thescientist | The relationship between an individual’s phenotype and genotype has been fundamental to the genetic analysis of traits and to models of evolutionary change for decades. Of course, scientists have long recognized that phenotype responds to nongenetic factors, such as environmental variation in nutrient availability or the presence of other, competing species. But by assuming that the genetic component of a particular trait is confined to your genes and only yours, scientists overlooked another important input: the genes of your neighbors.
Take field crickets as an example. To identify potential mates, female crickets listen with ears on their forelegs to the males’ songs, produced by the rubbing together of their forewings. Some males emit series of long, trill-like chirps, an advertisement of their fitness that females find very attractive. Songs dominated by short chirps have less pull. But female crickets don’t evaluate songs on their absolute merits; instead, their preferences are influenced by the songs they’ve heard in the past. Female crickets previously exposed only to songs with long chirps are less likely to respond to short-chirp songs than females that have been exposed to the songs of less-fit males already. The insects appear to be retaining information about available males and then using that information to assess the attractiveness of suitors.1
Choosing mates amidst competition is ubiquitous among animals, but the logistics of how such choice evolved is less straightforward: because male song type is largely determined by genetics, female mating behavior is under the influence of male genes. In other words, the females’ decision-making behaviors evolved based on the genetic composition of the entire social group. Such indirect genetic effects (IGEs), also called associative effects or extended phenotypes, are common and have profound implications for evolution. Beyond learning and behavior in social species, IGEs affect how organisms develop, how productive plants are, and whether individuals are attacked by predators, herbivores, and disease.
In some sense, examples of IGEs are intuitively obvious. No individual exists in a vacuum, isolated from the influences of others it encounters. Yet for decades, many prominent evolutionary theories assumed that all of the genetic influences on an individual’s phenotype came from genes within itself. What the field needs now is a clear framework that recognizes IGEs as additional factors in a population’s evolution, allowing for more-accurate predictions about how biological systems will change in the future. The genetic makeup of an individual not only influences phenotypes of individuals in its own species, but can have far-reaching effects on organisms at different trophic levels within its food web, impacting the dynamics of entire ecosystems. The role of commensal microbes in human health is a prime example of how IGEs can transcend species boundaries.
How IGEs affect evolutionary dynamics remains very much an open question. Recent theoretical strides in this area show how IGEs can greatly accelerate evolutionary change and hint at their hitherto unsuspected roles in such varied phenomena as animal mating rituals, the development of human agricultural systems, species range shifts in response to climate change, and even altruism. The influences of IGEs on diverse evolutionary processes are undoubtedly more complicated than most models can capture, and biologists must think creatively about new phenomena that IGEs may drive.
