No effect of host–parasite co‐evolution on host range expansion

Antagonistic co‐evolution between hosts and parasites (reciprocal selection for resistance and infectivity) is hypothesized to play an important role in host range expansion by selecting for novel infectivity alleles, but tests are lacking. Here, we determine whether experimental co‐evolution between a bacterium (Pseudomonas fluorescens SBW25) and a phage (SBW25Φ2) affects interstrain host range: the ability to infect different strains of P. fluorescens other than SBW25. We identified and tested a genetically and phenotypically diverse suite of co‐evolved phage variants of SBW25Φ2 against both sympatric and allopatric co‐evolving hosts (P. fluorescens SBW25) and a large set of other P. fluorescens strains. Although all co‐evolved phage had a greater host range than the ancestral phage and could differentially infect co‐evolved variants of P. fluorescens SBW25, none could infect any of the alternative P. fluorescens strains. Thus, parasite generalism at one genetic scale does not appear to affect generalism at other scales, suggesting fundamental genetic constraints on parasite adaptation for this virus.     

Parasite diversity drives rapid host dynamics and evolution of resistance in a bacteria‐phage system

Host–parasite evolutionary interactions are typically considered in a pairwise species framework. However, natural infections frequently involve multiple parasites. Altering parasite diversity alters ecological and evolutionary dynamics as parasites compete and hosts resist multiple infection. We investigated the effects of parasite diversity on host–parasite population dynamics and evolution using the pathogen Pseudomonas aeruginosa and five lytic bacteriophage parasites. To manipulate parasite diversity, bacterial populations were exposed for 24 hours to either phage monocultures or diverse communities containing up to five phages. Phage communities suppressed host populations more rapidly but also showed reduced phage density, likely due to interphage competition. The evolution of resistance allowed rapid bacterial recovery that was greater in magnitude with increases in phage diversity. We observed no difference in the extent of resistance with increased parasite diversity, but there was a profound impact on the specificity of resistance; specialized resistance evolved to monocultures through mutations in a diverse set of genes. In summary, we demonstrate that parasite diversity has rapid effects on host–parasite population dynamics and evolution by selecting for different resistance mutations and affecting the magnitude of bacterial suppression and recovery. Finally, we discuss the implications of phage diversity for their use as biological control agents.     

Short-term rates of parasite evolution predict the evolution of host diversity

Coevolution with parasites has been implicated as an important factor driving the evolution of host diversity. Studies to date have focussed on gross effects of parasites: how host diversity differs in the presence vs. absence of parasites. But parasite-imposed selection is likely to show rapid variation through time. It is unclear whether short-term fluctuations in the strength of parasite-imposed selection tend to affect host diversity, because increases in host diversity are likely to be constrained by both the supply of genetic variation and ecological processes. We followed replicate populations of coevolving, initially isogenic, bacteria and phages through time, measuring host diversity (with respect to bacterial colony morphologies), host density and rates of parasite evolution. Both host density and time-lagged rates of parasite evolution were good independent predictors of the magnitude of bacterial within- and between-population diversities. Rapid parasite evolution and low host density decreased host within-population diversity, but increased between-population diversity. This study demonstrates that short-term changes in the rate of parasite evolution can predictably drive patterns of host diversity.     

Shifts in diversification rates and host jump frequencies shaped the diversity of host range among Sclerotiniaceae fungal plant pathogens

The range of hosts that a parasite can infect in nature is a trait determined by its own evolutionary history and that of its potential hosts. However, knowledge on host range diversity and evolution at the family level is often lacking. Here, we investigate host range variation and diversification trends within the Sclerotiniaceae, a family of Ascomycete fungi. Using a phylogenetic framework, we associate diversification rates, the frequency of host jump events and host range variation during the evolution of this family. Variations in diversification rate during the evolution of the Sclerotiniaceae define three major macro‐evolutionary regimes with contrasted proportions of species infecting a broad range of hosts. Host–parasite cophylogenetic analyses pointed towards parasite radiation on distant hosts long after host speciation (host jump or duplication events) as the dominant mode of association with plants in the Sclerotiniaceae. The intermediate macro‐evolutionary regime showed a low diversification rate, high frequency of duplication events and the highest proportion of broad host range species. Our findings suggest that the emergence of broad host range fungal pathogens results largely from host jumps, as previously reported for oomycete parasites, probably combined with low speciation rates. These results have important implications for our understanding of fungal parasites evolution and are of particular relevance for the durable management of disease epidemics.     

Mistletoe species richness patterns are influenced more by host geographic range than nitrogen content

Mistletoes are hemiparasites that access water and nutrients from their hosts. Previous studies have suggested that host genera with high nitrogen are parasitized by more mistletoe species but these studies failed to take into account phylogenetic relationships among host genera. Our main question was whether more mistletoe species parasitize host genera with high nitrogen content when phylogenetic relationships were controlled. We also asked whether patterns in mistletoe parasitism were related to host geographic range size, host fruit type and host spinescence. Overall, we found no difference between conventional and phylogenetically controlled analyses. We also found no evidence for higher mistletoe species richness on host genera with high nitrogen, fleshy fruits or spinescence. However, similar to findings for animal parasites, we found that host genera with large geographic range had higher mistletoe species richness. This is likely because a greater number of mistletoe species will encounter hosts that have a greater geographic distribution. Mistletoe studies frequently assume that nitrogen status drives patterns in mistletoe parasitism but our study suggests that macroecological patterns in mistletoe assemblages are primarily determined by host geographic range.     

Do‐or‐die life cycles and diverse post‐infection resistance mechanisms limit the evolution of parasite host ranges

In light of the dynamic nature of parasite host ranges and documented potential for rapid host shifts, the observed high host specificity of most parasites remains an ecological paradox. Different variants of host‐use trade‐offs have become a mainstay of theoretical explanations of the prevalence of host specialism, but empirical evidence for such trade‐offs is rare. We propose an alternative theory based on basic features of the parasite life cycle: host selection and subsequent intrahost replication. We introduce a new concept of effective burst size that accounts for the fact that successful host selection does not guarantee intrahost replication. Our theory makes a general prediction that a parasite will expand its host range if its effective burst size is positive. An in silico model of bacteria‐phage coevolution verifies our predictions and demonstrates that the tendency for relatively narrow host ranges in parasites can be explained even in the absence of trade‐offs.     

The dynamics of preferential host switching: Host phylogeny as a key predictor of parasite distribution*

Parasites often jump to and become established in a new host species. There is much evidence that the probability of such host shifts decreases with increasing phylogenetic distance between donor and recipient hosts, but the consequences of such preferential host switching remain little explored. We develop a computational model to investigate the dynamics of parasite host shifts in the presence of this phylogenetic distance effect. In this model, a clade of parasites evolves on an evolving clade of host species where parasites can cospeciate with their hosts, switch to new hosts, speciate within hosts or become extinct. Our model predicts that host phylogenies are major determinants of parasite distributions across trees. In particular, we predict that trees consisting of few large clades of host species and those with fast species turnover should harbor more parasites than trees with many small clades and those that diversify more slowly. Within trees, large clades are predicted to exhibit a higher fraction of infected species than small clades. We discuss our results in the light of recent cophylogenetic studies in a wide range of host–parasite systems.     

Effects of antagonistic coevolution on parasite‐mediated host coexistence

Parasites can promote diversity by mediating coexistence between a poorer and superior competitor, if the superior competitor is more susceptible to parasitism. However, hosts and parasites frequently undergo antagonistic coevolution. This process may result in the accumulation of pleiotropic fitness costs associated with host resistance, and could breakdown coexistence. We experimentally investigated parasite‐mediated coexistence of two genotypes of the bacterium Pseudomonas fluorescens, where one genotype underwent coevolution with a parasite (a virulent bacteriophage), whereas the other genotype was resistant to the evolving phages at all time points, but a poorer competitor. In the absence of phages, the resistant genotype was rapidly driven extinct in all populations. In the presence of the phages, the resistant genotype persisted in four of six populations and eventually reached higher frequencies than the sensitive genotype. The coevolving genotype showed a reduction in the growth rate, consistent with a cost of resistance, which may be responsible for a decline in its relative fitness. These results demonstrate that the stability of parasite‐mediated coexistence of resistant and susceptible species or genotypes is likely to be affected if parasites and susceptible hosts coevolve.     

Host specificity of a generalist parasite: genetic evidence of sympatric host races in the seabird tick Ixodes uriae

Due to the close association between parasites and their hosts, many ‘generalist’ parasites have a high potential to become specialized on different host species. We investigated this hypothesis for a common ectoparasite of seabirds, the tick Ixodes uriae that is often found in mixed host sites. We examined patterns of neutral genetic variation between ticks collected from Black‐legged kittiwakes (Rissa tridactyla) and Atlantic puffins (Fratercula arctica) in sympatry. To control for a potential distance effect, values were compared to differences among ticks from the same host in nearby monospecific sites. As predicted, there was higher genetic differentiation between ticks from different sympatric host species than between ticks from nearby allopatric populations of the same host species. Patterns suggesting isolation by distance were found among tick populations of each host group, but no such patterns existed between tick populations of different hosts. Overall, results suggest that host‐related selection pressures have led to the specialization of I. uriae and that host race formation may be an important diversifying mechanism in parasites.     

Parasites lead to evolution of robustness against gene loss in host signaling networks

Many biological networks can maintain their function against single gene loss. However, the evolutionary mechanisms responsible for such robustness remain unclear. Here, we demonstrate that antagonistic host–parasite interactions can act as a selective pressure driving the emergence of robustness against gene loss. Using a model of host signaling networks and simulating their coevolution with parasites that interfere with network function, we find that networks evolve both redundancy and specific architectures that allow them to maintain their response despite removal of proteins. We show that when the parasite pressure is removed, subsequent evolution can lead to loss of redundancy while architecture‐based robustness is retained. Contrary to intuition, increased parasite virulence hampers evolution of robustness by limiting the generation of population level diversity in the host. However, when robustness emerges under high virulence, it tends to be stronger. These findings predict an increased presence of robustness mechanisms in biological networks operating under parasite interference. Conversely, the presence of such mechanisms could indicate current or past parasite interference.     

Higher parasite resistance in Daphnia populations with recent epidemics

Natural populations often show genetic variation in parasite resistance, forming the basis for evolutionary response to selection imposed by parasitism. We investigated whether previous epidemics selected for higher resistance to novel parasite isolates in a Daphnia galeata–microparasite system by comparing susceptibility of host clones from populations with varying epidemic history. We manipulated resource availability to evaluate whether diet influences Daphnia susceptibility as epidemics are common in nutrient‐rich lakes. Exposing clones from 10 lakes under two food treatments to an allopatric protozoan parasite, we found that Daphnia originating from lakes (mainly nutrient rich) with previous epidemics better resist infection. Despite this result, there was a tendency of higher susceptibility in the low food treatment, suggesting that higher resistance of clones from populations with epidemic background is not directly caused by lake nutrient level. Rather, our results imply that host populations respond to parasite‐mediated selection by evolving higher parasite resistance.     

Adaptation to abiotic conditions drives local adaptation in bacteria and viruses coevolving in heterogeneous environments

Parasite local adaptation, the greater performance of parasites on their local compared with foreign hosts, has important consequences for the maintenance of diversity and epidemiology. While the abiotic environment may significantly affect local adaptation, most studies to date have failed either to incorporate the effects of the abiotic environment, or to separate them from those of the biotic environment. Here, we tease apart biotic and abiotic components of local adaptation using the bacterium Pseudomonas fluorescens and its viral parasite bacteriophage Φ2. We coevolved replicate populations of bacteria and phages at three different temperatures, and determined their performance against coevolutionary partners from the same and different temperatures. Crucially, we measured performance at different assay temperatures, which allowed us to disentangle adaptation to biotic and abiotic habitat components. Our results show that bacteria and phages are more resistant and infectious, respectively, at the temperature at which they previously coevolved, confirming that local adaptation to abiotic conditions can play a crucial role in determining parasite infectivity and host resistance. Our work underlines the need to assess host–parasite interactions across multiple relevant abiotic environments, and suggests that microbial adaption to local temperatures can create ecological barriers to dispersal across temperature gradients.     

Global patterns in helminth host specificity: phylogenetic and functional diversity of regional host species pools matter

Host specificity has a major influence on a parasite's ability to shift between human and animal host species. Yet there is a dearth of quantitative approaches to explore variation in host specificity across biogeographical scales, particularly in response to the varying community compositions of potential hosts. We built a global dataset of intermediate host associations for nine of the world's most widespread helminth parasites (all of which infect humans). Using hierarchical models, we asked if realised parasite host specificity varied in response to regional variation in the phylogenetic and functional diversities of potential host species. Parasites were recorded in 4–10 zoogeographical regions, with some showing considerable geographical variation in observed versus expected host specificity. Parasites generally exhibited the lowest phylogenetic host specificity in regions with the greatest variation in prospective host phylogenetic diversity, namely the Neotropical, Saharo‐Arabian and Australian regions. Globally, we uncovered notable variation in parasite host shifting potential. Observed host assemblages for Hydatigera taeniaeformis and Hymenolepis diminuta were less phylogenetically diverse than expected, suggesting limited potential to spillover into unrelated hosts. Host assemblages for Echinococcus granulosus, Mesocestoides lineatus and Trichinella spiralis were less functionally diverse than expected, suggesting limited potential to shift across host ecological niches. By contrast, Hyd. taeniaeformis infected a higher functional diversity of hosts than expected, indicating strong potential to shift across hosts with different ecological niches. We show that the realised phylogenetic and functional diversities of infected hosts are determined by biogeographical gradients in prospective host species pools. These findings emphasise the need to account for underlying species diversity when assessing parasite host specificity. Our framework to identify variation in realised host specificity is broadly applicable to other host–parasite systems and will provide key insights into parasite invasion potential at regional and global scales.     

Parasite local maladaptation in the Canarian lizard Gallotia galloti (Reptilia: Lacertidae) parasitized by haemogregarian blood parasite

Biologists commonly assume that parasites are locally adapted since they have shorter generation times and higher fecundity than their hosts, and therefore evolve faster in the arms race against the host's defences. As a result, parasites should be better able to infect hosts within their local population than hosts from other allopatric populations. However, recent mathematical modelling has demonstrated that when hosts have higher migration rates than parasites, hosts may diversify their genes faster than parasites and thus parasites may become locally maladapted. This new model was tested on the Canarian endemic lizard and its blood parasite (haemogregarine genus). In this host–parasite system, hosts migrate more than parasites since lizard offspring typically disperse from their natal site soon after hatching and without any contact with their parents who are potential carriers of the intermediate vector of the blood parasite (a mite). Results of cross-infection among three lizard populations showed that parasites were better at infecting individuals from allopatric populations than individuals from their sympatric population. This suggests that, in this host–parasite system, the parasites are locally maladapted to their host.     

Brood parasitism causes female‐biased host nestling mortality regardless of parasite species

Inequality in male and female numbers may affect population dynamics and extinction probabilities and so has significant conservation implications. We previously demonstrated that Brown‐headed Cowbird Molothrus ater brood parasitism of Song Sparrows Melospiza melodia results in a 50% reduction in the proportion of female host offspring by day 6 post‐hatch and at fledging, which modelling demonstrated is as significant as nest predation in affecting demography. Many avian brood parasites possess special adaptations to parasitize specific hosts so this sex‐ratio effect could be specific to the interaction between these two species. Alternatively, perturbations associated with brood parasitism per se (e.g. the addition of an extra, larger, unrelated nestling), rather than a Cowbird nestling specifically, may be responsible. We experimentally eliminated the effects of Cowbird‐specific traits by parasitizing nests with a conspecific nestling rather than a Cowbird, while otherwise emulating the circumstances of Cowbird parasitism by adding an extra, larger (2‐day‐older), unrelated Song Sparrow nestling to Song Sparrow nests. Our parasitism treatment led to few host offspring deaths and no evidence of male‐biased sex ratios by day 6 post‐hatch. However, after day 6, female nestling mortality rates increased significantly in experimentally parasitized nests, resulting in a 60% reduction in the proportion of females fledging. Cowbird‐specific traits are thus not necessary to cause female‐biased host nestling mortality and far more general features associated with Cowbird parasitism instead appear responsible. Our results suggest, however, that Cowbird‐specific traits may help accelerate the pace of female host deaths. The conservation implications of our results could be wide reaching. Cowbirds are unrelated to all their hosts, are larger than the great majority, and a Cowbird nestling's presence can mean there is an extra mouth to feed. Thus, sex‐biased mortality in parasitized nests could be occurring across a range of host species.     

Priming of host resistance to protect cultured rainbow trout Oncorhynchus mykiss against eye flukes and parasite‐induced cataracts

In the present study, immunologically naive rainbow trout Oncorhynchus mykiss were experimentally exposed to a low‐level Diplostomum spathaceum (Trematoda) infection to stimulate acquired resistance and, along with unexposed controls, were subsequently exposed to natural infection for 8 weeks. The priming of the host resistance, designed to simulate a procedure applicable in aquaculture, decreased the number of establishing parasites compared to untreated controls by the end of the experiment. This effect was slow and did not protect the fish against the parasite‐induced cataracts. The results suggest that this type of priming of host resistance is probably inefficient in preventing the deleterious effects of D. spathaceum infection in aquaculture conditions.     

Pre‐adapting parasitic phages to a pathogen leads to increased pathogen clearance and lowered resistance evolution with Pseudomonas aeruginosa cystic fibrosis bacterial isolates

Recent years have seen renewed interest in phage therapy – the use of viruses to specifically kill disease‐causing bacteria – because of the alarming rise in antibiotic resistance. However, a major limitation of phage therapy is the ease at with bacteria can evolve resistance to phages. Here, we determined whether in vitro experimental coevolution can increase the efficiency of phage therapy by limiting the resistance evolution of intermittent and chronic cystic fibrosis Pseudomonas aeruginosa lung isolates to four different phages. We first pre‐adapted all phage strains against all bacterial strains and then compared the efficacy of pre‐adapted and nonadapted phages against ancestral bacterial strains. We found that evolved phages were more efficient in reducing bacterial densities than ancestral phages. This was primarily because only 50% of bacterial strains were able to evolve resistance to evolved phages, whereas all bacteria were able to evolve some level of resistance to ancestral phages. Although the rate of resistance evolution did not differ between intermittent and chronic isolates, it incurred a relatively higher growth cost for chronic isolates when measured in the absence of phages. This is likely to explain why evolved phages were more effective in reducing the densities of chronic isolates. Our data show that pathogen genotypes respond differently to phage pre‐adaptation, and as a result, phage therapies might need to be individually adjusted for different patients.     

Evolution of host resistance and trade‐offs between virulence and transmission potential in an obligately killing parasite

Standard epidemiological theory predicts that parasites, which continuously release propagules during infection, face a trade‐off between virulence and transmission. However, little is known how host resistance and parasite virulence change during coevolution with obligate killers. To address this question we have set up a coevolution experiment evolving Nosema whitei on eight distinct lines of Tribolium castaneum. After 11 generations we conducted a time‐shift experiment infecting both the coevolved and the replicate control host lines with the original parasite source, and coevolved parasites from generation 8 and 11. We found higher survival in the coevolved host lines than in the matching control lines. In the parasite populations, virulence measured as host mortality decreased during coevolution, while sporeload stayed constant. Both patterns are compatible with adaptive evolution by selection for resistance in the host and by trade‐offs between virulence and transmission potential in the parasite.     

On the role of host phenotypic plasticity in host shifting by parasites

Ecological speciation appears to contribute to the diversification of insect herbivores and other parasites, which together comprise a major component of Earth's biodiversity. Host shifts are likely an important step in ecological speciation, and understanding how such shifts occur is critical to forming and testing hypotheses explaining parasite diversity. In this article, I argue that phenotypic variation in hosts arising from environmental variation (phenotypic plasticity) can promote shifts in parasites by bridging both spatiotemporal and phenotypic gaps between ancestral and novel hosts. This hypothesis, which I call the ‘plastic‐bridge hypothesis’, is conceptually distinct from those invoking genetic variation in bridging these gaps. I describe the mechanistic basis of plastic bridges, review circumstantial evidence in support of the hypothesis and suggest strategies for testing it. I use herbivorous insects and their host plants as a model, but the proposed ideas apply to any system fitting a broad definition of a host‐parasite relationship. The plastic‐bridge perspective suggests that parasite diversity is not only due to divergent selection provided by hosts, but also to the intraspecific variation that facilitates shifts between them. This view is timely, as biological invasion and range shifts associated with climate change foster novel interactions between parasites and hosts.     

Relative number of generations of hosts and parasites does not influence parasite local adaptation in coevolving populations of bacteria and phages

A potential consequence of host-parasite coevolution in spatially structured populations is parasite local adaptation: local parasites perform better than foreign parasites on their local host populations. It has been suggested that the generally shorter generation times of parasites compared with their hosts contributes to parasites, rather than hosts, being locally adapted. We tested the hypothesis that relative generation times of hosts and parasites affect local adaptation of hosts and parasites, using the bacterium Pseudomonas fluorescens and a lytic phage as host and parasite, respectively. Generation times were not directly manipulated, but instead one of the coevolving partners was regularly removed and replaced with a population from an earlier time point. Thus, one partner underwent more generations than the other. Manipulations were carried out at both early and later periods of coevolutionary interactions. At early stages of coevolution, host and parasites that underwent relatively more generations displayed higher levels of resistance and infectivity, respectively. However, the relative number of generations that bacteria and phages underwent did not change the level of local adaptation relative to control populations. This is likely because generalist hosts and parasites are favoured during early stages of coevolution, preventing local adaptation. By contrast, at later stages manipulations had no effect on either average levels of resistance or infectivity, or alter the level of local adaptation relative to the controls, possibly because traits other than resistance and infectivity were under strong selection. Taken together, these data suggest that the relative generation times of hosts and parasites may not be an important determinant of local adaptation in this system.