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The evolutionary implications of genetic conflict

Final Report Summary - GENCON (The evolutionary implications of genetic conflict)

Research during the last two decades has made it clear that the DNA that forms our genes is only partly the harmonious, integrated and resilient unity it was once believed to be. In fact, it often seems more reminiscent of a quirky and imperfect battle-ground working surprisingly well. The realization that genes, or versions of genes (i.e. alleles), in an organism sometimes “disagree” over various issues is a tenet that has proven very consequential. It has led to important novel insights into our understanding of, for example, how our genes are organized, how new species are formed and why certain human genetic diseases arise. Several more or less distinct forms of genetic conflict can be recognized. First, genes that reside within the same individual may not entirely share interests. Second, conflict among genes that reside in individuals of the two sexes may have conflicting interests (sexual conflict). The research program in GENCON has followed several routes and has, collectively, provided a rich and diverse source of novel and ground-breaking information on distinct but related genetic conflicts. As empirical model systems, we have primarily used a variety of different insects (primarily beetles and flies). A major part of GENCON has concerned mitochondria. Mitochondria are the power plants of our cells. They carry their own genes (mtDNA) that are inherited only through females, and these are therefore exposed to natural selection solely in females. An allele that is beneficial for females, but bad for males, will thus readily spread in populations. This evolutionary “advantage” for females, which has been called "the mother's curse", may in theory lead to a genetic conflict by which males find themselves having problems with their fertility, metabolism and suffer reduced lifespan. Research conducted in GENCON has been able to confirm that mtDNA variation indeed has sizeable effects on both male metabolism and male reproduction. However, because the genes in the cell nucleus (nDNA) are inherited equally through the maternal and paternal line, they do not entirely share the interests of mtDNA genes and an evolutionary "tug of war" between the two types of genes can occur. Our work has shown that the interplay between mitochondrial and nuclear genes is important for organismal function (metabolism and reproduction) and that this is played out somewhat differently in males and females. More generally, the research of GENCON has reformed our view of mtDNA, from a passive bystander in adaptive evolution to key player in sex-specific adaptation. A second main part of GENCON concerns a slightly different form of evolutionary "tug of war", namely that between genes residing in two the sexes. Because life places different demands on males and females in the animal world, genes that benefit males may be at a disadvantage to females: natural selection can act differently in males and females. In a series of studies within GENCON, we have demonstrated that such evolutionary “tugs of war” between the sexes exist but that they depend on environmental conditions. We have also shown that these sexual conflicts are rooted in different optimal values for life history traits such as metabolic rate, body size and activity. Genes that are responsible for these effects often have unconventional effects and often interact in complicated ways with one another. We have also shown that sexual conflict contributes importantly to male genital evolution, the evolution of sex-roles and male and female reproductive behaviors and to the diversification of male signal substances (proteins) that are transferred to females with the ejaculate at mating.