On the role of host phenotypic plasticity in host shifting by parasites

Ecological speciation appears to contribute to the diversification of insect herbivores and other parasites, which together comprise a major component of Earth's biodiversity. Host shifts are likely an important step in ecological speciation, and understanding how such shifts occur is critical to forming and testing hypotheses explaining parasite diversity. In this article, I argue that phenotypic variation in hosts arising from environmental variation (phenotypic plasticity) can promote shifts in parasites by bridging both spatiotemporal and phenotypic gaps between ancestral and novel hosts. This hypothesis, which I call the ‘plastic‐bridge hypothesis’, is conceptually distinct from those invoking genetic variation in bridging these gaps. I describe the mechanistic basis of plastic bridges, review circumstantial evidence in support of the hypothesis and suggest strategies for testing it. I use herbivorous insects and their host plants as a model, but the proposed ideas apply to any system fitting a broad definition of a host‐parasite relationship. The plastic‐bridge perspective suggests that parasite diversity is not only due to divergent selection provided by hosts, but also to the intraspecific variation that facilitates shifts between them. This view is timely, as biological invasion and range shifts associated with climate change foster novel interactions between parasites and hosts.     

Genetic differentiation associated with host plants and geography among six widespread species of South American Blepharoneura fruit flies (Tephritidae)

Tropical herbivorous insects are astonishingly diverse, and many are highly host‐specific. Much evidence suggests that herbivorous insect diversity is a function of host plant diversity; yet, the diversity of some lineages exceeds the diversity of plants. Although most species of herbivorous fruit flies in the Neotropical genus Blepharoneura are strongly host‐specific (they deposit their eggs in a single host plant species and flower sex), some species are collected from multiple hosts or flowers and these may represent examples of lineages that are diversifying via changes in host use. Here, we investigate patterns of diversification within six geographically widespread Blepharoneura species that have been collected and reared from at least two host plant species or host plant parts. We use microsatellites to (1) test for evidence of local genetic differentiation associated with different sympatric hosts (different plant species or flower sexes) and (2) examine geographic patterns of genetic differentiation across multiple South American collection sites. In four of the six fly species, we find evidence of local genetic differences between flies collected from different hosts. All six species show evidence of geographic structure, with consistent differences between flies collected in the Guiana Shield and flies collected in Amazonia. Continent‐wide analyses reveal – in all but one instance – that genetically differentiated flies collected in sympatry from different host species or different sex flowers are not one another's closest relatives, indicating that genetic differences often arise in allopatry before, or at least coincident with, the evolution of novel host use.     

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.     

The evolution of climate tolerance in conifer‐feeding aphids in relation to their host's climatic niche

Climate adaptation has major consequences in the evolution and ecology of all living organisms. Though phytophagous insects are an important component of Earth's biodiversity, there are few studies investigating the evolution of their climatic preferences. This lack of research is probably because their evolutionary ecology is thought to be primarily driven by their interactions with their host plants. Here, we use a robust phylogenetic framework and species‐level distribution data for the conifer‐feeding aphid genus Cinara to investigate the role of climatic adaptation in the diversity and distribution patterns of these host‐specialized insects. Insect climate niches were reconstructed at a macroevolutionary scale, highlighting that climate niche tolerance is evolutionarily labile, with closely related species exhibiting strong climatic disparities. This result may suggest repeated climate niche differentiation during the evolutionary diversification of Cinara. Alternatively, it may merely reflect the use of host plants that occur in disparate climatic zones, and thus, in reality the aphid species' fundamental climate niches may actually be similar but broad. Comparisons of the aphids' current climate niches with those of their hosts show that most Cinara species occupy the full range of the climatic tolerance exhibited by their set of host plants, corroborating the hypothesis that the observed disparity in Cinara species' climate niches can simply mirror that of their hosts. However, 29% of the studied species only occupy a subset of their hosts' climatic zone, suggesting that some aphid species do indeed have their own climatic limitations. Our results suggest that in host‐specialized phytophagous insects, host associations cannot always adequately describe insect niches and abiotic factors must be taken into account.     

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.     

Global patterns in helminth host specificity: phylogenetic and functional diversity of regional host species pools matter

Host specificity has a major influence on a parasite's ability to shift between human and animal host species. Yet there is a dearth of quantitative approaches to explore variation in host specificity across biogeographical scales, particularly in response to the varying community compositions of potential hosts. We built a global dataset of intermediate host associations for nine of the world's most widespread helminth parasites (all of which infect humans). Using hierarchical models, we asked if realised parasite host specificity varied in response to regional variation in the phylogenetic and functional diversities of potential host species. Parasites were recorded in 4–10 zoogeographical regions, with some showing considerable geographical variation in observed versus expected host specificity. Parasites generally exhibited the lowest phylogenetic host specificity in regions with the greatest variation in prospective host phylogenetic diversity, namely the Neotropical, Saharo‐Arabian and Australian regions. Globally, we uncovered notable variation in parasite host shifting potential. Observed host assemblages for Hydatigera taeniaeformis and Hymenolepis diminuta were less phylogenetically diverse than expected, suggesting limited potential to spillover into unrelated hosts. Host assemblages for Echinococcus granulosus, Mesocestoides lineatus and Trichinella spiralis were less functionally diverse than expected, suggesting limited potential to shift across host ecological niches. By contrast, Hyd. taeniaeformis infected a higher functional diversity of hosts than expected, indicating strong potential to shift across hosts with different ecological niches. We show that the realised phylogenetic and functional diversities of infected hosts are determined by biogeographical gradients in prospective host species pools. These findings emphasise the need to account for underlying species diversity when assessing parasite host specificity. Our framework to identify variation in realised host specificity is broadly applicable to other host–parasite systems and will provide key insights into parasite invasion potential at regional and global scales.     

Host‐specific associations affect the microbiome of Philornis downsi,an introduced parasite to the Galápagos Islands

The composition and diversity of bacteria forming the microbiome of parasitic organisms have implications for differential host pathogenicity and host–parasite co‐evolutionary interactions. The microbiome of pathogens can therefore have consequences that are relevant for managing disease prevalence and impact on affected hosts. Here, we investigate the microbiome of an invasive parasitic fly Philornis downsi, recently introduced to the Galápagos Islands, where it poses extinction threat to Darwin's finches and other land birds. Larvae infest nests of Darwin's finches and consume blood and tissue of developing nestlings, and have severe mortality impacts. Using 16s rRNA sequencing data, we characterize the bacterial microbiota associated with P. downsi adults and larvae sourced from four finch host species, inhabiting two islands and representing two ecologically distinct groups. We show that larval and adult microbiomes are dominated by the phyla Proteobacteria and Firmicutes, which significantly differ between life stages in their distributions. Additionally, bacterial community structure significantly differed between larvae retrieved from strictly insectivorous warbler finches (Certhidea olivacea) and those parasitizing hosts with broader dietary preferences (ground and tree finches, Geospiza and Camarhynchus spp., respectively). Finally, we found no spatial effects on the larval microbiome, as larvae feeding on the same host (ground finches) harboured similar microbiomes across islands. Our results suggest that the microbiome of P. downsi changes during its development, according to dietary composition or nutritional needs, and is significantly affected by host‐related factors during the larval stage. Unravelling the ecological significance of bacteria for this parasite will contribute to the development of novel, effective control strategies.     

Body size and fecundity are correlated in feather lice (Phthiraptera: Ischnocera): implications for Harrison's rule

1. Harrison's rule, which predicts that large‐bodied species of hosts have large‐bodied species of parasites, has been documented in a wide diversity of parasites. 2. Harrison's rule has been most thoroughly studied in avian feather lice, which escape from host defence (preening) by hiding in the feathers. Lice that are unable to hide are selectively removed by preening. Preening selects for small lice on small hosts, which have small feathers in which to hide. 3. Preening should not, however, select for large lice on large hosts. Instead, the larger size of lice on large hosts is thought to result from a positive relationship between size and fecundity, as shown for many other insects. 4. This study tested for a size–fecundity correlation within Columbicola columbae, the host‐specific ‘wing louse’ of rock pigeons (Columba livia). 5. The results confirm a positive relationship between female body length and number of eggs laid. 6. The study thus supports a mechanism consistent with stabilising selection leading to the evolution of the Harrison's rule pattern among species of Columbicola and their hosts.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

Olfactory recognition and behavioural avoidance of angiosperm nonhost volatiles by conifer-inhabiting bark beetles

Abstract 1 When searching for suitable hosts in flight, especially in mixed forests, conifer‐inhabiting bark beetles will encounter not only suitable host trees and their odours, but also unsuitable hosts and nonhost trees. Rejection of these trees could be based on an imbalance of certain host characteristics and/or a negative response to some nonhost stimuli, such as nonhost volatiles (NHV). 2 Recent electrophysiological and behavioural studies clearly indicate that conifer‐inhabiting bark beetles are not only able to recognize, but also to avoid, nonhost habitats or trees by olfactory means. Green leaf volatiles (GLV), especially C₆‐alcohols, from the leaves (and partly from bark) of nonhost angiosperm trees, may represent nonhost odour signals at the habitat level. Specific bark volatiles such as trans‐conophthorin, C₈‐alcohols, and some aromatic compounds, may indicate nonhosts at the tree species level. Flying bark beetles are also capable of determining whether a possible host is unsuitable by reacting to signals from conspecifics or sympatric heterospecifics that indicate old or colonized host tree individuals. 3 Combined NHV signals in blends showed both redundancy and synergism in their inhibitory effects. The coexistence of redundancy and synergism in negative NHV signals may indicate different functional levels (nonhost habitats, species, and unsuitable hosts) in the host selection process. Combinations of NHV and verbenone significantly reduced the number of mass attacked host trees or logs on several economically important species (e.g. Dendroctonus ponderosae, Ips typographus, and I. sexdentatus). 4 We suggest a semiochemical‐diversity hypothesis, based on the inhibition by NHV of bark beetle host‐location, which might partly explain the lower outbreak rates of forest insects in mixed forests. This ‘semiochemical‐diversity hypothesis’ would provide new support to the general ‘stability‐diversity hypothesis’. 5 Natural selection appears to have caused conifer‐inhabiting bark beetles to evolve several olfactory mechanisms for finding their hosts and avoiding unsuitable hosts and nonhost species. NHV and unsuitable host signals have potential for use in protecting trees from attack. The use of these signals may be facilitated by the fact that their combination has an active inhibition radius of several metres in trap test, and by the observation of area effects for several trees near inhibitor soruces in tree protection experiments. Furthermore, incorporation of negative signals (such as NHV and verbenone) and pheromone‐based mass‐trapping in a ‘push–pull’ fashion may significantly increase the options for control against outbreaks of conifer‐inhabiting bark beetles, especially in high risk areas.     

Epiphytic ferns and bryophytes of Tasmanian tree‐ferns: A comparison of diversity and composition between two host species

Abstract Ferns, bryophytes and lichens are the most diverse groups of plants in wet forests in south‐eastern Australia. However, management of this diversity is limited by a lack of ecological knowledge of these groups and the difficulty in identifying species for non‐experts. These problems may be alleviated by the identification and characterization of suitable proxies for this diversity. Epiphytic substrates are potential proxies. To evaluate the significance of some epiphytic substrates, fern and bryophyte assemblages on a common tree‐fern species, Dicksonia antarctica (soft tree‐fern), were compared with those on a rare species, Cyathea cunninghamii (slender tree‐fern), in eastern Tasmania, Australia. A total of 97 fern and bryophyte species were recorded on D. antarctica from 120 trunks at 10 sites, and 64 species on C. cunninghamii from 39 trunks at four of these sites. The trunks of C. cunninghamii generally supported fewer species than D. antarctica, but two mosses (particularly Hymenodon pilifer) and one liverwort showed significant associations with this host. Several other bryophytes and epiphytic ferns showed an affinity for the trunks of D. antarctica. Species assemblages differed significantly between both sites and hosts, and the differences between hosts varied significantly among sites. The exceptionally high epiphytic diversity associated with D. antarctica suggests that it plays an important ecological role in Tasmanian forests. Evidently C. cunninghamii also supports a diverse suite of epiphytes, including at least one specialist species.     

Molecular tracking of individual host use in the Shiny Cowbird – a generalist brood parasite

Generalist parasites exploit multiple host species at the population level, but the individual parasite's strategy may be either itself a generalist or a specialist pattern of host species use. Here, we studied the relationship between host availability and host use in the individual parasitism patterns of the Shiny Cowbird Molothrus bonariensis, a generalist avian obligate brood parasite that parasitizes an extreme range of hosts. Using five microsatellite markers and an 1120‐bp fragment of the mtDNA control region, we reconstructed full‐sibling groups from 359 cowbird eggs and chicks found in nests of the two most frequent hosts in our study area, the Chalk‐browed Mockingbird Mimus saturninus and the House Wren Troglodytes aedon. We were able to infer the laying behavior of 17 different females a posteriori and found that they were mostly faithful to a particular laying area and host species along the entire reproductive season and did not avoid using previously parasitized nests (multiple parasitism) even when other nests were available for parasitism. Moreover, we found females using the same host nest more than once (repeated parasitism), which had not been previously reported for this species. We also found few females parasitizing more than one host species. The use of an alternative host was not related to the main hosts' nest availability. Overall, female shiny cowbirds use a spatially structured and host species specific approach for parasitism, but they do so nonexclusively, resulting in both detectable levels of multiple parasitism and generalism at the level of individual parasites.     

The origin and genetic differentiation of the socially parasitic aphid Tamalia inquilinus

Social and brood parasitisms are nonconsumptive forms of parasitism involving the exploitation of the colonies or nests of a host. Such parasites are often related to their hosts and may evolve in various ecological contexts, causing evolutionary constraints and opportunities for both parasites and their hosts. In extreme cases, patterns of diversification between social parasites and their hosts can be coupled, such that diversity of one is correlated with or even shapes the diversity of the other. Aphids in the genus Tamalia induce galls on North American manzanita (Arctostaphylos) and related shrubs (Arbutoideae) and are parasitized by nongalling social parasites or inquilines in the same genus. We used RNA sequencing to identify and generate new gene sequences for Tamalia and performed maximum‐likelihood, Bayesian and phylogeographic analyses to reconstruct the origins and patterns of diversity and host‐associated differentiation in the genus. Our results indicate that the Tamalia inquilines are monophyletic and closely related to their gall‐forming hosts on Arctostaphylos, supporting a previously proposed scenario for origins of these parasitic aphids. Unexpectedly, population structure and host‐plant‐associated differentiation were greater in the non‐gall‐inducing parasites than in their gall‐inducing hosts. RNA‐seq indicated contrasting patterns of gene expression between host aphids and parasites, and perhaps functional differences in host‐plant relationships. Our results suggest a mode of speciation in which host plants drive within‐guild diversification in insect hosts and their parasites. Shared host plants may be sufficient to promote the ecological diversification of a network of phytophagous insects and their parasites, as exemplified by Tamalia aphids.     

Density‐mediated indirect interactions alter host foraging behaviour of parasitoids without altering foraging efficiency

1. Foraging decisions of parasitoids are influenced by host density via density‐mediated indirect interactions. However, in the parasitoid's environment, non‐suitable herbivores are also present. These non‐hosts also occur in different densities, which can affect a parasitoid's foraging behaviour. 2. The influence of non‐host densities can be expressed during the first phase of the foraging process, when parasitoids use plant volatiles to locate plants infested by their host. They may also play a role during the second phase, when parasitoids use infochemicals from the host and plant to locate, recognise and accept the host. 3. By using laboratory and field setups, it was studied whether the density of non‐host herbivores influences these two phases of the foraging behaviour of the parasitoid Cotesia glomerata as well as the parasitoid's efficiency to find its host, Pieris brassicae caterpillars. 4. The findings show that a high non‐host density, regardless of the species used, negatively affected parasitoid preference for host‐infested plants, but that the behaviour on the plant and the total host‐finding efficiency of the parasitoids were not influenced by non‐host density. 5. These results are discussed in the context of density‐mediated indirect interactions.     

Interactions among Triatoma sanguisuga blood feeding sources,gut microbiota and Trypanosoma cruzi diversity in southern Louisiana

Integrating how biodiversity and infectious disease dynamics are linked at multiple levels and scales is highly challenging. Chagas disease is a vector‐borne disease, with specificities of the triatomine vectors and Trypanosoma cruzi parasite life histories resulting in a complex multihost and multistrain life cycle. Here, we tested the hypothesis that T. cruzi transmission cycles are shaped by triatomine host communities and gut microbiota composition by comparing the integrated interactions of Triatoma sanguisuga in southern Louisiana with feeding hosts, T. cruzi parasite and bacterial microbiota in two habitats. Bugs were collected from resident's houses and animal shelters and analysed for genetic structure, blood feeding sources, T. cruzi parasites, and bacterial diversity by PCR amplification of specific DNA markers followed by next‐generation sequencing, in an integrative metabarcoding approach. T. sanguisuga feeding host communities appeared opportunistic and defined by host abundance in each habitat, yielding distinct parasite transmission networks among hosts. The circulation of a large diversity of T. cruzi DTUs was also detected, with TcII and TcV detected for the first time in triatomines in the US. The bacterial microbiota was highly diverse and varied significantly according to the DTU infecting the bugs, indicating specific interactions among them in the gut. Expanding such studies to multiple habitats and additional triatomine species would be key to further refine our understanding of the complex life cycles of multihost, multistrain parasites such as T. cruzi, and may lead to improved disease control strategies.     

Within‐population variation in social strategies characterize the social and mating system of an Australian lizard,Egernia whitii

The lizard genus Egernia has been suggested as an excellent model system for examining the evolution of sociality as it exhibits considerable diversity in social organization both between and within species. To date the majority of work examining the factors responsible for the evolution of sociality within Egernia has advocated a broad scale approach; identifying the social structure of specific species or populations and comparing the degree of sociality between them. However, we argue that significant advancements could also be gained by examining variation in social strategies within populations. Here we integrate a detailed, 3‐year, field‐based examination of social spacing and juvenile dispersal with molecular analyses of paternity to determine the social and mating system of a Tasmanian population of White's skink (Egernia whitii). We show that E. whitii live in small stable family groups consisting of an adult male, his female partner(s), as well as juvenile or sub‐adults individuals. In addition, while the mating system is characterized by considerable genetic monogamy, extra‐pair fertilizations are relatively common, with 34% of litters containing offspring sired by males from outside the social group. We also show that traits related to social organization (social group composition, group size, stability and the level of extra‐pair paternity) vary both between and within individuals. We suggest that ecological factors, such as habitat saturation, quality and availability, play a key role in maintaining between individual variation in social strategies, and that examining these individual level processes will allow us to more clearly understand variation in sociality among species.     

Superinfection and the coevolution of parasite virulence and host recovery

Parasite strategies of host exploitation may be affected by host defence strategies and multiple infections. In particular, within‐host competition between multiple parasite strains has been shown to select for higher virulence. However, little is known on how multiple infections could affect the coevolution between host recovery and parasite virulence. Here, we extend a coevolutionary model introduced by van Baalen (Proc. R. Soc. B, 265, 1998, 317) to account for superinfection. When the susceptibility to superinfection is low, we recover van Baalen's results and show that there are two potential evolutionary endpoints: one with avirulent parasites and poorly defended hosts, and another one with high virulence and high recovery. However, when the susceptibility to superinfection is above a threshold, the only possible evolutionary outcome is one with high virulence and high investment into defence. We also show that within‐host competition may select for lower host recovery, as a consequence of selection for more virulent strains. We discuss how different parasite and host strategies (superinfection facilitation, competitive exclusion) as well as demographic and environmental parameters, such as host fecundity or various costs of defence, may affect the interplay between multiple infections and host–parasite coevolution. Our model shows the interplay between coevolutionary dynamics and multiple infections may be affected by crucial mechanistic or ecological details.     

Magnitude and direction of parasite‐induced phenotypic alterations: a meta‐analysis in acanthocephalans

Several parasite species have the ability to modify their host's phenotype to their own advantage thereby increasing the probability of transmission from one host to another. This phenomenon of host manipulation is interpreted as the expression of a parasite extended phenotype. Manipulative parasites generally affect multiple phenotypic traits in their hosts, although both the extent and adaptive significance of such multidimensionality in host manipulation is still poorly documented. To review the multidimensionality and magnitude of host manipulation, and to understand the causes of variation in trait value alteration, we performed a phylogenetically corrected meta‐analysis, focusing on a model taxon: acanthocephalan parasites. Acanthocephala is a phylum of helminth parasites that use vertebrates as final hosts and invertebrates as intermediate hosts, and is one of the few parasite groups for which manipulation is predicted to be ancestral. We compiled 279 estimates of parasite‐induced alterations in phenotypic trait value, from 81 studies and 13 acanthocephalan species, allocating a sign to effect size estimates according to the direction of alteration favouring parasite transmission, and grouped traits by category. Phylogenetic inertia accounted for a low proportion of variation in effect sizes. The overall average alteration of trait value was moderate and positive when considering the expected effect of alterations on trophic transmission success (signed effect sizes, after the onset of parasite infectivity to the final host). Variation in the alteration of trait value was affected by the category of phenotypic trait, with the largest alterations being reversed taxis/phobia and responses to stimuli, and increased vulnerability to predation, changes to reproductive traits (behavioural or physiological castration) and immunosuppression. Parasite transmission would thereby be facilitated mainly by changing mainly the choice of micro‐habitat and the anti‐predation behaviour of infected hosts, and by promoting energy‐saving strategies in the host. In addition, infection with larval stages not yet infective to definitive hosts (acanthella) tends to induce opposite effects of comparable magnitude to infection with the infective stage (cystacanth), although this result should be considered with caution due to the low number of estimates with acanthella. This analysis raises important issues that should be considered in future studies investigating the adaptive significance of host manipulation, not only in acanthocephalans but also in other taxa. Specifically, the contribution of phenotypic traits to parasite transmission and the range of taxonomic diversity covered deserve thorough attention. In addition, the relationship between behaviour and immunity across parasite developmental stages and host–parasite systems (the neuropsychoimmune hypothesis of host manipulation), still awaits experimental evidence. Most of these issues apply more broadly to reported cases of host manipulation by other groups of parasites.     

Nonhost diversity and density reduce the strength of parasitoid–host interactions

The presence of nonprey or nonhosts is known to reduce the strength of consumer– resource interactions by increasing the consumer's effort needed to find its resource. These interference effects can have a stabilizing effect on consumer–resource dynamics, but have also been invoked to explain parasitoid extinctions. To understand how nonhosts affect parasitoids, we manipulated the density and diversity of nonhost aphids using experimental host–parasitoid communities and tested how this affects parasitation efficiency of two aphid parasitoid species. To further study the behavioral response of parasitoids to nonhosts, we tested for changes in parasitoid time allocation in relation to their host‐finding strategies. The proportion of successful attacks (attack rate) in both parasitoid species was reduced by the presence of nonhosts. The parasitoid Aphidius megourae was strongly affected by increasing nonhost diversity with the attack rate dropping from 0.39 without nonhosts to 0.05 with high diversity of nonhosts, while Lysiphlebus fabarum responded less strongly, but in a more pronounced way to an increase in nonhost density. Our experiments further showed that increasing nonhost diversity caused host searching and attacking activity levels to fall in A. megourae, but not in L. fabarum, and that A. megourae changed its behavior after a period of time in the presence of nonhosts by increasing its time spent resting. This study shows that nonhost density and diversity in the environment are crucial determinants for the strength of consumer–resource interactions. Their impact upon a consumer's efficiency strongly depends on its host/prey finding strategy as demonstrated by the different responses for the two parasitoid species. We discuss that these trait‐mediated indirect interactions between host and nonhost species are important for community stability, acting either stabilizing or destabilizing depending on the level of nonhost density or diversity present.     

Relative fitness of a generalist parasite on two alternative hosts: a cross‐infestation experiment to test host specialization of the hen flea Ceratophyllus gallinae (Schrank)

Host range is a key element of a parasite's ecology and evolution and can vary greatly depending on spatial scale. Generalist parasites frequently show local population structure in relation to alternative sympatric hosts (i.e. host races) and may thus be specialists at local scales. Here, we investigated local population specialization of a common avian nest‐based parasite, the hen flea Ceratophyllus gallinae (Schrank), exploiting two abundant host species that share the same breeding sites, the great tit Parus major (Linnaeus) and the collared flycatcher Ficedula albicollis (Temminck). We performed a cross‐infestation experiment of fleas between the two host species in two distinct study areas during a single breeding season and recorded the reproductive success of both hosts and parasites. In the following year, hosts were monitored again to assess the long‐term impact of cross‐infestation. Our results partly support the local specialization hypothesis: in great tit nests, tit fleas caused higher damage to their hosts than flycatcher fleas, and in collared flycatcher nests, flycatcher fleas had a faster larval development rates than tit fleas. However, these results were significant in only one of the two studied areas, suggesting that the location and history of the host population can modulate the specialization process. Caution is therefore called for when interpreting single location studies. More generally, our results emphasize the need to explicitly account for host diversity in order to understand the population ecology and evolutionary trajectory of generalist parasites.