Gene Flow and Adaptive Potential in Drosophila melanogaster

Gene flow among historically isolated populations is expected to increase genetic diversity and consequently the ability of populations to adapt to environmental changes. Few experimental studies, however, have examined the relationship between gene flow and the adaptive potential of populations. The increase in adaptive potential that occurs as a result of gene flow is expected to depend on the genetic variance among populations that undergo genetic exchange. In the present study, we compared observed and expected changes in adaptive potential (as measured by the selection response of sternopleural bristle number) that occur as a result of gene flow among experimental populations of Drosophila melanogaster. We examined the effect of limited immigration (m = 0.05 over 3 generations) among a set of experimentally isolated lineages, in addition to the effect of complete hybridization among lineages. As expected, we found that limited immigration and hybridization both yielded increases in adaptive potential. However, whereas the effect of limited immigration agreed well with theoretical expectations, the increase in adaptive potential following complete hybridization of lineages was significantly less than expected. We discuss these findings in relation to endangered species conservation efforts, particularly with respect to the goal of maximizing the retention of adaptive potential within managed populations.     

An experimental comparison of selection alternatives to plateaued response

Three alternative selection methods for extending selection limits or breaking response plateaus were compared over ten generations in a replicated model experiment using two unrelated populations of Drosophila melanogaster that no longer responded to purebred selection for high egg number, a heterotic polygenic trait. The three methods were: (1) reciprocal recurrent selection (RRS) with selection within each of the plateaued populations based solely on crossbred performance, (2) a modification of reciprocal recurrent selection (MRRS) with selection within each population based on both purebred and crossbred performance, and (3) purebred selection within a new synthetic population formed by crossing the two plateaued populations.--Conflicting estimates were obtained for heritability of purebred egg number in each of the plateaued populations. The realized heritability values and estimates from diallel analyses indicated an absence of additive genetic variation for both populations; however, estimates from conventional intraclass correlation methods were positive. The diallel analyses revealed significant amounts of nonadditive gene effects for purebred egg number in each population, while the significant gene effects for crossbred egg numbers were additive. Estimates of the genetic correlation between purebred and crossbred egg number were negative (-0.85 +/- 0.68 and -0.32 +/- 0.25) for the two base populations.--All three alternatives to continued purebred selection gave significant responses, with the average gain per generation from MRRS being significantly superior to the other two methods. Observed purebred and crossbred responses under RRS were in agreement with quantitative genetic theory. Such was not the case for MRRS, which suggested the possibility of major gene segregation.--Evidence supporting a negative genetic correlation between purebred and crossbred performance and the possibility of overdominance is presented and discussed.     

Population mixing and the adaptive divergence of quantitative traits in discrete populations: a theoretical framework for empirical tests

Empirical tests for the importance of population mixing in constraining adaptive divergence have not been well grounded in theory for quantitative traits in spatially discrete populations. We develop quantitative-genetic models to examine the equilibrium difference between two populations that are experiencing different selective regimes and exchanging individuals. These models demonstrate that adaptive divergence is negatively correlated with the rate of population mixing (m, most strongly so when m is low), positively correlated with the difference in phenotypic optima between populations, and positively correlated with the amount of additive genetic variance (G, most strongly so when G is low). The approach to equilibrium is quite rapid (fewer than 50 generations for two populations to evolve 90% of the distance to equilibrium) when either heritability or mixing are not too low (h2 > 0.2 or m > 0.05). The theory can be used to aid empirical tests that: (1) compare observed divergence to that predicted using estimates of population mixing, additive genetic variance/covariance, and selection; (2) test for a negative correlation between population mixing and adaptive divergence across multiple independent population pairs; and (3) experimentally manipulate the rate of mixing. Application of the first two of these approaches to data from two well-studied natural systems suggests that population mixing has constrained adaptive divergence for color patterns in Lake Erie water snakes (Nerodia sipedon), but not for trophic traits in sympatric pairs of benthic and limnetic stickleback (Gasterosteus aculeatus). The theoretical framework we outline should provide an improved basis for future empirical tests of the role of population mixing in adaptive divergence.     

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

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

Stability of genetic variance and covariance for reproductive characters in the face of climate change in a wild bird population

Global warming has had numerous effects on populations of animals and plants, with many species in temperate regions experiencing environmental change at unprecedented rates. Populations with low potential for adaptive evolutionary change and plasticity will have little chance of persistence in the face of environmental change. Assessment of the potential for adaptive evolution requires the estimation of quantitative genetic parameters, but it is as yet unclear what impact, if any, global warming will have on the expression of genetic variances and covariances. Here we assess the impact of a changing climate on the genetic architecture underlying three reproductive traits in a wild bird population. We use a large, long-term, data set collected on great tits (Parus major) in Wytham Woods, Oxford, and an 'animal model' approach to quantify the heritability of, and genetic correlations among, laying date, clutch size and egg mass during two periods with contrasting temperature conditions over a 40-year period (1965-1988 [cooler] vs. 1989-2004 [warmer]). We found significant additive genetic variance and heritability for all traits under both temperature regimes. We also found significant negative genetic covariances and correlations between clutch size and egg weight during both periods, and among laying date and clutch size in the colder years only. The overall G matrix comparison among periods, however, showed only a minor difference among periods, thus suggesting that genotype by environment interactions are negligible in this context. Our results therefore suggest that despite substantial changes in temperature and in mean laying date phenotype over the last decades, and despite the large sample sizes available, we are unable to detect any significant change in the genetic architecture of the reproductive traits studied.     

Rapid response to artificial selection on flower size in Phlox

Quantitative characters are often said to evolve rather slowly, taking many generations to exhibit appreciable differences among populations. We tested this notion experimentally by performing bi-directional selection on corolla diameter of plants from a wild population of Phlox drummondii for three generations. By monitoring flower size, tube length and stigma-anther proximity of flowers, we obtained the direct and indirect responses to selection, and calculated genetic correlations, realized and narrow sense heritabilities using offspring-mother regression. Realized heritability of flower size was high (0.83), whereas genetic correlations among traits were weak or not significant. The per-generation average of the response in corolla diameter was about 5%. We found that P. drummondii has a great capacity to respond rapidly to selection, and this capacity may be in part responsible for the observed high degree of differentiation within the species. We also concluded that rapid evolution of morphological floral traits is possible.     

Consequences of fragmentation for the ability to adapt to novel environments in experimental <Emphasis Type="Italic">Drosophila</Emphasis> metapopulations

We used experimental populations of Drosophila melanogaster, which had either been subdivided (metapopulations) or kept undivided for 40 generations, to study the consequences of population subdivision for the tolerance and adaptive response after six generations of exposure to novel environmental factors (high temperature, medium with ethanol or salt added) for traits with different genetic architectures. In this setup, we attempted to separate the effects of the loss of fitness due to inbreeding (i.e., the survival upon first exposure to stress) from the loss of adaptive potential due to the lack of genetic variation. To place our experimental results in a more general perspective, we used individual-based simulations combining different options of levels of gene flow, intensity of selection and genetic architecture to derive quantitative hypotheses of the effects of these factors on the adaptive response to stress. We observed that population subdivision resulted in substantial inter-deme variation in tolerance due to redistribution of genetic variation from within demes to among demes. In line with the simulation results, the adaptive response was generally lower in the subdivided than in the undivided populations, particularly so for high temperature. We observed pronounced differences between stress factors that are likely related to the different genetic architectures involved in resistance to these factors. From a conservation genetics viewpoint, our results have two important implications: (i) Long-term fragmentation in combination with restricted gene flow will limit the adaptive potential of individual subpopulations because adaptive variation will become distributed among populations rather than within populations. (ii) The genetic architecture of the trait(s) under selection is of great significance to understand the possible responses to novel stresses that may be expected.     

How do reproductive skew and founder group size affect genetic diversity in reintroduced populations?

Reduced genetic diversity can result in short-term decreases in fitness and reduced adaptive potential, which may lead to an increased extinction risk. Therefore, maintaining genetic variation is important for the short- and long-term success of reintroduced populations. Here, we evaluate how founder group size and variance in male reproductive success influence the long-term maintenance of genetic diversity after reintroduction. We used microsatellite data to quantify the loss of heterozygosity and allelic diversity in the founder groups from three reintroductions of tuatara ( Sphenodon ), the sole living representatives of the reptilian order Rhynchocephalia. We then estimated the maintenance of genetic diversity over 400 years (∼10 generations) using population viability analyses. Reproduction of tuatara is highly skewed, with as few as 30% of males mating across years. Predicted losses of heterozygosity over 10 generations were low (1–14%), and populations founded with more animals retained a greater proportion of the heterozygosity and allelic diversity of their source populations and founder groups. Greater male reproductive skew led to greater predicted losses of genetic diversity over 10 generations, but only accelerated the loss of genetic diversity at small population size (<250 animals). A reduction in reproductive skew at low density may facilitate the maintenance of genetic diversity in small reintroduced populations. If reproductive skew is high and density-independent, larger founder groups could be released to achieve genetic goals for management.     

Impact of founder population, drift and selection on the genetic diversity of a recently translocated tree population

Recently established, temperate tree populations combine a high level of differentiation for adaptive traits, suggesting rapid genetic evolution, with a high level of genetic diversity within population, suggesting a limited impact of genetic drift and purifying selection. To study experimentally the evolutionary forces in a recently established population, we assessed the spatial and temporal patterns of genetic diversity within a disjunct population of Cedrus atlantica established 140 years ago in south-eastern France from a North African source. The population is expanding through natural regeneration. Three generations were sampled, including founder trees. We analysed 12 isozyme loci, three of which were previously found in tight association with selected genes, and quantitative traits. No bottleneck effect was detected in the founder generation, but a simple test of allelic association revealed an initial disequilibrium which disappeared in the following generations. The impact of genetic drift during secondary evolution was limited, as suggested by the weak temporal differentiation. The genetic load was not reduced after 3 generations, and the quantitative variation for adaptive traits did not change either. Thus, initial genetic changes first proceed from a rapid re-organisation of the diversity through mating and recombination, whereas genetic erosion through drift and selection is delayed due to temporal and spatial stochasticity. Two life-history traits of trees contribute to slowing down the processes of genetic erosion: perenniality and large spatial scale. Thus, one would expect recently established tree populations to have a higher diversity than older ones, which seems in accordance with experimental surveys.     

ADAPTIVE POPULATION DIVERGENCE IN CRYPTIC COLOR-PATTERN FOLLOWING A REDUCTION IN GENE FLOW

Adaptive population divergence is often driven by divergent natural selection, but can be constrained by the homogenizing effect of gene flow between populations. Indeed, a common pattern in nature is an inverse correlation between the degree of adaptive phenotypic divergence between populations and levels of gene flow between populations. However, there is essentially no experimental data on whether this correlation arises because gene flow constrains adaptation or, conversely, because adaptive divergence causes barriers to gene flow (ecological speciation). Here, I report increased adaptive divergence in cryptic color pattern between a pair of Timema insect populations following an experimental reduction in between-population gene flow. The reduction in gene flow arose due to a natural experiment, and thus was not replicated at a second site. However, temporal replication of the trends among six generations of data, coupled with a lack of increased adaptive divergence for two other population pairs where gene flow was not manipulated (i.e., control sites), argues that the results did not arise by chance. Estimates of dispersal ability and population size further support reduced gene flow, rather than increased genetic drift, as the cause of divergence. Thus, the findings provide experimental evidence that gene flow constrains adaptation in nature.     

TYPE I ERROR RATES FOR TESTING GENETIC DRIFT WITH PHENOTYPIC COVARIANCE MATRICES: A SIMULATION STUDY

Studies of evolutionary divergence using quantitative genetic methods are centered on the additive genetic variance–covariance matrix ( G ) of correlated traits. However, estimating G properly requires large samples and complicated experimental designs. Multivariate tests for neutral evolution commonly replace average G by the pooled phenotypic within‐group variance–covariance matrix ( W ) for evolutionary inferences, but this approach has been criticized due to the lack of exact proportionality between genetic and phenotypic matrices. In this study, we examined the consequence, in terms of type I error rates, of replacing average G by W in a test of neutral evolution that measures the regression slope between among‐population variances and within‐population eigenvalues (the Ackermann and Cheverud [AC] test) using a simulation approach to generate random observations under genetic drift. Our results indicate that the type I error rates for the genetic drift test are acceptable when using W instead of average G when the matrix correlation between the ancestral G and P is higher than 0.6, the average character heritability is above 0.7, and the matrices share principal components. For less‐similar G and P matrices, the type I error rates would still be acceptable if the ratio between the number of generations since divergence and the effective population size (t/N_e) is smaller than 0.01 (large populations that diverged recently). When G is not known in real data, a simulation approach to estimate expected slopes for the AC test under genetic drift is discussed.     

Investigating yellow dung fly body size evolution in the field: Response to climate change?

Uncovering genetic responses to selection in wild populations typically requires tracking individuals over generations and use of animal models. Our group monitored the body size of one Swiss Yellow Dung Fly (Scathophaga stercoraria; Diptera: Scathophagidae) field population over 15 years, including intermittent common‐garden rearing in the laboratory to assess body size with minimized environmental and maximized genetic variation. Contrary to expectations based on repeated heritability and phenotypic selection assessments over the years (reported elsewhere), field body sizes declined by >10% and common‐garden laboratory sizes by >5% from 1993 to 2009. Our results confirm the temperature‐size rule (smaller when warmer) and, albeit entirely correlational, could be mediated by climate change, as over this period mean temperature at the site increased by 0.5°C, although alternative systematic environmental changes cannot be entirely excluded. Monitoring genetic responses to selection in wild invertebrate populations is thus possible, though indirect, and wild populations may evolve in directions not consistent with strongly positive directional selection favoring large body size.     

Modelling problems in conservation genetics using Drosophila: consequences of fluctuating population sizes

Many natural populations fluctuate widely in population size. This is predicted to reduce effective population size, genetic variation, and reproductive fitness, and to increase inbreeding. The effects of fluctuating population size were examined in small populations of Drosophila melanogaster of the same average size, but maintained using either fluctuating ( FPS ) or equal ( EPS ) population sizes.FPS lines were maintained using seven pairs and one pair in alternate generations, and EPS lines with four pairs per generation. Ten replicates of each treatment were maintained. After eight generations, FPS had a higher inbreeding coefficient than EPS (0.60 vs. 0.38), a lower average allozyme heterozygosity (0.068 vs. 0.131), and a much lower relative fitness (0.03 vs. 0.25). Estimates of effective population sizes for FPS and EPS were 3.8 and 7.9 from pedigree inbreeding, and 4.9 vs. 7.1 from changes in average heterozygosities, as compared to theoretical expectations of 3.3 vs. 8.0. Results were generally in accordance with theoretical predictions. Management strategies for populations of rare and endangered species should aim to minimize population fluctuations over generations.     

Associations between environmental stress, selection history, and quantitative genetic variation in Drosophila melanogaster

Stressful environments may increase quantitative genetic variation in populations by promoting the expression of genetic variation that has not previously been eliminated or canalized by natural selection. This “selection history” hypothesis predicts that novel stressors will increase quantitative genetic variation, and that the magnitude of this effect will decrease following continued stress exposure. We tested these predictions using Drosophila melanogaster and sternopleural bristle number as a model system. In particular, we examined the effect of high temperature stress (31°C) on quantitative genetic variation before and after our study population had been reared at 31°C for 15 generations. High temperature stress was found to increase both additive genetic variance and heritability, but contrary to the selection history hypothesis prediction, the magnitude of this effect significantly increased after the study population had been reared for 15 generations under high temperature stress. These results demonstrate that high temperature stress increases quantitative genetic variation for bristle number, but do not support the selection history hypothesis as an explanation for this effect.     

Genetic adaptation to captivity in species conservation programs

As wild environments are often inhospitable, many species have to be captive-bred to save them from extinction. In captivity, species adapt genetically to the captive environment and these genetic adaptations are overwhelmingly deleterious when populations are returned to wild environments. I review empirical evidence on (i) the genetic basis of adaptive changes in captivity, (ii) factors affecting the extent of genetic adaptation to captivity, and (iii) means for minimizing its deleterious impacts. Genetic adaptation to captivity is primarily due to rare alleles that in the wild were deleterious and partially recessive. The extent of adaptation to captivity depends upon selection intensity, genetic diversity, effective population size and number of generation in captivity, as predicted by quantitative genetic theory. Minimizing generations in captivity provides a highly effective means for minimizing genetic adaptation to captivity, but is not a practical option for most animal species. Population fragmentation and crossing replicate captive populations provide practical means for minimizing the deleterious effects of genetic adaptation to captivity upon populations reintroduced into the wild. Surprisingly, equalization of family sizes reduces the rate of genetic adaptation, but not the deleterious impacts upon reintroduced populations. Genetic adaptation to captivity is expected to have major effects on reintroduction success for species that have spent many generations in captivity. This issue deserves a much higher priority than it is currently receiving.     

Effects of Population Size and Selection Intensity on Short-Term Response to Selection for Postweaning Gain in Mice

The effects of population size and selection intensity on the mean response was examined after 14 generations of within full-sib family selection for postweaning gain in mice. Population sizes of 1, 2, 4, 8 and 16 pair matings were each evaluated at selection intensities of 100% (control), 50% and 25% in a replicated experiment. Selection response per generation increased as selection intensity increased. Selection response and realized heritability tended to increase with increasing population size. Replicate variability in realized heritability was large at population sizes of 1, 2 and 4 pairs. Genetic drift was implicated as the primary factor causing the reduced response and lowered repeatability at the smaller population sizes. Lines with intended effective population sizes of 62 yielded larger selection responses per unit selection differential than lines with effective population sizes of 30 or less.     

Evolution in ecological field experiments: implications for effect size

Rapid evolution in response to strong selection, much of which is human-induced, has been indisputably documented. In this perspective, we suggest that adaptation may influence the effect size of treatments in ecological field experiments and alter our predictions of future dynamics in ecological systems. Field experiments often impose very strong and consistent selection over multiple generations. Focal populations may adapt to these treatments and, in the process, increase or decrease the magnitude of the treatment effect through time. We argue that how effect size changes through time will depend on the evolutionary history of the experimental population, the type of experimental manipulation, and the traits involved in adaptive responses. While no field study has conclusively demonstrated evolution in response to treatments with concomitant changes in ecological effect size, we present several examples that provide strong circumstantial evidence that such effects occur. We conclude with a consideration of the differences between plastic and genetic responses to treatments and discuss future research directions linking adaptation to ecological effect size.     

不同水分条件下春小麦种群中个体大小不整齐性及遗传学分析不同水分条件下春小麦种群中个体大小不整齐性及遗传学分析

 种群内个体大小不整齐性是种群数量结构的主要指标。本文研究了不同水分条件下,3个品种春小麦种群个体大小不整齐性的建立及变化规律。对春小麦种群不整齐性的遗传学分析表明：遗传结构与随机环境修饰对种群数量结构形成的相对重要性,因水分条件不同而异。种群不整齐性在自然选择中的作用可用下列简单模型表示：CSo＝SH×hSH2 CSo：自然选择强度;SH：大小不整齐性;hSH2：不整齐性的遗传力。     

Reduced inbreeding depression due to historical inbreeding in Drosophila melanogaster: evidence for purging

An important issue in conservation biology and the study of evolution is the extent to which inbreeding depression can be reduced or reversed by natural selection. If the deleterious recessive alleles causing inbreeding depression can be 'purged' by natural selection, outbred populations that have a history of inbreeding are expected to be less susceptible to inbreeding depression. This expectation, however, has not been realized in previous laboratory experiments. In the present study, we used Drosophila melanogaster as a model system to test for an association between inbreeding history and inbreeding depression. We created six 'purged' populations from experimental lineages that had been maintained at a population size of 10 male-female pairs for 19 generations. We then measured the inbreeding depression that resulted from one generation of full-sib mating in the purged populations and in the original base population. The magnitude of inbreeding depression in the purged populations was approximately one-third of that observed in the original base population. In contrast to previous laboratory experiments, therefore, we found that inbreeding depression was reduced in populations that have a history of inbreeding. The large purging effects observed in this study may be attributable to the rate of historical inbreeding examined, which was slower than that considered in previous experiments.     

Designing artificial selection experiments for specific objectives

The observed genetic gain (ΔP) from selection in a finite population is the possible expected genetic gain E(Δ G) minus the difference in inbreeding depression effects in the selected and control lines. The inbreeding depression can be avoided by crossing the control and selected ♂ and ♀ parents to unrelated mates and summing the observed gains. The possible expected gain will be reduced by an amount D from the predicted gain because of the effects of the genetic limit and random genetic drift, the magnitude of which is a function of effective population size, N. The expected value of D is zero in unselected control populations and in the first generation for selected populations. Therefore, this source of bias can be reduced by increasing N in the selected populations and can be avoided by selecting for a single generation. To obtain observed responses which are unbiased estimates of the predicted response from which to estimate the realized heritability (or regression) in the zero generation, or to test genetic theory based on infinite population size, single-generation selection with many replications would be most efficient. To measure the "total" effect or genetic efficiency of a selection criterion or method, including the effect of different selection intensities, effective population sizes, and space requirements, more than one generation of selection is required to estimate the expected response in breeding values. The efficiency, in the sense of minimum variance, of estimating the expected breeding values at any generation t will decline as the number of generations t increases. The variance of either the estimated mean gain or the regression of gain on selection differential can be reduced more by increasing the number of replicates K than by increasing the number of generations t. Also the general pattern of the response over t can be estimated if the N's are known. Therefore, two- or not more than three-generation selection experiments with many replications would be most efficient.