EXPRESSION OF GENETIC VARIATION IN BODY SIZE OF THE COLLARED FLYCATCHER UNDER DIFFERENT ENVIRONMENTAL CONDITIONS

Heritability of body size in two experimentally created environments, representing good and poor feeding conditions, respectively, was estimated using cross-fostered collared flycatcher Ficedula albicollis nestlings. Young raised under poor feeding conditions attained smaller body size (tarsus length) than their full-sibs raised under good feeding conditions. Parent-offspring regressions revealed lower heritability (h²) of body size under poor than under good feeding conditions. Hence, as the same set of parents were used in the estimation of h² in both environments, this suggests environment-dependent change in additive genetic component of variance (V_A), or that the genetic correlation between parental and poor offspring environment was less than that between parental and good offspring environment. However, full-sib analyses failed to find evidence for genotype-environment interactions, although the power of these tests might have been low. Full-sib heritabilities in both environments tended to be higher than estimates from parent-offspring regressions, indicating that prehatching or early posthatching common environment/maternal effects might have inflated full-sib estimates of V_A. The effect of sibling competition on estimates of V_A was probably small as the nestling size-hierarchy at day 2 posthatch was not generally correlated with size-hierarchy at fledging. Furthermore, there was no correlation between maternal body condition during the incubation and final size of offspring, indicating that direct maternal effects related to nutritional status were small. A review of earlier quantitative genetic studies of body size variation in birds revealed that in eight of nine cases, heritability of body size was lower in poor than in good environmental conditions. The main implication of this relationship will be a decreased evolutionary response to selection under poor environmental conditions. On the other hand, this will retard the loss of genetic variation by reducing the accuracy of selection and might help explain the moderate to high heritabilities of body-size traits under good environmental conditions.     

GENOTYPE-BY-ENVIRONMENT INTERACTIONS IN THE DETERMINATION OF THE SIZE OF A SECONDARY SEXUAL CHARACTER IN THE COLLARED FLYCATCHER (FICEDULA ALBICOLLIS)

Although genetic variation in characters closely related to fitness is expected to either become depleted by selection or masked by environmental variation, “good gene” models of sexual selection require moderate to high heritabilities of secondary sexual characters to explain the occurrence of costly female mate preferences. In this study, I investigated whether the estimated heritability of a condition-dependent secondary sexual character (i.e., the white forehead badge) in the collared flycatcher varied depending on environmental conditions experienced during offspring growth. The data were collected over a period of 14 years making it possible to exploit natural variation in natal conditions. In addition, natal conditions were experimentally altered through brood size manipulations. During unfavorable conditions caused by generally poor weather or experimentally enlarged brood size, no significant heritability based on father-sons regressions could be demonstrated (0.19 ? h² ? 0.27). In contrast, sons reared during years with favorable weather or in experimentally reduced broods significantly resembled their fathers (0.44 ? h² ? 0.65). In addition, the heritability estimates declined with increasing maternal age. The strong effect of natal environmental condition on the estimated heritability of forehead badge size suggests that the potential genetic benefit from mate choice vary according to environmental conditions (e.g., the benefit is reduced during unfavorable rearing conditions). Because sons reared during poor conditions have probably experienced a natal environment different from that experienced by their fathers, the low heritability estimates obtained under poor conditions seem to be caused by low additive genetic variation expressed in such environments and/or a low genetic correlation between the expression of the trait in the two different environments (i.e., good vs. bad). Both of these explanations imply the presence of genotype-by-environment interactions. If such interactions frequently affect the expression of secondary sexual characters, this may offer an explanation of the high heritabilites sometimes reported for such traits, despite their exposure to long-term directional selection.     

Natural selection on the genetical component of variance in body condition in a wild bird population

Although there is substantial evidence that skeletal measures of body size are heritable in wild animal populations, it is frequently assumed that the nonskeletal component of body weight (or ‘condition’) is determined primarily by environmental factors, in particular nutritional state. We tested this assumption by quantifying the genetic and environmental components of variance in fledgling body condition index (=relative body weight) in a natural population of collared flycatchers (Ficedula albicollis), and compared the strength of natural selection on individual breeding values with that on phenotypic values. A mixed model analysis of the components of variance, based on an ‘animal model’ and using 18 years of data on 17 717 nestlings, revealed a significant additive genetic component of variance in body condition, which corresponded to a narrow sense heritability (h²) of 0.30 (SE=0.03). Nongenetic contributions to variation in body condition were large, but there was no evidence of dominance variance nor of contributions from early maternal or common environment effects (pre‐manipulation environment) in condition at fledging. Comparison of pre‐ and post‐selection samples revealed virtually identical h² of body condition index, despite the fact that there was a significant decrease (35%) in the levels of additive genetic variance from fledging to breeding. The similar h² in the two samples occurred because the environmental component of variance was also reduced by selection, suggesting that natural selection was acting on both genotypic and environmental variation. The effects of selection on genetic variance were confirmed by calculation of the selection differentials for both phenotypic values and best linear unbiased predictor (BLUP) estimates of breeding values: there was positive directional selection on condition index both at the phenotypic and the genotypic level. The significant h² of body condition index is consistent with data from human and rodent populations showing significant additive genetic variance in relative body mass and adiposity, but contrasts with the common assumption in ecology that body condition reflects an individual’s nongenetic nutritional state. Furthermore, the substantial reduction in the additive genetic component of variance in body condition index suggests that selection on environmental deviations cannot alone explain the maintenance of additive genetic variation in heritable traits, but that other mechanisms are needed to explain the moderate to high heritabilities of traits under consistent and strong directional selection.     

Autosomal variation for male body size and sperm competition phenotypes is uncorrelated in Drosophila melanogaster

Correlations between male body size and phenotypes impacting post-copulatory sexual selection are commonly observed during the manipulation of male body size by environmental rearing conditions. Here, we control for environmental influences and test for genetic correlations between natural variation in male body size and phenotypes affecting post-copulatory sexual selection in Drosophila melanogaster. Dry weights of virgin males from 90 second-chromosome and 88 third-chromosome substitution lines were measured. Highly significant line effects (p<0.001) documented a genetic basis to variation in male body size. No significant correlations were identified between male body size and the components of sperm competitive ability. These results suggest that natural autosomal variation for male body size has little impact on post-copulatory sexual selection. If genetic correlations exist between male body size and post-copulatory sexual selection then variation in the sex chromosomes are likely candidates, as might be expected if sexually antagonistic coevolution was responsible.     

Evolution in a changing environment: a case study with great tit fledging mass

Heritable phenotypic traits under significant and consistent directional selection often fail to show the expected evolutionary response. A potential explanation for this contradiction is that because environmental conditions change constantly, environmental change can mask an evolutionary response to selection. We combined an "animal model" analysis with 36 years of data from a long-term study of great tits (Parus major) to explore selection on and evolution of a morphological trait: body mass at fledging. We found significant heritability of this trait, but despite consistent positive directional selection on both the phenotypic and the additive genetic component of body mass, the population mean phenotypic value declined rather than increased over time. However, the mean breeding value for body mass at fledging increased over time, presumably in response to selection. We show that the divergence between the response to selection observed at the levels of genotype and phenotype can be explained by a change in environmental conditions over time, that is, related both to increased spring temperature before breeding and elevated population density. Our results support the suggestion that measuring phenotypes may not always give a reliable impression of evolutionary trajectories and that understanding patterns of phenotypic evolution in nature requires an understanding of how the environment has itself changed.     

Genetic variation and causes of genotype-environment interaction in the body size of blue tit (Parus caeruleus).

In several studies of natural populations of birds, the heritability of body size estimated by parent-offspring regression has been lower when offspring have developed in poor feeding regimens than when they developed in good feeding regimens. This has led to the suggestion that adaptation under poor regimens may be constrained by lack of genetic variation. We examined the influence of environmental conditions on expression of genetic variation in body size of nestling blue tits (Parus caeruleus) by raising full sibs in artificially reduced and enlarged broods, corresponding to good and poor feeding regimens, respectively. Individuals grown in the poor regimen attained smaller body size than their sibs grown in the good regimen. However, there was among-family variation in response to the treatments--i.e., genotype-environment interactions (GEIs). Partitioning the GEI variance into contributions attributable to (1) differences in the among-family genetic variance between the treatments and (2) imperfect correlation of genotypic values across treatments identified the latter as the main cause of the GEI. Parent-offspring regressions were not significantly different when offspring were reared in the good environment (h2 = 0.75) vs. when they were reared in the poor environment (h2 = 0.63). Thus, there was little evidence that genetic variance in body size was lower under the poor conditions than under the good conditions. These results do not support the view that the genetic potential for adaptation to poor feeding conditions is less than that for adaptation to good conditions, but they do suggest that different genotypes may be favored under the different conditions.     

Variation in heritability of tadpole growth: an experimental analysis

Heritability characteristically shows large variation between traits, among populations and species, and through time. One of the reasons for this is its dependence on gene frequencies and how these are altered by selection and drift through the evolutionary process. We studied variation in heritability of tadpole growth rate in populations of the Swedish common frog, Rana temporaria. In populations evolving under warmer conditions, we have demonstrated elsewhere that tadpoles show better growth and physiological performance at relatively higher temperatures than tadpoles with an evolutionary history in a relatively cooler part of the distribution range. In the current study, we ask whether this process of divergence under natural selection has influenced the genetic architecture as visualised in estimates of heritability of growth rate at different temperature treatments under laboratory conditions. The results suggest that the additive genetic variance varies between treatments and is highest in a treatment that is common to both populations. Our estimates of narrow sense heritability are generally higher in the thermal regime that dominates in the natural environment. The reason for this appears not primarily to be because the component of additive genetic variation is higher in relation to the total phenotypic variation under these conditions, but because the part of the phenotypic variance explained by environmental variation increases at temperatures to which the current populations has been less frequently under selection.     

Environmentally induced morphological variation in the Barnacle Goose,Branta leucopsis

The environmental conditions to which juvenile barnacle geese (Branta leucopsis) were exposed during growth were found to affect their body size at fledging as well as their final adult body size. Small juveniles showed compensatory growth from the time of fledging up to one year of age, but this did not fully compensate the differences in body size that were established before fledging. The variation in protein content in plants eaten during growth could probably explain the observed body size differences, sometimes of more than 10%, between different categories of adult geese. Our results imply that one cannot infer selection on morphological characters from differences between samples of adult birds from different localities or from different cohorts within a population, without first showing that environmental conditions during growth do not affect the development of the characters under study.     

Inheritance of body size in the Barnacle Goose under different environmental conditions

Heritabilities, genetic variances and covariances for body size traits, i.e. tarsus length, head length and body mass, were estimated under different environmental conditions in a Barnacle Goose (Branta leucopsis) population. Under poor growth conditions, that is, when average body size of fully grown offspring in a given cohort was small, the offspring-parent regressions and full-sib analyses yielded heritability estimates not significantly different from zero. By contrast, when growth conditions were normal or good the heritability estimates were generally significantly positive. Comparisons of genetic covariance estimates indicated that they also differed across the analysed environmental conditions. This result, together with similar results obtained in studies of passerine birds, suggests that genotype-environment interactions might be frequent within the range of environments normally encountered by birds in natural populations. If general, such results might question the validity of assuming approximate constancy of additive genetic variances and covariances over time and environments in evolutionary models.     

Environmental quality and evolutionary potential: lessons from wild populations

An essential requirement to determine a population's potential for evolutionary change is to quantify the amount of genetic variability expressed for traits under selection. Early investigations in laboratory conditions showed that the magnitude of the genetic and environmental components of phenotypic variation can change with environmental conditions. However, there is no consensus as to how the expression of genetic variation is sensitive to different environmental conditions. Recently, the study of quantitative genetics in the wild has been revitalized by new pedigree analyses based on restricted maximum likelihood, resulting in a number of studies investigating these questions in wild populations. Experimental manipulation of environmental quality in the wild, as well as the use of naturally occurring favourable or stressful environments, has broadened the treatment of different taxa and traits. Here, we conduct a meta-analysis on recent studies comparing heritability in favourable versus unfavourable conditions in non-domestic and non-laboratory animals. The results provide evidence for increased heritability in more favourable conditions, significantly so for morphometric traits but not for traits more closely related to fitness. We discuss how these results are explained by underlying changes in variance components, and how they represent a major step in our understanding of evolutionary processes in wild populations. We also show how these trends contrast with the prevailing view resulting mainly from laboratory experiments on Drosophila. Finally, we underline the importance of taking into account the environmental variation in models predicting quantitative trait evolution.     

Adaptive divergence in body size overrides the effects of plasticity across natural habitats in the brown trout

The evolution of life-history traits is characterized by trade-offs between different selection pressures, as well as plasticity across environmental conditions. Yet, studies on local adaptation are often performed under artificial conditions, leaving two issues unexplored: (i) how consistent are laboratory inferred local adaptations under natural conditions and (ii) how much phenotypic variation is attributed to phenotypic plasticity and to adaptive evolution, respectively, across environmental conditions? We reared fish from six locally adapted (domesticated and wild) populations of anadromous brown trout (Salmo trutta) in one semi-natural and three natural streams and recorded a key life-history trait (body size at the end of first growth season). We found that population-specific reaction norms were close to parallel across different streams and Q_ST was similar – and larger than F_ST – within all streams, indicating a consistency of local adaptation in body size across natural environments. The amount of variation explained by population origin exceeded the variation across stream environments, indicating that genetic effects derived from adaptive processes have a stronger effect on phenotypic variation than plasticity induced by environmental conditions. These results suggest that plasticity does not “swamp” the phenotypic variation, and that selection may thus be efficient in generating genetic change.     

Environmental stress correlates with increases in both genetic and residual variances: A meta‐analysis of animal studies

Adaptive evolutionary responses are determined by the strength of selection and amount of genetic variation within traits, however, both are known to vary across environmental conditions. As selection is generally expected to be strongest under stressful conditions, understanding how the expression of genetic variation changes across stressful and benign environmental conditions is crucial for predicting the rate of adaptive change. Although theory generally predicts increased genetic variation under stress, previous syntheses of the field have found limited support for this notion. These studies have focused on heritability, which is dependent on other environmentally sensitive, but nongenetic, sources of variation. Here, we aim to complement these studies with a meta‐analysis in which we examine changes in coefficient of variation (CV) in maternal, genetic, and residual variances across stressful and benign conditions. Confirming previous analyses, we did not find any clear direction in how heritability changes across stressful and benign conditions. However, when analyzing CV, we found higher genetic and residual variance under highly stressful conditions in life‐history traits but not in morphological traits. Our findings are of broad significance to contemporary evolution suggesting that rapid evolutionary adaptive response may be mediated by increased evolutionary potential in stressed populations.     

ENVIRONMENTAL AND GENETIC CONTROL OF BRAIN AND SONG STRUCTURE IN THE ZEBRA FINCH

Birdsong is a classic example of a learned trait with cultural inheritance, with selection acting on trait expression. To understand how song responds to selection, it is vital to determine the extent to which variation in song learning and neuroanatomy is attributable to genetic variation, environmental conditions, or their interactions. Using a partial cross fostering design with an experimental stressor, we quantified the heritability of song structure and key brain nuclei in the song control system of the zebra finch and the genotype‐by‐environment (G × E) interactions. Neuroanatomy and song structure both showed low levels of heritability and are unlikely to be under selection as indicators of genetic quality. HVC, in particular, was almost entirely under environmental control. G × E interaction was important for brain development and may provide a mechanism by which additive genetic variation is maintained, which in turn may promote sexual selection through female choice. Our study suggests that selection may act on the genes determining vocal learning, rather than directly on the underlying neuroanatomy, and emphasizes the fundamental importance of environmental conditions for vocal learning and neural development in songbirds.     

Heritability of life-history tactics and genetic correlation with body size in a natural population of brook charr (Salvelinus fontinalis)

A common dimorphism in life-history tactic in salmonids is the presence of an anadromous pathway involving a migration to sea followed by a freshwater reproduction, along with an entirely freshwater resident tactic. Although common, the genetic and environmental influence on the adoption of a particular life-history tactic has rarely been studied under natural conditions. Here, we used sibship-reconstruction based on microsatellite data and an 'animal model' approach to estimate the additive genetic basis of the life-history tactic adopted (anadromy vs. residency) in a natural population of brook charr, Salvelinus fontinalis. We also assess its genetic correlation with phenotypic correlated traits, body size and body shape. Significant heritability was observed for life-history tactic (varying from 0.52 to 0.56 depending on the pedigree scenario adopted) as well as for body size (from 0.44 to 0.50). There was also a significant genetic correlation between these two traits, whereby anadromous fish were genetically associated with bigger size at age 1 (r(G) = -0.52 and -0.61). Our findings thus indicate that life-history tactics in this population have the potential to evolve in response to selection acting on the tactic itself or indirectly via selection on body size. This study is one of the very few to have successfully used sibship-reconstruction to estimate quantitative genetic parameters under wild conditions.     

Selection on heritable seasonal phenotypic plasticity of body mass

The ability to cope with environmental change is fundamental to a species' evolution. Organisms can respond to seasonal environmental variation through phenotypic plasticity. The substantial plasticity in body mass of temperate species has often been considered a simple consequence of change in environmental quality, but could also have evolved as an adaptation to seasonality. We investigated the genetic basis of, and selection acting on, seasonal plasticity in body mass for wild bighorn sheep ewes (Ovis canadensis) at Ram Mountain, Alberta, under two contrasting environmental conditions. Heritability of plasticity, estimated as mass-specific summer and winter mass changes, was low but significant. The additive genetic variance component of relative summer mass change was greater under good environmental conditions (characterized by a population increase and high juvenile survival) than under poor conditions (population decrease and low juvenile survival). Additive genetic variance of relative winter mass change appeared independent of environmental conditions. We found evidence of selection on summer (relative) and winter (relative and absolute) mass change. For a given mass, more plastic individuals (with greater seasonal mass changes) achieve greater fitness through reproduction in the following year. However, genetic correlations between mass parameters were positive. Our study supports the hypothesis that seasonal plasticity in body mass in vertebrates is an adaptation that evolved under natural selection to cope with environmental variation but genetic correlations with other traits might limit its evolutionary potential.     

Heritability of life‐history traits in the spruce budworm

The heritability of life‐history traits is of particular importance for insects that are very dependent on host conditions. Severe defoliation caused by the spruce budworm negatively impacts its food source, which in turn imposes environmental constraints on the insect. The heritability of those traits can help elucidate this species' evolutionary process. Heritability also helps identify which traits exhibit significant additive variance and can be key to understanding natural selection effects. Individuals were reared under laboratory conditions over three generations on an artificial diet. Heritability was estimated by parent–offspring regression. Fertility and fecundity demonstrated significant heritability followed by larval development, while pupal mass showed minimal heritable variation. These results suggest an important percent of additive variance in life‐history traits. This study contributes to our understanding of the relationship of this forest pest to its environmental conditions. This study also reveals an important genetic architectural structure of life‐history traits in the spruce budworm.     

Genetic variation in variability: Phenotypic variability of fledging weight and its evolution in a songbird population

Variation in traits is essential for natural selection to operate and genetic and environmental effects can contribute to this phenotypic variation. From domesticated populations, we know that families can differ in their level of within‐family variance, which leads to the intriguing situation that within‐family variance can be heritable. For offspring traits, such as birth weight, this implies that within‐family variance in traits can vary among families and can thus be shaped by natural selection. Empirical evidence for this in wild populations is however lacking. We investigated whether within‐family variance in fledging weight is heritable in a wild great tit (Parus major) population and whether these differences are associated with fitness. We found significant evidence for genetic variance in within‐family variance. The genetic coefficient of variation (GCV) was 0.18 and 0.25, when considering fledging weight a parental or offspring trait, respectively. We found a significant quadratic relationship between within‐family variance and fitness: families with low or high within‐family variance had lower fitness than families with intermediate within‐family variance. Our results show that within‐family variance can respond to selection and provides evidence for stabilizing selection on within‐family variance.     

HERITABILITY AND SELECTION ON CLUTCH SIZE IN DARWIN'S MEDIUM GROUND FINCHES (GEOSPIZA FORTIS)

I studied the causes of variation and selection on clutch size in a population of Darwin's Medium Ground Finches (Geospiza fortis) on Isla Daphne Major, using data collected over a nine-year period (1976–1984). Quantitative-genetic analyses were carried out using the first clutch laid by a female in a given year. I used both unadjusted clutch-size values and values adjusted for between-year differences in mean clutch size for repeatability and regression analyses. Repeatability of clutch size was small (≤8%) and nonsignificant in all cases. Sib-sib analyses and parent-offspring regressions gave no evidence of a significant additive genetic component to clutch-size variation. Slopes of mother-daughter regressions were actually negative, suggesting possible maternal effects of mother's clutch size on daughter's clutch size. There was a small positive relationship between female age and clutch size but no effect of male or female body size or of large-scale differences in habitat quality on clutch size. Selection on clutch size was generally directional and positive: in almost all years in which successful breeding occurred, large clutches tended to fledge more chicks and produce more young surviving to the following year, possibly because there was no trade-off between clutch size and the weights of individual chicks at fledging. Thus, sustained directional selection for large clutch size may have reduced additive genetic variation in clutch size to low levels in this population. The size of a female's clutch may be primarily determined by unidentified proximate environmental factors which vary from year to year, rather than by any long-term optimization of clutch size with respect to adult survival.     

Genetic and environmental components of growth in nestling blue tits (Parus caeruleus)

We investigated the effect of brood‐size mediated food availability on the genetic and environmental components of nestling growth in the blue tit (Parus caeruleus), using a cross‐fostering technique. We found genetic variation for body size at most nestling ages, and for duration of mass increase, but not of tarsus growth. Hence, nestling growth in our study population seems to have the potential to evolve further. Furthermore, significant genotype–environment interactions indicated heritable variation in reaction norms of growth rates and growth periods, i.e. that our study population had a heritable plasticity in the growth response to environmental conditions. The decreasing phenotypic variance with nestling age indicated compensatory growth in all body traits. Furthermore, the period of weight increase was longer for nestlings growing up in enlarged broods, while there was no difference to reduced broods in the period of tarsus growth. At fledging, birds in enlarged broods had shorter tarsi and lower weights than birds in reduced broods, but there was no difference in wing length or body condition between the two experimental groups. The observed flexibility in nestling growth suggests that growing nestlings are able to respond adaptively to food constraint by protecting the growth of ecologically important traits.     

Genetic parameters for early piglet weight,litter traits and number of functional teats in organic pigs

Knowledge remains limited on genetic variation and genetic correlations for traits in sows and piglets that are reared in an organic or outdoor setting. Here, we estimated genetic variance components for individual piglet weight, litter weight, litter size traits, and number of functional teats in a pig population raised under outdoor organic conditions. Data were collected from the largest organic multiplier farm in Denmark. Individual piglet weight was recorded at birth and on day 10. Number of live and dead piglets were recorded at birth, day 4, and day 11. Mean and total litter weight were calculated based on the individual weight of living piglets at birth and on day 10. The estimated heritability was highest for the number of functional teats (0.49), mean weight of a litter at birth (0.33) and on day 10 (0.25). In contrast, heritability was lowest for litter size traits (0.04–0.08) and piglet weight (0.06–0.07). Maternal heritability was much higher for individual piglet weight than direct heritability. The results showed that selection for higher mean weight results in smaller litters. Also, selection for individual birth weight of piglets results in heavier piglets at 10 days. In conclusion, this study confirmed that there is genetic variation in individual piglet weight, litter traits, and number of functional teats in organically and outdoor-reared pigs.