

   https://doi.org/10.1073/pnas.2528925123  

   Muralidhar, Pavitra (April 2026, Proceedings of the National Academy of Sciences)

   While sex chromosome systems show frequent evolutionary transitions in some clades, in many others they show long-term stability. Previous explanations of this stasis rely on evolutionary dynamics peculiar to sex chromosomes, such as the accumulation of deleterious mutations on the sex-specific chromosome or sexually antagonistic mutations on either sex chromosome. Here, I show that stabilizing selection on quantitative traits promotes stability of sex chromosome systems. The reason is that stabilizing selection, while keeping the value of the trait near its optimum, allows individual chromosomes’ contributions to the trait to drift, and this chromosome-specific drift reduces the fitness of the novel sex-determining genotypes necessarily produced during sex chromosome turnover. Given the ubiquity of stabilizing selection on quantitative traits, chromosome-specific drift could play a pivotal role in preventing the turnover of sex chromosome systems across multiple stages of their evolution. The theory generates several testable predictions for the evolution of sex chromosome systems that align well with observed phylogenetic patterns. For example, although chromosome-specific drift acts as a global impediment to sex chromosome turnover, those turnovers that do occur should be more likely to maintain the system of heterogamety than to change it. The theory further predicts a higher rate of transitions from environmental to genetic sex determination, versus the reverse. Finally, the theory shows that the evolution of sexual dimorphism in complex traits can drive long-term sex chromosome stability. 

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