Volumes 159–160, June–July 2024, Pages 27-37Author links open overlay panel, , Abstract

The evolutionary forces underlying the rapid evolution in sequences and functions of new genes remain a mystery. Adaptation by natural selection explains the evolution of some new genes. However, many new genes perform sex-biased functions that have rapidly evolved over short evolutionary time scales, suggesting that new gene evolution may often be driven by conflicting selective pressures on males and females. It is well established that such sexual conflict (SC) plays a central role in maintaining phenotypic and genetic variation within populations, but the role of SC in driving new gene evolution remains essentially unknown. This review explores the connections between SC and new gene evolution through discussions of the concept of SC, the phenotypic and genetic signatures of SC in evolving populations, and the molecular mechanisms by which SC could drive the evolution of new genes. We synthesize recent work in this area with a discussion of the case of Apollo and Artemis, two extremely young genes (<200,000 years) in Drosophila melanogaster, which offered the first empirical insights into the evolutionary process by which SC could drive the evolution of new genes. These new duplicate genes exhibit the hallmarks of sexually antagonistic selection: rapid DNA and protein sequence evolution, essential sex-specific functions in gametogenesis, and complementary sex-biased expression patterns. Importantly, Apollo is essential for male fitness but detrimental to female fitness, while Artemis is essential for female fitness but detrimental to male fitness. These sexually antagonistic fitness effects and complementary changes to expression, sequence, and function suggest that these duplicates were selected for mitigating SC, but that SC has not been fully resolved. Finally, we propose Sexual Conflict Drive as a self-driven model to interpret the rapid evolution of new genes, explain the potential for SC and sexually antagonistic selection to contribute to long-term evolution, and suggest its utility for understanding the rapid evolution of new genes in gametogenesis.

Section snippetsSexual conflict: the concept and the evidence

Males and females of the same species often develop strikingly divergent morphologies, physiologies, and behaviors despite sharing the vast majority of their genomes. In fact, sexual dimorphisms comprise some of the most extreme polymorphisms in the animal kingdom (Fig. 1). Males develop weaponry and large bodies with which to fight each other; bright and conspicuous color patterns to convince females of their virility; and perform elaborate courtship rituals to earn mates. Females develop

Genetics of sexual conflict

The proper development of any trait depends on the coordinated action of many genes across time and space, both within and between cells. Thus, a comprehensive understanding of the origins and evolution of sexual dimorphisms requires knowledge of the genes and genetic variation that contribute their development [14]. The development of sexually dimorphic traits is initiated by the sex determination pathway – in many organisms controlled by a single switch gene located on a sex chromosome. Yet

A powerful model system for studying the role of SC in evolution: new duplicate genes

A particularly attractive system for studying the role of SC in driving evolution is new duplicate genes. Unlike the evolutionary dynamics of alternate SA alleles, duplicate gene copies may optimize sex-specific functions that are limited to the benefitted sex [44]. Evidence is rapidly accumulating to indicate that duplicate genes quickly evolve divergent functions and expression patterns between males and females [45], [46]. The evolutionary forces underlying such rapid evolution of important

Sexually antagonistic functions

Apl and Arts are tandem duplicate genes that were formed and fixed specifically in D. melanogaster, within the last ~200,000 years, yet both are essential for fly development and fertility in surprising ways (Fig. 5). In the following subsections, we describe the specific patterns of divergence between the two copies that relate to the resolution of SC and highlight how these patterns can be used to test the generality and support of models of SC resolution by gene duplication. Finally, we

Concluding remarks

Species have evolved a vast array of sexually dimorphic morphological, physiological, and behavioral traits that require sex-specific genetic architectures for their development. Sexual conflict over traits has long been suspected to underlie the evolution and development of sexual dimorphism, but linking mutations to sexually dimorphic traits has proved challenging. Sexually antagonistic genetic variation is now known to be widespread in natural population, so linking that variation to sexual

Declaration of Competing Interest

None.

Acknowledgements

We thank the enthusiastic discussion with Drs. Shengqian Xia, Deanna Arsala and Esther Betran. The study of Apl and Arts was supported by the National Science Foundation grant NSF2020667 and the National Institutes of Health grant 1R01GM116113-01A1. The composition of this review was also supported by a John Simon Guggenheim Memorial Foundation Fellowship for Natural Sciences and a University of Chicago Division of Biological Science fund to M.L.

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