The roles of ecological fitting, phylogeny and physiological equivalence in understanding realized and fundamental host ranges in endoparasitoid wasps

Co-evolutionary theory underpins our understanding of interactions in nature involving plant-herbivore and host-parasite interactions. However, many studies that are published in the empirical literature that have explored life history and development strategies between endoparasitoid wasps and their hosts are based on species that have no evolutionary history with one another. Here, we investigated novel associations involving two closely related solitary endoparasitoids that originate from Europe and North America and several of their natural and factitious hosts from both continents. The natural hosts of both species are also closely related, all being members of the same family. We compared development and survival of both parasitoids on the four host species and predicted that parasitoid performance is better on their own natural hosts. In contrast with this expectation, survival, adult size and development time of both parasitoids were similar on all (with one exception) hosts, irrespective as to their geographic origin. Our results show that phylogenetic affinity among the natural and factitious hosts plays an important role in their nutritional suitability for related parasitoids. Evolved traits in parasitoids, such as immune suppression and development, thus enable them to successfully develop in novel host species with which they have no evolutionary history. Our results show that host suitability for specialized organisms like endoparasitoids is closely linked with phylogenetic history and macro-evolution as well as local adaptation and micro-evolution. We argue that the importance of novel interactions and 'ecological fitting' based on phylogeny is a greatly underappreciated concept in many resource-consumer studies.     

From micro- to macroevolution: brood parasitism as a driver of phenotypic diversity in birds

A fundamental question in biology is how diversity evolves and why some clades are more diverse than others. Phenotypic diversity has often been shown to result from morphological adaptation to different habitats. The role of behavioral interactions as a driver of broadscale phenotypic diversity has received comparatively less attention. Behavioral interactions, however, are a key agent of natural selection. Antagonistic behavioral interactions with predators or with parasites can have significant fitness consequences, and hence act as strong evolutionary forces on the phenotype of species, ultimately generating diversity between species of both victims and exploiters. Avian obligate brood parasites lay their eggs in the nests of other species, their hosts, and this behavioral interaction between hosts and parasites is often considered one of the best examples of coevolution in the natural world. In this review, we use the coevolution between brood parasites and their hosts to illustrate the potential of behavioral interactions to drive evolution of phenotypic diversity at different taxonomic scales. We provide a bridge between behavioral ecology and macroevolution by describing how this interaction has increased avian phenotypic diversity not only in the brood parasitic clades but also in their hosts.     

Chemical interaction between undamaged plants--effects on herbivores and natural enemies

Most research on plant-plant chemical interactions has focussed on events following herbivore or pathogen attack. However, undamaged plants also interact chemically as a natural facet of their behaviour, and this may have consequences for insects that use the plants as hosts. In this review, the links between allelopathy and insect behaviour are outlined. Findings on how chemical interactions between different plant species and genotypes affect aphid herbivores and their natural enemies are reviewed, and the role of plant diversity and chemical interaction for trophic interactions in crops is discussed.     

Role of saliva in tick/host interactions

Although several hosts mount efficient anti-tick immunity, natural tick/host associations are characterized by inefficient or non-existent anti-tick immunity. The absence of efficient anti-tick immunity in natural hosts could result from either host immune incompetence or the ectoparasite's successful evasion of the host's immune response. In this review I discuss data supporting the immune-evasion hypothesis and discuss its consequences to tick/host interactions.Supported by grants AI-18694-0481 from the National Institutes of Health and DAMD-17-87-C-7110 from the United States Army.     

Symbiont-mediated protection

Despite the fact that all vertically transmitted symbionts sequester resources from their hosts and are therefore costly to maintain, there is an extraordinary diversity of them in invertebrates. Some spread through host populations by providing their hosts with fitness benefits or by manipulating host sex ratio, but some do not: their maintenance in host lineages remains an enigma. In this review, I explore the evolutionary ecology of vertically transmitted symbionts and their impact on host resistance, and provide an overview of the evidence for the three-way interactions between these symbionts, natural enemies and invertebrate hosts. A number of recent empirical and theoretical studies suggest that vertically transmitted symbionts may protect their hosts from pathogens. If this 'symbiont-mediated protection' is widespread, it is likely that vertically transmitted symbionts contribute significantly to variation in measures of invertebrate resistance to natural enemies.     

QUANTITATIVE GENETICS,DEVELOPMENT, AND PHYSIOLOGICAL ADAPTATION IN HOST STRAINS OF FALL ARMYWORM

Two genetically differentiated host strains of fall armyworm were reared on their own and each other's host plants, rice and corn, to determine whether they were physiologically adapted to their natural hosts and whether they exhibited genetically based differences in development. Larval host had a greater impact on development in the rice strain than in the corn strain, indicating that physiology could have facilitated specialization in one strain but not the other. Consequently, behavioral mechanisms are also likely to be important in the maintenance of host specificity. Comparisons between strains indicated significant differences in one trait, the rate at which larvae gained weight. Because this character had consistently high heritabilities, genetic differentiation in development is indicated. An analysis of genotype-by-environment interactions within each strain detected significant interactions for three of five traits, suggesting that genotypic performance on one host was not indicative of performance on the other. Each strain thus exhibited genetic variation that would facilitate host-associated divergence and adaptation if coupled with a mechanism that reduced gene flow between hosts. Finally, significant genetic correlations between several characters were detected when strains were reared on their natural hosts but not when they were reared on nonnatural hosts. Apparently, feeding on novel hosts caused developmental uncoupling of characters. Release from genetic constraints could provide a mechanism for physiological adjustments to newly occupied habitats.     

Latency of Baculoviruses

Due to their widespread natural occurrence, baculoviruses and their insect hosts are a convenient model to study the pathogen-host interactions. However, the absence of reliable techniques for the detection of latent viral infection, which is common in insect populations, is among the constraints of such studies. The recent progress in molecular biology techniques made it possible to obtain the fundamental data on the detection of latent viruses in different insect species as well as on the mechanism of latent infection induction, which are reviewed below. The obtained data in many respects expand our knowledge about the role of latency in the system of interactions between baculoviruses and their insect hosts at different ecological levels.     

Advancing research on ectomycorrhizal fungal adaptation with landscape genomics

Ectomycorrhizal (ECM) fungi serve key functions in forest ecosystems by supplying water and nutrients to tree hosts, yet mutualistic plant–fungi interactions are jeopardised by environmental alterations. Here, we discuss the great potential and current limitations of landscape genomics in investigating signatures of local adaptation in natural populations of ECM fungi.     

自然植物种群中病原菌与寄主植物相互作用的遗传学

在农业种群中,作物和菌病相互作用的遗传学已为人们所广泛研究,但对自然植物种群中病原菌与其寄主相互作用体系的某些重要现象却缺乏足够的重视。本文主要论述寄主与病原菌相互作用的遗传学本质;寄主抗性基因和病原菌毒性基因的获得代价及对各自适应力的影响;简单介绍了寄主-病原菌作用体系在种群水平上的遗传学内容及共进化的意义。     

Coevolution Drives the Emergence of Complex Traits and Promotes Evolvability

The evolution of complex organismal traits is obvious as a historical fact, but the underlying causes—including the role of natural selection—are contested. Gould argued that a random walk from a necessarily simple beginning would produce the appearance of increasing complexity over time. Others contend that selection, including coevolutionary arms races, can systematically push organisms toward more complex traits. Methodological challenges have largely precluded experimental tests of these hypotheses. Using the Avida platform for digital evolution, we show that coevolution of hosts and parasites greatly increases organismal complexity relative to that otherwise achieved. As parasites evolve to counter the rise of resistant hosts, parasite populations retain a genetic record of past coevolutionary states. As a consequence, hosts differentially escape by performing progressively more complex functions. We show that coevolution''s unique feedback between host and parasite frequencies is a key process in the evolution of complexity. Strikingly, the hosts evolve genomes that are also more phenotypically evolvable, similar to the phenomenon of contingency loci observed in bacterial pathogens. Because coevolution is ubiquitous in nature, our results support a general model whereby antagonistic interactions and natural selection together favor both increased complexity and evolvability.     

Cascading effects of herbivore protective symbionts on hyperparasitoids

1. Microbial symbionts can play an important role in defending their insect hosts against natural enemies. However, researchers have little idea how the presence of such protective symbionts impacts food web interactions and species diversity. 2. This study investigated the effects of a protective symbiont (Hamiltonella defensa) in pea aphids (Acyrthosiphon pisum) on hyperparasitoids, which are a trophic level above the natural enemy target of the symbiont (primary parasitoids). 3. Pea aphids, with and without their natural infections of H. defensa, were exposed first to a primary parasitoid against which the symbiont provides partial protection (either Aphidius ervi or Aphelinus abdominalis), and second to a hyperparasitoid known to attack the primary parasitoid species. 4. It was found that hyperparasitoid hatch rate was substantially affected by the presence of the symbiont. This effect appears to be entirely due to the removal of potential hosts by the action of the symbiont: there was no additional benefit or cost experienced by the hyperparasitoids in response to symbiont presence. The results were similar across the two different aphid–parasitoid–hyperparasitoid interactions we studied. 5. It is concluded that protective symbionts can have an important cascading effect on multiple trophic levels by altering the success of natural enemies, but that there is no evidence for more complex interactions. These findings demonstrate that the potential influence of protective symbionts on the wider community should be considered in future food web studies.     

Genotype specificity among hosts,pathogens, and beneficial microbes influences the strength of symbiont‐mediated protection

The microbial symbionts of eukaryotes influence disease resistance in many host‐parasite systems. Symbionts show substantial variation in both genotype and phenotype, but it is unclear how natural selection maintains this variation. It is also unknown whether variable symbiont genotypes show specificity with the genotypes of hosts or parasites in natural populations. Genotype by genotype interactions are a necessary condition for coevolution between interacting species. Uncovering the patterns of genetic specificity among hosts, symbionts, and parasites is therefore critical for determining the role that symbionts play in host‐parasite coevolution. Here, we show that the strength of protection conferred against a fungal pathogen by a vertically transmitted symbiont of an aphid is influenced by both host‐symbiont and symbiont‐pathogen genotype by genotype interactions. Further, we show that certain symbiont phylogenetic clades have evolved to provide stronger protection against particular pathogen genotypes. However, we found no evidence of reciprocal adaptation of co‐occurring host and symbiont lineages. Our results suggest that genetic variation among symbiont strains may be maintained by antagonistic coevolution with their host and/or their host's parasites.     

Natural experiments and long-term monitoring are critical to understand and predict marine host–microbe ecology and evolution

Marine multicellular organisms host a diverse collection of bacteria, archaea, microbial eukaryotes, and viruses that form their microbiome. Such host-associated microbes can significantly influence the host’s physiological capacities; however, the identity and functional role(s) of key members of the microbiome (“core microbiome”) in most marine hosts coexisting in natural settings remain obscure. Also unclear is how dynamic interactions between hosts and the immense standing pool of microbial genetic variation will affect marine ecosystems’ capacity to adjust to environmental changes. Here, we argue that significantly advancing our understanding of how host-associated microbes shape marine hosts’ plastic and adaptive responses to environmental change requires (i) recognizing that individual host–microbe systems do not exist in an ecological or evolutionary vacuum and (ii) expanding the field toward long-term, multidisciplinary research on entire communities of hosts and microbes. Natural experiments, such as time-calibrated geological events associated with well-characterized environmental gradients, provide unique ecological and evolutionary contexts to address this challenge. We focus here particularly on mutualistic interactions between hosts and microbes, but note that many of the same lessons and approaches would apply to other types of interactions.

This Essay argues that in order to truly understand how marine hosts benefit from the immense diversity of microbes, we need to expand towards long-term, multi-disciplinary research focussing on few areas of the world’s ocean that we refer to as “natural experiments,” where processes can be studied at scales that far exceed those captured in laboratory experiments.     

Maladaptation in wild populations of the generalist plant pathogen Pseudomonas syringae

Multihost pathogens occur widely on both natural and agriculturally managed hosts. Despite the importance of such generalists, evolutionary studies of host-pathogen interactions have largely focused on tightly coupled interactions between species pairs. We characterized resistance in a collection of Arabidopsis thaliana hosts, including 24 accessions collected from the Midwest USA and 24 from around the world, and patterns of virulence in a collection of Pseudomonas syringae strains, including 24 strains collected from wild Midwest populations of A. thaliana (residents) and 18 from an array of cultivated species (nonresidents). All of the nonresident strains and half of the resident strains elicited a resistance response on one or more A. thaliana accessions. The resident strains that failed to elicit any resistance response possessed an alternative type III secretion system (T3SS) that is unable to deliver effectors into plant host cells; as a result, these seemingly nonpathogenic strains are incapable of engaging in gene for gene interactions with A. thaliana. The remaining resident strains triggered greater resistance compared to nonresident strains, consistent with maladaptation of the resident bacterial population. We weigh the plausibility of two explanations: general maladaptation of pathogen strains and a more novel hypothesis whereby community level epidemiological dynamics result in adaptive dynamics favoring ephemeral hosts like A. thaliana.     

Droplet digital PCR as a tool for investigating dynamics of cryptic symbionts

Interactions among symbiotic organisms and their hosts are major drivers of ecological and evolutionary processes. Monitoring the infection patterns among natural populations and identifying factors affecting these interactions are critical for understanding symbiont–host relationships. However, many of these interactions remain understudied since the knowledge about the symbiont species is lacking, which hinders the development of appropriate tools. In this study, we developed a digital droplet PCR (ddPCR) assay based on apicomplexan COX1 gene to detect an undescribed agamococcidian symbiont. We show that the method gives precise and reproducible results and enables detecting cryptic symbionts in low target concentration. We further exemplify the assay''s use to survey seasonally sampled natural host (Pygospio elegans) populations for symbiont infection dynamics. We found that symbiont prevalence differs spatially but does not show seasonal changes. Infection load differed between populations and was low in spring and significantly increased towards fall in all populations. We also found that the symbiont prevalence is affected by host length and population density. Larger hosts were more likely to be infected, and high host densities were found to have a lower probability of infection. The observed variations could be due to characteristics of both symbiont and host biology, especially the seasonal variation in encounter rates. Our findings show that the developed ddPCR assay is a robust tool for detecting undescribed symbionts that are otherwise difficult to quantify, enabling further insight into the impact cryptic symbionts have on their hosts.     

The impact of environmental change on host-parasite coevolutionary dynamics

Environmental factors are known to affect the strength and the specificity of interactions between hosts and parasites. However, how this shapes patterns of coevolutionary dynamics is not clear. Here, we construct a simple mathematical model to study the effect of environmental change on host-parasite coevolutionary outcome when interactions are of the matching-alleles or the gene-for-gene type. Environmental changes may effectively alter the selective pressure and the level of specialism in the population. Our results suggest that environmental change altering the specificity of selection in antagonistic interactions can produce alternating time windows of cyclical allele-frequency dynamics and cessation thereof. This type of environmental impact can also explain the maintenance of polymorphism in gene-for-gene interactions without costs. Overall, our study points to the potential consequences of environmental variation in coevolution, and thus the importance of characterizing genotype-by-genotype-by-environment interactions in natural host-parasite systems, especially those that change the direction of selection acting between the two species.     

Potential for Entomopathogenic Nematodes in Biological Control: A Meta-Analytical Synthesis and Insights from Trophic Cascade Theory

Entomopathogenic nematodes (EPN) are ubiquitous and generalized consumers of insects in soil food webs, occurring widely in natural and agricultural ecosystems on six continents. Augmentative releases of EPN have been used to enhance biological control of pests in agroecosystems. Pest managers strive to achieve a trophic cascade whereby natural-enemy effects permeate down through the food web to suppress host herbivores and increase crop production. Although trophic cascades have been studied in diverse aboveground arthropod-based systems, they are infrequently investigated in soil systems. Moreover, no overall quantitative assessment of the effectiveness of EPN in suppressing hosts with cascading benefits to plants has been made. Toward synthesizing the available but limited information on EPN and their ability to suppress prey and affect plant yield, we surveyed the literature and performed a meta-analysis of 35 published studies. Our analysis found that effect sizes for arthropod hosts as a result of EPN addition were consistently negative and indirect effects on plants were consistently positive. Results held across several different host metrics (abundance, fecundity and survival) and across measures of plant performance (biomass, growth, yield and survival). Moreover, the relationship between plant and host effect sizes was strikingly and significantly negative. That is, the positive impact on plant responses generally increased as the negative effect of EPN on hosts intensified, providing strong support for the mechanism of trophic cascades. We also review the ways in which EPN might interact antagonistically with each other and other predators and pathogens to adversely affect host suppression and dampen trophic cascades. We conclude that the food web implications of multiple-enemy interactions involving EPN are little studied, but, as management techniques that promote the long-term persistence of EPN are improved, antagonistic interactions are more likely to arise. We hope that the likely occurrence of antagonistic interactions in soil food webs should stimulate researchers to conduct field experiments explicitly designed to examine multiple-enemy interactions involving EPN and their cascading effects to hosts and plants.     

Host-Salmonella interaction: human trials.

Human clinical trials, including experimental challenges of volunteers with pathogenic Salmonella enterica serovar Typhi, small phase I and II trials that monitor the immune responses to vaccines, and large-scale controlled field trials that assess vaccine efficacy under conditions of natural challenge, have helped elucidate the interactions between Salmonella typhi and human hosts.     

Evolution of resistance and virulence in plant-herbivore and plant-pathogen interactions

Herbivores and pathogens often attack or infect the same plant parts, and the same plant traits can affect the likelihood and degree of damage. Research on plant-herbivore and plant-pathogen interactions in natural systems have, however, proceeded largely independently of each other. Our understanding of both types of plant-enemy interaction would be enhanced by greater exposure of researchers to developments in both disciplines and by more studies of interactions between pathogen and herbivore species associated with the same hosts.     

Tragedy of the commons among antibiotic resistance plasmids

As social interactions are increasingly recognized as important determinants of microbial fitness, sociobiology is being enlisted to better understand the evolution of clinically relevant microbes and, potentially, to influence their evolution to aid human health. Of special interest are situations in which there exists a "tragedy of the commons," where natural selection leads to a net reduction in fitness for all members of a population. Here, I demonstrate the existence of a tragedy of the commons among antibiotic resistance plasmids of bacteria. In serial transfer culture, plasmids evolved a greater ability to superinfect already-infected bacteria, increasing plasmid fitness when evolved genotypes were rare. Evolved plasmids, however, fell victim to their own success, reducing the density of their bacterial hosts when they became common and suffering reduced fitness through vertical transmission. Social interactions can thus be an important determinant of evolution for the molecular endosymbionts of bacteria. These results also identify an avenue of evolution that reduces proliferation of both antibiotic resistance genes and their bacterial hosts.