Facing change: forms and foundations of contemporary adaptation to biotic invasions

Ongoing adaptation in native populations to anthropogenic change both facilitates and challenges ecologically appropriate and sustainable management. Human disturbance promotes adaptive responses at the genomic, individual and population levels. Traits vary widely in whether adaptation occurs through plasticity or evolution, and these modes interact within and among traits. For example, plasticity in one trait may be adaptive because it permits homeostasis and lessens the intensity of selection in another. Both opportunity and catastrophe generate adaptive responses. Recently evolved adaptations characterize the responses of many native species to biotic invasions. Several well-known examples involve native phytophagous insects colonizing introduced plants. For example, our studies of North American and Australian soapberry bugs on nonindigenous plants demonstrate both diversifying and homogenizing contemporary evolution. Modes of adaptation differ among traits and populations and as a function of the host on which they develop. The genetic architecture of the evolving adaptations involves a substantial degree of nonadditive genetic variation. One important consequence of contemporary adaptation may be an enhanced capacity of native communities to provide adaptive biological control of invasive species. Conservation scientists may manipulate adaptation to achieve conservation goals, but must also decide how deeply they wish to attempt to control the phenotypes and genotypes of other species.     

Adaptive gradients and isolation-by-distance with postglacial migration in Picea sitchensis

Fossil pollen records suggest rapid migration of tree species in response to Quaternary climate warming. Long-distance dispersal and high gene flow would facilitate rapid migration, but would initially homogenize variation among populations. However, contemporary clinal variation in adaptive traits along environmental gradients shown in many tree species suggests that local adaptation can occur during rapid migration over just a few generations in interglacial periods. In this study, we compared growth performance and pollen genetic structure among populations to investigate how populations of Sitka spruce (Picea sitchensis) have responded to local selection along the historical migration route. The results suggest strong adaptive divergence among populations (average Q(ST)=0.61), corresponding to climatic gradients. The population genetic structure, determined by microsatellite markers (R(ST)=0.09; F(ST)=0.11), was higher than previous estimates from less polymorphic genetic markers. The significant correlation between geographic and pollen haplotype genetic (R(ST)) distances (r=0.73, P<0.01) indicates that the current genetic structure has been shaped by isolation-by-distance, and has developed in relatively few generations. This suggests relatively limited gene flow among populations on a recent timescale. Gene flow from neighboring populations may have provided genetic diversity to founder populations during rapid migration in the early stages of range expansion. Increased genetic diversity subsequently enhanced the efficiency of local selection, limiting gene flow primarily to among similar environments and facilitating the evolution of adaptive clinal variation along environmental gradients.     

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.     

FUNCTIONAL GENETIC DIVERGENCE IN HIGH CO2 ADAPTED EMILIANIA HUXLEYI POPULATIONS

Predicting the impacts of environmental change on marine organisms, food webs, and biogeochemical cycles presently relies almost exclusively on short‐term physiological studies, while the possibility of adaptive evolution is often ignored. Here, we assess adaptive evolution in the coccolithophore Emiliania huxleyi, a well‐established model species in biological oceanography, in response to ocean acidification. We previously demonstrated that this globally important marine phytoplankton species adapts within 500 generations to elevated CO₂. After 750 and 1000 generations, no further fitness increase occurred, and we observed phenotypic convergence between replicate populations. We then exposed adapted populations to two novel environments to investigate whether or not the underlying basis for high CO₂‐adaptation involves functional genetic divergence, assuming that different novel mutations become apparent via divergent pleiotropic effects. The novel environment “high light” did not reveal such genetic divergence whereas growth in a low‐salinity environment revealed strong pleiotropic effects in high CO₂ adapted populations, indicating divergent genetic bases for adaptation to high CO₂. This suggests that pleiotropy plays an important role in adaptation of natural E. huxleyi populations to ocean acidification. Our study highlights the potential mutual benefits for oceanography and evolutionary biology of using ecologically important marine phytoplankton for microbial evolution experiments.     

How phenotypic convergence arises in experimental evolution

Evolutionary convergence is a core issue in the study of adaptive evolution, as well as a highly debated topic at present. Few studies have analyzed this issue using a “real‐time” or evolutionary trajectory approach. Do populations that are initially differentiated converge to a similar adaptive state when experiencing a common novel environment? Drosophila subobscura populations founded from different locations and years showed initial differences and variation in evolutionary rates in several traits during short‐term (～20 generations) laboratory adaptation. Here, we extend that analysis to 40 more generations to analyze (1) how differences in evolutionary dynamics among populations change between shorter and longer time spans, and (2) whether evolutionary convergence occurs after 60 generations of evolution in a common environment. We found substantial variation in longer term evolutionary trajectories and differences between short‐ and longer term evolutionary dynamics. Although we observed pervasive patterns of convergence toward the character values of long‐established populations, populations still remain differentiated for several traits at the final generations analyzed. This pattern might involve transient divergence, as we report in some cases, indicating that more generations should lead to final convergence. These findings highlight the importance of longer term studies for understanding convergent evolution.     

The evolution of harm--effect of sexual conflicts and population size

Conflicts of interest between mates can promote the evolution of male traits that reduce female fitness and that drive coevolution between the sexes. The rate of adaptation depends on the intensity of selection and its efficiency, which depends on drift and genetic variability. This leads to the largely untested prediction that coevolutionary adaptations such as those driven by sexual conflict should evolve faster in large populations. We tested this using the bruchid beetle Callosobruchus maculatus, a species where harm inflicted by males is well documented. Although most experimental evolution studies remove sexual conflict, we reintroduced it in populations in which it had been experimentally removed. Both population size and standing genetic variability were manipulated in a factorial experimental design. After 90 generations of relaxed conflict (monogamy), the reintroduction of sexual conflicts for 30 generations favored males that harmed females and females that were more resistant to the genital damage inflicted by males. Males evolved to become more harmful when population size was large rather than when initial genetic variation was enriched. Our study shows that sexual selection can create conditions in which males can benefit from harming females and that selection may tend to be more intense and effective in larger populations.     

Locally adapted traits maintained in the face of high gene flow

Gene flow between phenotypically divergent populations can disrupt local adaptation or, alternatively, may stimulate adaptive evolution by increasing genetic variation. We capitalised on historical Trinidadian guppy transplant experiments to test the phenotypic effects of increased gene flow caused by replicated introductions of adaptively divergent guppies, which were translocated from high‐ to low‐predation environments. We sampled two native populations prior to the onset of gene flow, six historic introduction sites, introduction sources and multiple downstream points in each basin. Extensive gene flow from introductions occurred in all streams, yet adaptive phenotypic divergence across a gradient in predation level was maintained. Descendants of guppies from a high‐predation source site showed high phenotypic similarity with native low‐predation guppies in as few as ~12 generations after gene flow, likely through a combination of adaptive evolution and phenotypic plasticity. Our results demonstrate that locally adapted phenotypes can be maintained despite extensive gene flow from divergent populations.     

植物自然群体适应逆境的分子机理

Recent advances in studies of genetic variation at protein andDNA levels in plant natural populations and its relationship with environmental changes were reviewed with special reference to the works on the wild barley (Hordeum spontaneum C. Koch.). On one side, adaptation was shown in statistic data, on the other side, the fact that a considerable part of genetic variation does exist within populations (subpopulations) under same ecological condition indicated its maintainability of neutral or near-neutral mutations in natural populations. The researches on adaptive populations of plants, especially on wild soybean (Glycine soja Sieb. et Zucc.) mainly conducted in author's laboratory, have shown that the most part of molecular variation within and among populations can not be explained by selection particularly as far as the individual uniqueness was concerned. There are some data shown that adaptation may be caused by accumulation of a few near-neutral mutations. Recent publications on molecular mechanisms of morphological evolution has been received special attention to elucidate the discrepancy between molecular evolution and morphological adaptive evolution. A frame on the unified evolution theory has been built. Finally some related viewpoints of philosophy were discussed.     

Molecular Mechanisms of Stress Adaptation in Plant Natural Populations

Recent advances in studies of genetic variation at protein and DNA levels in plant natural populations and its relationship with environmental changes were reviewed with special reference to the works on the wild barley ( Hordeum spontaneum C. Koch.). On one side, adaptation was shown in statistic data, on the other side, the fact that a considerable part of genetic variation does exist within populations (subpopulations) under same ecological condition indicated its maintainability of neutral or near-neutral mutations in natural populations. The researches on adaptive populations of plants, especially on wild soybean ( Glycine soja Sieb. et Zucc.) mainly conducted in author's laboratory, have shown that the most part of molecular variation within and among populations can not be explained by selection particularly as far as the individual uniqueness was concerned. There are some data shown that adaptation may be caused by accumulation of a few near-neutral mutations. Recent publications on molecular mechanisms of morphological evolution has been received special attention to elucidate the discrepancy between molecular evolution and morphological adaptive evolution. A frame on the unified evolution theory has been built. Finally some related viewpoints of philosophy were discussed.     

Fitness and adaptation in a novel environment: effect of inbreeding, prior environment, and lineage

Abstract. The ability of populations to undergo adaptive evolution depends on the presence of genetic variation for ecologically important traits. The maintenance of genetic variation may be influenced by many variables, particularly long-term effective population size and the strength and form of selection. The roles of these factors are controversial and there is very little information on their impacts for quantitative characters. The aims of this study were to determine the impacts of population size and variable versus constant prior environmental conditions on fitness and the magnitude of response to selection. Outbred and inbred populations of Drosophila melanogaster were maintained under benign, constant stressful, and variably stressful conditions for seven generations, and then forced to adapt to a novel stress for seven generations. Fitness and adaptability were assayed in each replicate population. Our findings are that: (1) populations inbred in a variable environment were more adaptable than those inbred in a constant environment; (2) populations adapted to a prior stressful environment had greater fitness when reared in a novel stress than those less adapted to stress; (3) inbred populations had lower fitness and were less adaptable than the outbred population they were derived from; and (4) strong lineage effects were detectable across environments in the inbred populations.     

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.     

Adaptive evolution in invasive species

Many emerging invasive species display evidence of rapid adaptation. Contemporary genetic studies demonstrate that adaptation to novel environments can occur within 20 generations or less, indicating that evolutionary processes can influence invasiveness. However, the source of genetic or epigenetic variation underlying these changes remains uncharacterised. Here, we review the potential for rapid adaptation from standing genetic variation and from new mutations, and examine four types of evolutionary change that might promote or constrain rapid adaptation during the invasion process. Understanding the source of variation that contributes to adaptive evolution in invasive plants is important for predicting future invasion scenarios, identifying candidate genes involved in invasiveness, and, more generally, for understanding how populations can evolve rapidly in response to novel and changing environments.     

Environmental adaptations as windows on molecular evolution

Changes in gene regulation may play an important role in adaptive evolution, particularly during adaptation to a changing environment. However, little is known about the molecular mechanisms underlying adaptively significant variation in gene regulation. To address this question, we are using environmental adaptations in populations of a fish, Fundulus heteroclitus as a window into the molecular evolution of gene regulation. F. heteroclitus are found along the East Coast of North America, with populations distributed along a steep thermal gradient. At the extremes of the species range, populations have undergone local adaptation to their habitat temperatures. A variety of genes differ in their regulation between these populations. We have determined the mechanism responsible for changes in lactate dehydrogenase-B (Ldh-B) gene regulation. A limited number of mutations in the regulatory sequence of this gene result in changes in its expression. Both the phenotypic (increased LDH activity) and genotypic (changes in Ldh-B regulatory sequences) differences between populations have been shown to be affected by natural selection, rather than genetic drift. Therefore, even a small number of mutations within important regulatory sequences can provide evolutionarily significant variation and have an impact on environmental adaptation.     

THE QUANTITATIVE AND MOLECULAR GENETIC ARCHITECTURE OF A SUBDIVIDED SPECIES

In an effort to elucidate the evolutionary mechanisms that determine the genetic architecture of a species, we have analyzed 17 populations of the microcrustacean Daphnia pulex for levels of genetic variation at the level of life-history characters and molecular markers in the nuclear and mitochondrial genomes. This species is highly subdivided, with approximately 30% of the variation for nuclear molecular markers and 50% of the variation for mitochondrial markers being distributed among populations. The average level of genetic subdivision for quantitative traits is essentially the same as that for nuclear markers, which superficially suggests that the life-history characters are diverging at the neutral rate. However, the existence of a strong correlation between the levels of population subdivision and broadsense heritabilities of individual traits argues against this interpretation, suggesting instead that the among-population divergence of some quantitative traits (most notably body size) is being driven by local adaptation to different environments. The fact that the mean phenotypes of the individual populations are also strongly correlated with local levels of homozygosity indicates that variation in local inbreeding plays a role in population differentiation. Rather than being a passive consequence of local founder effects, levels of homozygosity may be selected for directly for their effects on the phenotype (adaptive inbreeding depression). There is no relationship between the levels of variation within populations for molecular markers and quantitative characters, and this is explained by the fact that the average standing genetic variation for life-history characters in this species is equivalent to only 33 generations of variation generated by mutation.     

Epigenetics in natural animal populations

Phenotypic plasticity is an important mechanism for populations to buffer themselves from environmental change. While it has long been appreciated that natural populations possess genetic variation in the extent of plasticity, a surge of recent evidence suggests that epigenetic variation could also play an important role in shaping phenotypic responses. Compared with genetic variation, epigenetic variation is more likely to have higher spontaneous rates of mutation and a more sensitive reaction to environmental inputs. In our review, we first provide an overview of recent studies on epigenetically encoded thermal plasticity in animals to illustrate environmentally‐mediated epigenetic effects within and across generations. Second, we discuss the role of epigenetic effects during adaptation by exploring population epigenetics in natural animal populations. Finally, we evaluate the evolutionary potential of epigenetic variation depending on its autonomy from genetic variation and its transgenerational stability. Although many of the causal links between epigenetic variation and phenotypic plasticity remain elusive, new data has explored the role of epigenetic variation in facilitating evolution in natural populations. This recent progress in ecological epigenetics will be helpful for generating predictive models of the capacity of organisms to adapt to changing climates.     

Genetic and evolutionary consequences of metapopulation structure

Extinction and recolonization of populations may have various effects on the degree and distribution of genetic variation, but turnover is generally associated with low levels of among-population variation, in both 'classical' and other types of metapopulation. Therefore, adaptive evolution is unlikely to be promoted by selection among populations. Whether adaptation is promoted or slowed by population subdivision, with or without turnover, remains a subject of theoretical debate.     

Influence of genetic architecture on contemporary local evolution in the soapberry bug,Jadera haematoloma: artificial selection on beak length

Little is known about the influence of genetic architecture on local adaptation. We investigated the genetic architecture of the rapid contemporary evolution of mouthparts, the flight polymorphism and life history traits in the soapberry bug Jadera haematoloma (Hemiptera) using laboratory selection. The mouthparts of these seed‐feeding bugs have adapted in 40–50 years by decreasing in length following novel natural selection induced by a host switch to the seeds of an introduced tree with smaller fruits than those of the native host vine. Laboratory selection on beak length in both an ancestral population feeding on the native host and a derived population feeding on the introduced host reveals genetic variance allowing a rapid response (heritabilities of 0.51–0.87) to selection for either longer or shorter beaks. This selection resulted in reverse evolution by restoring long beaks in the derived population and forward evolution by re‐creating short beaks in the ancestral bugs. There were strong genetic correlations (0.68–0.84) in both populations between beak lengths and the frequency of flight morphs, with short beaks associated with short wings. The results reveal a genetically interrelated set of adaptive multivariate traits including both beak length and flight morph. This suite of traits reflects host plant patchiness and seeding phenology. Weaker evidence suggests that egg mass and early egg production may be elements of the same suite. Reversible or forward evolution thus may occur in a broad set of genetically correlated multivariate traits undergoing rapid contemporary adaptation to altered local environments.     

HOW CLOSELY CORRELATED ARE MOLECULAR AND QUANTITATIVE MEASURES OF GENETIC VARIATION? A META‐ANALYSIS

The ability of populations to undergo adaptive evolution depends on the presence of quantitative genetic variation for ecologically important traits. Although molecular measures are widely used as surrogates for quantitative genetic variation, there is controversy about the strength of the relationship between the two. To resolve this issue, we carried out a meta-analysis based on 71 datasets. The mean correlation between molecular and quantitative measures of genetic variation was weak (r = 0.217). Furthermore, there was no significant relationship between the two measures for life-history traits (r = -0.11) or for the quantitative measure generally considered as the best indicator of adaptive potential, heritability (r = -0.08). Consequently, molecular measures of genetic diversity have only a very limited ability to predict quantitative genetic variability. When information about a population's short-term evolutionary potential or estimates of local adaptation and population divergence are required, quantitative genetic variation should be measured directly.     

Insight into the genetic bases of climatic adaptation in experimentally evolving wheat populations

Experimental populations evolving under natural selection represent an interesting tool to study genetic bases of adaptation. Evolution of genes possibly involved in adaptive response can be followed together with the corresponding phenotypic traits. Using experimental populations of hexaploid wheat, we studied the evolution of flowering time, a major adaptive trait that synchronizes the initiation of reproduction and the occurrence of favourable environmental conditions. During 12 generations, three populations were grown in contrasted environments (Vervins North France, Le Moulon near Paris, Toulouse South France) under the influence of natural selection, drift, mutation and recombination. Evolution of diversity at the major gene VRN-1 involved in wheat vernalization response has been analysed jointly with earliness estimated in controlled conditions. Whatever the population, rapid phenotypic changes as well as parallel genotypic variations were observed in the first seven generations, probably as the result of selection acting on this major gene which explains 80% of the trait variation overall. Different allelic combinations at physically unlinked copies of VRN-1 located on distinct genomes (A, B and D) were selected between populations. As theoretically expected, due to population differentiation, a high level of genetic diversity was maintained overall in generation 12. Surprisingly, in two populations out of three, the emergence of new alleles by mutation or migration, coupled with temporal variable selection or frequency-dependent selection, allowed to maintain within-population diversity despite local genetic drift and natural selection. This result may plead for an evolutionary approach of wheat genetic resource conservation.