Juha Merilä

Climate change and evolution: disentangling environmental and genetic responses

Rapid climate change is likely to impose strong selection pressures on traits important for fitness, and therefore, microevolution in response to climate‐mediated selection is potentially an important mechanism mitigating negative consequences of climate change. We reviewed the empirical evidence for recent microevolutionary responses to climate change in longitudinal studies emphasizing the following three perspectives emerging from the published data. First, although signatures of climate change are clearly visible in many ecological processes, similar examples of microevolutionary responses in literature are in fact very rare. Second, the quality of evidence for microevolutionary responses to climate change is far from satisfactory as the documented responses are often — if not typically — based on nongenetic data. We reinforce the view that it is as important to make the distinction between genetic (evolutionary) and phenotypic (includes a nongenetic, plastic component) responses clear, as it is to understand the relative roles of plasticity and genetics in adaptation to climate change. Third, in order to illustrate the difficulties and their potential ubiquity in detection of microevolution in response to natural selection, we reviewed the quantitative genetic studies on microevolutionary responses to natural selection in the context of long‐term studies of vertebrates. The available evidence points to the overall conclusion that many responses perceived as adaptations to changing environmental conditions could be environmentally induced plastic responses rather than microevolutionary adaptations. Hence, clear‐cut evidence indicating a significant role for evolutionary adaptation to ongoing climate warming is conspicuously scarce.

Comparison of genetic differentiation at marker loci and quantitative traits

The comparison of the degree of differentiation in neutral marker loci and genes coding quantitative traits with standardized and equivalent measures of genetic differentiation (FST and QST, respectively) can provide insights into two important but seldom explored questions in evolutionary genetics: (i) what is the relative importance of random genetic drift and directional natural selection as causes of population differentiation in quantitative traits, and (ii) does the degree of divergence in neutral marker loci predict the degree of divergence in genes coding quantitative traits? Examination of data from 18 independent studies of plants and animals using both standard statistical and meta‐analytical methods revealed a number of interesting points. First, the degree of differentiation in quantitative traits (QST) typically exceeds that observed in neutral marker genes (FST), suggesting a prominent role for natural selection in accounting for patterns of quantitative trait differentiation among contemporary populations. Second, the FST – QST difference is more pronounced for allozyme markers and morphological traits, than for other kinds of molecular markers and life‐history traits. Third, very few studies reveal situations were QST < FST, suggesting that selection pressures, and hence optimal phenotypes, in different populations of the same species are unlikely to be often similar. Fourth, there is a strong correlation between QST and FST indices across the different studies for allozyme (r=0.81), microsatellite (r=0.87) and combined (r=0.75) marker data, suggesting that the degree of genetic differentiation in neutral marker loci is closely predictive of the degree of differentiation in loci coding quantitative traits. However, these interpretations are subject to a number of assumptions about the data and methods used to derive the estimates of population differentiation in the two sets of traits.

Heritable variation and evolution under favourable and unfavourable conditions

Genetic variability in quantitative traits can change as a direct response to the environmental conditions in which they are expressed. Consequently, similar selection in different environments might not be equally effective in leading to adaptation. Several hypotheses, including recent ones that focus on the historical impact of selection on populations, predict that the expression of genetic variation will increase in unfavourable conditions. However, other hypotheses lead to the opposite prediction. Although a consensus is unlikely, recent Drosophila and bird studies suggest consistent trends for morphological traits under particular conditions.

Climate change, adaptation, and phenotypic plasticity: the problem and the evidence

Many studies have recorded phenotypic changes in natural populations and attributed them to climate change. However, controversy and uncertainty has arisen around three levels of inference in such studies. First, it has proven difficult to conclusively distinguish whether phenotypic changes are genetically based or the result of phenotypic plasticity. Second, whether or not the change is adaptive is usually assumed rather than tested. Third, inferences that climate change is the specific causal agent have rarely involved the testing – and exclusion – of other potential drivers. We here review the various ways in which the above inferences have been attempted, and evaluate the strength of support that each approach can provide. This methodological assessment sets the stage for 11 accompanying review articles that attempt comprehensive syntheses of what is currently known – and not known – about responses to climate change in a variety of taxa and in theory. Summarizing and relying on the results of these reviews, we arrive at the conclusion that evidence for genetic adaptation to climate change has been found in some systems, but is still relatively scarce. Most importantly, it is clear that more studies are needed – and these must employ better inferential methods – before general conclusions can be drawn. Overall, we hope that the present paper and special issue provide inspiration for future research and guidelines on best practices for its execution.

Ecological genomics of local adaptation

It is increasingly important to improve our understanding of the genetic basis of local adaptation because of its relevance to climate change, crop and animal production, and conservation of genetic resources. Phenotypic patterns that are generated by spatially varying selection have long been observed, and both genetic mapping and field experiments provided initial insights into the genetic architecture of adaptive traits. Genomic tools are now allowing genome-wide studies, and recent theoretical advances can help to design research strategies that combine genomics and field experiments to examine the genetics of local adaptation. These advances are also allowing research in non-model species, the adaptation patterns of which may differ from those of traditional model species.

Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis

Comparative studies of quantitative genetic and neutral marker differentiation have provided means for assessing the relative roles of natural selection and random genetic drift in explaining among‐population divergence. This information can be useful for our fundamental understanding of population differentiation, as well as for identifying management units in conservation biology. Here, we provide comprehensive review and meta‐analysis of the empirical studies that have compared quantitative genetic (QST) and neutral marker (FST) differentiation among natural populations. Our analyses confirm the conclusion from previous reviews – based on ca. 100% more data – that the QST values are on average higher than FST values [mean difference 0.12 (SD 0.27)] suggesting a predominant role for natural selection as a cause of differentiation in quantitative traits. However, although the influence of trait (life history, morphological and behavioural) and marker type (e.g. microsatellites and allozymes) on the variance of the difference between QST and FST is small, there is much heterogeneity in the data attributable to variation between specific studies and traits. The latter is understandable as there is no reason to expect that natural selection would be acting in similar fashion on all populations and traits (except for fitness itself). We also found evidence to suggest that QST and FST values across studies are positively correlated, but the significance of this finding remains unclear. We discuss these results in the context of utility of the QST–FST comparisons as a tool for inferring natural selection, as well as associated methodological and interpretational problems involved with individual and meta‐analytic studies.

Genetic architecture of fitness and nonfitness traits : empirical patterns and development of ideas

Comparative studies of the genetic architecture of different types of traits were initially prompted by the expectation that traits under strong directional selection (fitness traits) should have lower levels of genetic variability than those mainly under weak stabilizing selection (nonfitness traits). Hence, early comparative studies revealing lower heritabilities of fitness than nonfitness traits were first framed in terms of giving empirical support for this prediction, but subsequent treatments have effectively reversed this view. Fitness traits seem to have higher levels of additive genetic variance than nonfitness traits — an observation that has been explained in terms of the larger number loci influencing fitness as compared to nonfitness traits. This hypothesis about the larger functional architecture of fitness than nonfitness traits is supported by their higher mutational variability, which is hard to reconcile without evoking capture of mutational variability over many loci. The lower heritabilities of fitness than nonfitness traits, despite the higher additive genetic variance of the former, occur because of their higher residual variances. Recent comparative studies of dominance contributions for different types of traits, together with theoretical predictions and a large body of indirect evidence, suggest an important role of dominance variance in determining levels of residual variance for fitness-traits. The role of epistasis should not be discounted either, since a large number of loci increases the potential for epistatic interactions, and epistasis is strongly implicated in hybrid breakdown.

Lifetime Reproductive Success and Heritability in Nature

The observation that traits closely related to fitness (“fitness traits”) have lower heritabilities than traits more distantly associated with fitness has traditionally been framed in terms of Fisher’s fundamental theorem of natural selection—fitness traits are expected to have low levels of additive genetic variance due to rapid fixation of alleles conferring highest fitness. Subsequent treatments have challenged this view by pointing out that high environmental and nonadditive genetic contributions to phenotypic variation may also explain the low heritability of fitness traits. Analysis of a large data set from the collared flycatcher Ficedula albicollis confirmed a previous finding that traits closely associated with fitness tend to have lower heritability. However, analysis of coefficients of additive genetic variation (CVA) revealed that traits closely associated with fitness had higher levels of additive genetic variation (VA) than traits more distantly associated with fitness. Hence, the negative relationship between a trait’s association with fitness and its heritability was not due to lower levels of VA in fitness traits but was due to their higher residual variance. However, whether the high residual variance was mainly due to higher levels of environmental variance or due to higher levels of nonadditive genetic variance remains a challenge to be addressed by further studies. Our results are consistent with earlier suggestions that fitness‐related traits may have more complex genetic architecture than traits more distantly associated with fitness.

Paternal genetic contribution to offspring condition predicted by size of male secondary sexual character

Whether females can obtain genetic benefits from mate choice is contentious, and the main problem faced by previous studies of natural populations is that many factors other than paternal genes contribute to offspring fitness. Here, we use comparisons between sets of naturally occurring maternal half–sibling collared flycatchers, Ficedula albicollis, to control for this problem. We show, first, that there are paternal genetic effects on nestling fledging condition, a character related to fitness in this species. Further, the magnitude of the paternal genetic contribution to this character is related to the size of a condition–dependent male secondary sexual character. Our results demonstrate that genetic benefits from mate choice can be predicted by the size of a secondary sexual character, and therefore provide direct support for indicator models of sexual selection.

NATURAL SELECTION AND INHERITANCE OF BREEDING TIME AND CLUTCH SIZE IN THE COLLARED FLYCATCHER

Abstract Many characteristics of organisms in free‐living populations appear to be under directional selection, possess additive genetic variance, and yet show no evolutionary response to selection. Avian breeding time and clutch size are often‐cited examples of such characters. We report analyses of inheritance of, and selection on, these traits in a long‐term study of a wild population of the collared flycatcher Ficedula albicollis. We used mixed model analysis with REML estimation (“animal models”) to make full use of the information in complex multigenerational pedigrees. Heritability of laying date, but not clutch size, was lower than that estimated previously using parent‐offspring regressions, although for both traits there was evidence of substantial additive genetic variance (h2= 0.19 and 0.29, respectively). Laying date and clutch size were negatively genetically correlated (rA=–0.41 ± 0.09), implying that selection on one of the traits would cause a correlated response in the other, but there was little evidence to suggest that evolution of either trait would be constrained by correlations with other phenotypic characters. Analysis of selection on these traits in females revealed consistent strong directional fecundity selection for earlier breeding at the level of the phenotype (β=–0.28 ± 0.03), but little evidence for stabilising selection on breeding time. We found no evidence that clutch size was independently under selection. Analysis of fecundity selection on breeding values for laying date, estimated from an animal model, indicated that selection acts directly on additive genetic variance underlying breeding time (β=–0.20 ± 0.04), but not on clutch size (β= 0.03 ± 0.05). In contrast, selection on laying date via adult female survival fluctuated in sign between years, and was opposite in sign for selection on phenotypes (negative) and breeding values (positive). Our data thus suggest that any evolutionary response to selection on laying date is partially constrained by underlying life‐history trade‐offs, and illustrate the difficulties in using purely phenotypic measures and incomplete fitness estimates to assess evolution of life‐history trade‐offs. We discuss some of the difficulties associated with understanding the evolution of laying date and clutch size in natural populations.