COEVOLUTION DRIVES TEMPORAL CHANGES IN FITNESS AND DIVERSITY ACROSS ENVIRONMENTS IN A BACTERIA–BACTERIOPHAGE INTERACTION

Coevolutionary interactions are thought to play a crucial role in diversification of hosts and parasitoids. Furthermore, resource availability has been shown to be a fundamental driver of species diversity. Yet, we still do not have a clear understanding of how resource availability mediates the diversity generated by coevolution between hosts and parasitoids over time. We used experiments with bacteria and bacteriophage to test how resources affect variation in the competitive ability of resistant hosts and temporal patterns of diversity in the host and parasitoid as a result of antagonistic coevolution. Bacteria and bacteriophage coevolved for over 150 bacterial generations under high and low-resource conditions. We measured relative competitive ability of the resistant hosts and phenotypic diversity of hosts and parasitoids after the initial invasion of resistant mutants and again at the end of the experiment. Variation in relative competitive ability of the hosts was both time- and environment-dependent. The diversity of resistant hosts, and the abundance of host-range mutants attacking these phenotypes, differed among environments and changed over time, but the direction of these changes differed between the host and parasitoid. Our results demonstrate that patterns of fitness and diversity resulting from coevolutionary interactions can be highly dynamic.     

Interspecific extrinsic and intrinsic competitive interactions in egg parasitoids

Interspecific competitive interactions can occur either between adult parasitoids searching/exploiting hosts (extrinsic competition) or between parasitoid larvae developing within the same host (intrinsic competition). Understanding how interspecific competition between parasitoids can affect pest suppression is important for improving biological pest control. The purpose of this work was to review both extrinsic and intrinsic competition between egg parasitoid species. These are organisms that are often candidates for biological control programs due to their ability to kill the pest before the crop feeding stage. We first reviewed the literature about interspecific competitive abilities of adult parasitoids in terms of comparative host location strategies highlighting which ecological and behavioral factors are likely to shape extrinsic competition. Then we focused on the interspecific competitive interactions between immatures developing within the same host taking into account which factors play a key role in the outcome of intrinsic competition. Finally we conclude stressing on the need to elucidate the overall competitive interaction that parasitoid species may experience in the field in order to enhance biological control success.     

Ample genetic variation but no evidence for genotype specificity in an all‐parthenogenetic host–parasitoid interaction

Antagonistic coevolution between hosts and parasites can result in negative frequency‐dependent selection and may thus be an important mechanism maintaining genetic variation in populations. Negative frequency‐dependence emerges readily if interactions between hosts and parasites are genotype‐specific such that no host genotype is most resistant to all parasite genotypes, and no parasite genotype is most infective on all hosts. Although there is increasing evidence for genotype specificity in interactions between hosts and pathogens or microparasites, the picture is less clear for insect host–parasitoid interactions. Here, we addressed this question in the black bean aphid (Aphis fabae) and its most important parasitoid Lysiphlebus fabarum. Because both antagonists are capable of parthenogenetic reproduction, this system allows for powerful tests of genotype × genotype interactions. Our test consisted of exposing multiple host clones to different parthenogenetic lines of parasitoids in all combinations, and this experiment was repeated with animals from four different sites. All aphids were free of endosymbiotic bacteria known to increase resistance to parasitoids. We observed ample genetic variation for host resistance and parasitoid infectivity, but there was no significant host clone × parasitoid line interaction, and this result was consistent across the four sites. Thus, there is no evidence for genotype specificity in the interaction between A. fabae and L. fabarum, suggesting that the observed variation is based on rather general mechanisms of defence and attack.     

Coevolution across landscapes: a spatially explicit model of parasitoid-host coevolution

The geographic mosaic theory of coevolution suggests that population spatial structure may have a strong impact on coevolutionary dynamics. Therefore, coevolution must be studied across geographic scales, not just in single populations. To examine the impact of movement rate on coevolutionary dynamics, we developed a spatially explicit model of host–parasitoid coevolution. We described space as a coupled-map lattice and assumed that resistance (defined as the ability of a host to encapsulate a parasitoid egg) and virulence (defined as the successful parasitization of a host) traits were graded and costly. The model explicitly detailed population and evolutionary dynamics. When holding all parameters constant and varying only the movement rate of the host and parasitoid, profoundly different dynamics were observed. We found that fluctuations in the mean levels of resistance and virulence in the global population were greatest when the movement rate of the host and parasitoid was high. In addition, we found that the variation in resistance and virulence levels among neighboring patches was greatest when the movement rates of the host and parasitoid was low. However, as the distance among patches increased, so did the variation in resistance and virulence levels regardless of movement rate. These generalizations did not hold when spatial patterns in the distribution of resistance and virulence traits, such as spirals, were observed. Finally, we found that the evolution of resistance and virulence caused the abundance of hosts to increase and the abundance of parasitoids to decrease. As a result, the spatial distribution of hosts and parasitoids was influenced.     

Spatial variability of hosts,parasitoids and their interactions across a homogeneous landscape

Species assemblages and their interactions vary through space, generating diversity patterns at different spatial scales. Here, we study the local‐scale spatial variation of a cavity‐nesting bee and wasp community (hosts), their nest associates (parasitoids), and the resulting antagonistic network over a continuous and homogeneous habitat. To obtain bee/wasp nests, we placed trap‐nests at 25 sites over a 32 km² area. We obtained 1,541 nests (4,954 cells) belonging to 40 host species and containing 27 parasitoid species. The most abundant host species tended to have higher parasitism rate. Community composition dissimilarity was relatively high for both hosts and parasitoids, and the main component of this variability was species turnover, with a very minor contribution of ordered species loss (nestedness). That is, local species richness tended to be similar across the study area and community composition tended to differ between sites. Interestingly, the spatial matching between host and parasitoid composition was low. Host β‐diversity was weakly (positively) but significantly related to geographic distance. On the other hand, parasitoid and host‐parasitoid interaction β‐diversities were not significantly related to geographic distance. Interaction β‐diversity was even higher than host and parasitoid β‐diversity, and mostly due to species turnover. Interaction rewiring between plots and between local webs and the regional metaweb was very low. In sum, species composition was rather idiosyncratic to each site causing a relevant mismatch between hosts and parasitoid composition. However, pairs of host and parasitoid species tended to interact similarly wherever they co‐occurred. Our results additionally show that interaction β‐diversity is better explained by parasitoid than by host β‐diversity. We discuss the importance of identifying the sources of variation to understand the drivers of the observed heterogeneity.     

Host genotype affects the relative success of competing lines of aphid parasitoids under superparasitism

1. In solitary parasitoids, only one individual can complete development in a given host. Therefore, solitary parasitoids tend to prefer unparasitised hosts for oviposition, yet under high parasitoid densities, superparasitism is frequent and results in fierce competition for the host's limited resources. This may lead to selection for the best intra‐host competitors. 2. Increased intra‐host competitive ability may evolve under a high risk of superparasitism if this trait exhibits genetic variation, and if competitive differences among parasitoid genotypes are consistent across environments, e.g. different host genotypes. 3. These assumptions were addressed in the aphid parasitoid Lysiphlebus fabarum (Hymenoptera: Braconidae: Aphidiinae) and its main host, the black bean aphid, Aphis fabae (Scopoli) (Hemiptera: Aphididae). Three parthenogenetic lines of L. fabarum were allowed to parasitise three aphid clones singly and in all pairwise combinations (superparasitism). The winning parasitoid in superparasitised aphids was determined by microsatellite analysis. 4. The proportions of singly parasitised aphids that were mummified were similar for the three parasitoid lines and did not differ significantly among host clones. 5. Under superparasitism, significant biases in favour of one parasitoid line were observed for some combinations, indicating that there is genetic variation for intra‐host competitive ability. However, the outcome of superparasitism was inconsistent across aphid clones and thus influenced significantly by the host clone in which parasitoids competed. 6. Overall, this study shows that the fitness of aphid parasitoids under superparasitism is determined by complex interactions with competitors as well as hosts, possibly hampering the evolution of improved intra‐host competitive ability.     

Spatial and temporal variation in host–parasitoid interactions: leafcutter ant hosts and their phorid parasitoids

1. Parasitoid–host interactions are important components of ecological communities. Although parasitoid–host interactions are strongly shaped by evolutionary history, the abundance of both the parasitoid and the host may have a role in determining the nature of the interaction once phylogenetic relationships are considered. 2. Leafcutter ants are hosts of phorid parasitoids and represent a well‐defined and specialised module within a larger network of ant–symbiont interactions. A low specificity host taxa and a positive association between host abundance and parasitoid interaction frequency were expected due to the close phylogenetic relatedness of the hosts. 3. The interactions among all species of leafcutter ants and their parasitoids were quantified in two localities with different species richness. This study also characterised the spatial‐temporal variability of these interactions, determined the patterns of parasitoid specificity and host selection, and tested for an association between host abundance and parasitoid interaction frequency. 4. Contrary to expectation, most parasitoid species were highly specialised and interaction frequency for parasitoid species was not related to host abundance. All host ant species were attacked by more than one phorid species. Some phorid species used more than one host species and showed preference for the same species over space and time, suggesting that there are physiological and/or behavioural restrictions on host use. 5. These results show that there is a tendency for specialisation even when hosts are highly similar in their ecology. From a biological control perspective, these parasitoids may be effective candidates, due to the high specificity of some species and little host‐use variation through time.     

Coexistence in a competitive parasitoid-host system

The main objective of this work is to determine the conditions for coexistence and competitive exclusion in a discrete model for a community of three species: a stage-structured host and two competing parasitoids sharing the same host developmental stage. Coexistence of the community of the species is found to depend on the host life history parameters in the first place, and on competitive ability and parasitoid efficiency in the second place. In particular, parasitoids equilibrium densities are defined by the size of the refuge. Extinction is expected with low growth rate and with low adult survival. Host life histories are also associated with oscillations in population density, and depending on the combination of host adult survival from one generation to the next and host growth rate, the minimum of fluctuations approaches zero, implying a higher potential risk of extinction because of stochastic factors. Our results suggest that equally reduced survival of parasitoids in hosts parasitized by both species determines extinction of the parasitoid with lower population density, in contrast to the case when both parasitoids benefit with 50% of all doubly parasitized hosts, leading to the hypothesis that a community where competitors in multiparasitized hosts die, easily becomes extinct. Competitive exclusion is expected for highly asymmetric competitive interactions, independent of population densities, allowing us to hypothesize that coexistence of competitors in systems with limited resources and refuges is associated with a clearly defined competitive hierarchy.     

Exploitative competition and coexistence in a parasitoid assemblage

Most insect populations are exploited by a complex of different parasitoid species, providing ample opportunities for competitive interactions among the latter. Despite this, resource-mediated competition (i.e., exploitative competition) among insect parasitoids remains poorly documented in natural systems. Here we propose a novel way to infer the presence of competitive interactions from covariance patterns in parasitism levels, and illustrate the use of this approach on a relatively well-defined and simple host–parasitoid system. The parasitism levels caused by three parasitoid species on a shared host showed a highly consistent negative covariance among samples. With the levels of parasitism by one species increasing, the levels of parasitism attributable to the two others decreased. Importantly, negative covariance between parasitism levels by different species appeared at high abundance, but not at low abundance of the phenologically earlier parasitoid species. This as well as several other lines of evidence indicates the importance of competitive interactions in this system. Feeding biology and phenology of the parasitoids suggest that competition in this parasitoid assemblage is primarily resource-mediated rather than occurring through direct interference. The species attacking earlier stages of the host are competitively superior to those attacking their host later in the season. Better dispersal ability and use of alternative host species by the inferior species could contribute to the coexistence of these competing parasitoids.     

Traits across trophic levels interact to influence parasitoid establishment in biological control releases

A central goal in ecology is to predict what governs a species’ ability to establish in a new environment. One mechanism driving establishment success is individual species’ traits, but the role of trait combinations among interacting species across different trophic levels is less clear. Deliberate or accidental species additions to existing communities provide opportunities to study larger scale patterns of establishment success. Biological control introductions are especially valuable because they contain data on both the successfully established and unestablished species. Here, we used a recent dataset of importation biological control introductions to explore how life‐history traits of 132 parasitoid species and their herbivorous hosts interact to affect parasitoid establishment. We find that of five parasitoid and herbivore traits investigated, one parasitoid trait—host range—weakly predicts parasitoid establishment; parasitoids with higher levels of phylogenetic specialization have higher establishment success, though the effect is marginal. In addition, parasitoids are more likely to establish when their herbivore host has had a shorter residence time. Interestingly, we do not corroborate earlier findings that gregarious parasitoids and endoparasitoids are more likely to establish. Most importantly, we find that life‐history traits of the parasitoid species and their hosts can interact to influence establishment. Specifically, parasitoids with broader host ranges are more likely to establish when the herbivore they have been released to control is also more of a generalist. These results provide insight into how multiple species’ traits and their interactions, both within and across trophic levels, can influence establishment of species of higher trophic levels.     

Gene flow reverses an adaptive cline in a coevolving host-parasitoid interaction

Many natural populations are characterized by clinal patterns of adaptation, but it is unclear how gene flow and environmental gradients interact to drive such clines. We addressed this question by directly manipulating dispersal and productivity in an experimental landscape containing a microbial parasitoid, the bacteriophage T7, and its host, the bacterium Escherichia coli. We observed that the adaptation of parasitoids increased on hosts originating from lower-productivity communities in the absence of gene flow. However, adaptation decreased along the same productivity gradient with experimentally imposed gene flow of the host and parasitoid. This occurred despite relatively low rates of gene flow.     

Herbivore species identity rather than diversity of the non‐host community determines foraging behaviour of the parasitoid wasp Cotesia glomerata

Extensive research has been conducted to reveal how species diversity affects ecosystem functions and services. Yet, consequences of diversity loss for ecosystems as a whole as well as for single community members are still difficult to predict. Arthropod communities typically are species‐rich, and their species interactions, such as those between herbivores and their predators or parasitoids, may be particularly sensitive to changes in community composition. Parasitoids forage for herbivorous hosts by using herbivore‐induced plant volatiles (indirect cues) and cues produced by their host (direct cues). However, in addition to hosts, non‐suitable herbivores are present in a parasitoid's environment which may complicate the foraging process for the parasitoid. Therefore, ecosystem changes in the diversity of herbivores may affect the foraging efficiency of parasitoids. The effect of herbivore diversity may be mediated by either species numbers per se, by specific species traits, or by both. To investigate how diversity and identity of non‐host herbivores influence the behaviour of parasitoids, we created environments with different levels of non‐host diversity. On individual plants in these environments, we complemented host herbivores with 1–4 non‐host herbivore species. We subsequently studied the behaviour of the gregarious endoparasitoid Cotesia glomerata L. (Hymenoptera: Braconidae) while foraging for its gregarious host Pieris brassicae L. (Lepidoptera: Pieridae). Neither non‐host species diversity nor non‐host identity influenced the preference of the parasitoid for herbivore‐infested plants. However, after landing on the plant, non‐host species identity did affect parasitoid behaviour, whereas non‐host diversity did not. One of the non‐host species, Trichoplusia ni Hübner (Lepidoptera: Noctuidae), reduced the time the parasitoid spent on the plant as well as the number of hosts it parasitized. We conclude that non‐host herbivore species identity has a larger influence on C. glomerata foraging behaviour than non‐host species diversity. Our study shows the importance of species identity over species diversity in a multitrophic interaction of plants, herbivores, and parasitoids.     

Strong parasitoid-mediated selection in experimental populations of aphids

Clonal diversity in asexual populations may be maintained if different clones are favoured under different environmental conditions. For aphids, parasitoids are an important variable of the biotic environment. To test whether parasitoids can mediate selection among host clones, we used experimental populations consisting of 10 clones of the peach-potato aphid, Myzus persicae, and allowed them to evolve for several generations either without parasitoids or in the presence of two species of parasitoid wasps. In the absence of parasitoids, strong shifts in clonal frequencies occurred, mostly in favour of clones with high rates of increase. The parasitoid Diaeretiella rapae hardly affected aphid densities but changed the outcome of competition by favouring one entirely resistant clone and disfavouring a highly susceptible clone. Aphidius colemani, the more infective parasitoid, strongly reduced aphid densities and dramatically changed host clonal frequencies. The most resistant clone, not a successful clone without parasitoids, became totally dominant. These results highlight the potential of temporal or spatial variation in parasitoid densities to maintain clonal diversity in their aphid hosts.     

The shape of an ecological trade-off varies with environment

Central to most theories that explain the diversity of life is the concept that organisms face trade-offs. Theoretical work has shown that the precise shape of a trade-off relationship affects evolutionary predictions. One common trade-off is that between competitive ability and resistance to predators, parasitoids, pathogens or herbivores. We used a microbial experimental system to elucidate the shape of the relationship between parasitoid resistance and competitive ability. For each of 86 bacteriophage-resistant isolates of the bacterium Escherichia coli B, we measured the degree of resistance to bacteriophage T2 (a viral parasitoid) and relative competitive ability in both the resource environment in which strains were isolated and in two alternate environments. We observed that environmental change can alter trade-off shape, and that different physiological mechanisms can lead to different trade-off shapes and different sensitivities to environmental change. These results highlight the important interaction between environment and trade-off shape in affecting ecological and evolutionary dynamics.     

Abundance,not diversity,of host beetle communities determines abundance and diversity of parasitoids in deadwood

Most parasites and parasitoids are adapted to overcome defense mechanisms of their specific hosts and hence colonize a narrow range of host species. Accordingly, an increase in host functional or phylogenetic dissimilarity is expected to increase the species diversity of parasitoids. However, the local diversity of parasitoids may be driven by the accessibility and detectability of hosts, both increasing with increasing host abundance. Yet, the relative importance of these two mechanisms remains unclear. We parallelly reared communities of saproxylic beetle as potential hosts and associated parasitoid Hymenoptera from experimentally felled trees. The dissimilarity of beetle communities was inferred from distances in seven functional traits and from their evolutionary ancestry. We tested the effect of host abundance, species richness, functional, and phylogenetic dissimilarities on the abundance, species richness, and Shannon diversity of parasitoids. Our results showed an increase of abundance, species richness, and Shannon diversity of parasitoids with increasing beetle abundance. Additionally, abundance of parasitoids increased with increasing species richness of beetles. However, functional and phylogenetic dissimilarity showed no effect on the diversity of parasitoids. Our results suggest that the local diversity of parasitoids, of ephemeral and hidden resources like saproxylic beetles, is highest when resources are abundant and thereby detectable and accessible. Hence, in some cases, resources do not need to be diverse to promote parasitoid diversity.     

Superparasitism and host size effects in Oomyzus sokolowskii, a parasitoid of diamondback moth

Many aspects of a parasitoid's biology may be affected by its host. Host size, for example, could affect parasitoid fitness, especially in gregarious parasitoids, in which the resource is used by multiple siblings. Oomyzus sokolowskii (Kurdjumov) (Hymenoptera: Eulophidae) is a gregarious larval–pupal endoparasitoid of the diamondback moth, Plutella xylostella L. (Lepidoptera: Plutellidae), a major pest of crucifers worldwide, and is able to superparasitize the host. This study focuses on the hypothesis that because resource availability is higher in larger hosts, parasitoids developing in larger hosts will fare better. However, superparasitized hosts are expected to yield larger numbers of parasitoid offspring of smaller body size. Results showed that superparasitism increased the number of parasitoid offspring produced per host and increased offspring longevity, but decreased offspring body size. However, developmental time and sex ratio of parasitoid offspring was similar among hosts parasitized once, twice, or three times. Regardless of superparasitism, parasitoids emerging from larger hosts that were fed honey solution lived longer than similarly fed progeny from smaller hosts (36.4 vs. 22.1 days). The results partially support the hypothesis that Oomyzus gained fitness from an increase in host size; moreover, superparasitism seems advantageous for Oomyzus due to increased offspring numbers and longevity.     

Proteomes of the aphid Macrosiphum euphorbiae in its resistance and susceptibility responses to differently compatible parasitoids

Host insects are either susceptible or resistant to parasitoids, where resistant hosts express immunity factors and compatible parasitoids express virulence factors that may reveal the manipulation of susceptible hosts. Using proteomics we compared responses of the same host, the aphid Macrosiphum euphorbiae, challenged by a well-adapted parasitoid Aphidius nigripes or by a less adapted relative, Aphidius ervi. The host was found to be equally acceptable to both parasitoids, but while A. nigripes normally developed and killed hosts (high susceptibility), development of the incompatible A. ervi was arrested at the primary egg stage (high resistance). Two-dimensional gels at two stages of parasitism revealed divergence in patterns of protein regulation of the M. euphorbiae host, responding to A. ervi or A. nigripes, with the greatest number of protein modulations in the host resistance response. In A. ervi-resistant hosts, proPO was strongly up-regulated, as were also three cuticle proteins, suggesting a PO basis and exoskeleton reinforcement as early and late responses of M. euphorbiae to the risk of parasitism. Resistance also correlated with up-regulation of antioxidative, energy-related, cytoskeleton and heat shock proteins. In A. nigripes-susceptible hosts, various proteins implicated in host and bacterial symbiont metabolism were significantly altered, suggesting complex host nutritional modulation. Over-expression of energy-related proteins also increased when A. nigripes established and developed. Aphid proteomes of compatible and incompatible Aphidius parasitism provide an integrative basis for consolidating our knowledge of host-parasitoid interactions.     

Histories of host shifts and cospeciation among free‐living parasitoids of Rhagoletis flies

Host shifts by specialist insects can lead to reproductive isolation between insect populations that use different hosts, promoting diversification. When both a phytophagous insect and its ancestrally associated parasitoid shift to the same novel host plant, they may cospeciate. However, because adult parasitoids are free living, they can also colonize novel host insects and diversify independent of their ancestral host insect. Although shifts of parasitoids to new insect hosts have been documented in ecological time, the long‐term importance of such shifts to parasitoid diversity has not been evaluated. We used a genus of flies with a history of speciation via host shifting (Rhagoletis [Diptera: Tephritidae]) and three associated hymenopteran parasitoid genera (Diachasma, Coptera and Utetes) to examine cophylogenetic relationships between parasitoids and their host insects. We inferred phylogenies of Rhagoletis, Diachasma, Coptera and Utetes and used distance‐based cophylogenetic methods (ParaFit and PACo) to assess congruence between fly and parasitoid trees. We used an event‐based method with a free‐living parasitoid cost model to reconstruct cophylogenetic histories of each parasitoid genus and Rhagoletis. We found that the current species diversity and host–parasitoid associations between the Rhagoletis flies and parasitoids are the primary result of ancient cospeciation events. Parasitoid shifts to ancestrally unrelated hosts primarily occur near the branch tips, suggesting that host shifts contribute to recent parasitoid species diversity but that these lineages may not persist over longer time periods. Our analyses also stress the importance of biologically informed cost models when investigating the coevolutionary histories of hosts and free‐living parasitoids.     

Reconstructing community assembly in time and space reveals enemy escape in a Western Palearctic insect community

How geographically widespread biological communities assemble remains a major question in ecology. Do parallel population histories allow sustained interactions (such as host-parasite or plant-pollinator) among species, or do discordant histories necessarily interrupt them? Though few empirical data exist, these issues are central to our understanding of multispecies evolutionary dynamics. Here we use hierarchical approximate Bayesian analysis of DNA sequence data for 12 herbivores and 19 parasitoids to reconstruct the assembly of an insect community spanning the Western Palearctic and assess the support for alternative host tracking and ecological sorting hypotheses. We show that assembly occurred primarily by delayed host tracking from a shared eastern origin. Herbivores escaped their enemies for millennia before parasitoid pursuit restored initial associations, with generalist parasitoids no better able to track their hosts than specialists. In contrast, ecological sorting played only a minor role. Substantial turnover in host-parasitoid associations means that coevolution must have been diffuse, probably contributing to the parasitoid generalism seen in this and similar systems. Reintegration of parasitoids after host escape shows these communities to have been unsaturated throughout their history, arguing against major roles for parasitoid niche evolution or competition during community assembly.