Heritability of Two Morphological Characters within and among Natural Populations of Drosophila melanogaster

Heritabilities of wing length and abdominal bristle number, as well as genetic correlations between these characters, were determined within and among populations of Drosophila melanogaster in nature. Substantial "natural" heritabilities were found when wild-caught flies from one population were compared to their laboratory-reared offspring. Natural heritabilities of bristle number approximated those derived from laboratory-raised parents and offspring, but wing length heritability was significantly lower in nature than in the laboratory. Among-population heritabilities, estimated by regressing population means of wild-caught flies against those of their laboratory-reared descendants, were close to 0.5. The genetic differentiation of populations was clinal with latitude, and was accompanied by significant geographic differences in the norms of reaction to temperature. These clines are similar to those reported on other continents and in other Drosophila species, and are almost certainly caused by natural selection. Genetic regressions between the characters reveal that the cline in bristle number may be a correlated response to geographic selection on wing length, but not vice versa. Our results indicate that there is a sizable genetic component to phenotypic variation within and among populations of D. melanogaster in nature.     

Genetic basis of variation in morphological and life-history traits of a wild population of pink salmon

Understanding the genetic basis of phenotypic variation is essential for predicting the direction and rate of phenotypic evolution. We estimated heritabilities and genetic correlations of morphological (fork length, pectoral and pelvic fin ray counts, and gill arch raker counts) and life-history (egg number and individual egg weight) traits of pink salmon (Oncorhynchus gorbuscha) from Likes Creek, Alaska, in order to characterize the genetic basis of phenotypic variation in this species. Families were created from wild-caught adults, raised to the fry stage in the lab, released into the wild, and caught as returning adults and assigned to families using microsatellite loci and a growth hormone locus. Morphological traits were all moderately to highly heritable, but egg number and egg weight were not heritable, suggesting that past selection has eliminated additive genetic variation in egg number and egg weight or that there is high environmental variance in these traits. Genetic correlations were similar for nonadjacent morphological traits and adjacent traits. Genetic correlations predicted phenotypic correlations fairly accurately, but some pairs of traits with low genetic correlations had high phenotypic correlations, and vice versa, emphasizing the need to use caution when using phenotypic correlations as indices of genetic correlations. This is one of only a handful of studies to estimate heritabilities and genetic correlations for a wild population.     

Genetic and phenotypic correlations among size-related traits, and heritability variation between body parts in Drosophila buzzatii

Recent studies have shown that body size is a heritable trait phenotypically correlated with several fitness components in wild populations of the cactophilic fly Drosophila buzzatii. To obtain further information on size-related variation, heritabilities as well as genetic and phenotypic correlations among size-related traits of several body parts (head, thorax and wings) were estimated. The study was carried out on an Argentinean natural population in which size-related selection was previously detected. The genetic parameters were estimated using offspring-parent regressions (105 families) in the laboratory G₂ generation of a sample of wild flies. The traits were also scored in Wild-Caught Flies (WCF). Laboratory-Reared Flies (LRF) were larger and less variable than WCF. Although heritability estimates were significant for all traits, heritabilities were higher for thorax-wing traits than for head traits. Phenotypic and genetic correlations were all positive. The highest genetic correlations were found between traits which are both functionally and developmentally related. Genetic and phenotypic correlations estimated in the lab show similar correlation patterns (r = 0.49; TP = 0.02, Mantel's test). However, phenotypic correlations were found to be typically larger in WCF than in LRF. The genetic correlation matrix estimated in the relatively homogeneous lab environment is not simply a constant multiplicative factor of the phenotypic correlation matrix estimated in WCF. This revised version was published online in July 2006 with corrections to the Cover Date.     

Genetic and phenotypic correlations in a natural population of song sparrows

We estimated heritabilities, and genetic and phenotypic correlations between beak and body traits in the song sparrow ( Melospiza melodia ). We compared these estimates to values for the same traits in the Galápagos finches, Geospiza (Boag, 1983; Grant, 1983). Morphological variance is low in the song sparrow, and our results show that genetic and phenotypic correlations are considerably lower than correlations in the morphologically more variable Geospiza. Comparison using a larger sample of Galapagos populations confirms the existence of an association between variance and correlation for phenotypic values. We suggest two possible explanations for this association. First, most traits studied are functionally related, and the joint evolution of variance and correlation may have resulted from stabilizing selection about a line of optimal allometry between traits. Alternatively, introgression between populations and species could have caused correlation and variance to evolve jointly. Both selection and introgression were probably influential in producing the observed pattern, but it is not possible to estimate their relative importance with current data. Genetic and phenotypic correlations were correlated in the song sparrow, but heritabilities of traits varied greatly. As a result, the genetic variance-covariance matrix for traits is not simply a constant multiple of the phenotypic matrix. Evolutionary response to natural selection cannot, therefore, be predicted from the measurement of phenotypic characteristics alone.     

Quantitative genetics of larval life-history traits in Rana temporaria in different environmental conditions

The degree to which genetic variation in a given trait varies among different populations of the same species and across different environments has seldom been quantified in wild vertebrate species. We investigated the expression of genetic variability and maternal effects in three larval life-history traits of the amphibian Rana temporaria. In a factorial laboratory experiment, five widely separated populations (max. 1600 km) were subjected to two different environmental treatments. Animal model analyses revealed that all traits were heritable (h(2) approximately 0.20) in all populations and under most treatment combinations. Although the cross-food treatment genetic correlations were close to unity, heritabilities under a restricted food regime tended to be lower than those under an ad libitum food regime. Likewise, maternal effects (m(2) approximately 0.05) were detected in most traits, and they tended to be most pronounced under restricted food conditions. We detected several cross-temperature genetic and maternal effects correlations that were lower than unity, suggesting that genotype-environment interactions and maternal effect-environment interactions are a significant source of phenotypic variation. The results reinforce the perspective that although the expression of genetic and maternal effects may be relatively homogeneous across different populations of the same species, local variation in environmental conditions can lead to significant variation in phenotypic expression of quantitative traits through genotype-environment and maternal effect-environment interactions.     

Effects of temperature extremes on genetic variances for life history traits in Drosophila melanogaster as determined from parent-offspring comparisons

Parent-offspring comparisons were used to investigate the effects of temperature extremes on genetic variances for two life history traits and one morphological trait in Drosophila melanogaster. We considered three temperatures (14 °C, 25 °C and 28 °C) for culturing and testing flies, and considered heritabilities, coefficients of additive variation (CV_A) and evolvabilities (I_A) for fecundity, development time and wing length. For fecundity, heritabilities and evolvabilities were higher when parents were exposed to 14 °C compared to 28 °C. Parent-offspring comparisons suggested that genetic correlations among environments were close to 1, although lower correlations were obtained in comparisons of family means. Parent-offspring correlations across environments seemed to depend on parental temperature. For development time, heritabilities and evolvabilities were low at 14 °C compared to 28 °C. However, parent-offspring correlations were relatively high when the progeny of parents tested at 14 °C were raised at the opposite extreme, suggesting that genetic variation can be enhanced when parents and offspring experience different conditions. CV_As and I_As for development time were lower than for fecundity, even when heritability estimates were similar in magnitude. Genetic variation for wing length was generally not affected by the temperature extremes, and genetic correlations across the extremes estimated from the parent-offspring comparison were close to 1. There was no evidence for tradeoffs between traits; rapid development time was associated with high fecundity at both the phenotypic and genetic levels. The findings highlight inherent difficulties of estimating genetic parameters from parent-offspring comparisons when two generations experience different environmental extremes and also show how parent-offspring comparisons can lead to unexpected findings about the expression of genetic variation.     

HERITABILITIES OF DOMINANCE-RELATED TRAITS IN MALE BANK VOLES (CLETHRIONOMYS GLAREOLUS)

A number of studies have shown that in several animal species females prefer dominant males as mating partners, but fewer attempts have been made to measure possible indirect benefits of this choice. One reason for this may be that, even though dominance is a widely used concept, the definition of dominance still remains controversial Furthermore, defining and measuring the heritability of social behaviors is problematic because they are not individual traits but, by definition, involve interactions between at least two individuals. In this study we estimated heritabilities and coefficients of additive genetic variances (CV_A) for male traits that are closely associated with dominance and female mating preferences in bank voles (Clethrionomys glareolus). The heritability values were estimated using father-offspring regression. All heritability estimates were relatively high ranging from 0.531 (urine marking) to 0.767 (preputial glands). The CV_A-values indicated high levels of additive genetic variance especially in the characters most closely related to dominance: the weight of preputial glands and urine marking behavior. All phenotypic correlations among the traits measured were significantly positive and the genetic correlations were of similar magnitude as the corresponding phenotypic counterparts. Even though heritabilities may be lower in the natural environment than under controlled laboratory conditions, our results suggest that characters closely related to dominance may be at least partly genetically determined.     

Testing the phenotypic gambit: phenotypic, genetic and environmental correlations of colour

Evolutionary theory is primarily concerned with genetic processes, yet empirical testing of this theory often involves data collected on phenotypes. To make this tenable, the implicit assumption is often made that phenotypic patterns are good predictors of genetic patterns; an assumption that coined the phenotypic gambit. Although this assumption has been validated for traits with high heritability, such as morphology, its generality for traits with low heritabilities, such as life-history and behavioural traits, remains controversial. Using a large-scale cross-fostering experiment, we were able to measure genetic, common environmental and phenotypic correlations between four colour traits and two skeletal traits in a wild population of passerine birds, the blue tit (Parus caeruleus). Colour traits had little heritable variation but common environment effects were found to be important; skeletal traits showed the opposite pattern. Positive correlations because of a shared natal environment were found between all traits, obscuring negative genetic correlations between some colour and skeletal traits. Consequently, phenotypic patterns were poor surrogates for genetic patterns and we suggest that this may be common if trade-offs or substantial parental effects exist. For this group of traits, the phenotypic gambit cannot be made and we suggest caution when inferring genetic patterns from phenotypic data, especially for behavioural and life-history traits.     

Quantitative genetic analysis of brain size variation in sticklebacks: support for the mosaic model of brain evolution

The mosaic model of brain evolution postulates that different brain regions are relatively free to evolve independently from each other. Such independent evolution is possible only if genetic correlations among the different brain regions are less than unity. We estimated heritabilities, evolvabilities and genetic correlations of relative size of the brain, and its different regions in the three-spined stickleback (Gasterosteus aculeatus). We found that heritabilities were low (average h² = 0.24), suggesting a large plastic component to brain architecture. However, evolvabilities of different brain parts were moderate, suggesting the presence of additive genetic variance to sustain a response to selection in the long term. Genetic correlations among different brain regions were low (average r_G = 0.40) and significantly less than unity. These results, along with those from analyses of phenotypic and genetic integration, indicate a high degree of independence between different brain regions, suggesting that responses to selection are unlikely to be severely constrained by genetic and phenotypic correlations. Hence, the results give strong support for the mosaic model of brain evolution. However, the genetic correlation between brain and body size was high (r_G = 0.89), suggesting a constraint for independent evolution of brain and body size in sticklebacks.     

Multivariate approach to calculating the recurrence risk in families with multifactorial diseases

To resolve one of the main theoretical problems of genetic counselling, namely, calculation of the recurrence risk for common diseases, a multivariate approach is suggested, based on the multifactorial model. The model suggests partially different liability for several diseases or various forms of a disease. The specified recurrence risk for each family can be calculated with the account of different morbidity rates for different sexes and the degree of kinship to proband. The input data for computer calculations are: population incidence of diseases, their heritabilities as well as genetical and environmental correlations between the diseases. Our method is illustrated by calculation of the recurrence risk for diabetes mellitus (DM) and bronchial asthma (BA), each of which may be subdivided into several forms. It is proposed that the nature of genetic correlations is different for two diseases. The phenotypic forms of DM are genetically independent, whereas the forms of BA have a common genetic basis.     

Ecological Aspects of the Heritability of Body Size in Drosophila Buzzatii

The heritability of thorax length in the cactophilic Drosophila buzzatii was determined for flies from each of 10 rotting cactus cladodes. For each rot, emerging flies were used as parents of progeny reared in the laboratory. The methods used were full sib analysis with the parents mated assortatively and also offspring-parent regression. From this, heritabilities were measured for the laboratory environment and for the natural environment of the rotting cladode. For the laboratory environment, h2 = 0.3770 +/- 0.0203 and for the natural environment h2 = 0.0936 +/- 0.0087 within rots and h2 = 0.0595 +/- 0.0123 for a population drawn randomly from different rots. Because of the possibility of genotype-environment interaction between the laboratory and rot environments, the methods of B. Riska, T. Prout and M. Turelli were used to show it is possible that there is no such interaction, but if there is, the above natural heritabilities are approximate lower bounds. These results are related to the general problem of determining heritabilities in nature where it is impractical to measure both parents and progeny in nature. Determining heritability not only in nature but in relation to subdivision into ephemeral patches (cladodes in this case) has an important bearing on natural selection response and to general theories of stabilizing selection proposed to explain the existence of genetic variation. Attempts were made to detect selection by using the size of emerging adults as an indicator of various levels of larval stress. No selection was detected, but the power to do so was very weak. Differences between progeny means from different rots indicated some genetic differences between rots which can be adequately explained by small numbers of founders. This suggests a random fine scale subdivision amounting to FST = 0.1483 +/- 0.0462.     

FLUCTUATING ASYMMETRY IS NONGENETICALLY RELATED TO MATING SUCCESS IN DROSOPHILA BUZZATII

Abstract To date, there is still no consensus on the real significance of fluctuating asymmetry (FA) in evolutionary biology. Some studies have established links between FA and Darwinian fitness, and in a number of cases intermediate heritabilities for FA have been reported. However, many claims have been raised against the generality of these findings. I therefore tested if FA of a sexually selected trait (wing length) is indeed related to male mating success in Drosophila buzzatii from field and laboratory samples and whether FA has detectable heritability. Single, unsuccessful males had greater asymmetry for wing length than their mating counterparts both in nature and under nonoptimal rearing environments, but the higher FA in single males is most likely due to a poorer average phenotypic condition because there was no evidence of a genetic basis for this trait. Further evidence of an increase in FA under larval food stress is suggested when comparing the magnitude of the FA levels between stressful and optimal environments. On methodological grounds, a linear model is suggested that allows directional asymmetry (DA) and any genetic variation of DA that may be present to be statistically eliminated from estimates of FA.     

Quantitative genetic analysis of skin reflectance: a multivariate approach.

Skin color is a polygenically determined quantitative trait. Although it has been used extensively in studies of between-population variation, there have been relatively few studies of the inheritance of skin color. In this article we use measurements on 359 members of the Jirel population of eastern Nepal to assess the heritabilities and additive genetic correlations of three skin reflectance measures. Skin color was measured at the upper inner arm site at three wavelengths. A maximum likelihood approach was used to estimate sex and age effects on skin reflectance, heritabilities, and phenotypic variances at each wavelength and both additive genetic and environmental correlations between wavelengths. This technique incorporated information from 36 pedigrees with 2-25 members and 173 independent individuals. Likelihood ratio tests were used to assess the significance of specific variance/covariance components. The results indicate that skin reflectances are moderately heritable at all three wavelengths. The pairwise phenotypic correlations ranged from 0.76 to 0.88. The observed additive genetic correlations were not significantly different from 1.00, suggesting that the same loci influence variation at each wavelength. This evidence for relatively complete pleiotropy implies that measurements at multiple wavelengths yield little additional genetic information, although they may be useful for reducing measurement error. Based on estimates of the genetic and phenotypic covariance matrices, we determined that skin reflectance measurements are expected to provide only as much information for assessing local between-population genetic variation as a single two-allele polymorphic marker. Therefore microevolutionary studies based on skin color variation should be viewed with caution.     

In situ wood quality assessment in Douglas-fir

The genetic control and phenotypic and genotypic correlations among wood density, modulus of elasticity, height, diameter, and volume were assessed using 967 trees representing 20 unrelated 32-year-old coastal Douglas-fir full-sib families growing on four (spaced and pruned vs. control) comparable test sites. Generally, no significant differences were observed between treatments, indicating their limited effect at assessment time. Family effect did not differ for the growth traits; however, significant differences were observed for wood density and both in situ methods (drilling resistance and acoustic velocity). Growth and wood quality attributes, individually, produced high and positive phenotypic and genetic correlations; however, high and negative correlations were observed between individual variables belonging to the two suites of attributes. Individual tree heritabilities were low for growth (0.04 to 0.08) and modest to high for wood quality attributes (0.14 to 0.68). The observed heritabilities and phenotypic and genotypic correlations imply modest to strong genetic control; however, they operated in opposing direction. The significant and consistent genetic correlations between the in situ methods and wood density and stiffness support their use as a non-destructive and economic assessment approach. The reliability of the in situ assessments was verified through cumulative pith-to-bark wood density assessment, resulting in inconsistent genetic and phenotypic correlations for early growth years. These latter findings imply that caution should be used in employing these in situ techniques as early screening tools in breeding programs.     

Estimating heritabilities and genetic correlations: comparing the 'animal model' with parent-offspring regression using data from a natural population

Quantitative genetic parameters are nowadays more frequently estimated with restricted maximum likelihood using the 'animal model' than with traditional methods such as parent-offspring regressions. These methods have however rarely been evaluated using equivalent data sets. We compare heritabilities and genetic correlations from animal model and parent-offspring analyses, respectively, using data on eight morphological traits in the great reed warbler (Acrocephalus arundinaceus). Animal models were run using either mean trait values or individual repeated measurements to be able to separate between effects of including more extended pedigree information and effects of replicated sampling from the same individuals. We show that the inclusion of more pedigree information by the use of mean traits animal models had limited effect on the standard error and magnitude of heritabilities. In contrast, the use of repeated measures animal model generally had a positive effect on the sampling accuracy and resulted in lower heritabilities; the latter due to lower additive variance and higher phenotypic variance. For most trait combinations, both animal model methods gave genetic correlations that were lower than the parent-offspring estimates, whereas the standard errors were lower only for the mean traits animal model. We conclude that differences in heritabilities between the animal model and parent-offspring regressions were mostly due to the inclusion of individual replicates to the animal model rather than the inclusion of more extended pedigree information. Genetic correlations were, on the other hand, primarily affected by the inclusion of more pedigree information. This study is to our knowledge the most comprehensive empirical evaluation of the performance of the animal model in relation to parent-offspring regressions in a wild population. Our conclusions should be valuable for reconciliation of data obtained in earlier studies as well as for future meta-analyses utilizing estimates from both traditional methods and the animal model.     

Egg shell quality in Japanese quail: characteristics,heritabilities and genetic and phenotypic relationships

The objective of the present study was to estimate heritabilities as well as genetic and phenotypic correlations for egg weight, specific gravity, shape index, shell ratio, egg shell strength, egg length, egg width and shell weight in Japanese quail eggs. External egg quality traits were measured on 5864 eggs of 934 female quails from a dam line selected for two generations. Within the Bayesian framework, using Gibbs Sampling algorithm, a multivariate animal model was applied to estimate heritabilities and genetic correlations for external egg quality traits. The heritability estimates for external egg quality traits were moderate to high and ranged from 0.29 to 0.81. The heritability estimates for egg and shell weight of 0.81 and 0.76 were fairly high. The genetic and phenotypic correlations between egg shell strength with specific gravity, shell ratio and shell weight ranging from 0.55 to 0.79 were relatively high. It can be concluded that it is possible to determine egg shell quality using the egg specific gravity values utilizing its high heritability and fairly high positive correlation with most of the egg shell quality traits. As a result, egg specific gravity may be the choice of selection criterion rather than other external egg traits for genetic improvement of egg shell quality in Japanese quails.     

Testing Cheverud's conjecture for behavioral correlations and behavioral syndromes

Recent research regarding correlations among behaviors--under the labels of behavioral syndromes and animal personalities--has typically assumed that phenotypic correlations between behaviors are representative of underling genetic correlations. However, for behaviors, the concordance between phenotypic and genetic correlations has not been rigorously examined. I tested this assumption using published estimates and found phenotypic and genetic correlations to be strongly related but found that the average absolute difference between the two was quite high and similar to that observed in other traits. Using absolute differences as the sole criterion, phenotypic correlations do not reliably estimate the magnitude of genetic correlations for behaviors, which is problematic for behavioral syndrome researchers. However, phenotypic correlations explained 75% of the variation in genetic correlations and their sign was typically the same as that of genetic correlations. This suggests that phenotypic correlations between behaviors reliably estimate the direction of underling genetic relationships and provide considerable information regarding the magnitude of genetic correlations. Thus, if researchers are careful about the questions they ask, phenotypic correlations between behaviors can be informative regarding underling genetic correlations and their evolutionary implications.     

NATURAL HERITABILITIES: CAN THEY BE RELIABLY ESTIMATED IN THE LABORATORY?

The validity of the assumption, that laboratory estimates of heritabilities will tend to overestimate natural heritabilities, due to a reduction in environmental variability and thus the phenotypic variance of traits, is examined. One hundred sixty-five field estimates of narrow sense heritabilities derived from the literature are compared with 189 estimates from laboratory studies on wild, outbred animal populations derived from the data set of Mousseau and Roff. The results indicate that 84% of field heritabilities are significantly different from zero and that for morphological, behavioral, and life-history traits there are no significant differences between laboratory and field estimates of heritability. Unexpectedly, mean heritabilities for morphological and life-history traits are actually higher in the field than in the lab. Twenty-two cases were found for which both laboratory and natural heritabilities had been estimated on the same traits. For this subset of the data, laboratory heritabilities tended to be higher than field estimates, but the difference was not significant. Also, the correlation between lab and field estimates was high (r = 0.6, P < 0.001), and the regression slope did not differ significantly from one. The major implications of this study are that laboratory estimates of heritability should generally provide reasonable estimations of both the magnitude and the significance of heritabilities in nature.     

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

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

The quantitative genetics of two life history trade-offs in the yellow dung fly in abundant and limited food environments

The trade-offs between body size and development time and between egg size and egg number (clutch size) are central to life history theory, but evidence for them, particularly in terms of genetic correlations, is equivocal. For the yellow dung fly Scathophaga stercoraria (Diptera: Scathophagidae), we investigated variation in phenotypic and genetic variances and covariances, i.e. heritabilities and genetic correlations, of these life history traits (plus diapause) in benign and stressful larval field or adult laboratory food environments. We found both trade-offs to be weak, as evidenced by low phenotypic and genetic correlations, but stronger in the food limited environments. Broad sense heritabilities were generally significant for all traits considered, whereas the narrow sense heritabilities for egg and clutch size were nil. With regard to the question of how environmental stress affects heritabilities, we found a whole range of responses within one single species depending on the traits considered. All three possible patterns occurred, i.e. increased h² due to increased V_G or decreased decreased h² due to increased and no change in h² due to increased V_G and V_P. These can be explained by the particular ecological circumstances yellow dung flies face in their natural environment. Nevertheless, the majority of patterns was consistent with the idea that stressful conditions amplify phenotypic differences between genotypes. Such variable responses of traits even within one organism underscores the complexity of this issue and may well explain the multiple patterns found in various organisms.Co-ordinating editor: Leimar