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.

Mutational (genetic) robustness is phenotypic constancy in the face of mutational changes to the genome. Robustness is critical to the understanding of evolution because phenotypically expressed genetic variation is the fuel of natural selection. Nonetheless, the evidence for adaptive evolution of mutational robustness in biological populations is controversial. Robustness should be selectively favored when mutation rates are high, a common feature of RNA viruses. However, selection for robustness may be relaxed under virus co-infection because complementation between virus genotypes can buffer mutational effects. We therefore hypothesized that selection for genetic robustness in viruses will be weakened with increasing frequency of co-infection. To test this idea, we used populations of RNA phage φ6 that were experimentally evolved at low and high levels of co-infection and subjected lineages of these viruses to mutation accumulation through population bottlenecking. The data demonstrate that viruses evolved under high co-infection show relatively greater mean magnitude and variance in the fitness changes generated by addition of random mutations, confirming our hypothesis that they experience weakened selection for robustness. Our study further suggests that co-infection of host cells may be advantageous to RNA viruses only in the short term. In addition, we observed higher mutation frequencies in the more robust viruses, indicating that evolution of robustness might foster less-accurate genome replication in RNA viruses.

Populations experiencing similar selection pressures can sometimes diverge in the genetic architectures underlying evolved complex traits. We used RNA virus populations of large size and high mutation rate to study the impact of historical environment on genome evolution, thus increasing our ability to detect repeatable patterns in the evolution of genetic architecture. Experimental vesicular stomatitis virus populations were evolved on HeLa cells, on MDCK cells, or on alternating hosts. Turner and Elena (2000. Cost of host radiation in an RNA virus. Genetics. 156:1465-1470.) previously showed that virus populations evolved in single-host environments achieved high fitness on their selected hosts but failed to increase in fitness relative to their ancestor on the unselected host and that alternating-host-evolved populations had high fitness on both hosts. Here we determined the complete consensus sequence for each evolved population after 95 generations to gauge whether the parallel phenotypic changes were associated with parallel genomic changes. We also analyzed the patterns of allele substitutions to discern whether differences in fitness across hosts arose through true pleiotropy or the presence of not only a mutation that is beneficial in both hosts but also 1 or more mutations at other loci that are costly in the unselected environment (mutation accumulation [MA]). We found that ecological history may influence to what extent pleiotropy and MA contribute to fitness asymmetries across environments. We discuss the degree to which current genetic architecture is expected to constrain future evolution of complex traits, such as host use by RNA viruses.

Numerous studies have shown genotype-by-environment (G؋E) interactions for traits related to organismal fitness. However, the genetic architecture of the interaction is usually unknown because these studies used genotypes that differ from one another by many unknown mutations. These mutations were also present as standing variation in populations and hence had been subject to prior selection. Based on such studies, it is therefore impossible to say what fraction of new, random mutations contributes to G؋E interactions. In this study, we measured the fitness in four environments of 26 genotypes of Escherichia coli, each containing a single random insertion mutation. Fitness was measured relative to their common progenitor, which had evolved on glucose at 37°C for the preceding 10,000 generations. The four assay environments differed in limiting resource and temperature (glucose, 28°C; maltose, 28°C; glucose, 37°C; and maltose, 37°C). A highly significant interaction between mutation and resource was found. In contrast, there was no interaction involving temperature. The resource interaction reflected much higher among mutation variation for fitness in maltose than in glucose. At least 11 mutations (42%) contributed to this G؋E interaction through their differential fitness effects across resources. Beneficial mutations are generally thought to be rare but, surprisingly, at least three mutations (12%) significantly improved fitness in maltose, a resource novel to the progenitor. More generally, our findings demonstrate that G؋E interactions can be quite common, even for genotypes that differ by only one mutation and in environments differing by only a single factor.GϫE interaction ͉ GEI ͉ phenotypic plasticity ͉ fitness ͉ evolution

The effects of mutations on phenotype and fitness may depend on the environment (phenotypic plasticity), other mutations (genetic epistasis) or both. Here we examine the fitness effects of 18 random insertion mutations in E. coli in two resource environments and five genetic backgrounds. We tested each mutation for plasticity and epistasis by comparing its fitness effects across these ecological and genetic contexts. Some mutations had no measurable effect in any of these contexts. None of the mutations had effects on phenotypic plasticity that were independent of genetic background. However, half the mutations had epistatic interactions such that their effects differed among genetic backgrounds, usually in an environment-dependent manner. Also, the pattern of mutational effects across backgrounds indicated that epistasis had been shaped primarily by unique events in the evolutionary history of a population rather than by repeatable events associated with shared environmental history.How common are epistasis and plasticity? How do they arise during evolution? The evolutionary consequences of population subdivision 1,2 , the maintenance of sex 3-5 and the role of environmental heterogeneity in speciation 6 all depend on the answers to these questions. Most studies that have examined the effects of individual alleles in multiple environments or genetic backgrounds have focused on particular genes already known to have context-dependent function 7-10 .