Species-specific duplicate genes help resolve sexual conflict while evolving essential sex-specific functions

A pair of tandem duplicate fruit fly genes are required for proper spermatogenesis or oogenesis and evolved biased expression patterns that help alleviate ancestral intralocus sexual conflict.

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Feb 20, 2018
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The paper in Nature Ecology & Evolution is here: http://go.nature.com/2EPS6Wz

Males and females of sexual species frequently exhibit amazingly different phenotypes. Hundreds to millions of years of sexual and natural selection have produced species where members of one sex are flashy while the other sex is drab, one sex fights while the other observes, or one sex builds while the other inspects, among so many others. These traits directly affect the numbers of offspring that males and females produce. But how does a shared genome allow the two sexes develop such drastically different traits? More importantly, how do genes used by both sexes evolve to satisfy such different requirements for male and female reproductive success? These genes must be subject to intralocus sexual conflict (ISC), or selection in different directions on a trait shared by males and females.


Sexual dimorphism frequently leads to sexual conflict because selection cannot simultaneously optimize dimorphic traits with a shared genetic basis in both males and females. Photo Credit: (top left) allanlau2000 [CC0] and (top right) Obsidian_Tanto [CC0] via http://pixabay.com; (bottom) Nicolas Gompel [CC BY-SA 3.0]  via http://drosophilidae.myspecies.info


Here, the twins Apollo (Apl) and Artemis (Arts) are not the ancient Greek twins, but a pair of duplicate genes that suggest a widespread mechanism by which ISC can be resolved. Despite being only ~200,000 years old, Apl and Arts have essential, yet sexually antagonistic functions in fly reproduction: Apl functions are required for spermatogenesis but reduce female fertility while Arts functions are required for oogenesis but reduce male fertility. This finding is exciting for at least two reasons. First, it shows that species-specific genes can be essential for survival and reproduction and that these functions can evolve much more rapidly than classical theories predict (e.g. Jacob, 1976; Mayr, 1982; Ashburner et al, 1998). Second, it suggests that the gene duplicates have rapidly mitigated ISC that was present in their single-copy ancestor and lends some of the first empirical support to recent theoretical models of ISC resolution by gene duplication (Gallach and Betran, 2011; Connallon and Clark, 2011; Wyman et al, 2012).

Previous genome-wide screens in D. melanogaster revealed enormous amounts of standing genetic variation with sexually antagonistic fitness effects (e.g. 1,292 genes reported by Innocenti and Morrow, 2010, and 1,204 genes by Hill et al, 2017). Classic theory predicts that these sexually antagonistic alleles, although prevalent and likely existing at some equilibrium frequency in natural populations, should be purged by natural selection or quickly silenced as modifier mutations accumulate in the antagonistic locus or elsewhere in the genome (Rice, 1984). Thus, theories and evidence clearly suggest that sexually antagonistic alleles should be viewed as a class of genetic variants that has an ephemeral contribution, or no contribution, to evolution.

Amazingly, Apollo and Artemis were rapidly fixed in natural fly populations and have contributed to the long-term survival of the species, despite the harm they each inflict on one sex. Amazingly, these two genes have become integral components of the genetic machinery responsible for essential biological processes in males and females. Facing this paradox, one may lament that life, especially its genetic basis, is really starkly different from what standard biology textbooks tell us about the elegant structures and efficient, well-adapted processes that produce life. Instead, we have to listen to 159 year old, but often neglected, warning of Charles Darwin while we marvel at the masterpieces of natural selection: life is not perfect. 

Thus, we ought not marvel at the gain one sex may achieve at cost of the opposite sex because of the way genetic machinery works in evolution even when duplication is selected to mitigate the conflict. Nor should we be surprised that ISC may be a powerful force in shaping genome evolution. Every gene that is differentially used by males and females is subject to ISC, so there is a continual tug of war on these genes to perform those functions that are optimal for females or optimal for males. This tug of war may be a primary driver of gene duplication in general - many new gene copies exhibit male-biased expression while their parental copies exhibit broad or female-biased expression (e.g. Zhang et al., 2010).

Finally, there are plenty of new scientific problems raised by these Apl/Arts results. What was the function of the single-copy ancestral gene before the duplication took place? What were the consequences (and order) of substitutions in both non-coding and coding regions in Apl and Arts? And has ISC been resolved by duplication of the Apl/Arts ancestor in additional Drosophila species? Can we move beyond simply studying gene expression pattern biases to begin functionally testing if additional genes have sexually antagonistic functions in flies and other animals? Future work using ancestral gene resurrection or work in D. melanogaster’s relatives should help answer these questions and shed more light on the role of gene duplication in resolving sexual conflict.


Nicholas VanKuren & Manyuan Long


VanKuren NW & Long M. Gene duplicates resolving sexual conflict rapidly evolved essential gametogenesis functions. Nat Ecol Evol (2018). doi:10.1038/s41559-018-0471-0


References:

Ashburner, M. et al. An Exploration of the Sequence of a 2.9-Mb Region of the Genome of Drosophila melanogaster: The Adh Region. Genetics 153, 179–219 (1999). 

Connallon, T. & Clark, A. G. The resolution of sexual antagonism by gene duplication. Genetics 187, 919–937 (2011)

Gallach, M. & Betrán, E. Intralocus sexual conflict resolved through gene duplication. Trends Ecol. Evol. 26, 222–228 (2011). 

Hill M. S., et al. Sexual antagonism exerts evolutionarily persistent genomic constraints on sexual differentiation in Drosophila melanogaster. BioRxiv (2017). doi: https://doi.org/10.1101/117176

Innocenti, P. & Morrow, E. H. The sexually antagonistic genes of Drosophila melanogaster. PLoS Biol. 8, e1000335 (2010).

Jacob, F. Evolution and Tinkering. Science 196, 1161–1166 (1977). 

Mayr, E. The Growth of Biological Thought. (Belknap Press, 1982).

Rice, W. R. Sex chromosomes and the evolution of sexual dimorphism. Evolution 38, 735–742 (1984).

Wyman, M. J., Cutter, A. D. & Rowe, L. Gene duplication in the evolution of sexual dimorphism. Evolution. 66, 1556–1566 (2012).

Zhang, Y. E., Vibranovski, M. D., Krinsky, B. H. & Long, M. Age-dependent chromosomal distribution of male-biased genes in Drosophila. Genome Res. 20, 1526–33 (2010).


Go to the profile of Nicholas VanKuren

Nicholas VanKuren

Postdoctoral Scholar, The University of Chicago

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