Understanding specialism when the Jack of all trades can be the master of all

Abstract

Specialism is widespread in nature, generating and maintaining diversity, but recent work has demonstrated that generalists can be equally fit as specialists in some shared environments. This no-cost generalism challenges the maxim that 'the jack of all trades is the master of none', and requires evolutionary genetic mechanisms explaining the existence of specialism and no-cost generalism, and the persistence of specialism in the face of selection for generalism. Examining three well-described mechanisms with respect to epistasis and pleiotropy indicates that sign (or antagonistic) pleiotropy without epistasis cannot explain no-cost generalism and that magnitude pleiotropy without epistasis (including directional selection and mutation accumulation) cannot explain the persistence of specialism. However, pleiotropy with epistasis can explain all. Furthermore, epistatic pleiotropy may allow past habitat use to influence future use of novel environments, thereby affecting disease emergence and populations' responses to habitat change.

Figure 1.

Phenotypes in two environments. All phenotypes existing under a simplified scenario in which three levels of fitness are possible in each of two environments (designated red and blue). Generalists with equal fitness in the two environments lie on the marked diagonal.

Figure 2.

Genotype–phenotype maps. Fitness in two environments is depicted on the vertical axis (in red and blue) for (a) one-locus or (b–e) two-locus, two-allele genotype sequence spaces. (a) Under sign pleiotropy involving only one locus, cost-bearing generalist a is favoured in the blue environment or when exposure to the red and blue environments alternates, and A is favoured in the red environment. Two types of non-epistatic magnitude pleiotropy are shown. (b) Under directional selection, the B allele is favoured in the blue environment or alternating environments, the A allele is favoured under conditions of the red or alternating environments. (c) Under mutation accumulation, the A allele is favoured in both environments and in alternating environments, and in the red environment, the conditionally deleterious allele B can become fixed owing to drift or hitchhiking. (d) Epistatic pleiotropy with reciprocal sign epistasis. Here, the transition from specialism (aB) to no-cost generalism (Ab) requires a transient loss of fitness in the red environment and is therefore disfavoured in the red or alternating environments. (e) Epistatic pleiotropy facilitating escape from specialism (ab) to no-cost generalism (AB), via compensatory mutation for a deleterious mutation (aB), or via acquisition of cryptic variation (Ab).

Figure 3.

Evolution from a common ancestor. (a,b) Trajectories of fitness in the blue environment for specialist populations evolving in the blue environment (blue lines) and generalist populations evolving in alternating environments (purple lines) under (a) directional selection and (b) mutation accumulation. (c,d) Genomes of replicate independently evolving specialists (blue lines) and generalists (purple lines) at time t as indicated in (a,b), under (c) directional selection and (d) mutation accumulation. Mutations conferring benefit in blue, red or both environments depicted with blue, red and purple vertical lines, respectively. Conditionally deleterious alleles reducing fitness in red depicted with red crosses. Vertical lines occurring in the same location in the genomes indicate parallel substitutions in independently evolving populations.