Patterns of quantitative genetic variation in multiple dimensions

A fundamental question for both evolutionary biologists and breeders is the extent to which genetic correlations limit the ability of populations to respond to selection. Here I view this topic from three perspectives. First, I propose several nondimensional statistics to quantify the genetic variation present in a suite of traits and to describe the extent to which correlations limit their selection response. A review of five data sets suggests that the total variation differs substantially between populations. In all cases analyzed, however, the “effective number of dimensions” is less than two: more than half of the total genetic variation is explained by a single combination of traits. Second, I consider how patterns of variation affect the average evolutionary response to selection in a random direction. When genetic variation lies in a small number of dimensions but there are a large number of traits under selection, then the average selection response will be reduced substantially from its potential maximum. Third, I discuss how a low genetic correlation between male fitness and female fitness limits the ability of populations to adapt. Data from two recent studies of natural populations suggest this correlation can diminish or even erase any genetic benefit to mate choice. Together these results suggest that adaptation (in natural populations) and genetic improvement (in domesticated populations) may often be as much constrained by patterns of genetic correlation as by the overall amount of genetic variation.     

Variation,selection and evolution of function-valued traits

We describe an emerging framework for understanding variation, selection and evolution of phenotypic traits that are mathematical functions. We use one specific empirical example – thermal performance curves (TPCs) for growth rates of caterpillars – to demonstrate how models for function-valued traits are natural extensions of more familiar, multivariate models for correlated, quantitative traits. We emphasize three main points. First, because function-valued traits are continuous functions, there are important constraints on their patterns of variation that are not captured by multivariate models. Phenotypic and genetic variation in function-valued traits can be quantified in terms of variance-covariance functions and their associated eigenfunctions: we illustrate how these are estimated as well as their biological interpretations for TPCs. Second, selection on a function-valued trait is itself a function, defined in terms of selection gradient functions. For TPCs, the selection gradient describes how the relationship between an organism's performance and its fitness varies as a function of its temperature. We show how the form of the selection gradient function for TPCs relates to the frequency distribution of environmental states (caterpillar temperatures) during selection. Third, we can predict evolutionary responses of function-valued traits in terms of the genetic variance-covariance and the selection gradient functions. We illustrate how non-linear evolutionary responses of TPCs may occur even when the mean phenotype and the selection gradient are themselves linear functions of temperature. Finally, we discuss some of the methodological and empirical challenges for future studies of the evolution of function-valued traits.     

Using adaptive traits to consider potential consequences of temporal variation in selection: male guppy colour through time and space

Temporal variation in selection is typically evaluated by estimating and comparing selection coefficients in natural populations. Meta‐analyses of these coefficients have yielded important insights, but selection coefficients are limited in several respects, including low statistical power, imperfect fitness surrogates, and uncertainty regarding consequences for trait change. A complementary approach without these limitations is to examine temporal variation in adaptive traits themselves, which is mechanistically easier and more directly relevant to evolutionary consequences. We illustrate this approach by analyzing the colour patterns of male guppies, Poecilia reticulata, from each of six sites in Trinidad in each of 6 years. This system is particularly appropriate for our study because key aspects of colour variation are genetically‐based and responsive to selection. However, although spatial patterns of colour variation have been extensively considered in this system, no study has yet formally assessed annual temporal variation in non‐manipulated populations. Matching previous conclusions for the guppy system, we find that guppies from different sites manifest different colour patterns in association with different predation regimes. We here add the new finding that, although some temporal variation is present, spatial patterns of colour variation are generally consistent across years. These results suggest that, when considering adaptive traits, spatial variation is more important than temporal variation, although our study system might be exceptional in this regard. Additional studies examining spatiotemporal variation in adaptive traits could help to improve our understanding of the role that spatiotemporal variation in selection plays in the evolutionary process. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2014, 112 , 108–122.     

A test for the genetic basis of natural selection: an individual-based longitudinal study in a stream-dwelling fish

In addition to the well-studied evolutionary parameters of (1) phenotype-fitness covariance and (2) the genetic basis of phenotypic variation, adaptive evolution by natural selection requires that (3) fitness variation is effected by heritable genetic differences among individuals and (4) phenotype-fitness covariances must be, at least in part, underlain by genetic covariances. These latter two requirements for adaptive evolutionary change are relatively unstudied in natural populations. Absence of the latter requirements could explain stasis of apparently directionally selected heritable traits. We provide complementary analyses of selection and variation at phenotypic and genetic levels for juvenile growth rate in brook charr Salvelinus fontinalis in Freshwater River, Newfoundland, Canada. Contrary to the vast majority of reports in fish, we found very little viability selection of juvenile body size. Large body size appears nonetheless to be selectively advantageous via a relationship with early maturity. Genetic patterns in evolutionary parameters largely reflected phenotypic patterns. We have provided inference of selection based on longitudinal data, which are uncommon in high fecundity organisms. Furthermore we have provided a practicable framework for further studies of the genetic basis of natural selection.     

Strong ecological but weak evolutionary effects of elevated CO2 on a recombinant inbred population of Arabidopsis thaliana

Increases in atmospheric CO2 concentration have an impact on plant communities by influencing plant growth and morphology, species interactions, and ecosystem processes. These ecological effects may be accompanied by evolutionary change if elevated CO2 (eCO2) alters patterns of natural selection or expression of genetic variation. Here, a statistically powerful quantitative genetic experiment and manipulations of CO2 concentrations in a field setting were used to investigate how eCO2 impacts patterns of selection on ecologically important traits in Arabidopsis thaliana; heritabilities, which influence the rate of response to selection; and genetic covariances between traits, which may constrain responses to selection. CO2 had strong phenotypic effects; plants grown in eCO2 were taller and produced more biomass and fruits. Also, significant directional selection was observed on many traits and significant genetic variation was observed for all traits. However, no evolutionary effect of eCO2 was detected; patterns of selection, heritabilities and genetic correlations corresponded closely in ambient and elevated CO2 environments. The data suggest that patterns of natural selection and the quantitative genetic parameters of this A. thaliana population are robust to increases in CO2 concentration and that responses to eCO2 will be primarily ecological.     

Are more diverse parts of the mammalian skull more?labile?

Morphological variation is unevenly distributed within the mammalian skull; some of its parts have diversified more than others. It is commonly thought that this pattern of variation is mainly the result of the structural organization of the skull, as defined by the pattern and magnitude of trait covariation. Patterns of trait covariation can facilitate morphological diversification if they are aligned in the direction of selection, or these patterns can constrain diversification if oriented in a different direction. Within this theoretical framework, it is thought that more variable parts possess patterns of trait covariation that made them more capable of evolutionary change, that is, are more labile. However, differences in the degree of morphological variation among skull traits could arise despite variation in trait lability if, for example, some traits have evolved at a different rate and/or undergone stabilizing selection. Here, we test these hypotheses in the mammalian skull using 2D geometric morphometrics to quantify skull shape and estimating constraint, rates of evolution, and lability. Contrary to the expectations, more variable parts of the skull across mammalian species are less capable of evolutionary change than are less variable skull parts. Our results suggest that patterns of morphological variation in the skull could result from differences in rate of evolution and stabilizing selection.     

A framework for the study of genetic variation in migratory behaviour

Evolutionary change results from selection acting on genetic variation. For migration to be successful, many different aspects of an animal’s physiology and behaviour need to function in a co-coordinated way. Changes in one migratory trait are therefore likely to be accompanied by changes in other migratory and life-history traits. At present, we have some knowledge of the pressures that operate at the various stages of migration, but we know very little about the extent of genetic variation in various aspects of the migratory syndrome. As a consequence, our ability to predict which species is capable of what kind of evolutionary change, and at which rate, is limited. Here, we review how our evolutionary understanding of migration may benefit from taking a quantitative-genetic approach and present a framework for studying the causes of phenotypic variation. We review past research, that has mainly studied single migratory traits in captive birds, and discuss how this work could be extended to study genetic variation in the wild and to account for genetic correlations and correlated selection. In the future, reaction-norm approaches may become very important, as they allow the study of genetic and environmental effects on phenotypic expression within a single framework, as well as of their interactions. We advocate making more use of repeated measurements on single individuals to study the causes of among-individual variation in the wild, as they are easier to obtain than data on relatives and can provide valuable information for identifying and selecting traits. This approach will be particularly informative if it involves systematic testing of individuals under different environmental conditions. We propose extending this research agenda by using optimality models to predict levels of variation and covariation among traits and constraints. This may help us to select traits in which we might expect genetic variation, and to identify the most informative environmental axes. We also recommend an expansion of the passerine model, as this model does not apply to birds, like geese, where cultural transmission of spatio-temporal information is an important determinant of migration patterns and their variation.     

Pattern and process: evidence for the evolution of photosynthetic traits in natural populations

The patterns of interspecific variation identified by comparative studies provide valuable hypotheses about the role of physiological traits in evolutionary adaptation. This review covers tests of these hypotheses for photosynthetic traits that have used a microevolutionary perspective to characterize physiological variation among and within populations. Studies of physiological differentiation among populations show that evolutionary divergence in photosynthetic traits is common within species, and has a pattern that supports many adaptive hypotheses. These among-population studies imply that selection has influenced photosynthetic traits in some way, but they are not designed to identify the traits targeted by selection or the environmental agents that cause selection. Analyses of genetic and phenotypic variation within populations address these questions. Studies that have quantified genetic variation within populations show that levels of heritable variation can be adequate for evolutionary change in photosynthetic traits. Other studies have measured phenotypic selection for these traits by analyzing how the variation within populations is correlated with fitness. This work has shown that selection for photosynthetic traits may often operate indirectly via correlations with other traits, and emphasizes the importance of viewing the phenotype as an integrated function of growth, morphology, life-history and physiology. We also outline some methodological problems that may be encountered for ecophysiological traits by these types of studies, provide some potential solutions, and discuss future directions for the field of plant evolutionary ecophysiology.     

Cost of reproduction and covariation of life history traits in birds

Evolution of life history traits can be studied at two different levels: (1) current selection processes, including trade-offs in life history traits in natural populations as revealed by observations or, preferably, exieriments; and (2) patterns of variation in life history traits with each other and with ecology among extant species. Selection is not evolution, but selection pressures must have caused evolutionary change and led to current patterns of life history traits. These problems are exemplified by recent research on clutch size in birds.     

Using Microbial Microcosms to Study Host–parasite Coevolution

Microbial microcosm experiments with bacteria and their viral parasites allow us to observe host–parasite coevolution in action. Laboratory populations of microbes evolve rapidly, thanks to their short generation times and huge population sizes. By taking advantage of a “living fossil record” stored in the laboratory freezer, we can directly compare the fitness of hosts and parasites with their actual evolutionary ancestors. Such experiments demonstrate that host–parasite coevolution is an important evolutionary force and a cause of strong and divergent natural selection.     

The role of natural selection in circadian behaviour: a molecular-genetic approach

Circadian rhythms (~24 h) in biochemistry, physiology and behaviour are found in almost all eukaryotes and some bacteria. The elucidation of the molecular components of the 24 h circadian clock in a number of model organisms in recent years has provided an opportunity to assess the adaptive value of variation in clock genes. Laboratory experiments using artificially generated mutants reveal that the circadian period is adaptive in a 24 h world. Natural genetic variation can also be studied, and there are a number of ways in which the signature of natural selection can be detected. These include the study of geographical patterns of genetic variation, which provide a first indication that selection may be at work, and the use of sophisticated statistical neutrality tests, which examine whether the pattern of variation observed is consistent with a selective rather than a neutral (or drift) scenario. Finally, examining the probable selective agents and their differential effects on the circadian phenotype of the natural variants provides the final compelling evidence for selection. We present some examples of how these types of analyses have not only enlightened the evolutionary study of clocks, but have also contributed to a more pragmatic molecular understanding of the function of clock proteins.     

QUANTIFYING EVOLUTIONARY POTENTIAL OF MARINE FISH LARVAE: HERITABILITY,SELECTION, AND EVOLUTIONARY CONSTRAINTS

For many marine fish, intense larval mortality may provide considerable opportunity for selection, yet much less is known about the evolutionary potential of larval traits. We combined field demographic studies and manipulative experiments to estimate quantitative genetic parameters for both larval size and swimming performance for a natural population of a common coral‐reef fish, the bicolor damselfish (Stegastes partitus). We also examined selection on larval size by synthesizing information from published estimates of selective mortality. We introduce a method that uses the Lande–Arnold framework for examining selection on quantitative traits to empirically reconstruct adaptive landscapes. This method allows the relationship between phenotypic value and fitness components to be described across a broad range of trait values. Our results suggested that despite strong viability selection for large larvae and moderate heritability (h²= 0.29), evolutionary responses of larvae would likely be balanced by reproductive selection favoring mothers that produce more, smaller offspring. Although long‐term evolutionary responses of larval traits may be constrained by size‐number trade‐offs, our results suggest that phenotypic variation in larval size may be an ecologically important source of variability in population dynamics through effects on larval survival and recruitment to benthic populations.     

The maintenance of heritable variation through social competition

The paradoxical persistence of heritable variation for fitness-related traits is an evolutionary conundrum that remains a preeminent problem in evolutionary biology. Here we describe a simple mechanism in which social competition results in the evolutionary maintenance of heritable variation for fitness related traits. We demonstrate this mechanism using a genetic model with two primary assumptions: the expression of a trait depends upon success in social competition for limited resources; and competitive success of a genotype depends on the genotypes that it competes against. We find that such social competition generates heritable (additive) genetic variation for "competition-dependent" traits. This heritable variation is not eroded by continuous directional selection because, rather than leading to fixation of favored alleles, selection leads instead to allele frequency cycling due to the concerted coevolution of the social environment with the effects of alleles. Our results provide a mechanism for the maintenance of heritable variation in natural populations and suggest an area for research into the importance of competition in the genetic architecture of fitness related traits.     

Experimental Evolution and Its Role in Evolutionary Physiology

Four general approaches to the study of evolutionary physiology—phylogenetically-basedcomparisons, genetic analyses and manipulations, phenotypicplasticity and manipulation, and selection studies—areoutlined and discussed. We provide an example of the latter,the application of laboratory selection experiments to the studyof a general issue in environmental adaptation, differencesin adaptive patterns of generalists and specialists. A cloneof the bacterium Escherichia coli that had evolved in a constantenvironment of 37°C was replicated into 6 populations andallowed to reproduce for 2,000 generations in a variable thermalenvironment alternating between 32 and 42°C. As predictedby theory, fitness and efficiency of resource use increasedin this new environment, as did stress resistance. Contraryto predictions, however, fitness and efficiency in the constantancestral environment of 37°C did not decrease, nor didthermal niche breadth or phenotypic plasticity increase. Selectionexperiments can thus provide a valuable approach to testinghypotheses and assumptions about the evolution of functionalcharacters.     

Natural selection at genomic regions associated with obesity and type-2 diabetes: East Asians and sub-Saharan Africans exhibit high levels of differentiation at type-2 diabetes regions

Different populations suffer from different rates of obesity and type-2 diabetes (T2D). Little is known about the genetic or adaptive component, if any, that underlies these differences. Given the cultural, geographic, and dietary variation that accumulated among humans over the last 60,000 years, we examined whether loci identified by genome-wide association studies for these traits have been subject to recent selection pressures. Using genome-wide SNP data on 938 individuals in 53 populations from the Human Genome Diversity Panel, we compare population differentiation and haplotype patterns at these loci to the rest of the genome. Using an “expanding window” approach (100–1,600 kb) for the individual loci as well as the loci as ensembles, we find a high degree of differentiation for the ensemble of T2D loci. This differentiation is most pronounced for East Asians and sub-Saharan Africans, suggesting that these groups experienced natural selection at loci associated with T2D. Haplotype analysis suggests an excess of obesity loci with evidence of recent positive selection among South Asians and Europeans, compared to sub-Saharan Africans and Native Americans. We also identify individual loci that may have been subjected to natural selection, such as the T2D locus, HHEX, which displays both elevated differentiation and extended haplotype homozygosity in comparisons of East Asians with other groups. Our findings suggest that there is an evolutionary genetic basis for population differences in these traits, and we have identified potential group-specific genetic risk factors.     

EVOLUTION OF VARIATION AND VARIABILITY UNDER FLUCTUATING,STABILIZING, AND DISRUPTIVE SELECTION

How variation and variability (the capacity to vary) may respond to selection remain open questions. Indeed, effects of different selection regimes on variational properties, such as canalization and developmental stability are under debate. We analyzed the patterns of among‐ and within‐individual variation in two wing‐shape characters in populations of Drosophila melanogaster maintained under fluctuating, disruptive, and stabilizing selection for more than 20 generations. Patterns of variation in wing size, which was not a direct target of selection, were also analyzed. Disruptive selection dramatically increased phenotypic variation in the two shape characters, but left phenotypic variation in wing size unaltered. Fluctuating and stabilizing selection consistently decreased phenotypic variation in all traits. In contrast, within‐individual variation, measured by the level of fluctuating asymmetry, increased for all traits under all selection regimes. These results suggest that canalization and developmental stability are evolvable and presumably controlled by different underlying genetic mechanisms, but the evolutionary responses are not consistent with an adaptive response to selection on variation. Selection also affected patterns of directional asymmetry, although inconsistently across traits and treatments.     

Selection experiments and the study of phenotypic plasticity1

Abstract Laboratory selection experiments are powerful tools for establishing evolutionary potentials. Such experiments provide two types of information, knowledge about genetic architecture and insight into evolutionary dynamics. They can be roughly classified into two types: (1) artificial selection in which the experimenter selects on a focal trait or trait index, and (2) quasi‐natural selection in which the experimenter establishes a set of environmental conditions and then allows the population to evolve. Both approaches have been used in the study of phenotypic plasticity. Artificial selection experiments have taken various forms including: selection directly on a reaction norm, selection on a trait in multiple environments, and selection on a trait in a single environment. In the latter experiments, evolution of phenotypic plasticity is investigated as a correlated response. Quasi‐natural selection experiments have examined the effects of both spatial and temporal variation. I describe how to carry out such experiments, summarize past efforts, and suggest further avenues of research.     

SIZE VARIATION,GROWTH STRATEGIES,AND THE EVOLUTION OF MODULARITY IN THE MAMMALIAN SKULL

Allometry is a major determinant of within‐population patterns of association among traits and, therefore, a major component of morphological integration studies. Even so, the influence of size variation over evolutionary change has been largely unappreciated. Here, we explore the interplay between allometric size variation, modularity, and life‐history strategies in the skull from representatives of 35 mammalian families. We start by removing size variation from within‐species data and analyzing its influence on integration magnitudes, modularity patterns, and responses to selection. We also carry out a simulation in which we artificially alter the influence of size variation in within‐taxa matrices. Finally, we explore the relationship between size variation and different growth strategies. We demonstrate that a large portion of the evolution of modularity in the mammalian skull is associated to the evolution of growth strategies. Lineages with highly altricial neonates have adult variation patterns dominated by size variation, leading to high correlations among traits regardless of any underlying modular process and impacting directly their potential to respond to selection. Greater influence of size variation is associated to larger intermodule correlations, less individualized modules, and less flexible responses to natural selection.     

The effects of environmental heterogeneity on multivariate selection on reproductive traits in female great tits

Describing natural selection on phenotypic traits under varying environmental conditions is essential for a quantitative assessment of the scale at which adaptation might occur and of the impact of environmental variability on evolution. Here we analyzed patterns of multivariate selection via fecundity and viability on three reproductive traits (laying date, clutch size, and egg weight) in a population of great tits (Parus major). We quantified selection under different environmental conditions using (1) local variation in breeding density and (2) distinct areas of the population's habitat. We found that selection gradients were generally stronger for fecundity than for viability selection. We also found correlational selection acting on the combination of laying date and clutch size; this is the first documented evidence of such selection acting on these two traits in a passerine bird. Our analyses showed that both local breeding density and habitat significantly influenced selection patterns, hence favoring different patterns of reproductive investment at a small-scale relative to typical dispersal distances in this species. Canonical rotation of the nonlinear selection matrices yielded similar conclusions as traditional nonlinear selection analyses, and also showed that the main axes of selection and fitness surfaces varied over space within the population. Our results emphasize the importance of quantifying different forms of selection, and of including variation in environmental conditions at small scales to gain a better understanding of potential evolutionary dynamics in wild populations. This study suggests that the fitness landscape for this species is relatively rugged at scales relevant to the life histories of individual birds and their close relatives.     

Cranial evolution in sakis (Pithecia, Platyrrhini). II: Evolutionary processes and morphological integration

Patterns of interspecific differentiation in saki monkeys (Pithecia) are quantitatively described and possible evolutionary processes producing them are examined. The comparison of species correlation matrices to expected patterns of morphological integration reveal significant and similar patterns of development-based cranial integration among species. Aspects of the facial region are more heavily influenced by general size variation than features of the neural region. The comparison of pooled within- and between-groups V/CV matrices suggests that genetic drift might be a sufficient explanation for saki cranial evolution. Differential natural selection gradients are also reconstructed because selection may also have caused population differentiation through evolutionary time. These gradients illustrate the inherent multivariate nature of selection, being a consequence of the interaction between existing morphological integration (correlation) among traits and the action of natural selection. Yet, our attempt to interpret selection gradients in terms of their functional significance did not result in any clear association between selection and function. Perhaps this is also an indication that morphological evolution in sakis was mostly neutral.