Host allometry influences the evolution of parasite host-generalism: theory and meta-analysis

Parasites vary widely in the diversity of hosts they infect: some parasite species are specialists—infecting just a single host species, while others are generalists, capable of infecting many. Understanding the factors that drive parasite host-generalism is of basic biological interest, but also directly relevant to predicting disease emergence in new host species, identifying parasites that are likely to have unidentified additional hosts, and assessing transmission risk. Here, we use mathematical models to investigate how variation in host body size and environmental temperature affect the evolution of parasite host-generalism. We predict that parasites are more likely to evolve a generalist strategy when hosts are large-bodied, when variation in host body size is large, and in cooler environments. We then explore these predictions using a newly updated database of over 20 000 fish–macroparasite associations. Within the database we see some evidence supporting these predictions, but also highlight mismatches between theory and data. By combining these two approaches, we establish a theoretical basis for interpreting empirical data on parasites' host specificity and identify key areas for future work that will help untangle the drivers of parasite host-generalism. This article is part of the themed issue ‘Opening the black box: re-examining the ecology and evolution of parasite transmission’.

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title: Assembling evidence for identifying reservoirs of infection
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title: Specificity and host predictability: a comparative analysis among monogenean parasites of fish
abstract: 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.

title: Resource predictability and host specificity in fleas: the effect of host body mass
abstract: Ecological specialization is hypothesized to result from the exploitation of predictable resource bases. For parasitic organisms, one prediction is that parasites of large-bodied host species, which tend to be long-lived, should specialize on these hosts, whereas parasites of small host species, which represent more ephemeral and less predictable resources, should become generalists. We tested this prediction by quantifying the association between the level of host specificity of fleas and the mean body mass of their mammalian hosts, using published data from 2 large, distinct geographical regions (South Africa and northern North America). In general, we found supporting evidence that flea host specificity, measured either as the number of host species exploited or their taxonomic distinctness, became more pronounced with increasing host body mass. There were, however, some discrepancies among the results depending on the different measures of host specificity, the geographical region studied, or whether we used the raw values or phylogenetically independent contrasts. These are discussed with respect to other forces acting on the evolution of host specificity in parasites, as well as in the context of the regions' contrasting evolutionary histories. Overall, though, our findings indicate that the exploitation of large-bodied, and therefore long-lived, host species has promoted specialization in fleas, most likely because these hosts represent predictable resources.

title: Effects of Body Size and Temperature on Population Growth
abstract: For at least 200 years, since the time of Malthus, population growth has been recognized as providing a critical link between the performance of individual organisms and the ecology and evolution of species. We present a theory that shows how the intrinsic rate of exponential population growth, 
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title: Ecology of marine parasites : an introduction to marine parasitology
abstract: The nature of parasitism the types of marine parasites the variety of hosts of marine parasites parasites of parasites general adaptations of parasitic animals host-parasite interactions the ecological niches of parasites the structure of parasite communities characteristics of parasite faunas of different seas economic and hygienic importance of marine parasites future research.

title: Global Biodiversity, Biochemical Kinetics, and the Energetic-Equivalence Rule
abstract: The latitudinal gradient of increasing biodiversity from poles to equator is one of the most prominent but least understood features of life on Earth. Here we show that species diversity can be predicted from the biochemical kinetics of metabolism. We first demonstrate that the average energy flux of populations is temperature invariant. We then derive a model that quantitatively predicts how species diversity increases with environmental temperature. Predictions are supported by data for terrestrial, freshwater, and marine taxa along latitudinal and elevational gradients. These results establish a thermodynamic basis for the regulation of species diversity and the organization of ecological communities.

title: Free-living endohelminth stages: at the mercy of environmental conditions.
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title: Immune responses of teleost fish.
abstract: In fish all the pre-requisites to mount a specific immune response are present, but the main differences from the mammalian system are that the secondary response is relatively minor and IgG is not present. In teleosts mainly IgM is present, and IgD has been recently described but its function is, as yet, unknown. However, different forms of fish IgM and its observed flexibility of structure may compensate for a lack of Ig class diversity. The innate immune response of teleosts is highly developed. Multiple forms of key constitutive and inducible components, such as lysozyme, C3, alpha2-macroglobulin and C-reactive protein, are present, and may enhance immune recognition. Low ambient temperature appears to have an impact on all aspects of the immune response, particularly the T-dependent specific immune response due to the non-adaptive lipid composition of T-cell membranes. Temperature effects on the nonspecific immune system are less well characterised, but there is evidence that low temperatures are also suppressive. Knowledge of immune system function becomes essential for disease prevention strategies such as the development of vaccines, selection for increased disease resistance and identification of genes suitable for trangenesis.

title: Evolutionarily singular strategies and the adaptive growth and branching of the evolutionary tree
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title: Host specificity in phylogenetic and geographic space.
abstract: The measurement of host specificity goes well beyond counting how many host species can successfully be used by a parasite. In particular, specificity can be assessed with respect to how closely related the host species are, or whether a parasite exploits the same or different hosts across its entire geographic range. Recent developments in the measurement of biodiversity offer a new set of analytical tools that can be used to quantify the many aspects of host specificity. We describe here the multifaceted nature of host specificity, summarize the indices available to measure its different facets one at a time or in combination, and discuss their implications for parasite evolution and disease epidemiology.

title: Host range, host ecology, and distribution of more than 11 800 fish parasite species
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title: Co-infection and super-infection models in evolutionary epidemiology
abstract: Multiple infections are intensively studied because of their consequences for the health of the host but also because they can radically alter the selective pressures acting on parasites. I discuss how multiple infections have been modelled in evolutionary epidemiology. First, I briefly mention within-host models, which are at the root of these epidemiological models. Then, I present the super-infection framework, with an original focus on how the definition of the super-infection function can lead to evolutionary branching. There are several co-infection models and, for each of them, I briefly go through the underlying mathematics (especially the invasion fitness of a mutant strain) and I discuss the biological assumptions they make and the questions they consequently may ask. In particular, I show that a widely used co-infection model should not be invoked for invasion analyses because it confers a frequency-dependent advantage to rare neutral mutants. Finally, I present more recent frameworks, such as the Price equation framework in epidemiology, that can account for increased parasite diversity. To conclude, I discuss some perspectives for the study of multiple infections in evolutionary epidemiology.

title: Ecology and biogeography of marine parasites.
abstract: A review is given of (mainly recent) work on the biodiversity, ecology, biogeography and practical importance of marine parasites. Problems in estimating species numbers have been thoroughly discussed for free-living species, and the main points of these discussions are reviewed here. Even rough estimates of the richness of most parasite groups in the oceans are premature for the following reasons: species numbers of host groups, in particular in the deep sea and the meiofauna, are not known; most host groups have been examined only insufficiently for parasites or not at all; even in some of the best known groups, latitudinal, longitudinal and depth gradients in species richness are only poorly understood or not known at all; effects of hosts on parasite morphology and geographical variation have been studied only in a few cases; there are few studies using techniques of molecular biology to distinguish sibling species. Estimates of species richness in the best known groups, trematodes, monogeneans and copepods of marine fishes, are given. Parasites are found in almost all taxa of eukaryotes, but most parasitic species are concentrated in a few taxa. Important aspects of the ecology of marine parasites are discussed. It is emphasized that host specificity and host ranges should be distinguished, and an index that permits calculation of host specificity is discussed. The same index can be applied to measure site specificity. Central problems in ecology are the importance of interspecific competition and whether equilibrium or non-equilibrium conditions prevail. Marine parasites are among the few groups of organisms that have been extensively examined in this regard. A holistic approach, i.e. application of many methods, has unambiguously shown that metazoan ecto- (and probably endo-) parasites of marine fish live in largely non-saturated niche space under non-equilibrium conditions, i.e. they live in assemblages rather than in communities structured by competition. Nestedness occurs in such assemblages, but it can be explained by characteristics of the species themselves. There is little agreement on which other factors are involved in "structuring" parasite assemblages. Few studies on metapopulations of marine parasites have been made. A new approach, that of fuzzy chaos modelling, is discussed. It is likely that marine parasites are commonly found in metapopulations consisting of many subpopulations, and they are ideally suited to test the predictions of fuzzy chaos. Some recent studies on functional ecology and morphology--especially with regard to host, site and mate finding--are discussed, and attention is drawn to the amazing variety of sensory receptors in some marine parasites. Effects of parasites on hosts, and some studies on the evolution and speciation of marine parasites are discussed as well. A detailed overview of biogeographical studies is given, with respect to latitudinal gradients in species diversity, reproductive strategies and host ranges/specificity. Studies of marine parasites have contributed significantly to giving a non-equilibrium explanation for latitudinal diversity gradients. Recent studies on longitudinal and depth gradients are discussed, as well as parasites in brackish water, parasites as indicators of zoogeographical regions and barriers, and parasites as biological tags. The practical importance of marine parasites in mariculture, as monitors of pollution, agents of human disease, the use of parasites for controlling introduced marine pests, and some related aspects, are also discussed.

title: Next-generation tools for evolutionary invasion analyses
abstract: Evolutionary invasion analysis is a powerful technique for modelling in evolutionary biology. The general approach is to derive an expression for the growth rate of a mutant allele encoding some novel phenotype, and then to use this expression to predict long-term evolutionary outcomes. Mathematically, such ‘invasion fitness’ expressions are most often derived using standard linear stability analyses from dynamical systems theory. Interestingly, there is a mathematically equivalent approach to such stability analyses that is often employed in mathematical epidemiology, and that is based on so-called ‘next-generation’ matrices. Although this next-generation matrix approach has sometimes also been used in evolutionary invasion analyses, it is not yet common in this area despite the fact that it can sometimes greatly simplify calculations. The aim of this article is to bring the approach to a wider evolutionary audience in two ways. First, we review the next-generation matrix approach and provide a novel, and easily intuited, interpretation of how this approach relates to more standard techniques. Second, we illustrate next-generation methods in evolutionary invasion analysis through a series of informative examples. Although focusing primarily on evolutionary invasion analysis, we provide several insights that apply to biological modelling in general.

title: Conservation evaluation and phylogenetic diversity
abstract: Protecting biological diversity with limited resources may require placing conservation priorities on different taxa. A system of priorities that reflects the value of taxonomic diversity can be achieved by setting priorities such that the subset of taxa that is protected has maximum underlying feature diversity. Such feature diversity of taxon subsets is difficult to estimate directly, but can be predicted by the cladistic/phylogenetic relationships among the taxa. In this study, a simple measure of phylogenetic diversity is defined based on cladistic information. The measure of phylogenetic diversity, PD, is contrasted with a measure of taxic diversity recently developed by Vane-Wright et al. (Biol. Conserv., 55, 1991). In re-examining reserve-selection scenarios based on a phylogeny of bumble bees (Apidae), PD produces quite different priorities for species conservation, relative to taxic diversity. The potential application of PD at levels below that of the species is then illustrated using a mtDNA phylogeny for populations of crested newts Triturus cristatus. Calculation of PD for different population subsets shows that protection of populations at either of two extremes of the geographic range of the group can significantly increase the phylogenetic diversity that is protected.

title: Host traits and parasite species richness in even and odd-toed hoofed mammals, Artiodactyla and Perissodactyla
abstract: Host social, ecological and life history traits are predicted to influence both parasite establishment within host species and the distribution of parasites among host species. Yet only a few studies have investigated the role multiple host traits play in determining patterns of infection across diverse parasite groups. To explore the association between host traits and parasite species richness (PSR), we assembled a comprehensive database encompassing 601 parasites (including viruses, bacteria, protozoa, helminths and arthropods) reported to infect 96 species from two well-studied and diverse host clades: even- and odd-toed hoofed mammals (Artiodactyla and Perissodactyla). Comparative analyses were used to examine associations between three sets of host variables (life history and body mass, social and mating behavior, and ecological traits) and PSR for all parasites combined and for distinct parasite sub-groups. Results from a combination of phylogenetic and non-phylogenetic tests showed that PSR increased with host body size across all parasites groups. Counter to expectations, measures of parasite diversity decreased with host longevity and social group size, and associations between group size and PSR further depended on the underlying mating system of the host species. Our results suggest that body mass, longevity, and social organization influence the diversity and types of parasites reported to infect wild populations of hoofed mammals, and that multiple host and parasite traits can combine in unexpected ways to shape observed patterns.

title: Can host body size explain the parasite species richness in tropical freshwater fishes?
abstract: SummaryThe variability of monogenean gill ectoparasite species richness in 19 West African cyprinid species was analyzed using the following seven predictor variables: host size, number of drainage basins, number of sympatric cyprinid species, host diversity, association with mainland forest, host ecology, and monogenean biological labelling. The size of the host species accounted for 77% of the variation in the number of parasite species per host, and host ecology an additional 8%. Together the effects of host size and host ecology accounted for 85% of the variation in monogenean species richness. This study shows that the deciding factors for explaining monogenean species richness in West African cyprinid fishes are host species size and host ecology. These results were compared with main factors responsible for parasite species richness in fish communities. Other possible explanations of monogenean community structure in west African cyprinids are discussed.

title: Determinants of host-specificity in parasites of freshwater fishes.
abstract: Factors responsible for interspecific variability in host-specificity were investigated within 15 genera (including 176 species) of metazoan parasites found in Canadian freshwater fish. For each species in a genus, the parasite's number of known hosts was determined from published host-parasite records. The effects of the total number and mean size of potential hosts (i.e. all fish species belonging to the family or families that include a parasite's known hosts) on number of hosts of congeneric species were evaluated using multiple regressions. Since parasite species that have been recorded often tend to have greater numbers of known hosts than do seldom-recorded parasites, it was necessary to control for the confounding effect of study intensity. In all parasite genera, whether from highly specific taxa such as monogeneans or from less host-specific ones, there was a positive relationship between the number of potential hosts and the number of known hosts. However, no consistent relationships were observed between the mean size of potential hosts and number of known hosts. These results suggest that the availability of suitable host species may have been a key factor limiting the colonization of new hosts by fish parasites.

title: Assessing Functional Explanations of Host-Specificity
abstract: Many species of aphids, cyst-nematodes, and other parasites show considerable host-specificity. A number of factors have been invoked to explain this specificity: nutritional quality and host-plants' secondary chemicals (Ehrlich and Raven 1964; Feeny 1976), natural enemies (Lawton 1978; Bernays and Graham 1988), and the need to find mates by first seeking a host (Rohde 1979). What these explanations share is the implicit assumption that host-selection behavior is adaptive, that the observed host range is, or is close to, an evolutionarily stable strategy. In other words, the restricted host range observed is near-optimal because natural enemies or chemical defenses would reduce the fitness of any parasites that extended it. Although evidence is often presented that nonhosts, or nonpreferred hosts, are indeed less suitable than preferred hosts, it is difficult o determine whether the factors invoked can provide a sufficient explanation of the observed specificity. To do this we need to know how unsuitable a host must be for an optimally foraging parasite to reject it. Quantitative criteria are required for assessing the sufficiency of such implicitly game-theoretic explanations. The literature contains a number of models for the evolution of host range or habitat specificity (e.g., Levins and MacArthur 1969; Doyle 1975; Jaenike 1978; Ward 1987a), but these are difficult o apply since they include terms such as "rate of encounter" or "instantaneous mortality," which cannot easily be measured in the field. In this note I show how such models can be used to check whether proposed selection pressures are strong enough to account for hostspecificity, without the need for detailed measurements of behavior or mortality in the field. I first derive equations that express the conditions for specificity in terms of the proportion of dispersing parasites that find hosts; I then simplify these conditions, assuming that the parasite population is at equilibrium. Finally, I show how these conditions can be used to assess explanations of host-specificity.

title: Transmission rates and adaptive evolution of pathogens in sympatric heterogeneous plant populations
abstract: Diversification in agricultural cropping patterns is widely practised to delay the build–up of virulent races that can overcome host resistance in pathogen populations. This can lead to balanced polymorphism, but the long–term consequences of this strategy for the evolution of crop pathogen populations are still unclear. The widespread occurrence of sibling species and reproductively isolated sub–species among fungal and oomycete plant pathogens suggests that evolutionary divergence is common. This paper develops a mathematical model of host–pathogen interactions using a simple framework of two hosts to analyse the influences of sympatric host heterogeneity on the long–term evolutionary behaviour of plant pathogens. Using adaptive dynamics, which assumes that sequential mutations induce small changes in pathogen fitness, we show that evolutionary outcomes strongly depend on the shape of the trade–off curve between pathogen transmission on sympatric hosts. In particular, we determine the conditions under which the evolutionary branching of a monomorphic into a dimorphic population occurs, as well as the conditions that lead to the evolution of specialist (single host range) or generalist (multiple host range) pathogen populations.

title: Experimental evolution of parasites.
abstract: Serial passage experiments are a form of experimental evolution that is frequently used in applied sciences; for example, in vaccine development. During these experiments, molecular and phenotypic evolution can be monitored in real time, providing insights into the causes and consequences of parasite evolution. Within-host competition generally drives an increase in a parasite's virulence in a new host, whereas the parasite becomes avirulent to its former host, indicating a trade-off between parasite fitnesses on different hosts. Understanding why parasite virulence seldom escalates similarly in natural populations could help us to manage virulence and deal with emerging diseases.

title: Life-history traits in parasitic nematodes : a comparative approach for the search of invariants
abstract: 1. This study investigates the evolution of life-history traits in parasitic and free-living nematodes. A database on 35 species was assembled for values on: body size of female nematodes; egg production; life expectancies of both adult and free-stages; the length of maturation time for free-living nematodes and prepatent period for parasites (time needed for an infective stage to reach maturity in its definitive host). Comparative methods were used to account for the effects of phylogeny. 2. The well-known allometries of life-history traits with body size were found, such as the allometry between size and total fecundity. Daily fecundity and prepatent period of parasitic nematodes are both correlated with body size, suggesting that delaying maturity increases fecundity. 3. Phylogeny affects relationships between investigated life-history traits, i.e. daily reproductive output (b) and female life expectancy (1/M). 4. Prepatent period (a) in parasitic nematodes is equivalent to maturation time (a) of free-living nematodes. 5. A search was carried out for life-history invariants (Charnov 1993). There was no correlation between prepatent period (a) and daily reproductive output (b) and hence no invariant ab. This could be explained by constrained life styles of reproduction among Nematoda. Indeed, invariant aM (or aM, where M is the mortality rate of adult stage) were found for both parasites of vertebrate ((aM) = 0.23) and free-living, plant and insect nematodes ((aM) = 0.50). 6. A causal chain of evolution of life-history traits of parasite nematodes is proposed and discussed. It is suggested that adult mortality is the main factor driving the evolution of life-history traits.

title: Helminth fecundity: density dependence or statistical illusion?
abstract: Density-dependent constraints on fecundity or survival are critical for the regulation and stability o f all populations. Helminth parasites are no exception to this rule. In medical helminthology, it has been widely assumed that the most effective density-dependent constraints act upon parasite fecundity and are the result of intra-specific parasite competition or acquired immunity to infection. In this article, Anne Keymer and Andrew Slater advocate a more detailed examination of the evidence on which this assumption rests.

title: Home Range and Parasite Diversity in Mammals
abstract: Parasite diversity among and within host species is not solely the result of random processes; rather, it depends on a suite of physiological or ecological host traits as well as environmental factors. Because most macroparasites exhibit life cycles that include infective stages off the definitive host and that rely on host movements for dissemination, parasite acquisition by a host depends largely on hosts being present in a given area where and when infective stages are present. Consequently, host ranging pattern may have a major influence on parasite diversity. Larger home range size is hypothesized to be associated with higher parasite species richness because hosts living in large home ranges should encounter a greater diversity of habitats and other host individuals, which in turn may favor infection by a great diversity of parasite species. By focusing on helminths in wild mammals, we show that an increase in home range area does not lead to an increase in parasite diversity in ungulates and, moreover, that it is associated with a decrease in parasite species richness in carnivores and in glires (rodents and lagomorphs). We also show that home range size is negatively correlated with host density in mammals after correcting both variables for host body mass. We discuss these results from an epidemiological perspective.