Host-parasite coevolution: comparative evidence for covariation of life history traits in primates and oxyurid parasites.

The environmental factors that drive the evolution of parasite life histories are mostly unknown. Given that hosts provide the principal environmental features parasites have to deal with, and given that these features (such as resource availability and immune responses) are well characterized by the life history of the host, we may expect natural selection to result in covariation between parasite and host life histories. Moreover, some parasites show a high degree of host specificity, and cladistic analyses have shown that host and parasite phylogenies can be highly congruent. These considerations suggest that parasite and host life histories may covary. The central argument in the theory of life history evolution concerns the existence of trade-offs between traits. For parasitic nematodes it has been shown that larger body sizes induce higher fecundity, but this is achieved at the expense of delayed maturity. As high adult mortality would select for reduced age at maturity, the selective benefit of increased fecundity is expressed only if adult mortality is low. Parasite adult mortality may depend on a number of factors, including host longevity. Here we tested the hypothesis concerning the positive covariation between parasite body size (which reflects parasite longevity) and host longevity. To achieve this goal, we used the association between the pinworms (Oxyuridae, Nematoda) and their primate hosts. Oxyurids are highly host specific and are supposed to be involved in a coevolutionary process with their hosts. We found that female parasite body length was positively correlated with host longevity after correcting for phylogeny and host body mass. Conversely, male parasite body length and host longevity were not correlated. These results confirm that host longevity may represent a constraint on the evolution of body size in oxyurids, at least in females. The discrepancy between female and male oxyurids is likely to depend on the particular mode of reproduction of this taxon (haplodiploidy), which should result in weak (or even null) selection pressures to an increase of body size in males.     

The evolution of virulence and host specialization in malaria parasites of primates

Parasite virulence, i.e. the damage done to the host, may be a by-product of the parasite's effort to maximize its fitness. Accordingly, several life-history trade-offs may explain interspecific differences in virulence, but such constraints remain little tested in an evolutionary context. In this phylogenetic study of primate malarias, I investigated the relationship between virulence and other parasite life-history traits. I used peak parasitaemia as a proxy for virulence, because it reflected parasite reproductive success and parasite-induced mortality. Peak parasitaemia was higher in specialist than in generalist species, even when confounding life-history traits were controlled. While there was a significant phylogenetic relationship between the number of competitors per host and host specialization, peak parasitaemia was unrelated to within-host competition. Therefore, the key evolutionary factor that favours virulence is host specialization, and the evolutionary success of virulent parasites, such as Plasmodium falciparum , may be better understood when the trade-off in virulence between different hosts is considered. Such phylogenetic results may help us design better protection programmes against malaria.     

Host-parasite dynamics and the evolution of host immunity and parasite fecundity strategies

We explore evolutionarily stable co-evolution of host-macroparasite interactions in a discrete-time two-species population dynamics model, in which the dynamics may be stable, cyclic or chaotic. The macroparasites are assumed to harm host individuals through decreased reproductive output. Hosts may develop costly immune responses to defend themselves against parasites. Parasites compete with conspecifics by adjusting their fecundities. Overall, the presence of both parasites and the immune response in hosts produces more stable dynamics and lower host population sizes than that observed in the absence of the parasites. In our evolutionary analyses, we show that maximum parasite fecundity is always an evolutionarily stable strategy (ESS), irrespective of the type of population interaction, and that maximum parasite fecundity generally induces a minimum parasite population size through over-exploitation of the host. Phenotypic polymorphisms with respect to immunity in the host species are common and expected in ESS host strategies: the benefits of immunication depend on the frequency of the immune hosts in the population. In particular, the steady-state proportions of immune hosts depend, in addition to all the parameters of the parasite dynamics only on the cost of immunity and on the virulence of parasites in susceptible hosts. The implicit ecological dynamics of the host-parasite interaction affect the proportion of immune host individuals in the population. Furthermore, when changes in certain population parameters cause the dynamics of the host-parasite interaction to move from stability to cyclicity and then to chaos, the proportion of immune hosts tends to decrease; however, we also detected counter-examples to this result. As a whole, incorporating immunological and genetic aspects, as well as life-history trade-offs, into host-macroparasite dynamics produces a rich extension to the patterns observed in the models of ecological interactions and epidemics, and deserves more attention than is currently the case.     

Phylogenetic host specificity and understanding parasite sharing in primates

Understanding how parasites are transmitted to new species is of great importance for human health, agriculture and conservation. However, it is still unclear why some parasites are shared by many species, while others have only one host. Using a new measure of ‘phylogenetic host specificity’, we find that most primate parasites with more than one host are phylogenetic generalists, infecting less closely related primates than expected. Evolutionary models suggest that phylogenetic host generalism is driven by a mixture of host–parasite cospeciation and lower rates of parasite extinction. We also show that phylogenetic relatedness is important in most analyses, but fails to fully explain patterns of parasite sharing among primates. Host ecology and geographical distribution emerged as key additional factors that influence contacts among hosts to facilitate sharing. Greater understanding of these factors is therefore crucial to improve our ability to predict future infectious disease risks.     

Correlated evolution of host and parasite body size: tests of Harrison's rule using birds and lice

Large-bodied species of hosts often harbor large-bodied parasites, a pattern known as Harrison's rule. Harrison's rule has been documented for a variety of animal parasites and herbivorous insects, yet the adaptive basis of the body-size correlation is poorly understood. We used phylogenetically independent methods to test for Harrison's rule across a large assemblage of bird lice (Insecta: Phthiraptera). The analysis revealed a significant relationship between louse and host size, despite considerable variation among taxa. We explored factors underlying this variation by testing Harrison's rule within two groups of feather-specialist lice that share hosts (pigeons and doves). The two groups, wing lice (Columbicola spp.) and body lice (Physconelloidinae spp.), have similar life histories, despite spending much of their time on different feather tracts. Wing lice showed strong support for Harrison's rule, whereas body lice showed no significant correlation with host size. Wing louse size was correlated with wing feather size, which was in turn correlated with overall host size. In contrast, body louse size showed no correlation with body feather size, which also was not correlated with overall host size. The reason why body lice did not fit Harrison's rule may be related to the fact that different species of body lice use different microhabitats within body feathers. More detailed measurements of body feathers may be needed to explore the precise relationship of body louse size to relevant components of feather size. Whatever the reason, Harrison's rule does not hold in body lice, possibly because selection on body size is mediated by community-level interactions between body lice.     

Body size evolution of oxyurid (Nematoda) parasites: the role of hosts

Studying the diversification of body size in a taxon of parasites allows comparison of patterns of variation observed in the parasites with patterns found in free-living organisms. The distributions of body size of oxyurid nematodes (obligate parasites of vertebrates and invertebrates) are lognormally right-skewed, except for male oxyurids in invertebrates which show left-skewed distributions. In these parasitic forms, speciose genera do not have the smallest body sizes. Parasite body size is positively correlated with host body size, the largest hosts possessing the largest parasites. This trend is shown to occur within one monophyletic group of oxyurids, those of Old World primates. Comparative methods are used to take account of the effects of phylogeny. The use of multiple linear regression on distance matrices allows measurements of the contribution of phylogeny to the evolution of body size of parasites. Evolution of body size in female pinworms of Old World primates appears to be dependent only on the body size of their hosts. The tendency of parasite body size to increase with host body size is discussed in the light of the evolution of life-history traits.     

寄生虫与宿主的关系

对寄生虫与宿主的关系进行论述,探求寄生关系的实质,明确这二者之间的关系是认识寄生虫病发生发展规律,更好地防治寄生虫病的基础.     

Cooperation and life history evolution help obligate parasites to circumvent host genetic deficiencies*

How do obligate parasites cope with hosts that lack genetic elements required for parasite replication? Gupta et. al. (2020) illustrate an experimental evolution system where lambda bacteriophages circumvent a defective gene network in their E. coli host (which initially made it impossible for them to replicate) through both intracellular cooperation and evolutionary changes in phage life-history traits.     

The evolution of parasite host range in heterogeneous host populations

Theory on the evolution of niche width argues that resource heterogeneity selects for niche breadth. For parasites, this theory predicts that parasite populations will evolve, or maintain, broader host ranges when selected in genetically diverse host populations relative to homogeneous host populations. To test this prediction, we selected the bacterial parasite Serratia marcescens to kill Caenorhabditis elegans in populations that were genetically heterogeneous (50% mix of two experimental genotypes) or homogeneous (100% of either genotype). After 20 rounds of selection, we compared the host range of selected parasites by measuring parasite fitness (i.e. virulence, the selected fitness trait) on the two focal host genotypes and on a novel host genotype. As predicted, heterogeneous host populations selected for parasites with a broader host range: these parasite populations gained or maintained virulence on all host genotypes. This result contrasted with selection in homogeneous populations of one host genotype. Here, host range contracted, with parasite populations gaining virulence on the focal host genotype and losing virulence on the novel host genotype. This pattern was not, however, repeated with selection in homogeneous populations of the second host genotype: these parasite populations did not gain virulence on the focal host genotype, nor did they lose virulence on the novel host genotype. Our results indicate that host heterogeneity can maintain broader host ranges in parasite populations. Individual host genotypes, however, vary in the degree to which they select for specialization in parasite populations.     

Optimal killing for obligate killers: the evolution of life histories and virulence of semelparous parasites.

Many viral, bacterial and protozoan parasites of invertebrates first propagate inside their host without releasing any transmission stages and then kill their host to release all transmission stages at once. Life history and the evolution of virulence of these obligately killing parasites are modelled, assuming that within-host growth is density dependent. We find that the parasite should kill the host when its per capita growth rate falls to the level of the host mortality rate. The parasite should kill its host later when the carrying capacity, K, is higher, but should kill it earlier when the parasite-independent host mortality increases or when the parasite has a higher birth rate. When K(t), for parasite growth, is not constant over the duration of an infection, but increases with time, the parasite should kill the host around the stage when the growth rate of the carrying capacity decelerates strongly. In case that K(t) relates to host body size, this deceleration in growth is around host maturation.     

Patterns of host specificity and transmission among parasites of wild primates

Multihost parasites have been implicated in the emergence of new diseases in humans and wildlife, yet little is known about factors that influence the host range of parasites in natural populations. We used a comprehensive data set of 415 micro- and macroparasites reported from 119 wild primate hosts to investigate broad patterns of host specificity. The majority (68%) of primate parasites were reported to infect multiple host species, including animals from multiple families or orders. This pattern corresponds to previous studies of parasites found in humans and domesticated animals. Within three parasite groups (viruses, protozoans and helminths), we examined parasite taxonomy and transmission strategy in relation to measures of host specificity. Relative to other parasite groups, helminths were associated with the greatest levels of host specificity, whereas most viruses were reported to infect hosts from multiple families or orders. Highly significant associations between the degree of host specificity and transmission strategy arose within each parasite group, but not always in the same direction, suggesting that unique constraints influence the host range of parasites within each taxonomic group. Finally characteristics of over 100 parasite species shared between wild primates and humans, including those recognised as emerging in humans, revealed that most of these shared parasites were reported from multiple host orders. Furthermore, nearly all viruses that were reported to infect both humans and non-human primates were classified as emerging in humans.     

Coevolution of parasite virulence and host life history

Most models about the evolutionary interactions between a parasite's virulence and its host's life history neglect two potentially important aspects: epidemiological and coevolutionary feedback. We emphasize their importance by presenting models that describe the coevolution of a semelparous host's age at reproduction and a parasite's virulence in different environmental conditions. In particular, we first show that an epidemiological feedback will lead to a nonmonotonic response of the host's age at reproduction as virulence increases. We then show that the coevolutionary pressure on virulence can lead to complex associations between the host's life history and the parasite's virulence, which would not be expected with more traditional models of host or parasite evolution. Thus, for example, a high mortality rate of the host favours avirulent parasites and late reproduction of the host when the environmental conditions allow the host to grow rapidly, but early reproduction and high virulence when growth is slow.     

The impact of parasites on the life history evolution of guppies (Poecilia reticulata): the effects of host size on parasite virulence

There is large spatial and temporal variation in the Gyrodactylus parasite fauna across natural guppy (Poecilia reticulata) populations in Trinidad. The life history evolution of these fish could be affected differently in the various habitats depending on the local parasite selection pressure. Here, we experimentally infected three guppy populations with three gyrodactylid strains in the laboratory and monitored the infection by recording the number of parasites and host mortality in a full factorial design. The origin of the guppy population and parasite strain, and the size of the hosts explained significant variation in the survival of hosts. Larger fish carried the highest parasite loads and experienced the highest mortality rates, which suggests that parasite-mediated selection may favour smaller phenotypes, possibly counter-balancing selection pressures by gape-limited predators, mate choice and female fecundity. We observed significant variation in virulence between parasite strains with the captive-bred experimental strain (Gt3) causing the highest mortality of hosts whilst reaching only relatively low maximum burdens. This suggests that adaptations to the captive environment and/or inbreeding depression may alter the virulence of such captive-bred parasites. There were significant differences in survival rate between guppy populations, with infected guppies from the large population of the Lower Aripo River showing a higher survival rate than the fish from the small and genetically less diverse Upper Aripo River population.     

Encounter rate between local populations shapes host selection in complex parasite life cycle

The present study aimed to understand how a parasite with a complex life cycle selects a given host succession when several potential hosts are present. Ligula intestinalis (Cestoda, Pseudophyllidea) was considered, which presents a life cycle with three hosts: copepod, fish, and piscivorous bird. Encounter probability between each pair of hosts was calculated for Lavernose-Lacasse gravel pit (France) using a sum of the product of the host abundances over time. Among four potential copepod hosts, two potential fish hosts, and six potential bird hosts, the results demonstrate that the copepod Eudiaptomus gracilis , the roach ( Rutilus rutilus ), and the great crested grebe ( Podiceps cristatus ) had a maximal encounter probability due to their abundance, but also due to the similarities of the temporal dynamics of their life cycles. These results agree with previous experiments and field work identifying a high specificity of L. intestinalis to E. gracilis , R. rutilus , and P. cristatus in the study site. This suggests that the abundance of potential hosts and the temporal dynamics of their life cycles act together to determine encounter rates between hosts and parasites, and thus could constitute a crucial determinant in local host selection by parasites with a complex life cycle.  © 2006 The Linnean Society of London, Biological Journal of the Linnean Society , 2006, 89 , 99–106.     

Pace of life,predators and parasites: predator-induced life-history evolution in Trinidadian guppies predicts decrease in parasite tolerance

A common evolutionary response to predation pressure is increased investment in reproduction, ultimately resulting in a fast life history. Theory and comparative studies suggest that short-lived organisms invest less in defence against parasites than those that are longer lived (the pace of life hypothesis). Combining these tenets of evolutionary theory leads to the specific, untested prediction that within species, populations experiencing higher predation pressure invest less in defence against parasites. The Trinidadian guppy, Poecilia reticulata, presents an excellent opportunity to test this prediction: guppy populations in lower courses of rivers experience higher predation pressure, and as a consequence have evolved faster life histories, than those in upper courses. Data from a large-scale field survey showed that fish infected with Gyrodactylus parasites were of a lower body condition (quantified using the scaled mass index) than uninfected fish, but only in lower course populations. Although the evidence we present is correlational, it suggests that upper course guppies sustain lower fitness costs of infection, i.e. are more tolerant, than lower course guppies. The data are therefore consistent with the pace of life hypothesis of parasite defence allocation, and suggest that life-history traits mediate the indirect effect of predators on the parasites of their prey.     

Effects of shortened host life span on the evolution of parasite life history and virulence in a microbial host-parasite system

Background  

Ecological factors play an important role in the evolution of parasite exploitation strategies. A common prediction is that, as shorter host life span reduces future opportunities of transmission, parasites compensate with an evolutionary shift towards earlier transmission. They may grow more rapidly within the host, have a shorter latency time and, consequently, be more virulent. Thus, increased extrinsic (i.e., not caused by the parasite) host mortality leads to the evolution of more virulent parasites. To test these predictions, we performed a serial transfer experiment, using the protozoan Paramecium caudatum and its bacterial parasite Holospora undulata. We simulated variation in host life span by killing hosts after 11 (early killing) or 14 (late killing) days post inoculation; after killing, parasite transmission stages were collected and used for a new infection cycle.     

The evolution of host specialisation in avian brood parasites

Traditional ecological theory predicts that specialisation can promote speciation; hence, recently derived species are specialists. However, an alternative view is that new species have broad niches, which become narrower and specialised over time. Here, we test these hypotheses using avian brood parasites and three different measures of host specialisation. Brood parasites provide an ideal system in which to investigate the evolution of specialisation, because some exploit more than 40 host species and others specialise on only one. We find that young brood parasite species are smaller and specialise on a narrower range of host sizes, as expected, if specialisation is linked with the generation of new species. Moreover, we show that highly virulent parasites are more specialised, supporting findings in other host–parasite systems. Finally, we demonstrate that different measures of specialisation can lead to different conclusions, and specialisation indices should be designed taking into account the biology of each system.