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.     

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.     

The scaling of total parasite biomass with host body mass

The selective pressure exerted by parasites on their hosts will to a large extent be influenced by the abundance or biomass of parasites supported by the hosts. Predicting how much parasite biomass can be supported by host individuals or populations should be straightforward: ultimately, parasite biomass must be controlled by resource supply, which is a direct function of host metabolism. Using comparative data sets on the biomass of metazoan parasites in vertebrate hosts, we determined how parasite biomass scales with host body mass. If the rate at which host resources are converted into parasite biomass is the same as that at which host resources are channelled toward host growth, then on a log-log plot parasite biomass should increase with host mass with a slope of 0.75 when corrected for operating temperature. Average parasite biomass per host scaled with host body mass at a lower rate than expected (across 131 vertebrate species, slope=0.54); this was true independently of phylogenetic influences and also within the major vertebrate groups separately. Since most host individuals in a population harbour a parasite load well below that allowed by their metabolic rate, because of the stochastic nature of infection, it is maximum parasite biomass, and not average biomass, that is predicted to scale with metabolic rate among host species. We found that maximum parasite biomass scaled isometrically (i.e., slope=1) with host body mass. Thus, larger host species can potentially support the same parasite biomass per gram of host tissues as small host species. The relationship found between maximum parasite biomass and host body mass, with its slope greater than 0.75, suggests that parasites are not like host tissues: they are able to appropriate more host resources than expected from metabolically derived host growth rates.     

烟粉虱对寄主的选择行为

烟粉虱Bemisia tabaci(Gennadius)成虫对寄主植物选择行为的实验结果表明,烟粉虱是通过植物广谱的绿色气体识别植物材料,并进一步受到绿色的诱导。通过烟粉虱在适宜与非适宜寄主植物上滞留时间的差异,可以看出烟粉虱是通过口针刺探的寄主评估过程逐渐实现寄主偏好性的,存在一个短的时滞。综合来看,烟粉虱的寄主选择是通过嗅觉、视觉和味觉共同参与的一个决策过程,以寄主植物的气味、颜色和质量为线索,逐步定位到适宜的寄主植物上,因此在寄主选择过程中存在很大的可塑性。     

Synchronization of host-parasite cycles by means of diapause: host influence and parasite response to involuntary host shifting

Many parasites require synchronization of their infective phases with the appearance of susceptible host individuals and, for many species, diapause is one of the mechanisms contributing to such coincidence. A variety of ecological factors, like changes in host temperature produced by involuntary host shifting (substitution of the usual host by an infrequent one), can modify host-parasite synchronization of diapausing ectoparasites of endothermic species. To understand the influence of host shifting on the mechanisms of parasite synchronization, we conducted experiments using the system formed by the ectoparasitic fly Carnus hemapterus and its avian hosts. We simulated the occurrence of the usual host and natural cases of host shifting by exposing overwintering carnid pupae from Bee-eater nests (Merops apiaster) to the earlier incubation periods of two Carnus host species that frequently reoccupy Bee-eater nests. Pupae exposed to host shifting treatments advanced the mean date of emergence and produced an earlier and faster rate of emergence in comparison with pupae exposed both to the control (absence of any host) and Bee-eater treatments. The effect was more evident for the treatment resembling the host with the most dissimilar phenology to the one of the usual host. Our results show that host temperature is an environmental cue used by this nest-dwelling haematophagous ectoparasite and reveal that Carnus hemapterus has some potential to react to involuntary host shifting by means of plasticity in the termination of diapause.     

On the capacity of macroparasites to control insect populations

A graphical model of the population dynamics of macroparasites and their hosts is developed. Three principal means by which the parasites can be regulated are considered: reduction in host density as a result of parasite-induced host mortality, reduction in host density as a result of parasite-induced host sterility, and competition among parasites within multiply-infected hosts. The means by which parasites are regulated has a major effect on the degree to which they can depress host population densities. In particular, a parasite that sterilizes its host is expected to reduce host density more than one that causes an equivalent decline in host fitness through increased mortality. A special case of the model is developed for herbivorous insects that, in the absence of parasites, are limited by larval food resources. Parasites that are regulated via parasite-induced host sterility will control the insect populations below the level set by larval resources if the threshold host density for the parasites (N(T)) is less than the ratio of carrying capacity to net reproductive rate of the insects (K/R). Data are presented showing that all three means of parasite regulation, but especially parasite-induced host sterility, can operate in Howardula aoronymphium, a nematode parasite of mycophagous Drosophila flies. Data from a field cage experiment show that, if these nematodes are regulated primarily via reductions in host density due to this sterility, the parameters N(T), K, and R are such that Howardula is likely to play an important role in controlling Drosophila populations. However, this conclusion must be tempered by the fact that these nematodes also cause increased host mortality and experience within-host competition, making the conditions for parasite control of the flies more stringent.     

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.     

Cascading effects of host size and host plant species on parasitoid resource allocation

1. The bottom‐up factors that determine parasitoid host use are an important area of research in insect ecology. Host size is likely to be a primary cue for foraging parasitoids due to its potential influence on offspring development time, the risk of multiparasitism, and host immunocompetence. Host size is mediated in part by host‐plant traits that influence herbivore growth and potentially affect a herbivore's quality as a host for parasitoids. 2. Here, we tested how caterpillar host size and host plant species influence adult fly parasitoid size and whether host size influences wasp parasitoid sex allocation. We measured the hind tibia lengths and determined the sex of wasp and fly parasitoids reared from 11 common host species of polyphagous caterpillars (Limacodidae) that were in turn reared on foliage of seven different host plant species. 3. We also tested how host caterpillar species, host caterpillar size, and host and parasitoid phenology affect how the parasitoid community partitions host resources. We found evidence that parasitoids primarily partition their shared hosts based on size, but not by host species or phenology. One index of specialisation (d′) supports our observation that these parasitoids are quite generalised within the Limacodidae. In general, wasps were reared from caterpillars collected in early instars, while flies were reared from caterpillars collected in late instars. Furthermore, for at least one species of solitary wasp, host size influenced sex allocation of offspring by ovipositing females. 4. Host‐plant quality indirectly affected the size attained by a tachinid fly parasitoid through its direct effects on the size and performance of the caterpillar host. The host plants that resulted in the highest caterpillar host performance in the absence of enemies also yielded the largest parasitoid flies, which suggests that host plant quality can cascade up to influence the third trophic level.     

Geographical variation in host specificity of fleas (Siphonaptera) parasitic on small mammals: the influence of phylogeny and local environmental conditions

The evolution of host specificity remains a central issue in the study of host‐parasite relationships. Here we tackle three basic questions about host specificity using data on host use by fleas (Siphonaptera) from 21 geographical regions. First, are the host species exploited by a flea species no more than a random draw from the locally available host species, or do they form a taxonomically distinct subset? Using randomization tests, we showed that in the majority of cases, the taxonomic distinctness (measured as the average taxonomic distances among host species) of the hosts exploited by a flea is no different from that of random subsets of hosts taken from the regional pool. In the several cases where a difference was found, the taxonomic distinctness of the hosts used by a flea was almost always lower than that of the random subsets, suggesting that the parasites use hosts within a narrower taxonomic spectrum than what is available to them. Second, given the variation in host specificity among populations of the same flea species, is host specificity truly a species character? We found that host specificity measures are repeatable among different populations of the same flea species: host specificity varies significantly more among flea species than within flea species. This was true for both measures of host specificity used in the analyses: the number of host species exploited, and the index measuring the average taxonomic distinctness of the host species and its variance. Third, what causes geographical variation in host specificity among populations of the same flea species? In the vast majority of flea species, neither of our two measures of host specificity correlated with either the regional number of potential host species or their taxonomic distinctness, or the distance between the sampled region and the center of the flea's geographical range. However, in most flea species host specificity correlated with measures of the deviation in climatic conditions (precipitation and temperature) between the sampled region and the average conditions computed across the flea's entire range. Overall, these results suggest that host specificity in fleas is to a large extent phylogenetically constrained, while still strongly influenced by local environmental conditions.     

Abundance trumps quality: bi‐trophic performance and parasitism risk fail to explain host use in the fall webworm

Factors including host abundance, quality, and the degree to which hosts provide enemy‐free space (EFS) may drive host plant choice by phytophagous insects. Herbivores may also experience fitness tradeoffs among hosts, promoting polyphagy. The fall webworm Hyphantria cunea is a dietary generalist that feeds on a broad array of trees across its geographic range. Here, we investigate the drivers of host tree use by the fall webworm in Connecticut (CT) and Maryland (MD). Neither caterpillar performance nor EFS was associated with the frequency with which host trees were used, and no tradeoff between host quality and EFS was identified. Vegetation surveys adjacent to host trees showed that at both localities, host use was non‐random with respect to tree species, and that the main predictor of use among suitable host trees was host tree abundance. This suggests that webworms are under selection to reduce search time for oviposition sites. Although we did not detect a tradeoff between host plant quality and availability in MD, we did identify that tradeoff in CT. This disparity amid otherwise similar patterns of host use between CT and MD may be explained by the relative rarity of high quality hosts in CT compared to MD. Our results illustrate that geographic mosaics in patterns of host use may arise in the absence of local adaptation if host use is based upon availability rather than host plant attributes.     

A Host Creates an Enemy‐free Space for Mistletoes by Reducing Seed Predation Caused by a Woodboring Beetle: A Hypothesis

Parasitic plants rely on host plants for nutrition. The number of host species varies largely between groups, from single species or genus to hundreds of species. Relative abundance of the host and evolutionary history are the main requisites for parasitic plants to develop specificity to abundant hosts. In the present study, we suggest a novel mechanism by which a hemiparasitic mistletoe can develop local specificity mediated by its host. First, we describe a novel interaction in which a woodboring beetle (Hypothenemus obscurus) preys on mistletoe seeds (Psittacanthus plagiophyllus) attached to tree branches. This beetle preys more frequently on seeds deposited on branches of non‐host species than on branches of its unique local host species (53 percent on average vs. 26 percent respectively). We hypothesize that local host specificity for this mistletoe could be partly mediated by beetle‐host incompatibility, since the host offers a predation‐free space in which mistletoes have better chances to grow. Furthermore, that the exceptional gum exudates produced by this unique host species minimize beetle attacks on branches, thus reducing predation of mistletoe seeds. This novel tritrophic interaction opens an avenue for research on macroscopic host‐specificity mechanisms that occur at the level of the host bark and that have been poorly studied by plant ecologists.     

Host traits associated with species roles in parasite sharing networks

The community of host species that a parasite infects is often explained by functional traits and phylogeny, predicting that closely related hosts or those with particular traits share more parasites with other hosts. Previous research has examined parasite community similarity by regressing pairwise parasite community dissimilarity between two host species against host phylogenetic distance. However, pairwise approaches cannot target specific host species responsible for disproportionate levels of parasite sharing. To better identify why some host species contribute differentially to parasite diversity patterns, we represent parasite sharing using ecological networks consisting of host species connected by instances of shared parasitism. These networks can help identify host species and traits associated with high levels of parasite sharing that may subsequently identify important hosts for parasite maintenance and transmission within communities. We used global‐scale parasite sharing networks of ungulates, carnivores, and primates to determine if host importance – encapsulated by the network measures degree, closeness, betweenness, and eigenvector centrality – was predictable based on host traits. Our findings suggest that host centrality in parasite sharing networks is a function of host population density and range size, with range size reflecting both species geographic range and the home range of those species. In the full network, host taxonomic family became an important predictor of centrality, suggesting a role for evolutionary relationships between host and parasite species. More broadly, these findings show that trait data predict key properties of ecological networks, thus highlighting a role for species traits in understanding network assembly, stability, and structure.     

The response of Hyssopus pallidus to hosts previously parasitised by Ascogaster quadridentata: heterospecific discrimination and host quality

1. Two basic tenets of competition among parasitoids, that taxonomically distinct parasitoids are unable to discriminate against hosts that have previously been attacked by a competitor and that previous parasitism reduces the quality of a host, were tested by monitoring the oviposition response of Hyssopus pallidus, a gregarious ectoparasitoid, to healthy codling moth larvae and codling moth larvae that had previously been parasitised by a solitary endoparasitoid, Ascogaster quadridentata. 2. Hyssopus pallidus accepted both categories of host larva for oviposition when its competitor was constrained as a first‐instar larva by the diapause development of its host, but discriminated against previously parasitised host larvae when its competitor was present as a larger larva in a non‐diapausing host. 3. Hyssopus pallidus distinguished between the two categories of host larva by allocating twice as many eggs to host larvae previously parasitised by A. quadridentata, a response that was not influenced by previous oviposition experience. 4. The larger clutch sizes allocated to previously parasitised host larvae produced twice as many female progeny, each of a typical size, such that the total biomass was twice that produced from the smaller clutches laid on healthy host larvae. Possible confounding influences of host age and diapause are discounted. 5. These results demonstrate that interspecific discrimination does occur in H. pallidus and that host quality can be improved through previous parasitism by an endoparasitoid. Although interspecific discrimination appears rare among insect parasitoids, it may have been overlooked among ectoparasitoids and requires examination of the fitness consequences of interspecific interactions to clarify its adaptive significance.     

Parasite-driven extinction in spatially explicit host-parasite systems

General host-parasite theory suggests that parasites may be implicated in the extinction of their hosts by causing instability that leads to increased risk of stochastic extinction. In contrast, spatially explicit models suggest that the parasite may directly drive the host population to extinction. Here we examine the ecological characteristics of host-parasite interactions that favor parasite-driven host extinction. Pair approximations and simulations show that parasites only drive their hosts to extinction when they significantly reduce host reproduction. As a matter of interest, parasites that have a relatively small effect on host death rate are more likely to cause host extinction. Parasite-driven host extinction occurs at any population size, whereas extinction caused by stochastic effects is less likely to occur in large host populations. Populations may therefore be under threat from parasites that stop host reproduction, and this type of parasite may prove to be the most effective biological pesticide.     

半闭弯尾姬蜂寄主搜索中的学习行为

研究了半闭弯尾姬蜂寄主搜索过程中的学习行为。结果表明,成虫期之前的饲养寄主所取食的寄主植物对成蜂行为没有影响,而雌蜂早期的短暂经历可对其随后的行为反应产生显著影响,从而对已经历的植物气味表现出显著的嗜好,但这种通过学习所表现出的嗜好又可因新的经历而改变。雌成蜂不仅能对其所经历的虫伤寄主植物释放的信息化合物进行学习,而且对其所经历的寄主幼虫的信息化合物也能进行学习。     

Influence of larval experience on preference of a subterranean insect Delia antiqua on Allium hosts

Numerous studies have reported that larval experience can affect subsequent host plants selection and future oviposition decisions of many different species, but the investigation of pre‐imaginal experiences on host preference of adults has rarely been tested for soil‐dwelling insects. In this study, we present evidence that larval feeding experience can affect adult host preference in the onion maggot, Delia antiqua. By rearing D. antiqua on different host plants, we were able to examine the role of the natal host of different generations and the effect of larval density on host‐choice behaviour. We also performed bioassays by means of switched host treatment to evaluate the host‐selection principle. Choice bioassays among the three host species demonstrated that D. antiqua females preferred to oviposit on their natal host in each generation and host‐switching treatments. Additionally, increasing larval density could intensify this ovipositional preference on the natal host. The overall results showed that host preference of female D. antiqua is determined by larval experience and density. These findings also add support for the controversial Hopkins’ host‐selection principle.     

Coevolutionary arms races: increased host immune defense promotes specialization by avian fleas

We investigated the relationship between host defense and specialization by parasites in comparative analyses of bird fleas and T-cell mediated immune response of their avian hosts, showing that fleas with few main host species exploited hosts with weak or strong immune defenses, whereas flea species that parasitized a large number of host species only exploited hosts with weak immune responses. Hosts with strong immune responses were exploited by a larger number of flea species than hosts with weak responses. A path analysis model with an effect of T-cell response on the number of host species, or a model with host coloniality directly affecting host T-cell response, which in turn affected the number of host species used by fleas, best explained the data. Therefore, parasite specialization may have evolved in response to strong host defenses.     

In situ studies on incorporation of nucleic acid precursors into Chlamydia trachomatis DNA.

Chlamydiae are obligate intracellular bacteria that are dependent on eukaryotic host cells for ribonucleoside triphosphates. The purpose of the present study was to determine whether Chlamydia trachomatis obtains deoxyribonucleotides from the host cell. The study was aided by the finding that host and parasite DNA synthesis activity could be distinguished by their differing sensitivities to aphidicolin and norfloxacin. Results from isotope incorporation experiments indicated that any nucleobase or ribonucleoside that could serve as a precursor for host DNA synthesis could also be utilized by C. trachomatis for DNA replication. C. trachomatis utilized only those precursors which the host cell converted to the nucleotide level. Pyrimidine deoxyribonucleotides were efficient precursors for host DNA synthesis; however, they were not used by C. trachomatis. On the other hand, purine deoxyribonucleosides are rapidly catabolized by host cells, it is necessary to regulate their metabolism to determine whether they serve as direct precursors for C. trachomatis DNA synthesis. This was partially achieved by using a hypoxanthine-guanine phosphoribosyltransferase-negative cell line and using deoxycoformycin and 8-aminoguanosine as inhibitors of (deoxy)adenosine deaminase and purine nucleoside phosphorylase, respectively. The results indicated that purine deoxyribonucleosides are efficiently utilized for host cell DNA synthesis even if degradation pathways are inhibited and salvage to ribonucleotides is minimized. In sharp contrast, the purine deoxyribonucleosides were utilized by C. trachomatis as precursors for DNA synthesis only when host catabolic pathways and salvage reactions were intact. High-pressure liquid chromatographic analysis of nucleotide pools extracted from host cells pulsed with radiolabeled precursors suggests that infected cells transport and phosphorylate all deoxynucleosides as effectively as mock-infected control cultures. In aggregate, these results show that chlamydiae do not take up deoxyribonucleotides from the host cells.