The Ecological Theatre of Selfish Elements

Some selfish genetic elements enhance their transmission to the next generation by interfering with and eliminating competing variants within the same host, typically at a cost to host fitness. These higher-level fitness costs can constrain the spread of such transmission-distorting elements. We examine three specific transmission distorters (maternal-effect killers, cytoplasmic incompatibility, and spermatogenic drivers) and show how aspects of their organismal ecology-specifically, mating systems, reproductive compensation, and population structure-can weaken or altogether eliminate these constraints, shifting selection down from the level of the individual to the level of the selfish element. Despite the mechanistic differences between our three cases, a common principle emerges: when ecological conditions allow a transmission distorter's harm to be borne under soft rather than hard selection, higher-level constraints are weakened and more extreme forms of selfishness can evolve. We show how this softening of selection can arise theoretically and offer predictions about the taxonomic distribution of certain forms of selfish elements in light of it. Thus, to understand internal conflicts requires a consideration of not only the inner mechanisms by which selfish elements gain a transmission advantage but also the outer ecological context.