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.     

HERITABLE VARIATION FOR FECUNDITY IN FIELD-COLLECTED DROSOPHILA MELANOGASTER AND THEIR OFFSPRING REARED UNDER DIFFERENT ENVIRONMENTAL TEMPERATURES

Heritable variation for fitness components is normally measured under favorable laboratory conditions, but organisms in the field experience variable conditions that are often stressful and may affect the expression of heritable variation. We examined heritable variation for early fecundity in three samples of Drosophila melanogaster from the field. Flies were obtained from a rotting fruit pile in summer, autumn, and spring, and progeny were reared under laboratory conditions. Field parents were tested for fecundity at 14°C or 28°C depending on ambient temperatures. Wing/thorax length ratios measured on flies from the spring collection suggested that flies had developed at around 20°C. Progeny were reared and tested at 14°C, 25°C, and 28°C. In the summer collection, parent-offspring regression coefficients were high and significant, compared to nonsignificant values obtained in two of three autumn comparisons. In the spring collection, parent-offspring regressions were negative regardless of testing temperature, suggesting that field females with a high fecundity produced offspring with low scores. Comparisons of F₁ and F₂ laboratory generations indicated intermediate heritabilities for fecundity in the laboratory. The lower bound heritability estimate for fecundity in field individuals was 37% in summer and 59% in autumn. Estimates of field heritability and evolvability for wing length measured in the spring collection were lower than in the laboratory. The results indicate that heritabilities and additive genetic variances for fecundity can be high in field-reared flies, but that results may vary between field collections.     

Laboratory Estimates of Heritabilities and Genetic Correlations in Nature

A lower bound on heritability in a natural environment can be determined from the regression of offspring raised in the laboratory on parents raised in nature. An estimate of additive genetic variance in the laboratory is also required. The estimated lower bounds on heritabilities can sometimes be used to demonstrate a significant genetic correlation between two traits in nature, if their genetic and phenotypic correlations in nature have the same sign, and if sample sizes are large, and heritabilities and phenotypic and genetic correlations are high.     

Oviposition preference and life history traits in cactophilic Drosophila koepferae and D. buzzatii in association with their natural hosts

Drosophila koepferae and D. buzzatii are two closely related cactophilic species inhabiting the arid lands of southern South America. Previous studies have shown that D. buzzatii breeds primarily on the necrotic cladodes of several Opuntia cacti and D. koepferae on the rotting stems of columnar cacti of the genera Trichocereus and Cereus. In this paper, we analyze the patterns of host plant utilization in a locality where both Drosophila species are sympatric. Field studies showed an absence of differential attraction of adult flies to the rots of two major host cacti: O. sulphurea and T. terschekii. However, the proportion of D. buzzatii flies emerged from the rotting cladodes of O. sulphurea was significantly higher than in T. terschekii. In laboratory experiments, egg to adult viability in single species cultures varied when both Drosophila species were reared in media prepared with O. sulphurea or T. terschekii. In addition, between-species comparisons of flies emerged from single species cultures showed that D. buzzatii adults were smaller and developed faster than D. koepferae. Furthermore, analysis of flies emerged in mixed species cultures showed differences in oviposition preference and oviposition behavior. We discuss the observed between-species differences and suggest that these traits are the result of adaptation to specific patterns of spatial and temporal predictability of their respective preferred host plants: columnar are less dense and less ephemeral resources, whereas the opuntias are more abundant, and fast rotting cacti. This revised version was published online in July 2006 with corrections to the Cover Date.     

The evolutionary history of Drosophila buzzatii XXVII

The correlation between body size and longevity was tested in an Argentinian natural population of Drosophila buzzatii. Mean thorax length of flies newly emerging from rotting cladodes of Opuntia vulgaris was significantly smaller than that of two samples of flies caught at baits. The present results which might be interpreted as directional selection for longevity favoring larger flies are in agreement with previous results achieved in a Spanish natural population of D. buzzatii. Flies emerging from different substrates showed significant differences in thorax length, suggesting that an important fraction of phenotypic variance can be attributed to environmental variability. However, laboratory and field work in different populations of D. buzzatii showed a significant genetic component for thorax length variation.     

The vectoring of cactophilic yeasts by Drosophila

Summary At two locations in the Sonoran Desert, yeasts were sampled from species of Drosophila, the flies' cactus hosts, and other neighboring sources of cactophilic yeasts to determine the relation between the yeasts vectored by the fly and the yeasts found in their breeding sites. D. mojavensis, D. nigrospiracula, and D. mettleri vectored yeast assemblages significantly more similar to the yeast species found on the rot from which the flies were collected than to the yeasts found on other rots from the flies host cactus or other rotting cactus at the same site. Rots with Drosophila had fewer yeast species than those without flies, suggesting that flies were associated with younger rots. Rots with flies and the Drosophila also had more yeast species with the capability to produce ethyl acetate than rots without flies. The results support the contention that cactophilic Drosophila feed on a subset of the yeasts available in an area, and may act to maintain differences among the yeast communities found on different species of cactus.     

Inversion and allozyme polymorphism show contrasting patterns of microgeographical population structure in a natural population of Drosophila buzzatii from Argentina

Second chromosome inversions and genotypic frequencies at seven allozyme loci were determined in a natural population of the cactophilic species Drosophila buzzatii that uses as breeding sites the necrotic cladodes of the prickly pear Opuntia quimilo and the rotting stems of cardón, Trichocereus terschekii. Different processes govern the evolutionary fate of inversion and allozyme polymorphisms. A pattern of heterotic balance for inversions seems to be acting uniformly in each breeding site and could depend on different regimes of density‐dependent selection within cactus hosts. Patterns of variation of allozymes revealed significant heterogeneity in allele frequencies for Esterase‐1 (Est‐1) among O. quimilo rots and Aldehyde oxidase (Aldox) and Xanthine dehydrogenase (Xdh) among T. terschekii substrates and showed gene‐cactus effects only for Esterase‐2 (Est‐2). Consistent and significant excesses of homozygotes were detected at both the within‐rot and in the total population levels that could be accounted for by diversifying selection among individual breeding sites.     

F Statistics in Drosophila Buzzatii: Selection, Population Size and Inbreeding

Drosophila buzzatii is confined to reproducing in a well defined patchy environment consisting of rotting cactus cladodes which are ephemeral, permitting at most three generations. Flies emerging from such rots were used to estimate the additive genetic variance within rots and the genetic variance between rots for body size and also were electrophoresed to determine their genotypes at six polymorphic loci. F statistics were estimated from body size and allozyme data. The F(ST) derived from body size was significantly larger than the allozyme F(ST). It is proposed this is due to selective differentiation of body size. The allozyme F(ST) is used to estimate effective population size: 10 < N < 50. It is suggested that the regularly observed positive F(IS)'s could be due to partial sib mating, S. If so, the estimated lower bound is S = 0.258. Experiments are identified which could support or contradict these interpretations.     

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.     

Evolution of the male genitalia: morphological variation of the aedeagi in a natural population of <Emphasis Type="Italic">Drosophila mediopunctata</Emphasis>

To investigate the size and shape of the aedeagus of Drosophila mediopunctata, we used basic statistics and geometric morphometrics. We estimated the level of phenotypic variation, natural and laboratory heritability as well as the phenotypic correlations between aedeagus and wing measures. The wing was used as an indicator for both body size and shape. Positive significant correlation was obtained for centroid size of aedeagus and wing for field parents and their offspring reared in the laboratory. Many positive significant phenotypic correlations were found among linear measures of both organs. The phenotypic correlations were few for aedeagus and wing shape. Coefficients of variation of the measures were on average larger in the aedeagus than in the wing for offspring reared in laboratory, but not for flies coming from the field. Significant “natural” heritabilities were found for five linear measures of the aedeagus and only one for the wing. Few significant heritabilities were found for aedeagus and wing shape, mostly ones concerning the uniform components. In an exploratory analysis, we found that inversion DS-PC0 is associated with both uniform and nonuniform components of shape, respectively, in the wing and aedeagus. Our results do not support the lock-and-key hypothesis for the male genitalia evolution, but cannot refute the sexual selection and pleiotropy hypotheses.     

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.     

Temporal and spatial variation of inversion polymorphism in two natural populations of Drosophila buzzatii

The inversion polymorphism of the cactophilic fly Drosophila buzzatii was studied in two natural populations. We assessed the temporal changes and microspatial population structure. We observed a significant increase in the frequency of arrangement 2J at the expense of 2ST in both populations. These gene arrangements appear to affect the life-history of flies differently. Environmental heterogeneity explains the karyotype coexistence in nature. The analysis of population structure showed that differentiation of inversion frequencies among individual breeding sites, the rotting clacodes of Opuntia vulgaris, was highly significant. The karyotypic frequencies did not depart significantly from Hardy-Weinberg expectations, neither in individual rots nor in the total population. These results suggest that the observed population structure can be easily accounted by random genetic drift.     

Genetic Variance for Body Size in a Natural Population of Drosophila Buzzatii

Previous work has shown thorax length to be under directional selection in the Drosophila buzzatii population of Carboneras. In order to predict the genetic consequences of natural selection, genetic variation for this trait was investigated in two ways. First, narrow sense heritability was estimated in the laboratory F2 generation of a sample of wild flies by means of the offspring-parent regression. A relatively high value, 0.59, was obtained. Because the phenotypic variance of wild flies was 7-9 times that of the flies raised in the laboratory, "natural" heritability may be estimated as one-seventh to one-ninth that value. Second, the contribution of the second and fourth chromosomes, which are polymorphic for paracentric inversions, to the genetic variance of thorax length was estimated in the field and in the laboratory. This was done with the assistance of a simple genetic model which shows that the variance among chromosome arrangements and the variance among karyotypes provide minimum estimates of the chromosome's contribution to the additive and genetic variances of the trait, respectively. In males raised under optimal conditions in the laboratory, the variance among second-chromosome karyotypes accounted for 11.43% of the total phenotypic variance and most of this variance was additive; by contrast, the contribution of the fourth chromosome was nonsignificant. The variance among second-chromosome karyotypes accounted for 1.56-1.78% of the total phenotypic variance in wild males and was nonsignificant in wild females. The variance among fourth chromosome karyotypes accounted for 0.14-3.48% of the total phenotypic variance in wild flies. At both chromosomes, the proportion of additive variance was higher in mating flies than in nonmating flies.     

Temporal and Spatial Allozyme Variation in the South American Cactophilic Drosophila antonietae (Diptera; Drosophilidae)

Drosophila antonietae is an endemic South American cactophilic species that uses Cereus hildmaniannus rotting cladodes as breeding sites. We assessed temporal and spatial intrapopulational allozyme variation of two natural populations. Our results suggest that environmental variation (rain precipitation) is probably influencing allozyme temporal variation. Moreover, it seems that D. antonietae does not have intrapopulation structure and has N _ev (variance effective size) 83 and N _ec (number of adult flies that colonize each rotting cladode) = 21. The deficiency of heterozygotes found must be due to null alleles, a temporal Wahlund effect, or selection against heterozygotes. Assortative mating and inbreeding are discarded. This is the first report on allozyme variation in D. antonietae. It gives some insight on intrapopulational genetics through space and time for this species. This is important to understand its general genetic variability and will be essential to future works on the natural history and evolution of this species.     

Realized heritability of personalities in the great tit (Parus major)

Behaviour under conditions of mild stress shows consistent patterns in all vertebrates: exploratory behaviour, boldness, aggressiveness covary in the same way. The existence of highly consistent individual variation in these behavioural strategies, also referred to as personalities or coping styles, allows us to measure the behaviour under standardized conditions on birds bred in captivity, link the standardized measurements to the behaviour under natural conditions and measure natural selection in the field. We have bred the great tit (Parus major), a classical model species for the study of behaviour under natural conditions, in captivity. Here, we report a realized heritability of 54 +/- 5% for early exploratory behaviour, based on four generations of bi-directional artificial selection. In addition to this, we measured hand-reared juveniles and their wild-caught parents in the laboratory. The heritability found in the mid-offspring-mid-parent regression was significantly different from zero. We have thus established the presence of considerable amounts of genetic variation for personality types in a wild bird.     

Size and shape heritability in natural populations of Drosophila mediopunctata: temporal and microgeographical variation

‘Traditional morphometrics’ allows us to decompose morphological variation into its major independent sources, identifying them usually as size and shape. To compare and investigate the properties of size and shape in natural populations of Drosophila mediopunctata, estimating their heritabilities and analysing their temporal and microgeographic changes, we carried out collections on seven occasions in Parque Nacional do Itatiaia, Brazil. In one of these collections, we took samples from five different altitudes. Measurements were taken from wild caught inseminated females and up to three of their laboratory‐reared daughters. Through a principal component analysis, three major sources of variation were identified as due to size (the first one) and shape (the remaining two). The overall amount of variation among laboratory flies was about half of that observed among wild flies and this reduction was primarily due to size. Shape variation was about the same under natural and artificial conditions. A genetic altitudinal cline was detected for size and shape, although altitude explained only a small part of their variation. Differences among collections were detected both for size and shape in wild and laboratory flies, but no simple pattern emerged. Shape variation had high heritability in nature, close to or above 40% and did not vary significantly temporally. Although on the overall size heritability (18 ± 6%)was significant its estimates were not consistent along months – they were non‐significant in all but one month, when it reached a value of 51 ± 11%. Overall, this suggests that size and shape have different genetic properties. This revised version was published online in July 2006 with corrections to the Cover Date.     

Analysis of spatial and temporal variation in the community structure of yeasts associated with decayingOpuntia cactus

The microbial structure within, between, and over time in decaying cladodes of the common prickly pearOpuntia stricta was studied at each of two separate localities. In general, the effective number of yeast species and yeast species diversity increased as the rot aged to the observed maximum time of 4 weeks. Yeast heterogeneity at the two localities differed in the mode of environmental influence, with spatial variability (among rots) most important at one and temporal variability (within rots over time) most important at the other. Differences in cactus density and quality (age) are most likely determinants of the differences in yeast community structure.     

EVOLUTIONARY PREDICTABILITY IN NATURAL POPULATIONS: DO MATING SYSTEM AND NONADDITIVE GENETIC VARIANCE INTERACT TO AFFECT HERITABILITIES IN PLANTAGO LANCEOLATA?

Quantitative genetics has been an immensely powerful tool in manipulating the phenotypes of domesticated plants and animals. Much of the predictive power of quantitative genetics depends on the breeder's control over the context in which phenotype and mating are being expressed. In the natural world, these contexts are often difficult to describe, let alone control. We are left, therefore, with a poor understanding of the limits of quantitative genetics in natural populations. One of the crucial contextual elements for assessing breeding value is the genetic background in which an individual's genes are being assessed. When interacting genes are polymorphic within a population, the degree of mating among relatives can influence the correlations among mates and the predictions of a response to selection. Population structure can strongly influence the degree to which dominance and epistasis influences additive genetic variance and heritability. The extent of inbreeding can also influence heritabilities through its effect on the environmental component of phenotypic variance. The applicability of standard quantitative genetic breeding designs to the measurement of heritabilities in natural populations therefore depends in part on: (1) the mating system of the population; and (2) the importance of gene interactions in determining phenotypic variation. We tested for an effect of mating structure on the partitioning of phenotypic variance and heritability by comparing two breeding designs in a common environment. Both breeding designs used 139 pollen parents taken from mapped locations in a population of Plantago lanceolata L., and crossed to 280 seed parents from the same population. One design was random-mating, the second was biased toward near-neighbor matings to an extent determined by field measure of pollen-mediated gene flow distances. The offspring were grown randomly mixed in a common garden. Nine traits were measured: central corm diameter, number of leaves, area of the most recently fully expanded leaf, density of hairs (cm^-2) on the leaves, dry weight per unit leaf area, photosynthetic capacity, transpiration rates, water use efficiency, and reproductive dry weight. Heritabilities and variance components from the two designs were compared using randomization tests. None of the variance components or the heritabilities differed significantly between breeding designs at the 0.05 level. The test could distinguish differences between the heritabilities measured in the two breeding designs as small as 0.11, on average. Thus, for the degree of inbreeding normally exhibited in P. lanceolata there is insufficient gene interaction present within populations to influence the partitioning of variance between additive and nonadditive components or to influence heritability estimates to a meaningful extent. We suggest that for Plantago other sources of variation in heritability estimates, such as maternal effects and genotype × environment interactions, are more important influences than the interaction between inbreeding and gene interactions, and standard heritability estimate based on random breeding is as accurate as one taking the natural mating structure into account.     

EVOLUTION OF FLORAL TRAITS IN A HERMAPHRODITIC PLANT: FIELD MEASUREMENTS OF HERITABILITIES AND GENETIC CORRELATIONS

Genetic variances, heritabilities, and genetic correlations of floral traits were measured in the monocarpic perennial Ipomopsis aggregata (Polemoniaceae). A paternal half-sib design was employed to generate seeds in each of four years, and seeds were planted back in the field near the parental site. The progeny were followed for up to eight years to estimate quantitative genetic parameters subject to natural levels of environmental variation over the entire life cycle. Narrow-sense heritabilities of 0.2–0.8 were detected for the morphometric traits of corolla length, corolla width, stigma position, and anther position. The proportion of time spent by the protandrous flowers in the pistillate phase (“proportion pistillate”) also exhibited detectable heritability of near 0.3. In contrast, heritability estimates for nectar reward traits were low and not significantly different from zero, due to high environmental variance between and within flowering years. The estimates of genetic parameters were combined with phenotypic selection gradients to predict evolutionary responses to selection mediated by the hummingbird pollinators. One trait, corolla width, showed the potential for a rapid response to ongoing selection through male function, as it experienced both direct selection, by influencing pollen export, and relatively high heritability. Predicted responses were lower for proportion pistillate and corolla length, even though these traits also experienced direct selection. Stigma position was expected to respond positively to indirect selection of proportion pistillate but negatively to selection of corolla length, with the net effect sensitive to variation in the selection estimates. Anther position also was not directly selected but could respond to indirect selection of genetically correlated traits.     

Impact of reconstructed pedigrees on progeny-test breeding values in red spruce

Pedigrees reconstructed through DNA marker assigned paternities in polymix (PMX) and open pollinated (OP) progeny tests were analyzed using mixed models to test the effect of unequal male reproductive success and pedigree errors on quantitative genetic parameters. The reconstructed pedigree increased heritabilities in the larger PMX test. Increased heritability resulted from adding the paternities to the pedigree per se, not by correcting the male reproductive bias by specifying the exact pedigree. Removing hypothesized pedigree errors had no effect on quantitative parameters, either because the magnitude of the errors was too small (PMX) or the progeny test was too small to detect variance components reliably (OP). Although there was no advantage in backwards selection, the increased additive variance, heritabilities and accuracy of progeny with assigned paternities in the pedigree, should permit forward selection of offspring with greater genetic gain and complete control of coancestry for future breeding decisions. Some possible breeding population structures with the new genetic information are discussed.