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.     

Molecular detection of trophic links in a complex insect host-parasitoid food web

Previously, host-parasitoid links have been unveiled almost exclusively by time-intensive rearing, while molecular methods were used only in simple agricultural host-parasitoid systems in the form of species-specific primers. Here, we present a general method for the molecular detection of these links applied to a complex caterpillar-parasitoid food web from tropical rainforest of Papua New Guinea. We DNA barcoded hosts, parasitoids and their tissue remnants and matched the sequences to our extensive library of local species. We were thus able to match 87% of host sequences and 36% of parasitoid sequences to species and infer subfamily or family in almost all cases. Our analysis affirmed 93 hitherto unknown trophic links between 37 host species from a wide range of Lepidoptera families and 46 parasitoid species from Hymenoptera and Diptera by identifying DNA sequences for both the host and the parasitoid involved in the interaction. Molecular detection proved especially useful in cases where distinguishing host species in caterpillar stage was difficult morphologically, or when the caterpillar died during rearing. We have even detected a case of extreme parasitoid specialization in a pair of Choreutis species that do not differ in caterpillar morphology and ecology. Using the molecular approach outlined here leads to better understanding of parasitoid host specificity, opens new possibilities for rapid surveys of food web structure and allows inference of species associations not already anticipated.     

Strong specificity in the interaction between parasitoids and symbiont‐protected hosts

Coevolution between hosts and parasites may promote the maintenance of genetic variation in both antagonists by negative frequency‐dependence if the host–parasite interaction is genotype‐specific. Here we tested for specificity in the interaction between parasitoids (Lysiphlebus fabarum) and aphid hosts (Aphis fabae) that are protected by a heritable defensive endosymbiont, the γ‐proteobacterium Hamiltonella defensa. Previous studies reported a lack of genotype specificity between unprotected aphids and parasitoids, but suggested that symbiont‐conferred resistance might exhibit a higher degree of specificity. Indeed, in addition to ample variation in host resistance as well as parasitoid infectivity, we found a strong aphid clone‐by‐parasitoid line interaction on the rates of successful parasitism. This genotype specificity appears to be mediated by H. defensa, highlighting the important role that endosymbionts can play in host–parasite coevolution.     

Genotype matching in a parasitoid–host genotypic food web: an approach for measuring effects of environmental change

Food webs typically quantify interactions between species, whereas evolution operates through the success of alleles within populations of a single species. To bridge this gap, we quantify genotypic interaction networks among individuals of a single specialized parasitoid species and its obligate to cyclically parthenogenetic aphid host along a climatic gradient. As a case study for the kinds of questions genotype food webs could be used to answer, we show that genetically similar parasitoids became more likely to attack genetically similar hosts in warmer sites (i.e. there was network‐wide congruence between the within‐species shared allelic distance of the parasitoid and that of its host). Narrowing of host‐genotype‐niche breadth by parasitoids could reduce resilience of the network to changes in host genetic structure or invasion by novel host genotypes and inhibit biological control. Thus, our approach can be easily used to detect changes to sub‐species‐level food webs, which may have important ecological and evolutionary implications, such as promoting host‐race specialization or the accelerated loss of functional diversity following extinctions of closely related genotypes.     

Corrigendum to Streicker et al. (2013) Differential sources of host species heterogeneity influence the transmission and control of multi‐host parasites

In a recent article, we described a conceptual and analytical model to identify the key host species for parasite transmission in multi‐host communities and used data from 11 gastro‐intestinal parasites infecting up to five small mammal host species as an illustrative example of how the framework could be applied. A limitation of these empirical data was uncertainty in the identification of parasite species using egg/oocyst morphology, which could overestimate parasite sharing between host species. Here, we show that the key results of the original analysis, namely that (1) parasites naturally infect multiple host species, but typically rely on a small subset of infected host species for long‐term maintenance, (2) that different mechanisms underlie how particular host species dominate transmission and (3) that these different mechanisms influence the predicted efficiency of disease control measures, are robust to analysis of a smaller subset of host–parasite combinations that we have greatest confidence in identifying. We further comment briefly on the need for accurate parasite identification, ideally using molecular techniques to quantify cross‐species transmission and differentiate covert host specificity from true host generalism.     

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.     

Resource predictability and specialization in avian malaria parasites

We tested the hypothesis that avian haemosporidian (malaria) parasites specialize on hosts that can be characterized as predictable resources at a site in Amazonian Ecuador. We incorporated host phylogenetic relationship and relative abundance in assessing parasite specialization, and we examined associations between parasite specialization and three host characteristics – abundance, mass and longevity – using quantile regression, phylogenetic logistic regression and t‐tests. Hosts of specialist malaria parasite lineages were on average more abundant than hosts of generalist parasite lineages, but the relationship between host abundance and parasite specialization was not consistent across analyses. We also found support for a positive association between parasite specialization and host longevity, but this also was not consistent across analyses. Nonetheless, our findings suggest that the predictability of a host resource may play a role in the evolution of specialization. However, we also discuss two alternative explanations to the resource predictability hypothesis for specialization: (i) that interspecific interactions among the parasites themselves might constrain some parasites to a specialist strategy, and (ii) that frequent encounters with multiple host species, mediated by blood‐sucking insects, might promote generalization within this system.     

Molecular biogeography and host relations of a parasitoid fly

Successful geographic range expansion by parasites and parasitoids may also require host range expansion. Thus, the evolutionary advantages of host specialization may trade off against the ability to exploit new host species encountered in new geographic regions. Here, we use molecular techniques and confirmed host records to examine biogeography, population divergence, and host flexibility of the parasitoid fly, Ormia ochracea (Bigot). Gravid females of this fly find their cricket hosts acoustically by eavesdropping on male cricket calling songs; these songs vary greatly among the known host species of crickets. Using both nuclear and mitochondrial genetic markers, we (a) describe the geographical distribution and subdivision of genetic variation in O. ochracea from across the continental United States, the Mexican states of Sonora and Oaxaca, and populations introduced to Hawaii; (b) demonstrate that the distribution of genetic variation among fly populations is consistent with a single widespread species with regional host specialization, rather than locally differentiated cryptic species; (c) identify the more‐probable source populations for the flies introduced to the Hawaiian islands; (d) examine genetic variation and substructure within Hawaii; (e) show that among‐population geographic, genetic, and host song distances are all correlated; and (f) discuss specialization and lability in host‐finding behavior in light of the diversity of cricket songs serving as host cues in different geographically separate populations.     

Infochemical use and dietary specialization in parasitoids: a meta‐analysis

Many parasitoid species use olfactory cues to locate their hosts. In tritrophic systems, parasitoids of herbivores can exploit the chemical blends emitted by plants in reaction to herbivore‐induced damage, known as herbivore‐induced plant volatiles (HIPVs). In this study, we explored the specificity and innateness of parasitoid responses to HIPVs using a meta‐analysis of data from the literature. Based on the concept of dietary specialization and infochemical use, we hypothesized that (i) specialist parasitoids (i.e., with narrow host ranges) should be attracted to specific HIPV signals, whereas generalist parasitoids (i.e., with broad host ranges) should be attracted to more generic HIPV signals and (ii) specialist parasitoids should innately respond to HIPVs, whereas generalist parasitoids should have to learn to associate HIPVs with host presence. We characterized the responses of 66 parasitoid species based on published studies of parasitoid behavior. Our meta‐analysis showed that (i) as predicted, specialist parasitoids were attracted to more specific signals than were generalist parasitoids but, (ii) contrary to expectations, response innateness depended on a parasitoid's target host life stage rather than on its degree of host specialization: parasitoids of larvae were more likely to show an innate response to HIPVs than were parasitoids of adults. This result changes our understanding of dietary specialization and highlights the need for further theoretical research that will help clarify infochemical use by parasitoids.     

Compositional turnover in host and parasite communities does not change network structure

Decreasing similarity between ecological communities with increasing geographic distance (i.e. distance‐decay) is a common biogeographical observation in free‐living communities, and a slightly less common observation for parasite communities. Ecological networks of interacting species may adhere to a similar pattern of decreasing interaction similarity with increasing geographic distance, especially if species interactions are maintained across space. We extend this further, examining if host–parasite networks – independent of host and parasite species identities – become more structurally dissimilar with increasing geographic distance. Utilizing a global database of helminth parasite occurrence records, we find evidence for distance‐decay relationships in host and parasite communities at both regional and global scales, but fail to detect similar relationships in network structural similarity. Host and parasite community similarity were strongly related, and both decayed rapidly with increasing geographic distance, typically resulting in complete dissimilarity after approximately 2500 km. Our failure to detect a decay in network structural similarity suggests the possibility that different host and parasite species are filling the same functional roles in interaction networks, or that variation in network similarity may be better explained by other geographic variables or aspects of host and parasite ecology.     

Getting there and around: Host range oscillations during colonization of the Canary Islands by the parasitic nematode Spauligodon

Episodes of expansion and isolation in geographic range over space and time, during which parasites have the opportunity to expand their host range, are linked to the development of host–parasite mosaic assemblages and parasite diversification. In this study, we investigated whether island colonization events lead to host range oscillations in a taxon of host‐specific parasitic nematodes of the genus Spauligodon in the Canary Islands. We further investigated whether range oscillations also resulted in shifts in host breadth (i.e., specialization), as expected for parasites on islands. Parasite phylogeny and divergence time estimates were inferred from molecular data with Bayesian methods. Host divergence times were set as calibration priors after a priori evaluation with a global‐fit method of which individual host–parasite associations likely represent cospeciation links. Parasite colonization history was reconstructed, followed by an estimation of oscillation events and specificity level. The results indicate the presence of four Spauligodon clades in the Canary Islands, which originated from at least three different colonization events. We found evidence of host range oscillations to truly novel hosts, which in one case led to higher diversification. Contemporary host–parasite associations show strong host specificity, suggesting that changes in host breadth were limited to the shift period. Lineages with more frequent and wider taxonomic host range oscillations prior to the initial colonization event showed wider range oscillations during colonization and diversification within the archipelago. Our results suggest that a lineage's evolutionary past may be the best indicator of a parasite's potential for future range expansions.     

No evidence for host specialization or host-race formation in the European bitterling (Rhodeus amarus), a fish that parasitizes freshwater mussels

Coevolutionary relationships between parasites and hosts can elevate the rate of evolutionary changes owing to reciprocal adaptations between coevolving partners. Such relationships can result in the evolution of host specificity. Recent methodological advances have permitted the recognition of cryptic lineages, with important consequences for our understanding of biological diversity. We used the European bitterling (Rhodeus amarus), a freshwater fish that parasitizes unionid mussels, to investigate host specialization across regions of recent and ancient sympatry between coevolving partners. We combined genetic data (12 microsatellite and 2 mitochondrial markers) from five populations with experimental data for possible mechanisms of host species recognition (imprinting and conditioning). We found no strong evidence for the existence of cryptic lineages in R. amarus, though a small proportion of variation among individuals in an area of recent bitterling–mussel association was statistically significant in explaining host specificity. No other measures supported the existence of host‐specific lineages. Behavioural data revealed a weak effect of conditioning that biased behavioural preferences towards specific host species. Host imprinting had no effect on oviposition behaviour. Overall, we established that populations of R. amarus show limited potential for specialization, manifested as weak effects of host conditioning and genetic within‐population structure. Rhodeus amarus is the only species of mussel‐parasitizing fish in Europe, which contrasts with the species‐rich communities of bitterling in eastern Asia where several host‐specific bitterling occur. We discuss costs and constraints on the evolution of host‐specific lineages in our study system and more generally.     

The specialization and structure of antagonistic and mutualistic networks of beetles on rainforest canopy trees

Different kinds of species interactions can lead to different structures within ecological networks. Antagonistic interactions (such as between herbivores and host plants) often promote increasing host specificity within a compartmentalized network structure, whereas mutualistic networks (such as pollination networks) are associated with higher levels of generalization and form nested network structures. However, we recently showed that the host specificity of flower‐visiting beetles from three different feeding guilds (herbivores, fungivores, and predators) in an Australian rainforest canopy was equal to that of herbivores on leaves, suggesting that antagonistic herbivores on leaves are no more specialized than flower‐visitors. We therefore set out to test whether similarities in the host specificity of these different assemblages reflect similarities in underlying network structures. As shown before at the species level, mutualistic communities on flowers showed levels of specialization at the network scale similar to those of the antagonistic herbivore community on leaves. However, the network structure differed, with flower‐visiting assemblages displaying a significantly more nested structure than folivores, and folivores displaying a significantly more compartmentalized structure than flower‐visitors. These results, which need further testing in other forest systems, demonstrate that both antagonistic and mutualistic interactions can result in equally high levels of host specialization among beetle assemblages in tropical rainforests. If this is a widespread phenomenon, it may alter our current perceptions of food web dynamics, species diversity patterns, and co‐evolution in tropical rainforests. © 2014 The Linnean Society of London, Biological Journal of the Linnean Society, 2015, 114 , 287–295.     

Nested distributions of bat flies (Diptera: Streblidae) on Neotropical bats: artifact and specificity in host-parasite studies

We examined the structure of ectoparasitic bat fly infestations on 31 well‐sampled bat species, representing 4 Neotropical families. Sample sizes varied from 22 to 1057 bats per species, and bat species were infested by 4 to 27 bat fly species. Individual bats supported smaller infracommunities (the set of parasites co‐occurring on an individual host), ranging from 1 to 5 fly species in size, and no bat species had more than 6 bat fly species characteristically associated with it (its primary fly species). Nestedness analyses used system temperature (BINMATNEST algorithm) because it is particularly well‐suited for analysis of interaction networks, where parasite records may be nested among hosts and host individuals simultaneously nested among parasites. Most species exhibited very low system temperatures (mean 3.14°; range 0.14–12.28°). Simulations showed that nested structure for all 31 species was significantly stronger than simulated values under 2 of the 3 null hypotheses, and about half the species were also nested under the more stringent conditions of the third null hypothesis. Yet this structure disappears when analyses are restricted to “primary” associations of fly species (flies on their customary host species), which exclude records thought to be atypical, transient, or potential contaminants. Despite comprising a small fraction of total parasite records, such anomalies represent a considerable part of the statistical state‐space, offering the illusion of significant ecological structure. Only well understood and well documented systems can make distinctions between primary and other occurrence records. Generally, nestedness appears best developed in host‐parasite systems where infestations are long‐term and accumulate over time. Dynamic, short‐term infestations by highly mobile parasites like bat flies may appear to be nested, but such structure is better understood in terms of host specificity and accidental occurrences than in terms of prevalence, persistence, or hierarchical niche relations of the flies.     

Host–parasitoid development and survival strategies in a non-pollinating fig wasp community

In a tritrophic system, parasitoid development and galler host survival strategies have rarely been investigated simultaneously, an approach crucial for a complete understanding of the complexity of host–parasitoid interactions. Strategies in parasitoids to maximize host exploitation and in gallers to reduce predation risk can greatly affect the structure of tritrophic communities. In this study, the developmental strategies of galler hosts and their associated parasitoids in the tritrophic fig–fig wasp system are experimentally investigated for the first time. In this highly co-evolved system, wasp development is intrinsically tied with the phenology of the wasp brood sites that are restricted to the enclosed urn-shaped fig inflorescence called the syconium which can be regarded as a microcosm. Wasp exclusion experiments to determine host specificity, gall dissections and developmental assays were conducted with non-pollinating fig wasps in Ficus racemosa. Our results provide evidence for exceptions to the widely accepted koinobiont–idiobiont parasitoid dichotomy. This is also the first time fig wasps were raised ex situ from non-feeding stages onwards, a technique that enabled us to monitor their development from their pre-pupal to adult stages and record their development time more accurately. Based on variation in development time and host specificity, the possibility of a cryptic parasitoid species is raised. The frequency of different wasp species eclosing from the microcosms of individual syconia is explained using host–parasitoid associations and interactions under the modulating effect of host plant phenology.     

Phylogenetic evidence of host-specific cryptic species in the anther smut fungus

Cryptic structure of species complexes confounds an accurate accounting of biological diversity in natural systems. Also, cryptic sibling species often become specialized to different ecological conditions, for instance, with host specialization by cryptic parasite species. The fungus Microbotryum violaceum causes anther smut disease in plants of Caryophyllaceae, and the degree of specialization and gene flow between strains on different hosts have been controversial in the literature. We conducted molecular phylogenetic analyses on M. violaceum from 23 host species and different geographic origins using three single-copy nuclear genes (beta-tub, gamma-tub, and Ef1alpha). Congruence between the phylogenies identified several lineages that evolved independently for a long time. The lineages had overlapping geographic ranges but were highly specialized on different hosts. These results thus suggest that M. violaceum is a complex of highly specialized sibling species. Two incongruencies between the individual gene phylogenies and one intragene recombination event were detected at basal nodes, suggesting ancient introgression events or speciation events via hybridizations. However, incongruencies and recombination were not detected among terminal branches, indicating that the potentials for cross-infection and experimental hybridization are often not sufficient to suggest that introgressions would likely persist in nature.     

Host tissue identification for cryptic hymenopteran parasitoids associated with Sirex noctilio

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Deconstructing spatial patterns in species composition of ectoparasite communities: the relative contribution of host composition,environmental variables and geography

Aim We determined whether dissimilarity in species composition between parasite communities depends on geographic distance, environmental dissimilarity or host faunal dissimilarity, for different subsets of parasite species with different levels of host specificity. Location Communities of fleas parasitic on small mammals from 28 different regions of the Palaearctic. Method Dissimilarities in both parasite and host species composition were computed between each pair of regions using the Bray–Curtis index. Geographic distances between regions were also calculated, as were measures of environmental dissimilarity consisting of the pairwise Euclidean distances between regions derived from elevation, vegetation and climatic variables. The 136 flea species included in the dataset were divided into highly host‐specific species (using 1–2 host species per region, on average), moderately host‐specific species (2.2–4 hosts per region) and generalist species (>4 hosts per region). The relative influence of geographic distance, host faunal dissimilarity and environmental dissimilarity on dissimilarity of flea species composition among all regions was analysed for the entire set of flea species as well as for the three above subsets using multiple regressions on distance matrices. Results When including all flea species, dissimilarity in flea species composition was affected by all three independent variables, although the pure effect of dissimilarity in host species composition was the strongest. Results were different when the subsets of fleas differing in host specificity were treated separately. In particular, dissimilarity in species composition of highly host‐specific fleas increased solely with environmental dissimilarity, whereas dissimilarity for both moderately specific and non‐specific fleas increased with both geographic distance and dissimilarity in host species composition. Main conclusions Host specificity seems to dictate which of the three factors considered is most likely to affect the dissimilarity between flea communities. Counter‐intuitively, environmental dissimilarity played a key role in determining dissimilarity in species composition of highly host‐specific fleas, possibly because, although their presence in a region relies on the occurrence of particular host species, their abundance is itself mostly determined by climatic conditions. Our results show that deconstructing communities into subsets of species with different traits can make it easier to uncover the mechanisms shaping geographic patterns of diversity.