Genetic Variation For Fitness Research Articles

Mitochondrial function and sexual selection: can physiology resolve the 'lek paradox'?

Across many taxa, males use elaborate ornaments or complex displays to attract potential mates. Such sexually selected traits are thought to signal important aspects of male 'quality'. Female mating preferences based on sexual traits are thought to have evolved because choosy females gain direct benefits that enhance their lifetime reproductive success (e.g. greater access to food) and/or indirect benefits because high-quality males contribute genes that increase offspring fitness. However, it is difficult to explain the persistence of female preferences when males only provide genetic benefits, because female preferences should erode the heritable genetic variation in fitness that sexually selected traits signal. This 'paradox of the lek' has puzzled evolutionary biologists for decades, and inspired many hypotheses to explain how heritable variation in sexually selected traits is maintained. Here, we discuss how factors that affect mitochondrial function can maintain variation in sexually selected traits despite strong female preferences. We discuss how mitochondrial function can influence the expression of sexually selected traits, and we describe empirical studies that link the expression of sexually selected traits to mitochondrial function. We explain how mothers can affect mitochondrial function in their offspring by (a) influencing their developmental environment through maternal effects and (b) choosing a mate to increase the compatibility of mitochondrial and nuclear genes (i.e. the 'mitonuclear compatibility model of sexual selection'). Finally, we discuss how incorporating mitochondrial function into models of sexual selection might help to resolve the paradox of the lek, and we suggest avenues for future research.

Hidden genetic variation in plasticity provides the potential for rapid adaptation to novel environments.

Rapid environmental change is forcing populations into environments where plasticity will no longer maintain fitness. When populations are exposed to novel environments, evolutionary theory predicts that genetic variation in fitness will increase and should be associated with genetic differences in plasticity. If true, then genetic variation in plasticity can increase adaptive potential in novel environments, and population persistence via evolutionary rescue is more likely. To test whether genetic variation in fitness increases in novel environments and is associated with plasticity, we transplanted 8149 clones of 314 genotypes of a Sicilian daisy (Senecio chrysanthemifolius) within and outside its native range, and quantified genetic variation in fitness, and plasticity in leaf traits and gene expression. Although mean fitness declined by 87% in the novel environment, genetic variance in fitness increased threefold and was correlated with plasticity in leaf traits. High fitness genotypes showed greater plasticity in gene expression, but lower plasticity in most leaf traits. Interestingly, genotypes with the highestfitness in the novel environment had the lowest fitness at the native site. These results suggest that standing genetic variation in plasticity could help populations to persist and adapt to novel environments, despite remaining hidden in native environments.

Intrinsic emergence and modulation of sex-specific dominance reversals in threshold traits.

Sex‐specific dominance reversals (SSDRs) in fitness‐related traits, where heterozygotes' phenotypes resemble those of alternative homozygotes in females versus males, can simultaneously maintain genetic variation in fitness and resolve sexual conflict and thereby shape key evolutionary outcomes. However, the full implications of SSDRs will depend on how they arise and the resulting potential for evolutionary, ecological and environmental modulation. Recent field and laboratory studies have demonstrated SSDRs in threshold(‐like) traits with dichotomous or competitive phenotypic outcomes, implying that such traits could promote the emergence of SSDRs. However, such possibilities have not been explicitly examined. I show how phenotypic SSDRs can readily emerge in threshold traits given genetic architectures involving large‐effect loci alongside sexual dimorphism in the mean and variance in polygenic liability. I also show how multilocus SSDRs can arise in line‐cross experiments, especially given competitive reproductive systems that generate nonlinear fitness outcomes. SSDRs can consequently emerge in threshold(‐like) traits as functions of sexual antagonism, sexual dimorphism and reproductive systems, even with purely additive underlying genetic effects. Accordingly, I identify theoretical and empirical advances that are now required to discern the basis and occurrence of SSDRs in nature, probe forms of (co‐)evolutionary, ecological and environmental modulation, and evaluate net impacts on sexual conflict.

The quantitative genetics of fitness in a wild seabird.

ABSTRACTAdditive genetic variance in fitness is a prerequisite for adaptive evolution, as a trait must be genetically correlated with fitness to evolve. Despite its relevance, additive genetic variance in fitness has not often been estimated in nature. Here, we investigate additive genetic variance in lifetime and annual fitness components in common terns (Sterna hirundo). Using 28 years of data comprising approximately 6000 pedigreed individuals, we find that additive genetic variances in the zero‐inflated and Poisson components of lifetime fitness were effectively zero but estimated with high uncertainty. Similarly, additive genetic variances in adult annual reproductive success and survival did not differ from zero but were again associated with high uncertainty. Simulations suggested that we would be able to detect additive genetic variances as low as 0.05 for the zero‐inflated component of fitness but not for the Poisson component, for which adequate statistical power would require approximately two more decades (four tern generations) of data collection. As such, our study suggests heritable variance in common tern fitness to be rather low if not zero, shows how studying the quantitative genetics of fitness in natural populations remains challenging, and highlights the importance of maintaining long‐term individual‐based studies of natural populations.

Density-dependent selection and the maintenance of colour polymorphism in barn owls.

The capacity of natural selection to generate adaptive changes is (according to the fundamental theorem of natural selection) proportional to the additive genetic variance in fitness. In spite of its importance for development of new adaptations to a changing environment, processes affecting the magnitude of the genetic variance in fitness-related traits are poorly understood. Here, we show that the red-white colour polymorphism in female barn owls is subject to density-dependent selection at the phenotypic and genotypic level. The diallelic melanocortin-1 receptor gene explained a large amount of the phenotypic variance in reddish coloration in the females ([Formula: see text]). Red individuals (RR genotype) were selected for at low densities, while white individuals (WW genotype) were favoured at high densities and were less sensitive to changes in density. We show that this density-dependent selection favours white individuals and predicts fixation of the white allele in this population at longer time scales without immigration or other selective forces. Still, fluctuating population density will cause selection to fluctuate and periodically favour red individuals. These results suggest how balancing selection caused by fluctuations in population density can be a general mechanism affecting the level of additive genetic variance in natural populations.

Genetic variance in fitness indicates rapid contemporary adaptive evolution in wild animals.

The rate of adaptive evolution, the contribution of selection to genetic changes that increase mean fitness, is determined by the additive genetic variance in individual relative fitness. To date, there are few robust estimates of this parameter for natural populations, and it is therefore unclear whether adaptive evolution can play a meaningful role in short-term population dynamics. We developed and applied quantitative genetic methods to long-term datasets from 19 wild bird and mammal populations and found that, while estimates vary between populations, additive genetic variance in relative fitness is often substantial and, on average, twice that of previous estimates. We show that these rates of contemporary adaptive evolution can affect population dynamics and hence that natural selection has the potential to partly mitigate effects of current environmental change.

How full is the evolutionary fuel tank?

A meta-analysis quantifies the heritable genetic variance in fitness-the fuel of evolution.

Environmental variation and biotic interactions limit adaptation at ecological margins: lessons from rainforest Drosophila and European butterflies.

Models of local adaptation to spatially varying selection predict that maximum rates of evolution are determined by the interaction between increased adaptive potential owing to increased genetic variation, and the cost genetic variation brings by reducing population fitness. We discuss existing and new results from our laboratory assays and field transplants of rainforest Drosophila and UK butterflies along environmental gradients, which try to test these predictions in natural populations. Our data suggest that: (i) local adaptation along ecological gradients is not consistently observed in time and space, especially where biotic and abiotic interactions affect both gradient steepness and genetic variation in fitness; (ii) genetic variation in fitness observed in the laboratory is only sometimes visible to selection in the field, suggesting that demographic costs can remain high without increasing adaptive potential; and (iii) antagonistic interactions between species reduce local productivity, especially at ecological margins. Such antagonistic interactions steepen gradients and may increase the cost of adaptation by increasing its dimensionality. However, where biotic interactions do evolve, rapid range expansion can follow. Future research should test how the environmental sensitivity of genotypes determines their ecological exposure, and its effects on genetic variation in fitness, to predict the probability of evolutionary rescue at ecological margins. This article is part of the theme issue 'Species' ranges in the face of changing environments (Part II)'.

Maternal-Offspring Interactions: Reciprocally Coevolving Social Environments.

Maternal-zygotic co-evolution is one of the most common examples of indirect genetic effects. I investigate how maternal-zygotic gene interactions affect rates of evolution and adaptation. Using comparably parameterized population genetic models, I compare evolution to an abiotic environment with genotype-by-environment interaction (G × E) to evolution to a maternal environment with offspring genotype-by-maternal environment interaction (G × Gmaternal). There are strong parallels between the 2 models in the components of fitness variance but they differ in their rates of evolution measured in terms of ∆p, gene frequency change, or of ∆W, change in mean fitness. The Price Equation is used to partition ∆W into 2 components, one owing to the genetic variance in fitness by natural selection and a second owing to change in environment. Adaptive evolution is faster in the 2-locus model with G × Gmaternal with free recombination, than it is in the 1-locus model with G × E, because in the former the maternal genetic environment coevolves with the zygotic phenotype adapting to it. I discuss the relevance of these findings for the evolution of genes with indirect genetic effects.

Decomposing the sources of SARS-CoV-2 fitness variation in the United States.

The fitness of a pathogen is a composite phenotype determined by many different factors influencing growth rates both within and between hosts. Determining what factors shape fitness at the host population-level is especially challenging because both intrinsic factors like pathogen genetics and extrinsic factors such as host behavior influence between-host transmission potential. This challenge has been highlighted by controversy surrounding the population-level fitness effects of mutations in the SARS-CoV-2 genome and their relative importance when compared against non-genetic factors shaping transmission dynamics. Building upon phylodynamic birth–death models, we develop a new framework to learn how hundreds of genetic and non-genetic factors have shaped the fitness of SARS-CoV-2. We estimate the fitness effects of all amino acid variants and several structural variants that have circulated in the United States between February 2020 and March 2021 from viral phylogenies. We also estimate how much fitness variation among pathogen lineages is attributable to genetic versus non-genetic factors such as spatial heterogeneity in transmission rates. Before September 2020, most fitness variation between lineages can be explained by background spatial heterogeneity in transmission rates across geographic regions. Starting in late 2020, genetic variation in fitness increased dramatically with the emergence of several new lineages including B.1.1.7, B.1.427, B.1.429 and B.1.526. Our analysis also indicates that genetic variants in less well-explored genomic regions outside of Spike may be contributing significantly to overall fitness variation in the viral population.

Selection in males purges the mutation load on female fitness.

Theory predicts that the ability of selection and recombination to purge mutation load is enhanced if selection against deleterious genetic variants operates more strongly in males than females. However, direct empirical support for this tenet is limited, in part because traditional quantitative genetic approaches allow dominance and intermediate‐frequency polymorphisms to obscure the effects of the many rare and partially recessive deleterious alleles that make up the main part of a population's mutation load. Here, we exposed the partially recessive genetic load of a population of Callosobruchus maculatus seed beetles via successive generations of inbreeding, and quantified its effects by measuring heterosis—the increase in fitness experienced when masking the effects of deleterious alleles by heterozygosity—in a fully factorial sex‐specific diallel cross among 16 inbred strains. Competitive lifetime reproductive success (i.e., fitness) was measured in male and female outcrossed F1s as well as inbred parental “selfs,” and we estimated the 4 × 4 male‐female inbred‐outbred genetic covariance matrix for fitness using Bayesian Markov chain Monte Carlo simulations of a custom‐made general linear mixed effects model. We found that heterosis estimated independently in males and females was highly genetically correlated among strains, and that heterosis was strongly negatively genetically correlated to outbred male, but not female, fitness. This suggests that genetic variation for fitness in males, but not in females, reflects the amount of (partially) recessive deleterious alleles segregating at mutation‐selection balance in this population. The population's mutation load therefore has greater potential to be purged via selection in males. These findings contribute to our understanding of the prevalence of sexual reproduction in nature and the maintenance of genetic variation in fitness‐related traits.

Immigration counter-acts local micro-evolution of a major fitness component: Migration-selection balance in free-living song sparrows.

Ongoing adaptive evolution, and resulting “evolutionary rescue” of declining populations, requires additive genetic variation in fitness. Such variation can be increased by gene flow resulting from immigration, potentially facilitating evolution. But, gene flow could in fact constrain rather than facilitate local adaptive evolution if immigrants have low additive genetic values for local fitness. Local migration‐selection balance and micro‐evolutionary stasis could then result. However, key quantitative genetic effects of natural immigration, comprising the degrees to which gene flow increases the total local additive genetic variance yet counteracts local adaptive evolutionary change, have not been explicitly quantified in wild populations. Key implications of gene flow for population and evolutionary dynamics consequently remain unclear. Our quantitative genetic analyses of long‐term data from free‐living song sparrows (Melospiza melodia) show that mean breeding value for local juvenile survival to adulthood, a major component of fitness, increased across cohorts more than expected solely due to drift. Such micro‐evolutionary change should be expected given nonzero additive genetic variance and consistent directional selection. However, this evolutionary increase was counteracted by negative additive genetic effects of recent immigrants, which increased total additive genetic variance but prevented a net directional evolutionary increase in total additive genetic value. These analyses imply an approximate quantitative genetic migration‐selection balance in a major fitness component, and hence demonstrate a key mechanism by which substantial additive genetic variation can be maintained yet decoupled from local adaptive evolutionary change.

A simple completion of Fisher's fundamental theorem of natural selection.

Fisher's fundamental theorem of natural selection shows that the part of the rate of change of mean fitness that is due to natural selection equals the additive genetic variance in fitness. Fisher embedded this result in a model of total fitness, adding terms for deterioration of the environment and density dependence. Here, a quantitative genetic version of this neglected model is derived that relaxes its assumptions that the additive genetic variance in fitness and the rate of deterioration of the environment do not change over time, allows population size to vary, and includes an input of mutational variance. The resulting formula for total rate of change in mean fitness contains two terms more than Fisher's original, representing the effects of stabilizing selection, on the one hand, and of mutational variance, on the other, making clear for the first time that the fundamental theorem deals only with natural selection that is directional (as opposed to stabilizing) on the underlying traits. In this model, the total (rather than just the additive) genetic variance increases mean fitness. The unstructured population allows an explanation of Fisher's concept of fitness as simply birth rate minus mortality rate, and building up to the definition in structured populations.

Genetic variance in fitness and its cross-sex covariance predict adaptation during experimental evolution.

The additive genetic variation (VA ) of fitness in a population is of particular importance to quantify its adaptive potential and predict its response to rapid environmental change. Recent statistical advances in quantitative genetics and the use of new molecular tools have fostered great interest in estimating fitness VA in wild populations. However, the value of VA for fitness in predicting evolutionary changes over several generations remains mostly unknown. In our study, we addressed this question by combining classical quantitative genetics with experimental evolution in the model organism Tribolium castaneum (red flour beetle) in three new environmental conditions (Dry, Hot, Hot-Dry). We tested for potential constraints that might limit adaptation, including environmental and sex genetic antagonisms captured by negative genetic covariance between environments and female and male fitness, respectively. Observed fitness changes after 20 generations mainly matched our predictions. Given that body size is commonly used as a proxy for fitness, we also tested how this trait and its genetic variance (including nonadditive genetic variance) were impacted by environmental stress. In both traits, genetic variances were sex and condition dependent, but they differed in their variance composition, cross-sex and cross-environment genetic covariances, as well as in the environmental impact on VA .

Genetic variation among and within Quercus suber L. populations in survival, growth, vigor and plant architecture traits

Cork oak is an important forest tree species in the Western Mediterranean region due to the high economic value of its renewable cork and its ecological and social services. However, studies regarding the genetic variation within cork oak populations are scarce, and this gap of knowledge is contributing to the delay of the set-up of a breeding and conservation strategy for the species. In this study, the genetic variation in fitness (survival, height, and stem diameter) and plant architecture traits (apical dominance, stem straightness, stem inclination degree, branchiness), and tree vigor was evaluated among and within cork oak populations in two progeny field trials established in Portugal. Measurements were carried out in each trial in two different periods: ages 9 and 14 years at Monte da Fava trial and 8 and 14 years at Herdade da Caniceira trial. A significant genetic variation among and within cork oak populations was detected for survival, growth, and form traits (stem straightness and inclination). Growth traits presented high values of heritability estimates at the family mean level (≥0.75), and genetic gains were obtained when families with superior growth were selected. Additionally, results highlighted that early selection of families with superior performance could be performed, and it is possible to achieve improvement in both growth and form traits simultaneously, with implications on the profitability and sustainability of cork oak stands.

How does contemporary selection shape oak phenotypes?

Most existing forests are subjected to natural and human‐mediated selection pressures, which have increased due to climate change and the increasing needs of human societies for wood, fibre and fuel resources. It remains largely unknown how these pressures trigger evolutionary changes. We address this issue here for temperate European oaks (Quercus petraea and Q. robur), which grow in mixed stands, under even‐aged management regimes. We screened numerous functional traits for univariate selection gradients and for expected and observed genetic changes over two successive generations. In both species, growth, leaf morphology and physiology, and defence‐related traits displayed significant selection gradients and predicted shifts, whereas phenology, water metabolism, structure and resilience‐related traits did not. However, the direction of the selection response and the potential for adaptive evolution differed between the two species. Quercus petraea had a much larger phenotypic and genetic variance of fitness than Q. robur. This difference raises concerns about the adaptive response of Q. robur to contemporary selection pressures. Our investigations suggest that Q. robur will probably decline steadily, particularly in mixed stands with Q. petraea, consistent with the contrasting demographic dynamics of the two species.

Experimental evidence for effects of sexual selection on condition-dependent mutation rates.

Sexual selection depletes genetic variation but depleted genetic variation limits the efficacy of sexual selection-a long-standing enigma known as the lek paradox. Here we offer a twist to this paradox by showing that sexual selection and the generation of new genetic variation via mutation may be entangled in an evolutionary feedback loop. We induced DNA damage in the germline of male seed beetles evolved under regimes manipulating the opportunity for natural and sexual selection, and quantified de novo mutations in F2-F7 generations by measuring mutation load. Sexually selected males passed on smaller loads, suggesting that selection for male quality not only purges segregating deleterious alleles, but can also reduce the rate at which such alleles originate de novo. However, when engaging in socio-sexual interactions, males evolved exclusively under sexual selection transferred greater loads, suggesting that trade-offs between naturally and sexually selected fitness components can increase mutation rate. These results offer causality to the widely observed male mutation bias and have implications for the maintenance of genetic variation in fitness.

Estimation of Genetic Variance in Fitness, and Inference of Adaptation, When Fitness Follows a Log-Normal Distribution.

Additive genetic variance in relative fitness (σA2(w)) is arguably the most important evolutionary parameter in a population because, by Fisher's fundamental theorem of natural selection (FTNS; Fisher RA. 1930. The genetical theory of natural selection. 1st ed. Oxford: Clarendon Press), it represents the rate of adaptive evolution. However, to date, there are few estimates of σA2(w) in natural populations. Moreover, most of the available estimates rely on Gaussian assumptions inappropriate for fitness data, with unclear consequences. "Generalized linear animal models" (GLAMs) tend to be more appropriate for fitness data, but they estimate parameters on a transformed ("latent") scale that is not directly interpretable for inferences on the data scale. Here we exploit the latest theoretical developments to clarify how best to estimate quantitative genetic parameters for fitness. Specifically, we use computer simulations to confirm a recently developed analog of the FTNS in the case when expected fitness follows a log-normal distribution. In this situation, the additive genetic variance in absolute fitness on the latent log-scale (σA2(l)) equals (σA2(w)) on the data scale, which is the rate of adaptation within a generation. However, due to inheritance distortion, the change in mean relative fitness between generations exceeds σA2(l) and equals (exp⁡(σA2(l))-1). We illustrate why the heritability of fitness is generally low and is not a good measure of the rate of adaptation. Finally, we explore how well the relevant parameters can be estimated by animal models, comparing Gaussian models with Poisson GLAMs. Our results illustrate 1) the correspondence between quantitative genetics and population dynamics encapsulated in the FTNS and its log-normal-analog and 2) the appropriate interpretation of GLAM parameter estimates.

The left-hand side of the Fundamental Theorem of Natural Selection: A reply

In a recent paper, Grafen (2018) discussed the left-hand side in the equation stating Fisher’s (1930, 1958) “Fundamental Theorem of Natural Selection” (FTNS). Fisher’s original statement of the FTNS is, in effect, “The rate of increase in fitness of any organism is equal to its genetic variance in fitness at that time” with the rate of increase in fitness understood as the one “due to all changes in gene ratios” (Fisher, 1930, p. 35). For purposes of exposition, Grafen (2018) considered what is today called the analogous discrete-time model, and restated the FTNS on p. 181 as “The increase in population [mean fitness] due to changes in gene frequencies [is equal to the] additive genetic variance in fitness [divided by the] mean fitness”. Allowing for the fact that Grafen’s statement of the FTNS relates to a discrete-time model, his statement is in effect a discrete-time version of Fisher’s. It has however been widely accepted for many years, ever since Price’s (1972) deep analysis of the FTNS, that Fisher’s wording does not correctly describe the content of the FTNS. The same is therefore true of Grafen’s statement. The confusion caused by these misstatements is unfortunate and adds to a continuing misunderstanding of the FTNS, whose source can also be found in Fisher’s (1941) own explanation. Our purpose is to review the detailed analysis of the calculations leading to the FTNS to clarify the points at issue.

Indirect genetic effects clarify how traits can evolve even when fitness does not

AbstractThere are many situations in nature where we expect traits to evolve but not necessarily for mean fitness to increase. However, these scenarios are hard to reconcile simultaneously with Fisher's fundamental theorem of natural selection (FTNS) and the Price identity (PI). The consideration of indirect genetic effects (IGEs) on fitness reconciles these fundamental theorems with the observation that traits sometimes evolve without any adaptation by explicitly considering the correlated evolution of the social environment, which is a form of transmission bias. Although environmental change is often assumed to be absent when using the PI, here we show that explicitly considering IGEs as change in the social environment with implications for fitness has several benefits: (1) it makes clear how traits can evolve while mean fitness remains stationary, (2) it reconciles the FTNS with the evolution of maladaptation, (3) it explicitly includes density-dependent fitness through negative social effects that depend on the number of interacting conspecifics, and (4) it allows mean fitness to evolve even when direct genetic variance in fitness is zero, if related individuals interact and/or if there is multilevel selection. In summary, considering fitness in the context of IGEs aligns important theorems of natural selection with many situations observed in nature and provides a useful lens through which we might better understand evolution and adaptation.