A large-scale study led by researchers at the University of Chicago has uncovered pervasive genetic conflicts that influence reproductive success in males and females. By experimentally disabling genes in hundreds of thousands of fruit flies (Drosophila melanogaster), the team found that the vast majority of the genes they tested, whether newly evolved or ancient, have sex- and tissue-specific antagonistic effects on fitness. These conflicts, the researchers report, are a major and persistent force in evolution.
The findings, published in Nature Ecology & Evolution, challenge long-standing assumptions that natural selection primarily favors genes that benefit an organism as a whole for adaptation to their environment. Instead, the results reveal that the vast majority of genes improve reproductive success in one sex or tissue while harming another. Only 5% of newly evolved genes are advantageous in both reproductive and bodily tissues for both sexes, suggesting adaptive gene evolution.
“This is one of the first big picture studies to help understand the genetic basis of sexual dependent selection and sexual dimorphism, which have been challenging evolutionary biologists and geneticists for the past century and a half since Darwin,” said Manyuan Long, PhD, the Edna K. Papazian Distinguished Service Professor of Ecology and Evolution at UChicago and senior author of the study.
A ‘heroic,’ gene-by-gene test of evolutionary effects
To investigate how individual genes affect reproductive success, the team performed an exhaustive, 10-year set of experiments that the study’s reviewers called “heroic.” They selectively manipulated activity of 125 genes, including 92 genes that first evolved within the past 35 million years (so-called “young genes”) and 33 older genes that evolved more than 35 million years old.
Using various genetic tools, the researchers knocked down, or disabled, genes one by one in both somatic tissues (the body) or germline tissues (reproductive tissues like eggs and sperm), creating more than 15,000 experimental variations of flies that produced more than 732,000 viable offspring. This approach allowed the researchers to directly calculate how each gene influenced adult reproductive fitness, as measured by how many offspring the flies produced.
Manyuan Long, PhD
Edna K. Papazian Distinguished Service Professor of Ecology and Evolution
Committee on Genetics, Genomics and Systems Biology
The results revealed striking and unexpected patterns. When gene activity was reduced in somatic tissues, nearly two-thirds of genes showed “sexual antagonism,” meaning they boost reproduction in one sex while reducing it in the other. In these cases, experimentally disabling the gene harmed males (i.e. they produced fewer offspring) but improved female reproductive success (they produced more offspring).
By contrast, genes acting in the germline more often benefited both sexes. Still, over a quarter of germline genes showed beneficial effects for females with detrimental effects on males. These patterns were equally common in young and older genes, indicating that sexual conflict does not change over evolutionary time.
Beyond conflicts between sexes, the study uncovered extensive tissue-level conflicts as well. This means that some genes have a beneficial effect on somatic tissues at the expense of the germline. For example, a variant that produces stronger muscles might result in fewer eggs being produced, or vice versa.
More than one-third of strongly acting young genes had opposite effects in reproductive versus bodily tissues within the same sex. In females, these genes frequently boosted reproductive success through the germline, such as producing more viable eggs, while harming overall body fitness. In males, the opposite pattern was more common, with beneficial effects on somatic tissues but harmful effects on the germline.
This phenomenon, known as tissue antagonism, highlights how genes can be pulled in different evolutionary directions depending on where and how they are used.
Broader implications for evolution and biology
The results suggest that sexual selection and genetic conflict are fundamental drivers of evolutionary innovation, influencing how genes arise, persist, and diversify, as much if not more than genes that bestow beneficial functions.
By demonstrating that reproductive conflicts are widespread, persistent, and measurable at the level of individual genes, the study provides a new framework for understanding everything from fertility evolution to sex differences in disease.
The study, “Analysis of the impact of gene evolution on reproductive effects reveals prevalent sexual and germline-soma conflicts,” was supported by the National Institutes of Health and the National Science Foundation. Shengqian Xia, Deanna Arsala, and Andrea Gschwend from UChicago were co-first authors of the paper. Additional authors include William Koval, Jared Atlas, Shuaibo Han, Jianhai Chen, Laura Faulere, Muzi Li, Joseph Mihaljevic, Daniel J. Sanchez, Grace Rui-Tong Yu, Natalia Tamarina, Nicholas VanKuren, and Stefano Allesina, all from UChicago.
