Changing abiotic and biotic environments affect the genetics of adaptation and speciation

Abstract

Abiotic and biotic environments can change in different ways that affect how populations adapt, diverge, and speciate. However, many models of speciation only examine adaptation to constant environments. We used Fishers geometric model to study adaptation and speciation in different types of changing abiotic and biotic environments. We hypothesized that, when the magnitude of environmental change is equal, fitness would be lowered more by consistently directional abiotic change and by consistently antagonistic biotic conflict. As a result, directional changes and biotic conflict would cause a greater evolutionary response through fixation of adaptive mutations, greater divergence between populations, and lower migrant or hybrid fitnesses (higher speciation potential). Increasing the directionality of abiotic change did indeed have all these effects. However, populations evolving with conflict, despite showing the expected arms-race elevation of deleterious change and evolutionary response, did not result in decreased fitness of migrants and hybrids. Two factors seem to be involved. In tug-of-war conflict, high total phenotypic change does not lead to high phenotypic divergence because the phenotypic change churns around in the same general area of trait space. With victim-exploiter (trait matching) conflict, hybrids and migrants were frequently more fit than those with other kinds of change because of escape from locally adapted antagonists. In this case, foreign genes sometimes allowed populations in conflict to generate useful variation. These results show that different kinds of ecological change can affect adaptation and the formation of new species in distinct ways and that local divergence and incompatibility do not always go hand in hand. Significance StatementAdaptation and speciation are key processes in evolution. During the process of adapting, populations genetically diverge from each other and can become incompatible, leading to new species. The tendency for populations to diverge can be different in changing environments. Changes in the environment can consist of changes in the non-living parts like temperature or elevation (the abiotic environment) or changes in the species that a population interacts with (the biotic environment). Abiotic and biotic environments are thought to change in different ways because biotic environments are evolving but abiotic ones are not. In particular, antagonistic biotic evolution can lead to arms races. We modeled how abiotic change and biotic changes from antagonistic or mutualistic interactions affect adaptation and speciation. We found that, as expected, antagonistic biotic changes led to a large amount of evolutionary divergence but surprisingly this did not lead to correspondingly large reduction in migrant or hybrid fitness. In a tug-of- war antagonistic model, this was due evolutionary churn - high change did not lead to high divergence. In a victim-exploiter (trait matching) model, migrants and hybrids between diverging populations were often better off because antagonisms were broken up. As a result of migrants and hybrids having higher fitness, antagonistic biotic interactions may result in less speciation than expected from their evolutionary arm-races.