The Role of Adaptation to Host Plants in the Evolution of Reproductive Isolation: Negative Evidence from Tetranychus Urticae Koch

Reproductive isolation between demes of a phytophagous arthropod population that use different host plant species could evolve in two different ways. First, adaptation to different host species might result in reproductive isolation as a pleiotropic by-product. Second, if adaptation to one host species strongly reduces fitness on others, selection could favour mechanisms, such as host fidelity and assortative mating, that restrict gene flow between host-adapted demes. A laboratory selection experiment on the broadly polyphagous spider mite Tetranychus urticae gave information on these possibilities. A population allowed to adapt to tomato plants showed increased survival, development rate and fecundity on tomato relative to the base population from which it was derived. In spite of the large difference between the tomato-adapted and base populations in performance on tomato plants, the two populations showed no evidence of reproductive isolation, as measured by the hatching rate of eggs laid by F1 hybrids between the lines. Furthermore, a genetically variable population formed by hybridizing the tomato-adapted and base populations did not show evidence for a decline in ability to survive on tomato after more than ten generations of mass rearing on lima bean, indicating that tomato-adapted genotypes suffered little or no selective disadvantage on bean. These results give no support for the role of host plants in the evolution of reproductive isolation in T. urticae.     

Reverse evolution of fitness in Drosophila melanogaster

Abstract The evolution of fitness is central to evolutionary theory, yet few experimental systems allow us to track its evolution in genetically and environmentally relevant contexts. Reverse evolution experiments allow the study of the evolutionary return to ancestral phenotypic states, including fitness. This in turn permits well‐defined tests for the dependence of adaptation on evolutionary history and environmental conditions. In the experiments described here, 20 populations of heterogeneous evolutionary histories were returned to their common ancestral environment for 50 generations, and were then compared with both their immediate differentiated ancestors and populations which had remained in the ancestral environment. One measure of fitness returned to ancestral levels to a greater extent than other characters did. The phenotypic effects of reverse evolution were also contingent on previous selective history. Moreover, convergence to the ancestral state was highly sensitive to environmental conditions. The phenotypic plasticity of fecundity, a character directly selected for, evolved during the experimental time frame. Reverse evolution appears to force multiple, diverged populations to converge on a common fitness state through different life‐history and genetic changes.     

The evolution of dispersal polymorphisms in insects: The influence of habitats,host plants and mates

Wing-dimorphic, delphacid planthoppers were used to test hypotheses concerning the effects of habitat persistence and architectural complexity on the occurrence of dispersal. For reasons concerning both the durational stability of the habitat and the reduced availability of mates, selection has favored high levels of dispersal in species occupying temporary habitats. Flightlessness predominates in species occupying persistent habitats, and is promoted by a phenotypic trade-off between reproductive success and flight capability. Wings are retained in tree-inhabiting species, probably for reasons concerning the more effective negotiation of three-dimensional habitats. In contrast, flightlessness is characteristic of those species inhabiting low profile host plants. For several delphacid genera, migratory species are larger than their sedentary congeners. Because body size and fecundity are positively related in planthoppers, the large body size observed in migratory taxa may result from selection for increased fecundity in colonizing species.     

Molecular evolution and population genetics of two Drosophila mettleri cytochrome P450 genes involved in host plant utilization

Understanding the genetic basis of adaptation is one of the primary goals of evolutionary biology. The evolution of xenobiotic resistance in insects has proven to be an especially suitable arena for studying the genetics of adaptation, and resistant phenotypes are known to result from both coding and regulatory changes. In this study, we examine the evolutionary history and population genetics of two Drosophila mettleri cytochrome P450 genes that are putatively involved in the detoxification of alkaloids present in two of its cactus hosts: saguaro (Carnegiea gigantea) and senita (Lophocereus schottii). Previous studies demonstrated that Cyp28A1 was highly up-regulated following exposure to rotting senita tissue while Cyp4D10 was highly up-regulated following exposure to rotting saguaro tissue. Here, we show that a subset of sites in Cyp28A1 experienced adaptive evolution specifically in the D. mettleri lineage. Moreover, neutrality tests in several populations were also consistent with a history of selection on Cyp28A1. In contrast, we did not find evidence for positive selection on Cyp4D10, although this certainly does not preclude its involvement in host plant use. A surprising result that emerged from our population genetic analyses was the presence of significant genetic differentiation between flies collected from different host plant species (saguaro and senita) at Organ Pipe National Monument, Arizona, USA. This preliminary evidence suggests that D. mettleri may have evolved into distinctive host races that specialize on different hosts, a possibility that warrants further investigation.     

Intrinsic rate of population increase of the spider mite Tetranychus urticae on the ornamental crop gerbera: intraspecific variation in host plant and herbivore

Eight cultivars of the ornamental crop Gerbera jamesonii Bolus (Asteraceae) were compared in host plant suitability for the two spotted spider mite Tetranychus urticae Koch (Acarina: Tetranychidae). This was done by determining the intrinsic rate of population increase, rm, of spider mites on leaf discs of plants from each of the cultivars. Large differences in rm values were found, ranging from 0.088/day on cultivar Bianca to 0.242/day on cultivar Sirtaki. This variation in rm was mainly caused by differences in developmental time of the spider mites.We assessed the performance of spider mites on young and old leaves of the two gerbera cultivars Bianca and Sirtaki. On Sirtaki the spider mites had a shorter developmental time and higher peak oviposition rate on young leaves than on old leaves. However, on Bianca such an effect was not found.We also determined the performance of two spider mite strains on the resistant gerbera cultivar Bianca. We compared the rm of a strain that had been reared on this cultivar for approximately half a year with the rm of a strain that was reared on bean. The rm of the strain that was reared on cultivar Bianca increased to 0.208/day, which is however still substantially lower than the rm on the susceptible cultivar Sirtaki.     

Evolutionary origins of a novel host plant detoxification gene in butterflies

Chemical interactions between plants and their insect herbivoresprovide an excellent opportunity to study the evolution of speciesinteractions on a molecular level. Here, we investigate themolecular evolutionary events that gave rise to a novel detoxifyingenzyme (nitrile-specifier protein [NSP]) in the butterfly familyPieridae, previously identified as a coevolutionary key innovation.By generating and sequencing expressed sequence tags, genomiclibraries, and screening databases we found NSP to be a memberof an insect-specific gene family, which we characterized andnamed the NSP-like gene family. Members consist of variabletandem repeats, are gut expressed, and are found across Insectaevolving in a dynamic, ongoing birth–death process. Inthe Lepidoptera, multiple copies of single-domain major allergengenes are present and originate via tandem duplications. Multipledomain genes are found solely within the brassicaceous-feedingPieridae butterflies, one of them being NSP and another calledmajor allergen (MA). Analyses suggest that NSP and its paralogMA have a unique single-domain evolutionary origin, being formedby intragenic domain duplication followed by tandem whole-geneduplication. Duplicates subsequently experienced a period ofrelaxed constraint followed by an increase in constraint, perhapsafter neofunctionalization. NSP and its ortholog MA are stillexperiencing high rates of change, reflecting a dynamic evolutionconsistent with the known role of NSP in plant–insectinteractions. Our results provide direct evidence to the hypothesisthat gene duplication is one of the driving forces for speciationand adaptation, showing that both within- and whole-gene tandemduplications are a powerful force underlying evolutionary adaptation.     

Boechera, a model system for ecological genomics

The selection and development of a study system for evolutionary and ecological functional genomics (EEFG) depend on a variety of factors. Here, we present the genus Boechera as an exemplary system with which to address ecological and evolutionary questions. Our focus on Boechera is based on several characteristics as follows: (i) native populations in undisturbed habitats where current environments reflect historical conditions over several thousand years; (ii) functional genomics benefitting from its close relationship to Arabidopsis thaliana; (iii) inbreeding tolerance enabling development of recombinant inbred lines, near-isogenic lines and positional cloning; (iv) interspecific crosses permitting mapping for genetic analysis of speciation; (v) apomixis (asexual reproduction by seeds) in a genetically tractable diploid; and (vi) broad geographic distribution in North America, permitting ecological genetics for a large research community. These characteristics, along with the current sequencing of three Boechera species by the Joint Genome Institute, position Boechera as a rapidly advancing system for EEFG studies.     

Intraspecific variation in a generalist herbivore accounts for differential induction and impact of host plant defences

Plants and herbivores are thought to be engaged in a coevolutionary arms race: rising frequencies of plants with anti-herbivore defences exert pressure on herbivores to resist or circumvent these defences and vice versa. Owing to its frequency-dependent character, the arms race hypothesis predicts that herbivores exhibit genetic variation for traits that determine how they deal with the defences of a given host plant phenotype. Here, we show the existence of distinct variation within a single herbivore species, the spider mite Tetranychus urticae, in traits that lead to resistance or susceptibility to jasmonate (JA)-dependent defences of a host plant but also in traits responsible for induction or repression of JA defences. We characterized three distinct lines of T. urticae that differentially induced JA-related defence genes and metabolites while feeding on tomato plants (Solanum lycopersicum). These lines were also differently affected by induced JA defences. The first line, which induced JA-dependent tomato defences, was susceptible to those defences; the second line also induced JA defences but was resistant to them; and the third, although susceptible to JA defences, repressed induction. We hypothesize that such intraspecific variation is common among herbivores living in environments with a diversity of plants that impose diverse selection pressure.     

The genomic and physiological basis of life history variation in a butterfly metapopulation

Unravelling the mechanisms underlying variation in life history traits is of fundamental importance for our understanding of adaptation by natural selection. While progress has been made in mapping fitness-related phenotypes to genotypes, mainly in a handful of model organisms, functional genomic studies of life history adaptations are still in their infancy. In particular, despite a few notable exceptions, the genomic basis of life history variation in natural populations remains poorly understood. This is especially true for the genetic underpinnings of life history phenotypes subject to diversifying selection driven by ecological dynamics in patchy environments--as opposed to adaptations involving strong directional selection owing to major environmental changes, such as latitudinal gradients, extreme climatic events or transitions from salt to freshwater. In this issue of Molecular Ecology,Wheat et al. (2011) now make a significant leap forward by applying the tools of functional genomics to dispersal-related life history variation in a butterfly metapopulation. Using a combination of microarrays, quantitative PCR and physiological measurements, the authors uncover several metabolic and endocrine factors that likely contribute to the observed life history phenotypes. By identifying molecular candidate mechanisms of fitness variation maintained by dispersal dynamics in a heterogeneous environment,they also begin to address fascinating interactions between the levels of physiology, ecology and evolution.     

Multiple host use by a sap-sucking membracid: population consequences of nymphal development on primary and secondary host plant species

Aconophora compressa is a gregarious, sap-sucking insect that uses multiple host plant species. Nymphal host plant species (and variety) significantly affected nymphal survival, nymphal development rate and the subsequent size and fecundity of adults, with fiddlewood (Citharexylum spinosum) being significantly best in all respects. Nymphs that developed on a relatively poor host (Duranta erecta var “geisha girl”) and which were moved to fiddlewood as adults laid significantly fewer eggs (mean ± SE = 836 ± 130) than those that developed solely on fiddlewood (1,329 ± 105). Adults on geisha girl, regardless of having been reared as nymphs on fiddlewood or geisha girl, laid significantly fewer eggs (342 ± 83 and 317 ± 74, respectively) than adults on fiddlewood. A simple model that incorporates host plant related survival, development rate and fecundity suggests that the population dynamics of A. compressa are governed mainly by fiddlewood, the primary host. The results have general implications for understanding the population dynamics of herbivores that use multiple host plant species, and also for the way in which weed biological control host testing methods should be conducted. Handling Editor: Robert Glinwood     

Local adaptation and effect of host genotype on the rate of pathogen evolution: an experimental test in a plant pathosystem

Abstract Virulence is thought to be a driving force in host–pathogen coevolution. Theoretical models suggest that virulence is an unavoidable consequence of pathogens evolving towards a high rate of intrahost reproduction. These models predict a positive correlation between the reproductive fitness of a pathogen and its level of virulence. Theoretical models also suggest that the demography and genetic structure of a host population can influence the evolution of virulence. If evolution occurs faster in pathogen populations than in host populations, the predicted result is local adaptation of the pathogen population. In our studies, we used a combination of molecular and physiological markers to test these hypotheses in an agricultural system. We isolated five strains of the fungal pathogen Mycosphaerella graminicola from each of two wheat cultivars that differed in their level of resistance to this pathogen. Each of the 10 fungal strains had distinct genotypes as indicated by different DNA fingerprints. These fungal strains were re‐inoculated onto the same two host cultivars in a field experiment and their genotype frequencies were monitored over several generations of asexual reproduction. We also measured the virulence of these 10 fungal strains and correlated it to the reproductive fitness of each fungal strain. We found that host genotypes had a strong impact on the dynamics of the pathogen populations. The pathogen population collected from the moderately resistant cultivar Madsen showed greater stability, higher genotype diversity, and smaller selection coefficients than the pathogen populations collected from the susceptible cultivar Stephens or a mixture of the two host cultivars. The pathogen collection from the mixed host population was midway between the two pure lines for most parameters measured. Our results also revealed that the measures of reproductive fitness and virulence of a pathogen strain were not always correlated. The pathogen strains varied in their patterns of local adaptation, ranging from locally adapted to locally maladapted.     

Pyrrolizidine alkaloids in arctiid moths (Lep.) with a discussion on host plant relationships and the role of these secondary plant substances in the Arctiidae

Pyrrolizidine alkaloids (PA) have been identified in six species of Arctiidae reared on Senecio and Crotalaria. These include senecionine, seneciphylline, integerrimine, jacobine, jacozine, jacoline, jaconine and a metabolite (C₁₅H₂₅NO₅) from Senecio , and monocrotaline, trichodesmine and crispatine from Crotalaria.
The all-red aberration of Tyria jacobaeae (var. conyi) contained much less of the metabolite than normal examples of this species. Female Spilosoma lutea reared on the same plants of S. jacobaea contained markedly more jacobine and jacoline than die males.
Host plant relationships and secondary plant substances are discussed. It is suggested that the Arctiid moths' own deterrent secretions, directed against vertebrate predators, pre-adapts them for feeding on foliage likewise protected against large herbivores by toxic secondary plant substances such as cardenolides and pyrrolizidine alkaloids. These latter substances are more toxic to vertebrate than to insect herbivores, and their dual function of deterrent and insect aphrodisiac puts a premium on their sequestration and storage once a species has achieved the initial steps, and occupied the plant niche concerned. It is further suggested that the polyphagous habits of the Arctiidae result in a more equitable distribution of die secondary plant substances within the Mullerian complex concerned, thus providing a generalized warning message for the potential vertebrate predator.     

Trade-offs in performance on different plants may not restrict the host plant range of the phytophagous mite, Tetranychus urticae

We examined sib-mated lines of the phytophagous mite, Tetranychus urticae Koch, for trade-offs in performance on different plants. We found no significant trade-offs among 10 potential host plants examined. Trade-offs in performance were not detected in most cases, even when the variations in general performance (mean performance on all potential host plants) among the sib-mated lines were statistically adjusted, denying the possibility that this may be due to the variations in general performance among the lines. No evidence for trade-offs was obtained in an artificial selection experiment; on all tested plants, a line adapted to one marginal host plant exhibited higher performance than the control line. However, the general performance seemed to be negatively correlated with other adaptive traits of the mite, such as competition ability of adult males for their mates and overcrowding response of adult females. Such correlations may contribute to the maintenance of genetic variation in the general performance of T. urticae.     

Ecological genetics of host plant exploitation in the green peach aphid, Myzus persicae

The ecological consequences of genetic variability in host plant exploitation of Myzus persicae (Hemiptera, Aphididae) were studied in several agro-ecosystems, differing in crop plant heterogeneity. An analysis of aphid populations sampled from sugar beet, potatoes, and lettuce revealed changes in the frequency distribution of aphid clones according to their respective host plant adaptations. The spatial unit of differentiation was below an average field size of 3–5 hectares and a differentiation could be found in the centre of potato and sugar beet fields but not at the edge of the fields. On a temporal scale, the differentiation of populations is transitory even on a large-scale basis of highly specialized cropping areas. The ecological parameters of differentiation are discussed with special reference to agro-ecosystems and integrated pest management. Increasing the genetic heterogeneity of crop fields may help to reduce population outbreaks.

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Zusammenfassung Die ökologischen Konsequenzen genetischer Variabilität in der Wirtspflanzennutzung von Myzus persicae (Hemiptera, Aphididae) wurden in mehreren Agro-Ökosystemen untersucht, die sich in der Kulturpflanzenheterogenität unterscheiden. Eine Analyse von auf Rüben, Kartoffeln und Salat siedelnden Populationen zeigte eine genetische Differenzierung in Wirtspflanzen-angepaßte Feld-populationen. Die räumliche Einheit solcher Differenzierungen liegt unterhalb einer Feldgröße von 3–5 ha. Eine Differenzierung konnte hier in der Mitte der Felder aber nicht am Rand festgestellt werden. Aus zeitlicher Sicht ist die Differenzierung selbst in großräumigen, spezialisierten Anbaugebieten nur vorübergehend feststellbar. Die ökologischen Parameter der Differenzierung werden besonders in Hinsicht auf die integrierte Schädlingsbekämpfung in Agro-ökosystemen diskutiert. Eine Erhöhung der genetischen Heterogenität von Kulturpflanzenbeständen kann möglicherweise zu einer Verringerung von Blattlaus-Massenvermehrungen beitragen.

     

The earliest stages of adaptation in an experimental plant population: strong selection on QTLS for seed dormancy

Colonizing species may often encounter strong selection during the initial stages of adaptation to novel environments. Such selection is particularly likely to act on traits expressed early in development since early survival is necessary for the expression of adaptive phenotypes later in life. Genetic studies of fitness under field conditions, however, seldom include the earliest developmental stages. Using a new set of recombinant inbred lines, we present a study of the genetic basis of fitness variation in Arabidopsis thaliana in which genotypes, environments, and geographic location were manipulated to study total lifetime fitness, beginning with the seed stage. Large‐effect quantitative trait loci (QTLs) for fitness changed allele frequency and closely approached 90% in some treatments within a single generation. These QTLs colocated with QTLs for germination phenology when seeds were dispersed following a schedule of a typical winter annual, and they were detected in two geographic locations at different latitudes. Epistatically interacting loci affected both fitness and germination in many cases. QTLs for field germination phenology colocated with known QTLs for primary dormancy induction as assessed in laboratory tests, including the candidate genes DOG1 and DOG6. Therefore fitness, germination phenology, and primary dormancy are genetically associated at the level of specific chromosomal regions and candidate loci. Genes associated with the ability to arrest development at early life stages and assess environmental conditions are thereby likely targets of intense natural selection early in the colonization process.     

Genetic and phenotypic population divergence on a microgeographic scale in brown trout

Salmonid populations of many rivers are rapidly declining. One possible explanation is that habitat fragmentation increases genetic drift and reduces the populations' potential to adapt to changing environmental conditions. We measured the genetic and eco-morphological diversity of brown trout (Salmo trutta) in a Swiss stream system, using multivariate statistics and Bayesian clustering. We found large genetic and phenotypic variation within only 40 km of stream length. Eighty-eight percent of all pairwise F(ST) comparisons and 50% of the population comparisons in body shape were significant. High success rates of population assignment tests confirmed the distinctiveness of populations in both genotype and phenotype. Spatial analysis revealed that divergence increased with waterway distance, the number of weirs, and stretches of poor habitat between sampling locations, but effects of isolation-by-distance and habitat fragmentation could not be fully disentangled. Stocking intensity varied between streams but did not appear to erode genetic diversity within populations. A lack of association between phenotypic and genetic divergence points to a role of local adaptation or phenotypically plastic responses to habitat heterogeneity. Indeed, body shape could be largely explained by topographic stream slope, and variation in overall phenotype matched the flow regimes of the respective habitats.     

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.     

The impact of intraspecific variation in a fish predator on the evolution of phenotypic plasticity and investment in sex in Daphnia ambigua

Theory predicts that the evolution of phenotypic plasticity depends upon cues that indicate environmental change. Predators typically induce plastic responses in prey. However, variation among populations of predators alters the frequency of predation and, possibly, the evolution of plasticity. We compared responses to predator cues in Daphnia ambigua from lakes where alewife (Alosa pseudoharengus) either do (anadromous) or do not (landlocked) migrate between marine and freshwater. In 'anadromous' lakes, Daphnia are abundant each spring but eliminated by alewives in summer, whereas Daphnia are constantly under the threat of predation in 'landlocked' lakes. Daphnia from 'anadromous' lakes grew faster, matured earlier and larger, produced more offspring and invested more in sex than Daphnia from landlocked lakes. We observed several significant lake type-by-predator treatment interactions. These interactions, whereby the differences between lakes were greater in predator-conditioned water, agree with theory and argue that Daphnia plasticity has been influenced by variation in alewives.