Genetic constraints on adaptation: a theoretical primer for the genomics era

Abstract

Genetic constraints are features of inheritance systems that slow or prohibit adaptation. Several population genetic mechanisms of constraint have received sustained attention within the field since they were first articulated in the early 20th century. This attention is now reflected in a rich, and still growing, theoretical literature on the genetic limits to adaptive change. In turn, empirical research on constraints has seen a rapid expansion over the last two decades in response to changing interests of evolutionary biologists, along with new technologies, expanding data sets, and creative analytical approaches that blend mathematical modeling with genomics. Indeed, one of the most notable and exciting features of recent progress in genetic constraints is the close connection between theoretical and empirical research. In this review, we discuss five major population genetic contexts of genetic constraint: genetic dominance, pleiotropy, fitness trade-offs between types of individuals of a population, sign epistasis, and genetic linkage between loci. For each, we outline historical antecedents of the theory, specific contexts where constraints manifest, and their quantitative consequences for adaptation. From each of these theoretical foundations, we discuss recent empirical approaches for identifying and characterizing genetic constraints, each grounded and motivated by this theory, and outline promising areas for future work.

Infection in patchy populations: Contrasting pathogen invasion success and dispersal at varying times since host colonization

“…As host populations transitioned toward the stationary phase, not only did the average invasion success decline, but so too did the differences among genotypes. Together, these observations suggest that newly colonized host populations are the most evolutionarily liable for the pathogen, allowing for higher invasion success and greater adaptive potential (i.e., more genetic variability; Connallon and Hall ), in concert with a host population that is free from density‐dependent regulation and is rapidly expanding (e.g., Giometto et al. ; Fronhofer et al.…”

Quantifying how constraints limit the diversity of viable routes to adaptation

“…However, the same example can also be interpreted as being severely constrained in terms of the diversity of forms, since there are so few viable alternative genetic solutions that actually evolve [19]. Thus, evolutionary constraints can be considered along two related but distinct axes: factors that affect the potential for any adaptive response [22,23] vs. factors that affect the diversity of forms (i.e., genetic routes to adaptation). A scenario that is highly constrained in terms of the diversity of forms may be least constrained in terms of the potential for a rapid adaptive response to a change in environment, and low redundancy in the mapping of genotype-phenotypefitness may itself be a product of adaptation over deep time.…”

Evolutionary Consequences of Sex-Specific Selection in Variable Environments: Four Simple Models Reveal Diverse Evolutionary Outcomes

“…A-E are available online). Several studies have derived approximations for the diploid selection case, assuming modest to weak selection and arbitrary dominance relations between alleles (e.g., Campos Rosado and Robertson 1966;Turner 1968;Connallon and Hall 2018). For these cases, the change in frequency of the A allele is well approximated by…”

“…represents the square of the allele frequency difference between breeding females and males (see Connallon and Hall 2018). Equation (3) shows once again that natural selection increases W f W m .…”