Heritable Fitness Research Articles

The heritability of fitness in a wild annual plant population with hierarchical size structure.

The relative magnitude of additive genetic vs. residual variation for fitness traits is important in models for predicting the rate of evolution and population persistence in response to changes in the environment. In many annual plants, lifetime reproductive fitness is correlated with end-of-season plant biomass, which can vary significantly from plant to plant in the same population. We measured end-of-season plant biomasses and obtained single nucleotide polymorphism (SNP) genotypes of plants in a dense, natural population of the annual plant species Impatiens capensis with hierarchical size structure. These data were used to estimate the amount of heritable variation for position in the size hierarchy and for plant biomass. Additive genetic variance for a position in the size hierarchy and plant biomass were both significantly different from zero. These results are discussed in relationship to the theory for the heritability of fitness in natural populations and ecological factors that potentially influence heritable variation for fitness in this species.

Macroecological predictors of evolutionary and plastic potential do not apply at microgeographic scales for a freshwater cladoceran under climate change.

Rapid evolutionary adaptation could reduce the negative impacts of climate change if sufficient heritability of key traits exists under future climate conditions. Plastic responses to climate change could also reduce negative impacts. Understanding which populations are likely to respond via evolution or plasticity could therefore improve estimates of extinction risk. A large body of research suggests that the evolutionary and plastic potential of a population can be predicted by the degree of spatial and temporal climatic variation it experiences. However, we know little about the scale at which these relationships apply. Here, we test if spatial and temporal variation in temperature affects genetic variation and plasticity of fitness and a key thermal tolerance trait (critical thermal maximum; CTmax) at microgeographic scales using a metapopulation of Daphnia magna in freshwater rock pools. Specifically, we ask if (a) there is a microgeographic adaptation of CTmax and fitness to differences in temperature among the pools, (b) pools with greater temporal temperature variation have more genetic variation or plasticity in CTmax or fitness, and (c) increases in temperature affect the heritability of CTmax and fitness. Although we observed genetic variation and plasticity in CTmax and fitness, and differences in fitness among pools, we did not find support for the predicted relationships between temperature variation and genetic variation or plasticity. Furthermore, the genetic variation and plasticity we observed in CTmax are unlikely sufficient to reduce the impacts of climate change. CTmax plasticity was minimal and heritability was 72% lower when D. magna developed at the higher temperatures predicted under climate change. In contrast, the heritability of fitness increased by 53% under warmer temperatures, suggesting an increase in overall evolutionary potential unrelated to CTmax under climate change. More research is needed to understand the evolutionary and plastic potential under climate change and how that potential will be altered in future climates.

Perceptions of inferred parental ability through sexually dimorphic facial features

AbstractIn addition to providing robust cues diagnostic of prospective mates' heritable fitness, various physical features could be similarly utilized in inferring individuals' parental abilities. This study sought to explore how variations in sexually dimorphic facial features inform perceptions of social targets as motivated to provide parental care. American undergraduates (N = 244) viewed a series of 12 total male and female faces manipulated at varying degrees of sex‐typicality (i.e., masculinized versus feminized versus unaltered controls) on a within‐subjects basis, and rated the perceived motivation of each target to nurture and protect a child using items derived from the Parental Care and Tenderness Scale. Female targets were perceived as more motivated by parental care than male targets, F(1, 240) = 14.86, p < .001, ηp2 = 0.058, whereas male targets were perceived as specifically motivated to protect offspring, F(1, 240) = 177.32, p < .001, ηp2 = 0.425. Feminized targets were additionally perceived as more motivated by nurturance, though such inferences were apparent for both male and female targets, F(1, 240) = 7.36, p < .001, ηp2 = 0.058. Findings represent an understanding of perceivers use of functional heuristics of sexual dimorphism in identifying optimal parents.

Transcriptomic analysis provides insights into molecular mechanisms of thermal physiology

Physiological trait variation underlies health, responses to global climate change, and ecological performance. Yet, most physiological traits are complex, and we have little understanding of the genes and genomic architectures that define their variation. To provide insight into the genetic architecture of physiological processes, we related physiological traits to heart and brain mRNA expression using a weighted gene co-expression network analysis. mRNA expression was used to explain variation in six physiological traits (whole animal metabolism (WAM), critical thermal maximum (CTmax), and four substrate specific cardiac metabolic rates (CaM)) under 12 °C and 28 °C acclimation conditions. Notably, the physiological trait variations among the three geographically close (within 15 km) and genetically similar F. heteroclitus populations are similar to those found among 77 aquatic species spanning 15–20° of latitude (~ 2,000 km). These large physiological trait variations among genetically similar individuals provide a powerful approach to determine the relationship between mRNA expression and heritable fitness related traits unconfounded by interspecific differences. Expression patterns explained up to 82% of metabolic trait variation and were enriched for multiple signaling pathways known to impact metabolic and thermal tolerance (e.g., AMPK, PPAR, mTOR, FoxO, and MAPK) but also contained several unexpected pathways (e.g., apoptosis, cellular senescence), suggesting that physiological trait variation is affected by many diverse genes.

Environmental and genetic influences on fitness-related traits in a hatchery coho salmon population

Many natural and managed organisms will require substantial functional genetic variation to respond to selection in the face of rapid environmental change. Pacific salmon have experienced strong fluctuations in critical fitness traits over the past five decades. We examined genetic and phenotypic variability over three generations in a pedigreed hatchery population of coho salmon (Oncorhynchus kisutch) by monitoring seven fitness-related traits. Three-year-old adult return numbers varied more than fivefold, and jack (2-year-old males) numbers varied 13-fold. Body sizes of Inch Creek coho salmon decreased consistently such that fish were only 40.7% as heavy in 2015 as in 2006, and female reproductive traits also decreased. During the study period, the majority of families produced returning adult progeny, and effective population size was relatively constant. Heritability estimates for phenotypic traits were significantly greater than zero except for condition factor, and the estimated heritability for jacking was 0.42. The Inch Creek coho salmon population harbours substantial heritability for fitness and reproductive traits and thus likely retains substantial capacity for adaptation despite many years of hatchery propagation.

Estimating the genome-wide contribution of selection to temporal allele frequency change

Rapid phenotypic adaptation is often observed in natural populations and selection experiments. However, detecting the genome-wide impact of this selection is difficult since adaptation often proceeds from standing variation and selection on polygenic traits, both of which may leave faint genomic signals indistinguishable from a noisy background of genetic drift. One promising signal comes from the genome-wide covariance between allele frequency changes observable from temporal genomic data (e.g., evolve-and-resequence studies). These temporal covariances reflect how heritable fitness variation in the population leads changes in allele frequencies at one time point to be predictive of the changes at later time points, as alleles are indirectly selected due to remaining associations with selected alleles. Since genetic drift does not lead to temporal covariance, we can use these covariances to estimate what fraction of the variation in allele frequency change through time is driven by linked selection. Here, we reanalyze three selection experiments to quantify the effects of linked selection over short timescales using covariance among time points and across replicates. We estimate that at least 17 to 37% of allele frequency change is driven by selection in these experiments. Against this background of positive genome-wide temporal covariances, we also identify signals of negative temporal covariance corresponding to reversals in the direction of selection for a reasonable proportion of loci over the time course of a selection experiment. Overall, we find that in the three studies we analyzed, linked selection has a large impact on short-term allele frequency dynamics that is readily distinguishable from genetic drift.

Dad and Mom Bods? Inferences of Parenting Ability from Bodily Cues

Though much research has explored how facial and bodily features connote heritable fitness, particularly in the context of short-term mating, such cues similarly may influence perceptions of potential parenting ability. The current study explored how body fat variation and breast size in female targets and body fat and muscularity variation in male targets influence men’s and women’s perceptions of targets’ positive (e.g., nurturance) and negative (e.g., hostility) parenting capacities. Participants viewed 4 female targets orthogonally manipulated along dimensions of adiposity (high vs. low) and breast size (small vs. large), and 4 male targets orthogonally manipulated along similar adiposity dimensions and muscularity (small vs. large) before indicating targets’ inferred parenting ability. High-fat female targets were perceived to have more positive and less negative parenting abilities relative to low-fat female targets, an effect that was most pronounced among women; breast size did not influence perceptions of female parenting ability. For male targets, high fat and small muscles were perceived as more indicative of positive parenting abilities and less indicative toward negative abilities; the low body fat/high muscle male target was perceived to have especially negative parenting abilities. These results suggest body cues often associated with good genes and short-term mating success also systematically influence perceptions of parenting ability.

No evidence for an association between facial fluctuating asymmetry and vocal attractiveness in men and women

Facial fluctuating asymmetry (FA), presumably a proxy measure of developmental instability, has been proposed to inversely relate to vocal attractiveness, which may convey information on heritable fitness benefits. Using an improved method of measuring facial FA, we sought to replicate two recent studies that showed an inverse correlation of facial FA with vocal attractiveness. In two samples of men (N = 165) and women (N = 157), we investigated the association of automatically measured facial FA based on 3D face scans with male and female observer-rated attractiveness of voice recordings. No significant associations were found for men or women, also when controlling for facial attractiveness, age, and body mass index. Equivalence tests show that effect sizes were significantly smaller than previous meta-analytic effects, providing robust evidence against a link of facial FA with vocal attractiveness. Thus, our study contradicts earlier findings that vocal attractiveness may signal genetic quality in humans via an association with FA.

No evidence for an association between facial fluctuating asymmetry and vocal attractiveness in men or women.

Facial fluctuating asymmetry (FA), presumably a proxy measure of developmental instability, has been proposed to inversely relate to vocal attractiveness, which may convey information on heritable fitness benefits. Using an improved method of measuring facial FA, we sought to replicate two recent studies that showed an inverse correlation of facial FA with vocal attractiveness. In two samples of men (N = 165) and women (N = 157), we investigated the association of automatically measured facial FA based on 3D face scans with male and female observer-rated attractiveness of voice recordings. No significant associations were found for men or women, also when controlling for facial attractiveness, age, and body mass index. Equivalence tests show that effect sizes were significantly smaller than previous meta-analytic effects, providing robust evidence against a link of facial FA with vocal attractiveness. Thus, our study contradicts earlier findings that vocal attractiveness may signal genetic quality in humans via an association with FA.

Low adaptive potential for tolerance to ethynylestradiol, but also low toxicity, in a grayling population (Thymallus thymallus)

BackgroundThe presence of a novel pollutant can induce rapid evolution if there is additive genetic variance for the tolerance to the stressor. Continuous selection over some generations can then reduce the toxicity of the pollutant but also deplete the additive genetic variance for the tolerance and thereby slow down adaptation. One common pollutant that has been ecologically relevant for some time is 17alpha-ethynylestradiol (EE2), a synthetic compound of oral contraceptives since their market launch in the 1960s. EE2 is typically found in higher concentrations in rivers than in lakes. Recent experimental work revealed significant genetic variance for the tolerance to EE2 in two lake-spawning salmonid species but no such variance in river-spawning brown trout. We used another river-spawning salmonid, the European grayling Thymallus thymallus, to study the toxicity of an ecologically relevant concentration of EE2. We also used a full-factorial in vitro breeding design and singly rearing of 1555 embryos and larvae of 40 sib groups to test whether there is additive genetic variance for the tolerance to this pollutant.ResultsWe found that exposure to EE2 reduced larval growth after hatching, but contrary to what has been found in the other salmonids, there were no significant effects of EE2 on embryo growth and survival. We found additive genetic variance for embryo viability, i.e. heritability for fitness. However, there was no significant additive variance for the tolerance to EE2.ConclusionsOur findings support the hypothesis that continuous selection has reduced the toxicity of EE2 and depleted genetic variance for tolerance to this synthetic stressor.

The Linked Selection Signature of Rapid Adaptation in Temporal Genomic Data.

The majority of empirical population genetic studies have tried to understand the evolutionary processes that have shaped genetic variation in a single sample taken from a present-day population. However, genomic data collected over tens of generations in both natural and laboratory populations are increasingly used to find selected loci underpinning adaptation over these short timescales. Although these studies have been quite successful in detecting selection on large-effect loci, the fitness differences between individuals are often polygenic, such that selection leads to allele frequency changes that are difficult to distinguish from genetic drift. However, one promising signal comes from polygenic selection's effect on neutral sites that become stochastically associated with the genetic backgrounds that lead to fitness differences between individuals. Previous theoretical work has established that the random associations between a neutral allele and heritable fitness backgrounds act to reduce the effective population size experienced by this neutral allele. These associations perturb neutral allele frequency trajectories, creating autocovariance in the allele frequency changes across generations. Here, we show how temporal genomic data allow us to measure the temporal autocovariance in allele frequency changes and characterize the genome-wide impact of polygenic selection. We develop expressions for these temporal autocovariances, showing that their magnitude is determined by the level of additive genetic variation, recombination, and linkage disequilibria in a region. Furthermore, by using analytic expressions for the temporal variances and autocovariances in allele frequency, we demonstrate that one can estimate the additive genetic variation for fitness and the drift-effective population size from temporal genomic data. We also show how the proportion of total variation in allele frequency change due to linked selection can be estimated from temporal data. Overall, we demonstrate that temporal genomic data offer opportunities to identify the role of linked selection on genome-wide diversity over short timescales, and can help bridge population genetic and quantitative genetic studies of adaptation.

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.

Genome-wide sexually antagonistic variants reveal long-standing constraints on sexual dimorphism in fruit flies.

The evolution of sexual dimorphism is constrained by a shared genome, leading to ‘sexual antagonism’, in which different alleles at given loci are favoured by selection in males and females. Despite its wide taxonomic incidence, we know little about the identity, genomic location, and evolutionary dynamics of antagonistic genetic variants. To address these deficits, we use sex-specific fitness data from 202 fully sequenced hemiclonal Drosophila melanogaster fly lines to perform a genome-wide association study (GWAS) of sexual antagonism. We identify approximately 230 chromosomal clusters of candidate antagonistic single nucleotide polymorphisms (SNPs). In contradiction to classic theory, we find no clear evidence that the X chromosome is a hot spot for sexually antagonistic variation. Characterising antagonistic SNPs functionally, we find a large excess of missense variants but little enrichment in terms of gene function. We also assess the evolutionary persistence of antagonistic variants by examining extant polymorphism in wild D. melanogaster populations and closely related species. Remarkably, antagonistic variants are associated with multiple signatures of balancing selection across the D. melanogaster distribution range and in their sister species D. simulans, indicating widespread and evolutionarily persistent (about 1 million years) genomic constraints on the evolution of sexual dimorphism. Based on our results, we propose that antagonistic variation accumulates because of constraints on the resolution of sexual conflict over protein coding sequences, thus contributing to the long-term maintenance of heritable fitness variation.

Evolutionary design of regulatory control. II. Robust error-correcting feedback increases genetic and phenotypic variability

As systems become more robust against perturbations, they can compensate for greater sloppiness in the performance of their components. That robust compensation reduces the force of natural selection on the system’s components, leading to component decay. The paradoxical coupling of robustness and decay predicts that robust systems evolve cheaper, lower performing components, which accumulate greater mutational genetic variability and which have greater phenotypic stochasticity in trait expression. Previous work noted the paradox of robustness. However, no general theory for the evolutionary dynamics of system robustness and component decay has been developed. This article takes a first step by linking engineering control theory with the genetic theory of evolutionary dynamics. Control theory emphasizes error-correcting feedback as the single greatest principle in robust system design. Linking control theory to evolution leads to a theory for the evolutionary dynamics of error-correcting feedback, a unifying approach for the evolutionary analysis of robust systems. This article shows how increasingly robust systems accumulate more genetic variability and greater stochasticity of expression in their components. The theory predicts different levels of variability between different regulatory control architectures and different levels of variability between different components within a particular regulatory control system. The theory also shows that increasing robustness reduces the frequency of system failures associated with disease and, simultaneously, causes a strong increase in the heritability of disease. Thus, robust error correction in biological regulatory control may partly explain the puzzlingly high heritability of disease and, more generally, the surprisingly high heritability of fitness.

Epigenetic paternal effects as costly, condition-dependent traits.

It is now recognized that post-copulatory traits, such as sperm and ejaculate production can impose metabolic costs, and such traits are therefore expected to exhibit condition-dependent expression, whereby, low condition individuals experience a greater marginal cost of investment compared to high condition individuals. Ejaculates are especially costly in species where males invest in offspring quality through nutrient-rich spermatophores or other seminal nuptial gifts. However, recent evidence shows that, in species where males do not provision females or offspring, males can still influence offspring development through paternal effects mediated by epigenetic factors, such as non-coding RNAs, DNA methylation and chromatin structure. Because such epigenetic paternal effects do not involve the transfer of substantial quantities of resources, such as nutrients, the costs of conferring such effects have not been considered. Here we argue that if selection favours paternal investment in offspring quality through epigenetic factors, then the epigenetic machinery required to bring about such effects may also be expected to evolve strongly condition-dependent expression. We outline indirect evidence suggesting that epigenetic paternal effects could impose substantial metabolic costs, consider the conditions under which selection may act on such effects, and suggest ways to test for differential costs and condition-dependence of these effects. Incorporating epigenetic paternal effects into condition-dependent life history theory will further our understanding of the heritability of fitness and the evolution of paternal investment strategies.

Inherent aerobic capacity-dependent differences in breast carcinogenesis.

Although regular physical activity is associated with improvement in aerobic capacity and lower breast cancer risk, there are heritable sets of traits that affect improvement in aerobic capacity in response to physical activity. Although aerobic capacity segregates risk for a number of chronic diseases, the effect of the heritable component on cancer risk has not been evaluated. Therefore, we investigated breast carcinogenesis in rodent models of heritable fitness in the absence of induced physical activity. Female offspring of N:NIH rats selectively bred for low (LIAC) or high (HIAC) inherent aerobic capacity were injected intraperitoneally with 1-methyl-1-nitrosurea (70 mg/kg body wt). At study termination 33 weeks post-carcinogen, cancer incidence (14.0 versus 47.3%; P < 0.001) and multiplicity (0.18 versus 0.85 cancers per rat; P < 0.0001) were significantly decreased in HIAC versus LIAC rats, respectively. HIAC had smaller visceral and subcutaneous body fat depots than LIAC and activity of two proteins that regulated the mammalian target of rapamycin, protein kinase B (Akt), and adenosine monophosphate-activated protein kinase were suppressed and activated, respectively, in HIAC. Although many factors distinguish between HIAC and LIAC, it appears that the protective effect of HIAC against breast carcinogenesis is mediated, at least in part, via alterations in core metabolic signaling pathways deregulated in the majority of human breast cancers.

Measuring fitness heritability: Life history traits versus morphological traits in humans.

Traditional interpretation of Fisher's Fundamental Theorem of Natural Selection is that life history traits (LHT), which are closely related with fitness, show lower heritabilities, whereas morphological traits (MT) are less related with fitness and they are expected to show higher heritabilities. In humans, although few studies have examined the heritability of LHT and MT, none of them have analyzed the same sample for comparative purposes. Here we assessed, for the first time, the heritability, additive genetic variance (VA ), residual variance (VR ) and coefficient of genetic additive variation (CVA ) values of LHT and MT in a singular collection of identified skulls with associated demographic records from Hallstatt (Austria). LHT, such as lifespan, number of offspring, age at birth of first and last child, reproductive span, and lifetime reproductive success, were estimated from 18,134 individuals from the Hallstatt Catholic parish records, which represent seven generations and correspond to a time span of 400 years. MT were assessed through 17 craniofacial indices and 7 angles obtained from 355 adult crania from the same population. Heritability, VA , VR , and CVA values of LHT and MT were calculated using restricted maximum likelihood methods. LHT heritabilities ranged from 2.3 to 34% for the whole sample, with men showing higher heritabilities (4-45%) than women (0-23.7%). Overall, MT presented higher heritability values than most of LHT, ranging from 0 to 40.5% in craniofacial indices, and from 13.8 to 32.4% in craniofacial angles. LHT showed considerable additive genetic variance values, similar to MT, but also high environmental variance values, and most of them presenting a higher evolutionary potential than MT. Our results demonstrate that, with the exception of lifespan, LHT show lower heritability values, than MT. The lower heritability of LHT is explained by a higher influence of environmental and cultural factors.

The (De-)evolution of Evolution Games: A Content Analysis of the Representation of Evolution Through Natural Selection in Digital Games

Given the diversity and complexity of education game mechanisms and topics, this article contributes to a theoretical understanding of how game mechanisms “map” to educational topics through inquiry-based learning. Namely, the article examines the presence of evolution through natural selection (ENS) in digital games. ENS is a fundamentally important and widely misunderstood theory. This analysis of ENS portrayal in digital games provides insight into the use of games in teaching ENS. Systematic database search results were coded for the three principles of ENS: phenotypic variation, differential fitness, and fitness heritability. Though thousands of games use the term evolution, few presented elements of evolution, and even fewer contained all principles of ENS. Games developed to specifically teach evolution were difficult to find through Web searches. These overall deficiencies in ENS games reflect the inherent incompatibility between game control elements and the automatic process of ENS.

Social niche construction and evolutionary transitions in individuality.

Social evolution theory conventionally takes an externalist explanatory stance, treating observed cooperation as explanandum and the positive assortment of cooperative behaviour as explanans. We ask how the circumstances bringing about this positive assortment arose in the first place. Rather than merely push the explanatory problem back a step, we move from an externalist to an interactionist explanatory stance, in the spirit of Lewontin and the Niche Construction theorists. We develop a theory of ‘social niche construction’ in which we consider biological entities to be both the subject and object of their own social evolution. Some important cases of the evolution of cooperation have the side-effect of causing changes in the hierarchical level at which the evolutionary process acts. This is because the traits (e.g. life-history bottlenecks) that act to align the fitness interests of particles (e.g. cells) in a collective can also act to diminish the extent to which those particles are bearers of heritable fitness variance, while augmenting the extent to which collectives of such particles (e.g. multicellular organisms) are bearers of heritable fitness variance. In this way, we can explain upward transitions in the hierarchical level at which the Darwinian machine operates in terms of particle-level selection, even though the outcome of the process is a collective-level selection regime. Our theory avoids the logical and metaphysical paradoxes faced by other attempts to explain evolutionary transitions.

Height and Body Mass on the Mating Market

People with traits that are attractive on the mating market are better able to pursue their preferred mating strategy. Men who are relatively tall may be preferred by women because taller height is a cue to dominance, social status, access to resources, and heritable fitness, leading them to have more mating opportunities and sex partners. We examined height, education, age, ethnicity, and body mass index (BMI) as predictors of sexual history among heterosexual men and women ( N = 60,058). The linear and curvilinear associations between self-reported height and sex partner number were small for men when controlling for education, BMI, and ethnicity (linear β = .05; curvilinear β = −.03). The mean and median number of sex partners for men of different heights were: very short (9.4; 5), short (11.0; 7), average (11.7; 7), tall (12.0; 7), very tall (12.1; 7), and extremely tall (12.3; 7). Men who were “overweight” reported a higher mean and median number of sex partners than men with other body masses. The results for men suggested limited variation in reported sex partner number across most of the height continuum, but that very short men report fewer partners than other men.