Integrating ecology with genetics to explain gene reuse during repeated evolution

The role of determinism and chance in the evolutionary history of life is often analyzed through the lens of the repeatability of evolution. Although it is now clear that evolution often repeats itself, we are only beginning to understand why this varies in degree. For example, the probability of gene reuse during repeated bouts of adaptation often declines with time since divergence, but the causes of this pattern remain unclear. Here, we explore two core hypotheses for time-dependent variation in the repeatability of gene reuse during adaptation. Specifically, gene reuse depends on the extent to which lineages have 1) similar genomes such that they have similar genetic architectures, mutations, and mutational effects (i.e., a fairly well-appreciated "shared genetics" hypothesis), and 2) similar ecologies such that they have similar environments and patterns of natural selection (i.e., a mostly unexplored "shared ecology" hypothesis). The latter hypothesis emphasizes ecology's role in gene reuse and has received little explicit attention. In particular, testing the shared ecology hypothesis requires moving beyond a simple dichotomous characterization of ecology to embracing ecological divergence as a multivariate and continuous phenomenon. Although such tests are only beginning to emerge, they already illustrate how integration of ecological factors can help explain variation in gene reuse. Here, we advocate a framework that integrates the influence of both genetic and ecological factors in the repeatability of evolution and can be applied to a range of organisms to better understand the role of determinism and chance in biological diversification.