Host plant adaptation in Drosophila mettleri populations

The process of local adaptation creates diversity among allopatric populations, and may eventually lead to speciation. Plant-feeding insect populations that specialize on different host species provide an excellent opportunity to evaluate the causes of ecological specialization and the subsequent consequences for diversity. In this study, we used geographically separated Drosophila mettleri populations that specialize on different host cacti to examine oviposition preference for and larval performance on an array of natural and non-natural hosts (eight total). We found evidence of local adaptation in performance on saguaro cactus (Carnegiea gigantea) for populations that are typically associated with this host, and to chemically divergent prickly pear species (Opuntia spp.) in a genetically isolated population on Santa Catalina Island. Moreover, each population exhibited reduced performance on the alternative host. This finding is consistent with trade-offs associated with adaptation to these chemically divergent hosts, although we also discuss alternative explanations for this pattern. For oviposition preference, Santa Catalina Island flies were more likely to oviposit on some prickly pear species, but all populations readily laid eggs on saguaro. Experiments with non-natural hosts suggest that factors such as ecological opportunity may play a more important role than host plant chemistry in explaining the lack of natural associations with some hosts.     

Dispersal in cactophilic Drosophila

Three species of Drosophila each breed in necrotic tissue of specific columnar cacti endemic to the Sonoran Desert. Drosophila pachea breeds in senita ( Lophocereus schottii) , D. nigrospiracula breeds in saguaro ( Carnegiea gigantea ) or cardón ( Pachycereus pringlei ), and D. mojavensis uses organ pipe ( Stenocereus thurberi ) in Sonora, Mexico and southern Arizona. Patches of these three host cacti have very different spatial distributions, with those of senita being quite frequent and close together, while those of the other hosts are much father apart. Testing all three species simultaneously, we used capture-mark-release-recapture methods to ask if dispersal differed in these species and if differences were those predicted by the spatial availability of the host patches. D. pachea dispersed the shortest distance in all experiments. Furthermore, D. pachea was the only species showing sex-biased dispersal, with male flies exhibiting the greater propensity to disperse. The observations suggest that across similar spatial scales, D. pachea should show greater population genetic structure than the other two species, and that mitochondrial DNA, because of its maternal inheritance, might show greater evidence of structure than nuclear markers.     

Rapid specialization of counter defenses enables two-spotted spider mite to adapt to novel plant hosts

Genetic adaptation, occurring over a long evolutionary time, enables host-specialized herbivores to develop novel resistance traits and to efficiently counteract the defenses of a narrow range of host plants. In contrast, physiological acclimation, leading to the suppression and/or detoxification of host defenses, is hypothesized to enable broad generalists to shift between plant hosts. However, the host adaptation mechanisms used by generalists composed of host-adapted populations are not known. Two-spotted spider mite (TSSM; Tetranychus urticae) is an extreme generalist herbivore whose individual populations perform well only on a subset of potential hosts. We combined experimental evolution, Arabidopsis thaliana genetics, mite reverse genetics, and pharmacological approaches to examine mite host adaptation upon the shift of a bean (Phaseolus vulgaris)-adapted population to Arabidopsis. We showed that cytochrome P450 monooxygenases are required for mite adaptation to Arabidopsis. We identified activities of two tiers of P450s: general xenobiotic-responsive P450s that have a limited contribution to mite adaptation to Arabidopsis and adaptation-associated P450s that efficiently counteract Arabidopsis defenses. In approximately 25 generations of mite selection on Arabidopsis plants, mites evolved highly efficient detoxification-based adaptation, characteristic of specialist herbivores. This demonstrates that specialization to plant resistance traits can occur within the ecological timescale, enabling the TSSM to shift to novel plant hosts.

Mites can evolve highly efficient detoxification-based adaptation in approximately 25 generations on an initially unfavorable plant host, revealing that specialization can occur within the ecological timescale.     

Functional genomics of cactus host shifts in Drosophila mojavensis

Understanding the genetic basis of adaptation to novel environments remains one of the major challenges confronting evolutionary biologists. While newly developed genomic approaches hold considerable promise for addressing this overall question, the relevant tools have not often been available in the most ecologically interesting organisms. Our study organism, Drosophila mojavensis, is a cactophilic Sonoran Desert endemic utilizing four different cactus hosts across its geographical range. Its well-known ecology makes it an attractive system in which to study the evolution of gene expression during adaptation. As a cactophile, D. mojavensis oviposits in the necrotic tissues of cacti, therefore exposing larvae and even adults to the varied and toxic compounds of rotting cacti. We have developed a cDNA microarray of D. mojavensis to examine gene expression associated with cactus host use. Using a population from the Baja California population we examined gene expression differences of third instar larvae when reared in two chemically distinct cactus hosts, agria (Stenocereus gummosus, native host) vs. organpipe (Stenocereus thurberi, alternative host). We have observed differential gene expression associated with cactus host use in genes involved in metabolism and detoxification.     

New paradigms for the evolution of beneficial infections

A longstanding paradigm predicts that microbial parasites and mutualists exhibit disparate evolutionary patterns. Parasites are predicted to promote arms races with hosts, rapid evolution and sexual recombination. By contrast, mutualists have been linked with beneficial coadaptation, evolutionary stasis and asexuality. In this review we discuss the recent surge of molecular data on microbes that are being used to test and reshape these ideas. New analyses reveal that beneficial microbes often share mechanisms of infection and defense with parasites, and can also exhibit rapid evolution and extensive genetic exchange. To explain these patterns, new paradigms must take into account the varied population biology of beneficial microbes, their potential conflicts with hosts, and the mosaic nature of genome evolution that requires locus-based tests to analyze the genetics of host adaptation.     

The genetic architecture of a niche: variation and covariation in host use traits in the Colorado potato beetle

The genetic basis of host plant use by phytophagous insects can provide insight into the evolution of ecological niches, especially phenomena such as specialization and phylogenetic conservatism. We carried out a quantitative genetic analysis of multiple host use traits, estimated on five species of host plants, in the Colorado potato beetle, Leptinotarsa decemlineata (Coleoptera: Chrysomelidae). Mean values of all characters varied among host plants, providing evidence that adaptation to plants may require evolution of both behavioral (preference) and post-ingestive physiological (performance) characteristics. Significant additive genetic variation was detected for several characters on several hosts, but not in the capacity to use the two major hosts, a pattern that might be caused by directional selection. No negative genetic correlations across hosts were detected for any 'performance' traits, i.e. we found no evidence of trade-offs in fitness on different plants. Larval consumption was positively genetically correlated across host plants, suggesting that diet generalization might evolve as a distinct trait, rather than by independent evolution of feeding responses to each plant species, but several other traits did not show this pattern. We explored genetic correlations among traits expressed on a given plant species, in a first effort to shed light on the number of independent traits that may evolve in response to selection for host-plant utilization. Most traits were not correlated with each other, implying that adaptation to a novel potential host could be a complex, multidimensional 'character' that might constrain adaptation and contribute to the pronounced ecological specialization and the phylogenetic niche conservatism that characterize many clades of phytophagous insects.     

Wing morphology is related to host plants in cactophilic Drosophila gouveai and Drosophila antonietae (Diptera,Drosophilidae)

A central issue in evolutionary biology is to understand the mechanisms promoting morphological evolution during speciation. In a previous study, we showed that the Neotropical cactophilic sibling species Drosophila gouveai and Drosophila antonietae can be reared in media prepared with their presumptive natural host plants (Pilosocereus machrisis and Cereus hildmaniannus) and that egg to adult viability is not independent of the cactus host. In the present study, we investigate the effects of ecological and genetic factors on interspecific divergence in wing morphology, in relation to the pattern of wing venation and phenotypic plasticity in D. gouveai and D. antonietae, by means of the comparative analysis of isofemale lines reared in the two cactus hosts. The species differed significantly in wing size and shape, although specific differences were mainly localized in a particular portion of the wing. We detected significant variation in form among lines, which was not independent of the breeding cactus, suggesting the presence of genetic variation for phenotypic plasticity and wing shape variation in both species. We discuss the results considering the plausible role of host plant use in the evolutionary history of cactophilic Drosophila inhabiting the arid zones of South America. © 2008 The Linnean Society of London, Biological Journal of the Linnean Society, 2008, 95 , 655–665.     

THE GENETIC STRUCTURE OF HOST PLANT ADAPTATION IN A SPATIAL PATCHWORK: DEMOGRAPHIC VARIABILITY AMONG RECIPROCALLY TRANSPLANTED PEA APHID CLONES

Populations of insect herbivores that feed on several host plant species may experience different selective forces on each host. When the hosts cooccur in a local area, herbivore populations can provide useful models for the study of evolutionary mechanisms in patchy environments. A first step in such a study involves determination of the genetic structure of host adaptation in the region: how is genetic variation for host use structured within and between subpopulations of herbivores on each host? The structure of genetic variation for host use reveals patterns of local adaptation, probable selective consequences of migration between hosts, and the potential for further evolution. To estimate the population structure of host adaptation in a patchwork, 7–11 pea aphid clones were collected at the beginning of the summer from each of two alfalfa and two red clover fields within a very localized area (about 15–20 km²). Using a reciprocal transplant in the field, replicates of these 35 clones were allowed to develop individually on each of the two crops. A complete life table was made for each replicate. Individual fitness was calculated from the life tables as the expected rate of population increase; longevity, age at first reproduction, and total fecundity were also measured for each clonal replicate. Currently, experimental estimates of genetic variation in complete life tables are virtually nonexistent for natural populations, even for single environments (Charlesworth, 1987); field studies are even less common. Because clones from each of two source crops were tested reciprocally on both hosts, variation in relative genotypic fitness on alfalfa and clover could be partitioned among clones within source crops, between fields of the same crop, and between source crops (alfalfa or red clover), providing a view of population structure. Significant clonal variation in relative performance on alfalfa and red clover was found: clones tended to have higher fitness on the crop from which they had been collected (the “home” crop) than they did on the “away” crop, suggesting local adaptation in response to patchy patterns of selection. Clonal variability within collections from the two crops suggests the potential for changes in the genetic constitution of these aphid populations within established fields as a result of clonal selection during the summer season. Significantly negative genetic correlations across crops were found for fitness and its major components. The possibility that these negative cross-environment correlations could act as evolutionary constraints on adaptation to the patchwork is considered.     

Multihost experimental evolution of a plant RNA virus reveals local adaptation and host-specific mutations

For multihost pathogens, adaptation to multiple hosts has important implications for both applied and basic research. At the applied level, it is one of the main factors determining the probability and the severity of emerging disease outbreaks. At the basic level, it is thought to be a key mechanism for the maintenance of genetic diversity both in host and pathogen species. Using Tobacco etch potyvirus (TEV) and four natural hosts, we have designed an evolution experiment whose strength and novelty are the use of complex multicellular host organism as hosts and a high level of replication of different evolutionary histories and lineages. A pattern of local adaptation, characterized by a higher infectivity and virulence on host(s) encountered during the experimental evolution was found. Local adaptation only had a cost in terms of performance on other hosts in some cases. We could not verify the existence of a cost for generalists, as expected to arise from antagonistic pleiotropy and other genetic mechanisms generating a fitness trade-off between hosts. This observation confirms that this classical theoretical prediction lacks empirical support. We discuss the reasons for this discrepancy between theory and experiment in the light of our results. The analysis of full genome consensus sequences of the evolved lineages established that all mutations shared between lineages were host specific. A low degree of parallel evolution was observed, possibly reflecting the various adaptive pathways available for TEV in each host. Altogether, these results reveal a strong adaptive potential of TEV to new hosts without severe evolutionary constraints.     

Evolutionary feedback mediated through population density, illustrated with viruses in chemostats

A cornerstone of evolutionary ecology is that population density affects adaptation: r and K selection is the obvious example. The reverse is also appreciated: adaptation impacts population density. Yet, empirically demonstrating a direct connection between population density and adaptation is challenging. Here, we address both evolution and ecology of population density in models of viral (bacteriophage) chemostats. Chemostats supply nutrients for host cell growth, and the hosts are prey for viral reproduction. Two different chemostat designs have profoundly different consequences for viral evolution. If host and virus are confined to the same chamber, as in a predator-prey system, viral regulation of hosts feeds back to maintain low viral density (measured as infections per cell). Viral adaptation impacts host density but has a small effect on equilibrium viral density. More interesting are chemostats that supply the viral population with hosts from a virus-free refuge. Here, a type of evolutionary succession operates: adaptation at low viral density leads to higher density, but high density then favors competitive ability. Experiments support these models with both phenotypic and molecular data. Parallels to these designs exist in many natural systems, so these experimental systems may yield insights to the evolution and regulation of natural populations.     

Local adaptation, resistance, and virulence in a hemiparasitic plant-host plant interaction

Abstract.— Coevolution may lead to local adaptation of parasites to their sympatric hosts. Locally adapted parasites are, on average, more infectious to sympatric hosts than to allopatric hosts of the same species or their fitness on the sympatric hosts is superior to that on allopatric hosts. We tested local adaptation of a hemiparasitic plant, Rhinanthus serotinus (Scrophulariaceae), to its host plant, the grass Agrostis capillaris . Using a reciprocal cross-infection experiment, we exposed host plants from four sites to hemiparasites originating from the same four sites in a common environment. The parasites were equally able to establish haustorial connections to sympatric and allopatric hosts, and their performance was similar on both host types. Therefore, these results do not indicate local adaptation of the parasites to their sympatric hosts. However, the parasite populations differed in average biomass and number of flowers per plant and in their effect on host biomass. These results indicate that the virulence of the parasite varied among populations, suggesting genetic variation. Theoretical models suggest that local adaptation is likely to be detected if the host and the parasite have different evolutionary potentials, different migration rates, and the parasite is highly virulent. In the interaction between R. serotinus and A. capillaris all the theoretical prerequisites for local adaptation may not be fulfilled.     

Rapid appearance of epistasis during adaptive divergence following colonization

Theory predicts that short-term adaptation within populations depends on additive (A) genetic effects, while gene-gene interactions 'epistasis (E)' are important only in long-term evolution. However, few data exist on the genetic architecture of adaptive variation, and the relative importance of A versus non-additive genetic effects continues to be a central controversy of evolutionary biology after more than 70 years of debate. To examine this issue directly, we conducted hybridization experiments between two populations of wild soapberry bugs that have strongly differentiated in 100 or fewer generations following a host plant shift. Contrary to expectation, we found that between-population E and dominance (D) have appeared quickly in the evolution of new phenotypes. Rather than thousands of generations, adaptive gene differences between populations have evolved in tens. Such complex genetic variation could underlie the seemingly extreme rates of evolution that are increasingly reported in many taxa. In the case of the soapberry bug, extraordinary ecological opportunity, rather than mortality, may have created hard selection for genetic variants. Because ultimate division of populations into genetic species depends on epistatic loss of hybrid compatibility, local adaptation based on E may accelerate macro-evolutionary diversification.     

Contrasting population genetic patterns and evolutionary histories among sympatric Sonoran Desert cactophilic Drosophila

We studied population genetic differentiation in the sympatric Sonoran Desert cactophilic flies Drosophila pachea, D. mettleri and D. nigrospiracula across their continental and peninsular ranges. These flies show marked differences in ecology and behaviour including dispersal distances and host cactus specialization. Examination of a fragment of the mitochondrial cytochrome oxidase subunit I gene (mtCOI) reveals that the Sea of Cortez has constituted an effective dispersal barrier for D. pachea, leading to significant genetic differentiation between the continental and peninsular ranges of this species. No genetic differentiation was detected, however, within its continental and peninsular ranges. In contrast, our mtCOI-based results for D. mettleri and D. nigrospiracula are consistent with a previous allozyme-based study that showed no significant genetic differentiation between continental and peninsular ranges of these two species. For D. mettleri, we also found that the insular population from Santa Catalina Island, California, is genetically differentiated with respect to continental and peninsular localities. We discuss how differences in the genetic structure patterns of D. pachea, D. mettleri and D. nigrospiracula may correspond to differences in their dispersal abilities, host preferences and behaviour.     

Local adaptation and ecological genetics of host-plant specialization in a leaf beetle

The tendency of insect species to evolve specialization to one or a few plant species is probably a major reason for the remarkable diversity of herbivorous insects. The suggested explanations for this general trend toward specialization include a range of evolutionary mechanisms, whose relative importance is debated. Here we address two potentially important mechanisms: (i) how variation in the geographic distribution of host use may lead to the evolution of local adaptation and specialization; (ii) how selection for specialization may lead to the evolution of trade‐offs in performance between different hosts. We performed a quantitative genetic experiment of larval performance in three different populations of the alpine leaf beetle Oreina elongata reared on two of its main host plants. Due to differences in host availability, each population represents a distinctly different selective regime in terms of host use including selection for specialization on one or the other host as well as selection for utilizing both hosts during the larval stage. The results suggest that selection for specialization has lead to some degree of local adaptations in host use: both single‐host population had higher larval growth rate on their respective native host plant genus, while there was no difference between plant treatments in the two‐host population. However, differences between host plant treatments within populations were generally small and the degree of local adaptation in performance traits seems to be relatively limited. Genetic correlations in performance traits between the hosts ranged from zero in the two‐host population to significantly positive in the single‐host populations. This suggests that selection for specialization in single host populations typically also increased performance on the alternative host that is not naturally encountered. Moreover, the lack of a positive genetic correlation in the two host‐population give support for the hypothesis that performance trade‐offs between two host plants may typically evolve when a population have adapted to both these plants. We conclude that although there is selection for specialization in larval performance traits it seems as if the genetic architecture of these traits have limited the divergence between populations in relative performance on the two hosts.     

Adaptation in a spider mite population after long-term evolution on a single host plant

Evolution in a single environment is expected to erode genetic variability, thereby precluding adaptation to novel environments. To test this, a large population of spider mites kept on cucumber for approximately 300 generations was used to establish populations on novel host plants (tomato or pepper), and changes in traits associated to adaptation were measured after 15 generations. Using a half-sib design, we investigated whether trait changes were related to genetic variation in the base population. Juvenile survival and fecundity exhibited genetic variation and increased in experimental populations on novel hosts. Conversely, no variation was detected for host choice and developmental time and these traits did not evolve. Longevity remained unchanged on novel hosts despite the presence of genetic variation, suggesting weak selection for this trait. Hence, patterns of evolutionary changes generally matched those of genetic variation, and changes in some traits were not hindered by long-term evolution in a constant environment.     

Rapid climate change and the rate of adaptation: insight from experimental quantitative genetics

CONTENTS: Summary 752 I. Introduction 752 II. Will migration be enough? 753 III. Can adaptation proceed fast enough? 754 IV. Fitness links demographic and evolutionary processes 755 V. Experimental studies: what do they tell us and how can we improve them? 756 VI. Predicting evolutionary change based on genetic variation and natural selection 757 VII. The chronosequence approach 758 VIII. Resurrection of ancestral propagules 759 IX. The mean and variance in fitness, a link between genetics and demography 760 X. Conclusions 762 Acknowledgements 762 References 762 SUMMARY: Evolution proceeds unceasingly in all biological populations. It is clear that climate-driven evolution has molded plants in deep time and within extant populations. However, it is less certain whether adaptive evolution can proceed sufficiently rapidly to maintain the fitness and demographic stability of populations subjected to exceptionally rapid contemporary climate change. Here, we consider this question, drawing on current evidence on the rate of plant range shifts and the potential for an adaptive evolutionary response. We emphasize advances in understanding based on theoretical studies that model interacting evolutionary processes, and we provide an overview of quantitative genetic approaches that can parameterize these models to provide more meaningful predictions of the dynamic interplay between genetics, demography and evolution. We outline further research that can clarify both the adaptive potential of plant populations as climate continues to change and the role played by ongoing adaptation in their persistence.     

Genetics of host-parasite interactions

The evolution of host susceptibility or resistance to parasites has important consequences for the evolution of parasite virulence, host sexual selection, population dynamics of both host and parasite populations, and programs of biological control. The general observation of a fraction of Individuals within a population that is not parasitized, and/or the variability in parasite intensity among hosts, may reflect several phenomena acting at different levels of ecological organization. Yet, host-parasite coevolution requires host susceptibility and parasite virulence to be genetically variable. In spite of evolutionary and epidemiological implications of genetic heterogeneities in host-parasite systems, evidence concerning natural populations is still scarce. Here, we wish to emphasize why we need a better knowledge of the genetics of host-parasite interaction in natural populations and to review the evidence concerning the heritability of host susceptibility or resistance to parasites in natural populations of animals.     

Experimental evolution of field populations of Daphnia magna in response to parasite treatment

Although there is little doubt that hosts evolve to reduce parasite damage, little is known about the evolutionary time scale on which host populations may adapt under natural conditions. Here we study the effects of selection by the microsporidian parasite Octosporea bayeri on populations of Daphnia magna. In a field study, we infected replicated populations of D. magna with the parasite, leaving control populations uninfected. After two summer seasons of experimental evolution (about 15 generations), the genetic composition of infected host populations differed significantly from the control populations. Experiments revealed that hosts from the populations that had evolved with the parasite had lower mortality on exposure to parasite spores and a higher competitive ability than hosts that had evolved without the parasite. In contrast, the susceptibility of the two treatment groups to another parasite, the bacterium Pasteuria ramosa, which was not present during experimental evolution of the populations, did not differ. Fitness assays in the absence of parasites revealed a higher fitness for the control populations, but only under low population density with high resource availability. Overall, our results show that, under natural conditions, Daphnia populations are able to adapt rapidly to the prevailing conditions and that this evolutionary change is specific to the environment.     

Origin, fate, and architecture of ecologically relevant genetic variation

Recent advances in molecular genetics combined with field manipulations are yielding new insight into the origin, evolutionary fate, and genetic architecture of phenotypic variation in natural plant populations, with two surprising implications for the evolution of plant genomes. First, genetic loci exhibiting antagonistic pleiotropy across natural environments appear rare relative to loci that are adaptive in one or more environments and neutral elsewhere. These 'conditionally neutral' alleles should sweep to fixation when they arise, yet genome comparisons find little evidence for such selective sweeps. Second, genes under biotic selection tend to be of larger effect than genes under abiotic selection. Recent theory suggests this may be a consequence of high gene flow among populations under selection for local adaptation.     

Phylogenetic analysis reveals positive correlations between adaptations to diverse hosts in a group of pathogen‐like herbivores

A jack of all trades can be master of none—this intuitive idea underlies most theoretical models of host‐use evolution in plant‐feeding insects, yet empirical support for trade‐offs in performance on distinct host plants is weak. Trade‐offs may influence the long‐term evolution of host use while being difficult to detect in extant populations, but host‐use evolution may also be driven by adaptations for generalism. Here we used host‐use data from insect collection records to parameterize a phylogenetic model of host‐use evolution in armored scale insects, a large family of plant‐feeding insects with a simple, pathogen‐like life history. We found that a model incorporating positive correlations between evolutionary changes in host performance best fit the observed patterns of diaspidid presence and absence on nearly all focal host taxa, suggesting that adaptations to particular hosts also enhance performance on other hosts. In contrast to the widely invoked trade‐off model, we advocate a “toolbox” model of host‐use evolution in which armored scale insects accumulate a set of independent genetic tools, each of which is under selection for a single function but may be useful on multiple hosts.