Analysis of the impact of gene evolution on reproductive effects reveals prevalent sexual and germline–soma conflicts

Functional innovation is conventionally viewed as a consequence of natural selection for environmental adaptation. However, impacts of other evolutionary forces, including genetic conflicts, have not been explored through direct manipulations of individual genes when assessing overall genetic basis of fitness. Here we conducted a comprehensive RNA interference screen targeting 125 young and old genes in somatic and germline tissues of male and female Drosophila melanogaster, plus CRISPR knockouts of some genes. We analysed sex-specific adult fitness effects, fertility phenotypes of central importance in evolution, in a total of 732,710 adult offspring scored from over 15,000 repeated knockdown crosses and controls. Bayesian statistical analysis of the fitness data revealed that 62.6% of the young and old genes that underwent somatic knockdowns reveal remarkable intralocus sexual conflict with the vast majority being male advantageous and female detrimental, as knockdowns are male detrimental and female beneficial. Germline knockdowns detected a majority of genes with adaptive sexual concordance and over a quarter of genes under sexual antagonism mostly female advantageous and male detrimental. We also detected 36.7% of young genes that have strong effects in both germline and soma exhibit tissue conflicts within sex although female effects are stronger. These analyses of sex-specific distributions of fitness effects reveal a prevalent role for antagonistic selection between sexes and tissues, while finding no association between chromosomal locations and sexually antagonistic genes, nor with sex-biased expression and gene age.