Red queen meets Santa Rosalia: arms races and the evolution of host specialization in organisms with parasitic lifestyles

I argue that nonequilibrium allele frequency dynamics due to coevolution can drive the evolution of specialized host races in parasites capable of host choice-for example, herbivorous insects or parasitoids. The proposed mechanism does not require genetic trade-offs in performance on different host species. It is based on the premise that the ability of the parasite to overcome the resistance of different host species is to a large degree genetically independent-that is, controlled by different loci. The intuitive rationale is that the genetic lineage of a parasite that evolves host preference becomes more consistently exposed to selection for performance on its preferred host. Such a choosy lineage can thus coevolve faster in response to evolving host defenses than a generalist lineage distributed among several host species. Given genetic variation in host preference, an initially generalist parasite population evolves toward specialized host races, each choosing one host species. This idea is supported by a series of multilocus models of coevolution between a parasite and two host species, in which the parasite virulence on each host is affected by a different set of loci and an additional locus or two loci control host choice.     

Flexible Use of Patch-Leaving Mechanisms in a Parasitoid Wasp

Classical optimal-foraging theory predicts that a parasitoid is less likely to leave a patch after a host encounter when the host distribution is aggregated, whereas a parasitoid is more likely to leave after a host encounter when the host distribution is regular. Field data on host distributions in the area of origin of the whitefly parasitoid Encarsia formosa showed that whiteflies aggregate at several spatial scales. However, infested leaves most likely contained a single host. This suggests that a host encounter is not enough to decide when to leave. We therefore tested the effect of host distribution and parasitoid experience on patch-leaving behavior. Each parasitoid was observed for several consecutive days in a three-dimensional arena with leaflets containing on average one host per leaflet in an either regular or aggregated host distribution. A proportional hazards model showed that a host encounter decreased the leaving tendency on a leaflet with one host when the time since the latest host encounter was short, but increased the leaving tendency when the time since the latest host encounter was long, independent of host distribution. We conclude that a parasitoid can switch from decreasing to increasing its tendency to leave a patch after a host encounter. We propose two hypotheses that may explain the evolution of such a switching mechanism.     

Ectoparasite fitness in auxiliary hosts: phylogenetic distance from a principal host matters

We studied reproductive performance in two flea species (Parapulex chephrenis and Xenopsylla ramesis) exploiting either a principal or one of eight auxiliary host species. We predicted that fleas would produce more eggs and adult offspring when exploiting (i) a principal host than an auxiliary host and (ii) an auxiliary host phylogenetically close to a principal host than an auxiliary host phylogenetically distant from a principal host. In both flea species, egg production per female after one feeding and production of new imago after a timed period of an uninterrupted stay on a host differed significantly between host species. In general, egg and/or new imago production in fleas feeding on an auxiliary host was lower than in fleas feeding on the principal host, except for the auxiliary host that was the closest relative of the principal host. When all auxiliary host species were considered, we did not find any significant relationship between either egg or new imago production in fleas exploiting an auxiliary host and phylogenetic distance between this host and the principal host. However, when the analyses were restricted to auxiliary hosts belonging to the same family as the principal host (Muridae), new imago production (for P. chephrenis) or both egg and new imago production (for X. ramesis) in an auxiliary host decreased significantly with an increase in phylogenetic distance between the auxiliary and principal host. Our results demonstrated that a parasite achieves higher fitness in auxiliary hosts that are either the most closely related to or the most distant from its principal host. This may affect host associations of a parasite invading new areas.     

Two different strategies of host manipulation allow parasites to persist in intermediate–definitive host systems

Trophically transmitted parasites start their development in an intermediate host, before they finish the development in their definitive host when the definitive host preys on the intermediate host. In intermediate–definitive host systems, two strategies of host manipulation have been evolved: increasing the rate of transmission to the definitive host by increasing the chance that the definitive host will prey on the intermediate host, or increasing the lifespan of the parasite in the intermediate host by decreasing the predation chance when the intermediate host is not yet infectious. As the second strategy is less well studied than the first, it is unknown under what conditions each of these strategies is prevailed and evolved. We analysed the effect of both strategies on the presence of parasites in intermediate–definitive host systems with a structured population model. We show that the parasite can increase the parameter space where it can persist in the intermediate–definitive host system using one of these two strategies of host manipulation. We found that when the intermediate host or the definitive host has life‐history traits that allow the definitive host to reach large population densities, that is high reproduction rate of the intermediate host or high conversion efficiency of the definitive host (efficiency at which the uninfected definitive host converts caught intermediate hosts into offspring), respectively, evolving manipulation to decrease the predation chance of the intermediate host will be more beneficial than manipulation to increase the predation chance to enhance transmission. Furthermore, manipulation to decrease the predation chance of the intermediate host results in higher population densities of infected intermediate hosts than manipulation that increases the predation chance to enhance transmission. Our study shows that host manipulation in early stages of the parasite development to decrease predation might be a more frequently evolved way of host manipulation than is currently assumed.     

Foliar fungal endophyte community structure is independent of phylogenetic relatedness in an Asteraceae common garden

Phylogenetic distance among host species represents a proxy for host traits that act as biotic filters to shape host‐associated microbiome community structure. However, teasing apart potential biotic assembly mechanisms, such as host specificity or local species interactions, from abiotic factors, such as environmental specificity or dispersal barriers, in hyperdiverse, horizontally transmitted microbiomes remains a challenge. In this study, we tested whether host phylogenetic relatedness among 18 native Asteraceae plant species and spatial distance between replicated plots in a common garden affects foliar fungal endophyte (FFE) community structure. We found that FFE community structure varied significantly among host species, as well as host tribes, but not among host subfamilies. However, FFE community dissimilarity between host individuals was not significantly correlated with phylogenetic distance between host species. There was a significant effect of spatial distance among host individuals on FFE community dissimilarity within the common garden. The significant differences in FFE community structure among host species, but lack of a significant host phylogenetic effect, suggest functional differences among host species not accounted for by host phylogenetic distance, such as metabolic traits or phenology, may drive FFE community dissimilarity. Overall, our results indicate that host species identity and the spatial distance between plants can determine the similarity of their microbiomes, even across a single experimental field, but that host phylogeny is not closely tied to FFE community divergence in native Asteraceae.     

Specialized avian Haemosporida trade reduced host breadth for increased prevalence

Parasite specialization on one or a few host species leads to a reduction in the total number of available host individuals, which may decrease transmission. However, specialists are thought to be able to compensate by increased prevalence in the host population and increased success in each individual host. Here, we use variation in host breadth among a community of avian Haemosporida to investigate consequences of generalist and specialist strategies on prevalence across hosts. We show that specialist parasites are more prevalent than generalist parasites in host populations that are shared between them. Moreover, the total number of infections of generalist and specialist parasites within the study area did not vary significantly with host breadth. This suggests that specialists can infect a similar number of host individuals as generalists, thus compensating for a reduction in host availability by achieving higher prevalence in a single host species. Specialist parasites also tended to infect older hosts, whereas infections by generalists were biased towards younger hosts. We suggest that this reflects different abilities of generalists and specialists to persist in hosts following infection. Higher abundance and increased persistence in hosts suggest that specialists are more effective parasites than generalists, supporting the existence of a trade‐off between host breadth and average host use among these parasites.     

A sex-specific size–number tradeoff in clonal broods

Polyembryonic parasitoids producing single-sex broods of clonal offspring provide an unusually clear window into the classic tradeoff between the number and size of offspring. We conducted a laboratory study of the encyrtid parasitoid Copidosoma bakeri parasitizing the noctuid Agrotis ipsilon to examine the way that size and number of offspring tradeoff in broods of each sex and to determine how the fit between host and parasitoid brood is achieved. We found that brood mass (wasp body mass ×brood size) was proportional to host mass, independent of brood sex, indicating a tight fit between brood and host and ensuring a size–number tradeoff. By correcting brood size and body mass of each brood for host mass, we demonstrated the expected inverse relationship between wasp variables. We postulated that the wasp brood might achieve the fit to the host by (1) adjusting brood size based on information available early in host development before and during division of the embryo, (2) manipulating host size late in host development after completion of embryo division, or (3) simply adjusting individual wasp mass to fill the host. We evaluated host responses to parasitism – and correlations between brood size and host growth early and late in development – for broods of each sex. The data are consistent with adjustment of brood size to the amount of host growth early in host development and with manipulation of host mass late in host development. The tight link between host mass and brood mass also suggests a final adjustment by parasitoid growth to achieve complete filling. Within the tight fit, female broods were smaller but contained larger individuals than male broods. The sex-specific balance point of the tradeoff and sex differences in balancing mechanisms and responses to host size suggest different selection pressures on each sex requiring future investigation.     

Conflicts over host manipulation between different parasites and pathogens: Investigating the ecological and medical consequences

When parasites have different interests in regard to how their host should behave this can result in a conflict over host manipulation, i.e. parasite induced changes in host behaviour that enhance parasite fitness. Such a conflict can result in the alteration, or even complete suppression, of one parasite's host manipulation. Many parasites, and probably also symbionts and commensals, have the ability to manipulate the behaviour of their host. Non‐manipulating parasites should also have an interest in host behaviour. Given the frequency of multiple parasite infections in nature, potential conflicts of interest over host behaviour and manipulation may be common. This review summarizes the evidence on how parasites can alter other parasite's host manipulation. Host manipulation can have important ecological and medical consequences. I speculate on how a conflict over host manipulation could alter these consequences and potentially offer a new avenue of research to ameliorate harmful consequences of host manipulation.     

Escaping the matrix: a new algorithm for phylogenetic comparative studies of co-evolution

An algorithm for generating host cladograms from parasite‐host cladograms derived from parasite phylogenies, Phylogenetic Analysis for Comparing Trees (PACT), is described. PACT satisfies Assumption 0, that all the information in each parasite‐host cladogram must be used in a co‐evolutionary analysis, and that the host relationships depicted in the final host cladogram must be logically consistent with the phylogenetic relationships depicted in every part of every parasite‐host cladogram used to construct the host cladogram. It accounts for cases of speciation by host switching and expansion of host range, and reticulated host relationships, in addition to co‐speciation, sympatric speciation, and extinction in all input parasite‐host cladograms, and does so without a priori weighting schemes and without a posteriori manipulation of the data.     

Molecular and genetic analysis of factors controlling host range in Agrobacterium tumefaciens

Summary We have investigated the factors which contribute to the host specificity of a tumor inducing plasmid of Agrobacterium, pTiAg162, which confers a narrow host range. Determinants both within the T-DNA and virulence regions contribute to host specificity. Within the T-DNA a defective cytokinin biosynthetic gene limits host range. Nucleotide sequence analysis revealed a large deletion in the 5 coding region of this gene when compared with the homologous gene from the wide host range tumor inducing plasmid, pTiA6. Introduction of the wide host range cytokinin biosynthesis gene into the T-DNA of the limited host range strain expanded the host range and suppressed the rooty morphology of tumors incited by the limited host range strain. Two genes from the virulence region of the wide host range plasmid, designated virA and virC, must also be introduced into the limited host range strain in order to restore a wide host range phenotype. The wide host range strain is avirulent on some cultivars of Vitis plants on which the limited host range strain induces tumors. This avirulence is apparently due to a hypersensitive response in which infected plant cells are killed at the site of inoculation. Mutations within the virC locus of the wide host range plasmid prevented the hypersensitive response and allowed the formation of tumors by the wide host range strain.     

Revisiting the particular role of host shifts in initiating insect speciation

The notion that shifts to new hosts can initiate insect speciation is more than 150 years old, yet widespread conflation with paradigms of sympatric speciation has led to confusion about how much support exists for this hypothesis. Here, we review 85 insect systems and evaluate the relationship between host shifting, reproductive isolation, and speciation. We sort insects into five categories: (1) systems in which a host shift has initiated speciation; (2) systems in which a host shift has made a contribution to speciation; (3) systems in which a host shift has caused the evolution of new reproductive isolating barriers; (4) systems with host‐associated genetic differences; and (5) systems with no evidence of host‐associated genetic differences. We find host‐associated genetic structure in 65 systems, 43 of which show that host shifts have resulted in the evolution of new reproductive barriers. Twenty‐six of the latter also support a role for host shifts in speciation, including eight studies that definitively support the hypothesis that a host shift has initiated speciation. While this review is agnostic as to the fraction of all insect speciation events to which host shifts have contributed, it clarifies that host shifts absolutely can and do initiate speciation.     

烟粉虱(Bemisia tabaci)的寄主选择性

通过田间系统调查、实验室嗅觉测定、笼内和培养皿内自由扩散观察,对烟粉虱的寄主选择性进行了研究.结果表明,在田间,烟粉虱对不同的寄主植物存在明显的寄主选择性,其中对茄子、花椰菜、黄瓜等植物具有较强的嗜性,而对蕹菜、芹菜、苋菜等植物的嗜性较差;烟粉虱对同一植物的不同品种也有明显的选择性.烟粉虱对寄主植物颜色有明显的选择性,选择结果与烟粉虱对这些寄主的嗜性趋势基本一致.烟粉虱对单株寄主植物的嗅觉反应不敏感,但对植物叶片的乙醇抽提物有明显的嗅觉反应,并表现出较强的寄主选择性.在养虫笼内,烟粉虱从虫源皿向寄主植物自由扩散的过程中,在不同寄主植物和同一植物的不同品种上着落的成虫数量不同,并且在一定的时间范围内,着落在寄主叶片上的虫量还会不断的发生变化.     

Fitness consequences of superparasitism and mechanism of host discrimination in the stemborer parasitoid Cotesia flavipes

The fitness consequences of superparasitism and the mechanism of host discrimination in Cotesia flavipes, a larval parasitoid of concealed stemborer larvae was investigated. Naive females readily superparasitized and treated the already parasitized host as an unparasitized host by allocating the same amount of eggs as in an unparasitized host. However, there was no significant increase in the number of emerging parasitoids from superparasitized hosts due to substantial mortality of parasitoid offspring in superparasitized hosts. Furthermore, the developmental time of the parasitoids in a superparasitized host was significantly longer than in a singly parasitized host and the emerging progeny were significantly smaller (body length and head width). Naive females entered a tunnel in which the host was parasitized 4 h previously and accepted it for oviposition. Experienced females (oviposition experience in unparasitized host) refused to enter a tunnel with a host parasitized by herself or by another female. In experiments where the tunnel and/or host was manipulated it was demonstrated that the female leaves a mark in the tunnel when she parasitizes a host. The role of patch marking in C. flavipes is discussed in relation to the ecology of the parasitoid.     

Effects of pre-adult and adult experience on host acceptance in choice and non-choice tests in two strains ofTrichogramma

The effect of adult learning through an oviposition experience, and pre-adult learning through development inside a host was investigated in two strains of an Australian egg parasitoid,Trichogramma nrivelae (Hymenoptera: Trichogrammatidae). Host response was measured in two types of laboratory preference tests. In single host tests, females reared on three lepidopteran hosts (Heliothis punctigera (Noctuidae),Papilio aegeus (Papilionidae), andHypolimnas bolina (Nymphalinae)) were presented host eggs individually, and allowed two ovipositions. Pre-adult experience affected host preference in only one strain, while acceptance of a host was increased in both strains when they had previously oviposited in this host species. An oviposition experience had a stronger effect on host preference than pre-adult experience. In choice tests, pairwise combinations of hosts were arranged in an alternating grid. The ratio of host acceptances to host contacts was computed for the whole test and up to the first oviposition. These indicated that effects of rearing host were weak or absent, but the host chosen initially had a strong effect on host preference. Relative size of the hosts had a strong effect on choice of the first host. The implications of learning inTrichogramma are discussed in relation to host preference testing procedures and the selection of candidate strains for mass rearing and inundative release.     

Feeding performance of fleas on different host species: is phylogenetic distance between hosts important?

We asked if and how feeding performance of fleas on an auxiliary host is affected by the phylogenetic distance between this host and the principal host of a flea. We investigated the feeding of 2 flea species, Parapulex chephrenis and Xenopsylla ramesis, on a principal (Acomys cahirinus and Meriones crassus, respectively) and 8 auxiliary host species. We predicted that fleas would perform better (higher proportion of fleas would feed and take larger bloodmeals) on (a) a principal rather than an auxiliary host and (b) auxiliary hosts phylogenetically closer to a principal host. Although feeding performance of fleas differed among different hosts, we found that: (1) fleas did not always perform better on a principal host than on an auxiliary host; and (2) flea performance on an auxiliary host was not negatively correlated with phylogenetic distance of this host from the principal host. In some cases, fleas fed better on hosts that were phylogenetically distant from their principal host. We concluded that variation in flea feeding performance among host species results from interplay between (a) inherent species-specific host defence abilities, (b) inherent species-specific flea abilities to withstand host defences and (c) evolutionary tightness of association between a particular host species and a particular flea species.     

Genetics, experience, and host-plant preference in Eurosta solidaginis: implications for host shifts and speciation

Host-associated mating is crucial in maintaining the partial reproductive isolation between the host races of Eurosta solidaginis (Diptera: Tephritidae), a fly that forms galls on Solidago altissima and S. gigantea. (We refer to flies reared from S. gigantea as gigantea flies and those reared from S. altissima as altissima flies.) We measured the host preference of males and females of both host races, F1 hybrids between the host races, F2, and backcrosses to both host races. Male and female altissima flies and female gigantea flies had high host fidelity, whereas male gigantea flies had low host fidelity. This result suggests that there may be gene flow between the host races due to nonassortative mating that occurs when male gigantea mate with altissima females on S. altissima. This indicates assortative-mating mechanisms in addition to host-associated mating are required to produce the partial reproductive isolation between the host races that has been observed. Nongenetic factors had no influence on host preference. Larval conditioning did not influence host preference: reciprocal F1 hybrids reared in S. altissima and S. gigantea both preferred S. gigantea. Adult experience had no impact on host preference: females preferred their natal host plant regardless of which host they encountered first as an adult. The hypothesis that maternal effects influence preferences was rejected because male and female flies did not show a consistent preference for the host plant of their mother. We also found no evidence that preference was a sex-linked trait because F1 and backcrosses to the host races with different combinations of X chromosomes from the two host races preferred S. gigantea. Our results indicate that host preference is not determined by a large number of genes because preference of hybrids did not correspond to the proportion of the genome derived from each host race. The strength of the ovipuncture preference for S. gigantea by gigantea females, the females of both reciprocal F1 hybrids, the backcross to gigantea, and F2s indicates that preference is inherited nonadditively at a limited number of loci. The F1 female hybrids, however, had a weaker host preference for S. gigantea than the pure gigantea host race, indicating that there may be incomplete dominance or modifier loci. Males had different host preference patterns than females, with individual male gigantea and male F1 hybrids usually exhibiting preference exclusively for S. gigantea or S. altissima. One hypothesis explaining the difference in host preference between males and females is that the same gene influences both female and male host preference, but it is a sex-influenced gene. Thus, males carrying the gene for S. gigantea preference have an intermediate host preference, whereas females have a strong host preference to S. gigantea. In summary, we found that the host preference that produces host-associated mating is inherited nonadditively at a relatively small number of loci on autosomal genes. This mode of inheritance meets the assumptions of models of sympatric speciation, indicating that the host races could have evolved in sympatry.     

Covariance of phenotypically plastic traits induces an adaptive shift in host selection behaviour

Flexibility in adult body size allows generalist parasitoids to use many host species at a cost of producing a range of adult sizes. Consequently, host selection behaviour must also maintain a level of flexibility as adult size is related to capture efficiency. In the present study, we investigated covariance of two plastic traits--size at pupation and host size selection behaviour-using Aphidius ervi reared on either Acyrthosiphon pisum or Aulacorthum solani, generating females of disparate sizes. Natal host was shown to change the ranking of perceived host quality with relation to host size. Parasitoids preferentially attacked hosts that corresponded to the size of the second instar of their natal host species. This resulted in optimal host selection behaviour when parasitoids were exposed to the same host species from which they emerged. Parasitoid size was positively correlated with host size preference, indicating that females use relative measurements when selecting suitable hosts. These coadapted gene complexes allow generalist parasitoids to effectively use multiple host species over several generations. However, the fixed nature of the behavioural response, within a parasitoid's lifetime, suggests that these traits may have evolved in a patchy host species environment.     

Eutrophication,biodiversity loss,and species invasions modify the relationship between host and parasite richness during host community assembly

Host and parasite richness are generally positively correlated, but the stability of this relationship in response to global change remains poorly understood. Rapidly changing biotic and abiotic conditions can alter host community assembly, which in turn, can alter parasite transmission. Consequently, if the relationship between host and parasite richness is sensitive to parasite transmission, then changes in host composition under various global change scenarios could strengthen or weaken the relationship between host and parasite richness. To test the hypothesis that host community assembly can alter the relationship between host and parasite richness in response to global change, we experimentally crossed host diversity (biodiversity loss) and resource supply to hosts (eutrophication), then allowed communities to assemble. As previously shown, initial host diversity and resource supply determined the trajectory of host community assembly, altering post‐assembly host species richness, richness‐independent host phylogenetic diversity, and colonization by exotic host species. Overall, host richness predicted parasite richness, and as predicted, this effect was moderated by exotic abundance—communities dominated by exotic species exhibited a stronger positive relationship between post‐assembly host and parasite richness. Ultimately, these results suggest that, by modulating parasite transmission, community assembly can modify the relationship between host and parasite richness. These results thus provide a novel mechanism to explain how global environmental change can generate contingencies in a fundamental ecological relationship—the positive relationship between host and parasite richness.     

Multiple choice: hemiparasite performance in multi‐species mixtures

Hemiparasitic plants have green leaves, but extract water and solutes from neighbouring plants. It is still poorly understood how different host plants in communities contribute to parasite performance, as species that are good hosts in single‐host experiments may not necessarily be preferred hosts in mixtures. We grew the root hemiparasite Rhinanthus alectorolophus (Orobanchaceae) together with each of 13 host species (experiment 1) and with 15 different four‐species mixtures of these hosts (experiment 2) that differed in the number of legumes and of host functional groups. Parasites profited from mixtures including more legumes and from mixtures including different host functional groups. Some host species and mixtures were very tolerant of parasitism and supported large parasites without being strongly suppressed in their own growth, but the suppression of a species in the single‐host experiment did not explain the suppression of a species in a host mixture. We thus calculated for each host species an index of the difference in suppression between the two experiments which may be related to host use in a mixture. Host quality (mean parasite biomass with a host species) in the single‐host experiment could explain 64% of the variation in parasite biomass with a host mixture when it was weighted by the proportion of the host species in the mixture without the parasite and by the suppression difference index. Our results suggest that plant species which are the best hosts in single‐host experiments are not always those used most strongly by a parasite growing with a mixture. Together with the finding that hemiparasites benefit from a mixed diet based on hosts from different functional groups this suggests that parasites prefer certain host species to obtain a mixed diet.     

Socially acquired host-specific mimicry and the evolution of host races in Horsfield's bronze-cuckoo Chalcites basalis

Coevolution between parasites and their hosts typically leads to increasing specialization on host species by the parasite. Where multiple hosts are parasitized, specialization on each host can result in genetic divergence within the parasite population to create host races, and, ultimately, new species. We investigate how host-specific traits arise in Horsfield's bronze-cuckoo Chalcites basalis nestlings. Newly hatched cuckoos evict host young from the nest, yet in the absence of a model they accurately mimic the different begging calls of a primary host (superb fairy-wren, Malurus cyaneus) and a secondary host (buff-rumped thornbill, Acanthiza reguloides). Using cross-fostering experiments, we show that begging calls are modified after parasitism, through experience. Further, we demonstrate the mechanism by which mimetic calls are acquired. All cuckoo nestlings initially produced the call of their primary host. When cross-fostered as eggs to a secondary host, calls increased in variability and were rapidly modified to resemble those of the secondary host through shaping by host parents. We suggest that plasticity in the development of host-specific traits after parasitism is likely to reduce selection for host race formation.