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.     

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.     

Correlated evolution between host immunity and parasite life histories in primates and oxyurid parasites

Maturation time is a pivotal life-history trait of parasitic nematodes, determining adult body size, as well as daily and total fecundity. Recent theoretical work has emphasized the influence of prematurational mortality on the optimal values of age and size at maturity in nematodes. Eosinophils are a family of white blood cells often associated with infections by parasitic nematodes. Although the role of eosinophils in nematode resistance is controversial, recent work has suggested that the action of these immune effectors might be limited to the larval stages of the parasite. If eosinophils act on larval survival, one might predict, in line with theoretical models, that nematode species living in hosts with large eosinophil numbers should show reduced age and size at maturity. We tested this prediction using the association between the pinworms (Oxyuridae, Nematoda) and their primate hosts. Pinworms are highly host specific and are expected to be involved in a coevolutionary process with their hosts. We found that the body size of female parasites was negatively correlated with eosinophil concentration, whereas the concentration of two other leucocyte families-neutrophils and lymphocytes-was unrelated to female body size. Egg size of parasites also decreased with host eosinophil concentration, independently of female size. Male body size was unrelated to host immune parameters. Primates with the highest immune defence, therefore, harbour small female pinworms laying small eggs. These results are in agreement with theoretical expectations and suggest that life histories of oxyurid parasites covary with the immune defence of their hosts. Our findings illustrate the potential for host immune defence as a factor driving parasite life-history evolution.     

Parasitic castration of a vertebrate: Effect of the cymothoid isopod, Anilocra apogonae, on the five-lined cardinalfish, Cheilodipterus quinquelineatus

Parasitic castration, the specific blocking of host reproductive output by an individual parasite, is a host-parasite interaction common to many invertebrates, particularly crustaceans, echinoderms and molluscs. It can reduce host density, alter host population dynamics and the evolution of host life history traits. Here we show that parasitisation by a single female cymothoid isopod, Anilocra apogonae, castrates its vertebrate host, the five-lined cardinalfish, Cheilodipterus quinquelineatus. Parasitised male fish fail to mouthbrood their young. The gonads of parasitised fish are smaller and parasitised female fish have substantially fewer and smaller ova than do the gonads of unparasitised fish. As for parasitic castrators of invertebrate hosts, A. apogonae on C. quinquelineatus are uniformly dispersed amongst infested hosts (one adult female isopod per host), are site specific, and their body size is highly correlated with that of their host. These isopods are large relative to the body size of their hosts, averaging 3.8% of the weight of the host. Parasitised fish also weigh less and are shorter than unparasitised fish of the same age. Despite the presence of other potential hosts, A. apogonae only infests C. quinquelineatus. The consistency of the ecological correlates amongst known parasitic castrators suggests that the parasitic castrator host-parasite relationship will be recognised for other parasites of vertebrates.     

Parasites and the regional distribution of bumblebee species

Parasites and regional processes may be important to structure local species assemblages In particular, it has been hypothesized that widely distributed and abundant species should harbour more parasite species which could give them a competitive advantage in local species assemblages Empirical evidence bearing on these points are scarce and mainly restricted to vertebrate hosts or plants The aim of this study was to provide data in insect hosts and to test whether the patterns in field populations conform with those correlates expected from the parasite-host distribution hypothesis We investigated species assemblages of bumblebees at 12 different sites in a mesoscale region with their parasites over two consecutive years Parasites included dipteran and hymenopteran parasitoids. nematodes, mites, and protozoa The mean number of parasite species per host species ranged from 1 to 8 To account for sampling effort, all data were corrected for sample size effects The number of parasite species per average host individual (parasite load) ranged from 0 09 to 0 75 In cross-species comparisons, the number of parasite species per host species was positively correlated with regional distribution, i e the number of sites a host species occupied m the region, and with the average local host abundance The same relationships were found for parasite load In addition, parasite load correlated positively with average colony size of the host species, but not with body size of the individuals Bumblebee species were bimodally distributed When separated into widely-distributed and locally-occurring species, common hosts harboured more parasite species than rare ones Moreover, workers of common species individually had higher parasite loads From these results, we conclude that some of the necessary preconditions for parasites being able to affect the distribution and occurrence of their hosts are met in bumblebees The findings support a general pattern that parasite loads correlate positively with local abundance and geographical distribution of their hosts, also on mesoscales usually considered in ecological studies     

Covariation of sexual size dimorphism and adult sex ratio in parasitic nematodes

Females are larger than males in most invertebrate taxa, a phenomenon believed to result from the pressures exerted on female body size by size-dependent fecundity. Male-male competition, which can act on male body size, is not thought to play as important a role in the evolution of sexual size dimorphism in invertebrates as it apparently does in some vertebrate groups. Here, using a comparative approach, the relationship between sexual size dimorphism and adult sex ratio is examined across 46 natural populations (41 species) and 30 experimental populations (21 species) of parasitic nematodes. If male-male competition via physical contests is important, relative male size should increase as the sex ratio becomes less female-biased. This is exactly what was found in the analyses, where residuals of male size regressed on female size were used as measures of sexual size dimorphism. This result was independent of any phylogenetic influences, and was obtained for both natural and experimental nematode populations. In addition, there was no evidence of any Allometric relationship between male and female body size. The average ratio of male size to female size was roughly constant across all species and independent of body size. The results are consistent with a role for male-male competition in explaining specific deviations from the average ratio of male to female body size, suggesting a significant role for sexual selection in the evolution of nematode body sizes.     

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.     

Virulence and competitive ability in an obligately killing parasite

Mixed infections are thought to have a major influence on the evolution of parasite virulence. During a mixed infection, higher within‐host parasite growth is favored under the assumption that it is critical to the competitive success of the parasite. As within‐host parasite growth may also increase damage to the host, a positive correlation is predicted between virulence and competitive success. However, when parasites must kill their hosts in order be transmitted, parasites may spend energy on directly attacking their host, even at the cost of their within‐host growth. In such systems, a negative correlation between virulence and competitive success may arise. We examined virulence and competitive ability in three sympatric species of obligately killing nematode parasites in the genus Steinernema. These nematodes exist in a mutualistic symbiosis with bacteria in the genus Xenorhabdus. Together the nematodes and their bacteria kill the insect host soon after infection, with reproduction of both species occurring mainly after host death. We found significant differences among the three nematode species in the speed of host killing. The nematode species with the lowest and highest levels of virulence were associated with the same species of Xenorhabdus, indicating that nematode traits, rather than the bacterial symbionts, may be responsible for the differences in virulence. In mixed infections, host mortality rate closely matched that associated with the more virulent species, and the more virulent species was found to be exclusively transmitted from the majority of coinfected hosts. Thus, despite the requirement of rapid host death, virulence appears to be positively correlated with competitive success in this system. These findings support a mechanistic link between parasite growth and both anti‐competitor and anti‐host factors.     

Increased parasite abundance associated with reproductive maturity of the clam Anodonta piscinalis.

Several studies on vertebrates have demonstrated that reproductive activities may increase the parasite load, but this has not been shown in invertebrate hosts. We studied abundance of a potentially harmful gill parasite, the ergasilid copepod Paraergasilus rylovi, from the freshwater bivalve host Anodonta piscinalis in relation to reproductive maturity of the host in the field. Prevalence of this previously unstudied parasite varied from 90 to 100%, and the mean parasite abundance from 16.3 to 28.8 among 3 study populations. Abundance of P. rylovi increased with host size. In the maturating age groups (3-5 yr) the length-adjusted mean parasite abundance among mature, reproducing female clams that brooded glochidia larvae was 2 times higher than in nonreproducing females, the observed pattern being consistent among the 3 study lakes. Alternative, mutually nonexclusive explanations may be found for the result. For example, changes in clam behavior or filtration activity accompanying maturation can increase host exposure to parasites, or reproduction may decrease energy available to host immunologic defense. However, the present result indicates that maturation, and reproduction, is associated with increased parasite abundance in A. piscinalis, an invertebrate host.     

Ecological correlates of body size and egg size in parasitic Ascothoracida and Rhizocephala (Crustacea)

In order to identify key factors in the evolution of life history traits in Ascothoracida and Rhizocephala (two groups of crustacean parastes of invertebrates), comparative analyses were performed using phylogenetically independent contrasts. Among 59 ascothoracidan species, latitude correlated positively with body size, whereas there was no relationship between water depth and body size. Body size also correlated strongly with egg size; however, once corrected for body size, egg size was not related to either latitude or water depth. Among 91 rhizocephalan species, neither latitude nor water depth correlated with body size. However, host species of larger sizes harboured larger species of rhizocephalan parasites. Egg size of rhizocephalans did not correlate with body size, and was not influenced by either latitude or water depth. The patterns observed in this study show both differences from an similarities to those reported for other groups of crustacean parasites, and suggest that adaptations to similar selective pressures are not always identical among distantly-related taxa.     

Specificity and host predictability: a comparative analysis among monogenean parasites of fish

1. This article compares generalist (parasite species found on two or more host species) and specialist (found on only one host species) monogenean parasite species of fish. The reduction of the host range – that is an increase in host specificity – may correspond with a better adaptation of the parasite to a more predictable host environment. A more predictable environment may allow the parasite species to develop specific adaptations.
2. We assume that the more predictable host environment can be evaluated by host body size, since numerous life-traits, such as longevity, are positively correlated with size.
3. We found that specialist parasites parasitize larger hosts species than generalist parasites. We also found a good relationship between host body size and parasite body size for specialist parasite species.
4. An adaptation to the mechanical problems encountered in the host's gill chamber may lead to an increase in parasite body size. The infection of a larger part of the host population in order to decrease the chances of local extinction due to fluctuations of host abundance may be another adaptive mechanism.
5. We found a negative correlation between parasite body size and prevalence for generalist parasite species. This relationship disappeared when using the comparative method controlling for phylogeny, which proved that it was a phylogenetic effect.     

Parasite co-infection and interaction as drivers of host heterogeneity

We examined the hypothesis that the interaction between concomitant infecting parasites modifies host susceptibility, parasite intensity and the pattern of parasite distribution within the host population. We used a 26 year time series of three common parasites in a natural population of rabbits: two gastrointestinal nematodes (Trichostrongylus retortaeformis and Graphidium strigosum) and the immunosuppressive myxoma virus. The frequency distribution of nematodes in the host population and the relationship between host age and nematode intensity were explored in rabbits with either single or dual nematode infections and rabbits infected with the nematodes and myxoma virus. The aggregation of T. retortaeformis and G. strigosum among the rabbits varied with the nature of the co-infection both in male and female hosts. The two nematodes exhibited different age-intensity profiles: G. strigosum intensity increased exponentially with host age while T. retortaeformis intensity exhibited a convex shape. The presence of a secondary infection did not change the age-intensity profile for G. strigosum but for T. retortaeformis co-infection (either both nematodes or myxoma-nematodes) resulted in significantly greater intensities in adult hosts. Results suggest that multi-species infections contributed to aggregation of parasites in the host population and to seasonal variation in intensity, but also enhanced differences in parasitism between sexes. This effect was apparent for T. retortaeformis, which appears to elicit a strong acquired immune response but not for G. strigosum which does not produce any evident immune reaction. We concluded that concomitant infections mediated by host immunity are important in modifying host susceptibility and influencing heterogeneity amongst individual hosts.     

Biotic and abiotic effects on endoparasites infecting Dipodomys and Perognathus species

Between 1989 and 1998, 3,504 rodents of the genera Dipodomys and Perognathus were collected from 4 permanent collecting sites on the University of New Mexico's Long Term Ecological Research station, located on the Sevilleta National Wildlife Refuge (SNWR), Socorro County. New Mexico. All animals were killed and examined for endoparasites (acanthocephalans, cestodes, coccidia, and nematodes). The present report focuses on 3 endoparasite groups, cestodes, coccidia, and nematodes. Specific analyses address how prevalence changes were related to abiotic factors such as habitat, season, or precipitation, and how prevalence of each parasite species in each host species differed in relation to host age, host sex, host reproductive status, host body mass, host density, parasite-parasite interactions, and host specificity. A logistic regression was used to determine which host characters and which abiotic factors are correlated with a parasite infection. Significant variables for at least half of the parasites include season, site, and winter precipitation. However, no parasite prevalences were correlated, and significant variables were not identical between parasites, indicating that each parasite species varied independently and that no generalizations can be drawn. The parasite prevalences in these rodents on the SNWR vary in independent and complex ways.     

An ecological law and its macroecological consequences as revealed by studies of relationships between host densities and parasite prevalence

Epidemiological models predict a positive relationship between host population density and abundance of macroparasites. Here I lest these by a comparative study. I used data on communities of four groups of parasites inhabiting the gastrointestinal tract of mammals, nematodes of the orders Oxyurida. Ascarida. Enoplida and Spirurida. respectively. The data came from 44 mammalian species and represent examination of 16886 individual hosts. I studied average prevalence of all nematodes within an order in a host species, a measure of community level abundance, and considered the potential confounding effects of host body weight, fecundity, age at maturity and diet. Host population density was positively correlated with parasite prevalence within the order Oxyurida, where all species have direct life cycles. Considering the effects of other variables did not change this. This supports the assumption that parasite transmission rate generally is a positive function of host population density_: It also strengthens the hypothesis that host densities generally act as important determinants of species richness among directly transmitted parasites and suggests that negative influence of such parasites on host population growth rate increase with increasing host population density among host species. Within the other three nematode orders, where a substantial number of the species have indirect life cycles, no relationships between prevalence and host population density were seen, Again. considering the effects of other variables did not affect this conclusion. This suggests that host population density is a poor predictor of species richness of indirectly transmitted parasites and that effects of such parasites on host population dynamics do not scale with host densities among species of hosts.     

Life history, ecology and parasite community structure in Soviet birds

The paper describes an investigation of parasite richness in relation to host life history and ecology using data from an extensive survey of helminth parasites (cestodes, trematodes and nematodes) in Soviet birds. Correlates of parasite richness (number of parasite species per host species) were sought among 13 life-history variables, 13 ecological variables and one non-biological variable (number of host individuals examined) across a sample of 158 species of host. A statistical method to control for the effects of phylogenetic association was adopted throughout. Parasite richness correlates positively with the number of hosts examined (sample size) in all three parasite groups. Positive correlations (after controlling for the effects of sample size) were also found between host body weight and parasite richness for trematodes and nematodes, but not for cestodes.
A number of ecological variables were associated with parasite richness. However, when the effects of sample size and body weight were controlled for, only a single significant correlation (an association between trematode richness and aquatic habitat) remained. Similarly, a number of significant correlates of parasite richness were found among the life-history variables examined. Though several of these were robust to the confounding effects of sample size, all could be explained by the co-variation between life-history traits and body weight among the host species under investigation.     

How Many Parasites Species a Frog Might Have? Determinants of Parasite Diversity in South American Anurans

There is an increasing interest in unveiling the dynamics of parasite infection. Understanding the interaction patterns, and determinants of host-parasite association contributes to filling knowledge gaps in both community and disease ecology. Despite being targeted as a relevant group for conservation efforts, determinants of the association of amphibians and their parasites in broad scales are poorly understood. Here we describe parasite biodiversity in South American amphibians, testing the influence of host body size and geographic range in helminth parasites species richness (PSR). We also test whether parasite diversity is related to hosts’ phylogenetic diversity. Results showed that nematodes are the most common anuran parasites. Host-parasite network has a nested pattern, with specialist helminth taxa generally associated with hosts that harbour the richest parasite faunas. Host size is positively correlated with helminth fauna richness, but we found no support for the association of host geographic range and PSR. These results remained consistent after correcting for uneven study effort and hosts’ phylogenic correlation. However, we found no association between host and parasite diversity, indicating that more diversified anuran clades not necessarily support higher parasite diversity. Overall, considering both the structure and the determinants of PRS in anurans, we conclude that specialist parasites are more likely to be associated with large anurans, which are the ones harbouring higher PSR, and that the lack of association of PSR with hosts’ clade diversification suggests it is strongly influenced by ecological and contemporary constrains.     

Sexual differentiation and development in the malaria parasite

The protozoan parasites belonging to the genus Plasmodium have a complex life cycle in which the asexual multiplication of parasites in the vertebrate host alternates with an obligate sexual reproduction in the mosquito. Gametocytes (male and female) produced in the vertebrate host are responsible for transmitting parasites to mosquitoes. Although our understanding of the biology and genetics of sexual differentiation in Plasmodium is expanding, the most basic questions concerning molecular mechanisms of sexual differentiation and sex determination still remain unanswered. Recently, insight into the control of this complex process in P. falciparum and P. berghei has come from studying parasite mutants with aberrant capacities for gametocyte production. Here, Cheryl-Ann Lobo and Nirbhay Kumar review these analyses in P. falciparum.     

The parasites of Anolis lizards in the northern Lesser Antilles

Summary The helminth communities from ten species of lizard on seven islands in the Caribbean were sampled by collecting one hundred specimens of each species. Nine genera of parasites were identified; these included six nematodes, two digeneans and an acanthocephalan. No relationship was discernible between parasite density or abundance and island area or altitude, although dry islands tend to have fewer species of parasites. Anolis lizards of the bimaculatus and wattsi series share similar parasites with four out of nine species common to both series. The parasite community of lizards on these islands is depauperate with respect to similar surveys on the larger islands of the Greater Antilles.On three of the islands lizards were sub-sampled by collecting from moist woodland and more xeric habitats. These data suggest that differences between habitats are as significant as differences between islands in determining parasite burdens. Worm burdens of the commonest parasite species, T. cubensis, increased monotonically with host body size and no evidence was found to suggest that these parasites affect either host survival or fecundity. The sex-ratio of this species correlated with mean abundance of the parasite, with females the dominant sex on islands or in habitats where the parasite was common. This pattern may reflect haplodiploid sexual determination in this species.     

Why do fish have so few roundworm (nematode) parasites?

Synopsis Although they are the oldest and most diverse members of the subphylum, the fishes have relatively few nematode parasites in comparison with other vertebrate classes. It is hypothesized that this paucity of parasite species has occurred because nematode parasites first evolved in terrestrial hosts and only a few lines of these parasites were able to transfer to fish after the appearance of heteroxeny (use of intermediate hosts) and paratenesis (use of transport hosts). The inability of nematodes to initiate parasitism in aquatic ecosystems restricted fish parasites mainly to forms first adapted to terrestrial vertebrates and at the same time deprived large groups of aquatic invertebrates such as the crustaceans, annelids and molluscs of a nematode parasite fauna.Invited editorial     

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.