Adaptation without Specialization Early in a Host Shift.

AbstractStudents of speciation debate the role of performance trade-offs across different environments early in speciation. We tested for early performance trade-offs with a host shift experiment using a member of the Enchenopa binotata species complex of treehoppers (Hemiptera: Membracidae). In this clade of plant-feeding insects, different species live on different host plants and exhibit strong behavioral and physiological host specialization. After five generations, the experimental host shifts resulted either in no adaptation or in adaptation without specialization. The latter result was more likely in sympatry; in allopatry, populations on novel host plants were more likely to become extinct. We conclude that in the early stages of speciation, adaptation to novel host plants does not necessarily bring about performance trade-offs on ancestral environments. Adaptation may be facilitated rather than hindered by gene flow, which prevents extinction. Additional causes of specialization and assortative mating may be required if colonization of novel environments is to result in speciation.

Collateral fitness effects of mutations.

The distribution of fitness effects of mutation plays a central role in constraining protein evolution. The underlying mechanisms by which mutations lead to fitness effects are typically attributed to changes in protein specific activity or abundance. Here, we reveal the importance of a mutation's collateral fitness effects, which we define as effects that do not derive from changes in the protein's ability to perform its physiological function. We comprehensively measured the collateral fitness effects of missense mutations in the Escherichia coli TEM-1 ß-lactamase antibiotic resistance gene using growth competition experiments in the absence of antibiotic. At least 42% of missense mutations in TEM-1 were deleterious, indicating that for some proteins collateral fitness effects occur as frequently as effects on protein activity and abundance. Deleterious mutations caused improper posttranslational processing, incorrect disulfide-bond formation, protein aggregation, changes in gene expression, and pleiotropic effects on cell phenotype. Deleterious collateral fitness effects occurred more frequently in TEM-1 than deleterious effects on antibiotic resistance in environments with low concentrations of the antibiotic. The surprising prevalence of deleterious collateral fitness effects suggests they may play a role in constraining protein evolution, particularly for highly expressed proteins, for proteins under intermittent selection for their physiological function, and for proteins whose contribution to fitness is buffered against deleterious effects on protein activity and protein abundance.

The effect of induced mutations on quantitative traits in Arabidopsis thaliana: Natural versus artificial conditions.

Mutations are the ultimate source of all genetic variations. New mutations are expected to affect quantitative traits differently depending on the extent to which traits contribute to fitness and the environment in which they are tested. The dogma is that the preponderance of mutations affecting fitness will be skewed toward deleterious while their effects on nonfitness traits will be bidirectionally distributed. There are mixed views on the role of stress in modulating these effects. We quantify mutation effects by inducing mutations in Arabidopsis thaliana (Columbia accession) using the chemical ethylmethane sulfonate. We measured the effects of new mutations relative to a premutation founder for fitness components under both natural (field) and artificial (growth room) conditions. Additionally, we measured three other quantitative traits, not expected to contribute directly to fitness, under artificial conditions. We found that induced mutations were equally as likely to increase as decrease a trait when that trait was not closely related to fitness (traits that were neither survivorship nor reproduction). We also found that new mutations were more likely to decrease fitness or fitness-related traits under more stressful field conditions than under relatively benign artificial conditions. In the benign condition, the effect of new mutations on fitness components was similar to traits not as closely related to fitness. These results highlight the importance of measuring the effects of new mutations on fitness and other traits under a range of conditions.

Fisher's geometric model predicts the effects of random mutations when tested in the wild.

Fisher's geometric model of adaptation (FGM) has been the conceptual foundation for studies investigating the genetic basis of adaptation since the onset of the neo Darwinian synthesis. FGM describes adaptation as the movement of a genotype toward a fitness optimum due to beneficial mutations. To date, one prediction of FGM, the probability of improvement is related to the distance from the optimum, has only been tested in microorganisms under laboratory conditions. There is reason to believe that results might differ under natural conditions where more mutations likely affect fitness, and where environmental variance may obscure the expected pattern. We chemically induced mutations into a set of 19 Arabidopsis thaliana accessions from across the native range of A. thaliana and planted them alongside the premutated founder lines in two habitats in the mid-Atlantic region of the United States under field conditions. We show that FGM is able to predict the outcome of a set of random induced mutations on fitness in a set of A. thaliana accessions grown in the wild: mutations are more likely to be beneficial in relatively less fit genotypes. This finding suggests that FGM is an accurate approximation of the process of adaptation under more realistic ecological conditions.

Evidence for parallel adaptation to climate across the natural range of Arabidopsis thaliana.

How organisms adapt to different climate habitats is a key question in evolutionary ecology and biological conservation. Species distributions are often determined by climate suitability. Consequently, the anthropogenic impact on earth's climate is of key concern to conservation efforts because of our relatively poor understanding of the ability of populations to track and evolve to climate change. Here, we investigate the ability of Arabidopsis thaliana to occupy climate space by quantifying the extent to which different climate regimes are accessible to different A. thaliana genotypes using publicly available data from a large-scale genotyping project and from a worldwide climate database. The genetic distance calculated from 149 single-nucleotide polymorphisms (SNPs) among 60 lineages of A. thaliana was compared to the corresponding climate distance among collection localities calculated from nine different climatic factors. A. thaliana was found to be highly labile when adapting to novel climate space, suggesting that populations may experience few constraints when adapting to changing climates. Our results also provide evidence of a parallel or convergent evolution on the molecular level supporting recent generalizations regarding the genetics of adaptation.

One hundred years of pleiotropy: a retrospective.

Pleiotropy is defined as the phenomenon in which a single locus affects two or more distinct phenotypic traits. The term was formally introduced into the literature by the German geneticist Ludwig Plate in 1910, 100 years ago. Pleiotropy has had an important influence on the fields of physiological and medical genetics as well as on evolutionary biology. Different approaches to the study of pleiotropy have led to incongruence in the way that it is perceived and discussed among researchers in these fields. Furthermore, our understanding of the term has changed quite a bit since 1910, particularly in light of modern molecular data. This review traces the history of the term "pleiotropy" and reevaluates its current place in the field of genetics.