Adaptive genetic structure in phytophagous insect populations

Genetic variation in insect populations is frequently structured into discrete groups, or demes, that form in response to stochastic forces or natural selection. Because host-plant populations are often highly heterogeneous, phytophagous insects may form demes that are adapted to the unique traits of individual plants. Recent field experiments indicate that selection pressures imposed by host-plants can promote rapid adaptive evolution in natural insect populations at very fine spatial scales. Adaptive deme formation may be more common among endophagous insects, which feed and reside within plant tissue, than for externally feeding insects, because internal feeders experience stronger plant-mediated selection pressures.     

Deme formation in scale insects: a test with the pinyon needle scale and a review of other evidence

ABSTRACT. 1. Deme formation is the transformation of a generalist population into one which is adapted to its local conditions. This adaptation has been inferred from many things but should be inferred from higher survival or fecundity of scale insects on their natal tree compared to that of immigrant scales on the same tree.
2. Transfers of the scale insect Matsucoccus acalyptus Herbert within and between infested host trees ( Pinus monophylla (Torr. & Frem.) resulted in significant differences in scale survivorship among recipient trees. Survival on individual trees was correlated across years, indicating stable differences in tree susceptibility to scale.
3. A significant natal tree colonized tree interaction was observed for late stage scale survival in one experiment but the interaction was not caused by superior survivorship of scales transferred back to the natal tree. Hence, we found no evidence of deme formation in M.acalyptus.
4. Previous studies have concluded that deme formation occurs in the black pineleaf scale based on a significant natal tree by colonized tree interaction in scale survival. We question this conclusion because the experimental design employed did not include transfers back onto the natal tree. Other indirect evidence for deme formation in scale insects is critically discussed.     

Variability in leaf traits,insect herbivory and herbivore performance within and among individuals of four broad-leaved tree species

Individual plants may vary in their suitability as hosts for insect herbivores. The adaptive deme formation hypothesis predicts that this variability will lead to the fine-scale adaptation of herbivorous insects to host individuals. We studied individual and temporal variation in the quality of leaves of the tree species ash, lime, common oak, and sycamore in the field as food for herbivores. We determined herbivore attack and leaf consumption and performance of the generalist caterpillars of Spodoptera littoralis in the laboratory. We further assessed the concentrations of carbon, nitrogen and water in the leaves.All measures of leaf tissue quality varied among and within individuals for all tree species. The level of herbivory differed among the tree individuals in lime, oak and sycamore, but not in ash. Within host individuals, differences in herbivory between the upper and lower crown layer varied in direction and magnitude depending on tree species. In feeding experiments, herbivore performance also varied among and within tree individuals. However, variation in palatability was not consistently related to the leaf traits measured or to herbivory levels in the field. The ranking of individuals with respect to the quality of leaf tissue for herbivorous insects varied between years in lime and oak. Thus, trees of both species might present moving targets for herbivores which prevents fine-scale adaptations. In contrast, among individuals of ash and sycamore the pattern of insect performance remained constant over 2 years. These species may be more suitable hosts for the formation of adapted demes in herbivores.     

昆虫记忆的形成机制及生态适应性

介绍近十几年来利用蜜蜂Apis mellifera L.、果蝇Drosophila melanogaster Meigen和寄生蜂等昆虫对学习和记忆行为研究的成果。这些研究表明昆虫的记忆形成是多阶段的。从短时记忆向长时记忆的形成过程中,cAMP反应元件结合蛋白(cAMP response element-bindingprotein,CREB)起重要的作用;而蘑菇体是学习、记忆形成的主要位点。已有的研究还表明昆虫记忆的动态是适应于不同物种的生态学需要。这些研究为探索昆虫和其它动物记忆的形成和生态适应性提供了理论基础。     

Estimate of chitin in raw whole insects

Insects contain significant amounts of fiber as measured by crude fiber, acid detergent fiber (ADF) or neutral detergent fiber (NDF). It has always been assumed that the fiber in insects represents chitin based on the structural similarity between cellulose and chitin and the fact that the ADF fraction from insects contains nitrogen. In this study, a number of insect species that are raised commercially as food for insectivores were analyzed for moisture, crude protein (nitrogen × 6.25), fat, ash, NDF, ADF, and amino acids. Additionally, the ADF fraction was analyzed for nitrogen and amino acids to determine if proteins might be present in the ADF fraction. The ADF fraction contained a significant amount of amino acids accounting for 9.3–32.7% of the ADF (by weight). The presence of amino acids in the ADF fraction means that using ADF to estimate insect chitin results in an overestimation of insect chitin content. Using ADF adjusted for its amino acid content, the estimated chitin content of these insect species ranged from 2.7–49.8 mg/kg (as is) and 11.6–137.2 mg/kg (dry matter basis). Additionally, these data suggest that for the species measured here the amount of chitin nitrogen is quite small (as a % of total nitrogen) and that crude protein (nitrogen × 6.25) provides a reasonable estimate of the true protein for most species of insects. Zoo Biol 0:1–11, 2007. © 2007 Wiley‐Liss, Inc.     

Environmentally dependent expression of heritable variation on early recruitment traits induced by light conditions and provenance in the columnar cactus Pilosocereus leucocephalus

Response to selection depends on heritable genetic variation, which is affected by environmental conditions. The present study experimentally assessed whether the effect of light-related stress and the attenuating effect of shade as a facilitator of seedling germination, survival and growth affect the expression of heritable variation and the potential for a response to selection in the columnar cactus Pilosocereus leucocephalus. A reciprocal transplant experiment combined with the artificial manipulation of light/shade conditions within greenhouses was performed using seeds from controlled crosses of two natural populations (demes PN and SI). Additive genetic variance (V_A), heritability (h²) and the coefficient of variation of additive variance (CV_A) were estimated for per cent of germination, per cent of seedling survival and growth (biomass) under each treatment combination. Although all three recruitment traits showed evidence of different from zero heritability, this result was highly dependent upon the particular transplant site, deme and light treatment combination. The deme that is still not locally adapted (SI) showed significant heritability for all traits and much more potential for a response selection as indicated by a higher CV_A than the locally adapted deme PN. The effect of light conditions on the expression of V_A, h² and CV_A depended on whether the deme was grown in its native or an alien site, but this interaction was only detected for the less adapted deme of SI. Shade conditions promoted by facilitation reduced the evolutionary potential for germination of both demes through an attenuation of genetic differences among genotypes.     

Integrating ancient patterns and current dynamics of insect–plant interactions: Taxonomic and geographic variation in herbivore specialization

Abstract The search for pattern in the ecology and evolutionary biology of insect–plant associations has fascinated biologists for centuries. High levels of tropical (low-latitude) plant and insect diversity relative to poleward latitudes and the disproportionate abundance of host-specialized insect herbivores have been noted. This review addresses several aspects of local insect specialization, host use abilities (and loss of these abilities with specialization), host-associated evolutionary divergence, and ecological (including “hybrid”) speciation, with special reference to the generation of biodiversity and the geographic and taxonomic identification of “species borders” for swallowtail butterflies (Papilionidae). From ancient phytochemically defined angiosperm affiliations that trace back millions of years to recent and very local specialized populations, the Papilionidae (swallowtail butterflies) have provided a model for enhanced understanding of localized ecological patterns and genetically based evolutionary processes. They have served as a useful group for evaluating the feeding specialization/physiological efficiency hypothesis. They have shown how the abiotic (thermal) environment interacts with host nutrirional suitability to generate “voltinism/suitability” gradients in specialization or preference latitudinally, and geographical mosaics locally. Several studies reviewed here suggest strongly that the oscillation hypothesis for speciation does have considerable merit, but at the same time, some species-level host specializations may lead to evolutionary dead-ends, especially with rapid environmental/habitat changes involving their host plants. Latitudinal gradients in species richness and degree of herbivore feeding specialization have been impacted by recent developments in ecological genetics and evolutionary ecology. Localized insect–plant associations that span the biospectrum from polyphenisms, polymorphisms, biotypes, demes, host races, to cryptic species, remain academically contentious, with simple definitions still debated. However, molecular analyses combined with ecological, ethological and physiological studies, have already begun to unveil some answers for many important ecological/evolutionary questions.     

An omics evolutionary perspective on phytophagous insect–host plant interactions in Anastrepha obliqua: a review

Phytophagous insects have a close relationship with their host plants. For this reason, their interactions can lead to important changes in insect population dynamics and evolutionary trajectories. Next generation sequencing (NGS) has provided an opportunity to analyze omics data on a large scale, facilitating the change from a classical genetics approach to a more holistic understanding of the underlying molecular mechanisms of host plant use by insects. Most studies have been carried out on model species in Holarctic and temperate zones. In tropical zones, however, the effects of use of various host plants on evolutionary insect history is less understood. In the current review, we describe how omics methodologies help us to understand phytophagous insect–host plant interactions from an evolutionary perspective, using as example the Neotropical phytophagous insect West Indian fruit fly, Anastrepha obliqua (Macquart) (Diptera: Tephritidae), an economically important fruit crop pest in the Americas. Anastrepha obliqua could adopt a generalist or a specialist lifestyle. We first review the adaptive molecular mechanisms of phytophagous insects to host plants, and then describe the main tools to study phytophagous insect–host plant interactions in the era of omics sciences. The omics approaches will advance the understanding of insect molecular mechanisms and their influence on diversification and evolution. Finally, we discuss the importance of a multidisciplinary approach that integrates the use of omics tools and other, more classical methodologies in evolutionary studies.     

Phytophagous insect-microbe mutualisms and adaptive evolutionary diversification.

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect-microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

PHYTOPHAGOUS INSECT–MICROBE MUTUALISMS AND ADAPTIVE EVOLUTIONARY DIVERSIFICATION

Adaptive diversification is a process intrinsically tied to species interactions. Yet, the influence of most types of interspecific interactions on adaptive evolutionary diversification remains poorly understood. In particular, the role of mutualistic interactions in shaping adaptive radiations has been largely unexplored, despite the ubiquity of mutualisms and increasing evidence of their ecological and evolutionary importance. Our aim here is to encourage empirical inquiry into the relationship between mutualism and evolutionary diversification, using herbivorous insects and their microbial mutualists as exemplars. Phytophagous insects have long been used to test theories of evolutionary diversification; moreover, the diversification of a number of phytophagous insect lineages has been linked to mutualisms with microbes. In this perspective, we examine microbial mutualist mediation of ecological opportunity and ecologically based divergent natural selection for their insect hosts. We also explore the conditions and mechanisms by which microbial mutualists may either facilitate or impede adaptive evolutionary diversification. These include effects on the availability of novel host plants or adaptive zones, modifying host-associated fitness trade-offs during host shifts, creating or reducing enemy-free space, and, overall, shaping the evolution of ecological (host plant) specialization. Although the conceptual framework presented here is built on phytophagous insect–microbe mutualisms, many of the processes and predictions are broadly applicable to other mutualisms in which host ecology is altered by mutualistic interactions.     

Polyembryony in parasitic wasps: evolution of a novel mode of development

Major developmental innovations have been associated with adaptive radiations that have allowed particular groups of organisms to occupy empty ecospace. Well-known developmental novelties associated with the conquest of new habitats include the evolution of the tetrapode limb, allowing the radiation of vertebrates into a terrestrial habitat, and formation of insect wings that permitted their dispersal into the air. However, an understanding of the evolutionary forces and molecular mechanisms behind developmental novelties still remains tenuous. A little-studied adaptive radiation in insects from the developmental perspective is the evolution of parasitism. The parasitic lifestyle has allowed parasitic insects to occupy a novel ecological niche where they have evolved a plethora of life history strategies and modes of embryogenesis, developing on or within the body of the host. One of the most striking adaptations to development within the body of the host includes polyembryonic development, where certain wasps form clonally up to 2000 embryos from a single egg. Taking advantage of well-established insect phylogeny, techniques developed in a model insect, the fruit fly, and a wealth of knowledge in comparative insect embryology, we are starting to tease apart the evolutionary events that have led to this novel mode of development in insects.     

Herbivore deme formation on individual trees: a test case

We examined the deme-formation hypothesis, which states that sessile herbivores on long-lived hosts become locally adapted to the defensive phenotypes of individual trees. We showed a five-fold increase in resistance by individual pinyon pines (Pinus edulis) to the pinyon pine needle scale (Matsucoccus acalyptus). Although such variation could represent a significant selection pressure favoring deme formation, two lines of evidence led to rejection of the hypothesis. First, there were no significant differences in mortality among scale populations in a reciprocal transfer experiment. Second, a seven-year experiment showed that mortality of newly founded, incipient scale populations was similar to established scale populations. While our experiments fail to support the deme-formation hypothesis, they do demonstrate significant variation in the resistance traits of a natural tree population. Although we feel that demeformation is still probable in this system, it is likely to occur on a larger geographic scale than individual trees as proposed by Edmunds and Alstad.     

Polyketides in insects: ecological role of these widespread chemicals and evolutionary aspects of their biogenesis

Polyketides are known to be used by insects for pheromone communication and defence against enemies. Although in microorganisms (fungi, bacteria) and plants polyketide biogenesis is known to be catalysed by polyketide synthases (PKS), no insect PKS involved in biosynthesis of pheromones or defensive compounds have yet been found. Polyketides detected in insects may also be biosynthesized by endosymbionts. From a chemical perspective, polyketide biogenesis involves the formation of a polyketide chain using carboxylic acids as precursors. Fatty acid biosynthesis also requires carboxylic acids as precursors, but utilizes fatty acid synthases (FAS) to catalyse this process. In the present review, studies of the biosynthesis of insect polyketides applying labelled carboxylic acids as precursors are outlined to exemplify chemical approaches used to elucidate insect polyketide formation. However, since compounds biosynthesised by FAS may use the same precursors, it still remains unclear whether the structures that are formed from e.g. acetate chains (acetogenins) or propanoate chains (propanogenins) are PKS or FAS products. A critical comparison of PKS and FAS architectures and activities supports the hypothesis of a common evolutionary origin of these enzyme complexes and highlights why PKS can catalyse the biosynthesis of much more complex products than can FAS. Finally, we summarise knowledge which might assist researchers in designing approaches for the detection of insect PKS genes.     

PHYLOGENESIS OF INSECT/PLANT INTERACTIONS: HAVE PHYLLOBROTICA LEAF BEETLES (CHRYSOMELIDAE) AND THE LAMIALES DIVERSIFIED IN PARALLEL?

The relative importance of conservative versus locally adapted traits for species interactions is an increasingly common theme in evolutionary ecology. Obligate interactions such as those between parasites and hosts often exhibit such strong phylogenetic conservatism that current associations may reflect diversification in parallel. Parallel phylogenesis, documented for animal parasites, has been doubted for insect/plant interactions, but phylogenetic studies of highly specific insect/plant associations are very few. A comparison of phylogeny estimates for the strictly monophagous Phyllobrotica leaf beetles and their lamialean hostplants shows nearly complete concordance, strongly supporting the hypothesis of parallel diversification. The cladogram concordance is significant or nearly so (consensus index values equalling or exceeding the critical value) under randomization distributions based on Adams (though not Nelson) consensus trees. The one clear exception shows unusual natural history, suggesting an isolated host transfer. Insect distributions and plant fossil ages are consistent with a mid-Tertiary age for both clades, further disfavoring the alternative hypothesis of entirely subsequent evolution. The dependence of both larval and adult beetles on the hostplants, larval endophagy, and possible dependence of beetles on toxic host compounds for defense against predators are suggested to underlie the evolutionary persistence of this interaction. Current host use in these beetles appears to reflect primarily the phylogeny of the interaction, strengthening the thesis that history can play a major role in structuring insect/plant relationships.     

Modeling a version of the good-genes hypothesis: female choice of locally adapted males

In addition to other potential causes, immigration into locally adapted populations has been suggested to maintain the genetic variance in fitness that is necessary for the good-genes hypothesis. Using population-genetic simulations, the present contribution shows that co-occurring local adaptation and migration can maintain genetic variance in fitness. In combination with an effect of local adaptation on condition and condition-dependent sexual signaling, such a scenario therefore enables the evolution and maintenance of female choice for locally adapted males. The simulations show that this mechanism can also work when choice is costly, and that the potential benefit is similar to that in other good-genes mechanisms. As a consequence of female choice in favor of locally adapted males, differentiation between populations can be expected to increase due to the decreased effective gene flow between populations. Based on such effects, choice of locally adapted males has the potential to play an important role in speciation and adaptive radiation.     

Arbuscular mycorrhizal fungi affect phytophagous insect specialism

The majority of phytophagous insects eat very few plant species, yet the ecological and evolutionary forces that have driven such specialism are not entirely understood. The hypothesis that arbuscular mycorrhizal (AM) fungi can determine phytophagous insect specialism, through differential effects on insect growth, was tested using examples from the British flora. In the UK, plant families and species in the family Lamiaceae that are strongly mycorrhizal have higher proportions of specialist insects feeding on them than those that are weakly mycorrhizal. We suggest that AM fungi can affect the composition of insect assemblages on plants and are a hitherto unconsidered factor in the evolution of insect specialism.     

Genomic and morphological evidence converge to resolve the enigma of Strepsiptera

The phylogeny of insects, one of the most spectacular radiations of life on earth, has received considerable attention. However, the evolutionary roots of one intriguing group of insects, the twisted-wing parasites (Strepsiptera), remain unclear despite centuries of study and debate. Strepsiptera exhibit exceptional larval developmental features, consistent with a predicted step from direct (hemimetabolous) larval development to complete metamorphosis that could have set the stage for the spectacular radiation of metamorphic (holometabolous) insects. Here we report the sequencing of a Strepsiptera genome and show that the analysis of sequence-based genomic data (comprising more than 18 million nucleotides from nearly 4,500 genes obtained from a total of 13 insect genomes), along with genomic metacharacters, clarifies the phylogenetic origin of Strepsiptera and sheds light on the evolution of holometabolous insect development. Our results provide overwhelming support for Strepsiptera as the closest living relatives of beetles (Coleoptera). They demonstrate that the larval developmental features of Strepsiptera, reminiscent of those of hemimetabolous insects, are the result of convergence. Our analyses solve the long-standing enigma of the evolutionary roots of Strepsiptera and reveal that the holometabolous mode of insect development is more malleable than previously thought.     

QTL mapping of freezing tolerance: links to fitness and adaptive trade‐offs

Local adaptation, defined as higher fitness of local vs. nonlocal genotypes, is commonly identified in reciprocal transplant experiments. Reciprocally adapted populations display fitness trade‐offs across environments, but little is known about the traits and genes underlying fitness trade‐offs in reciprocally adapted populations. We investigated the genetic basis and adaptive significance of freezing tolerance using locally adapted populations of Arabidopsis thaliana from Italy and Sweden. Previous reciprocal transplant studies of these populations indicated that subfreezing temperature is a major selective agent in Sweden. We used quantitative trait locus (QTL) mapping to identify the contribution of freezing tolerance to previously demonstrated local adaptation and genetic trade‐offs. First, we compared the genomic locations of freezing tolerance QTL to those for previously published QTL for survival in Sweden, and overall fitness in the field. Then, we estimated the contributions to survival and fitness across both field sites of genotypes at locally adaptive freezing tolerance QTL. In growth chamber studies, we found seven QTL for freezing tolerance, and the Swedish genotype increased freezing tolerance for five of these QTL. Three of these colocalized with locally adaptive survival QTL in Sweden and with trade‐off QTL for overall fitness. Two freezing tolerance QTL contribute to genetic trade‐offs across environments for both survival and overall fitness. A major regulator of freezing tolerance, CBF2, is implicated as a candidate gene for one of the trade‐off freezing tolerance QTL. Our study provides some of the first evidence of a trait and gene that mediate a fitness trade‐off in nature.     

Local maladaptation in the soft scale insect Saissetia coffeae (Hemiptera: Coccidae)

Local adaptation has often been documented in herbivorous insects. The potential for local maladaptation in phytophagous insects, however, has not been widely considered. I performed a two-generation reciprocal cross-transplant experiment with the generalist soft scale insect Saissetia coffeae (Hemiptera: Coccidae) on two common species of host plants in rain forest habitat in Costa Rica. In this system, S. coffeae showed significant local maladaptation at the level of the host species. Lineages originally collected from Witheringia enjoyed a strong advantage over those collected from Lomariopsis when both sets of lineages were placed on Lomariopsis; however, when both sets of lineages were raised on Witheringia, their fitnesses were statistically indistinguishable. While some aspects of the biology of S. coffeae may impair its ability to adapt to local selection pressures, scale insects are often locally adapted on fine spatial scales, and local maladaptation is therefore especially surprising. Other documented cases of local maladaptation in parasites appear to be due to evolution on the part of the host. The possibility that hosts or natural enemies may place local genotypes at a disadvantage, producing a pattern of local maladaptation, is one that deserves more consideration in the context of plant-insect interactions.