Evolution of virulence under intensive farming: salmon lice increase skin lesions and reduce host growth in salmon farms

Parasites rely on resources from a host and are selected to achieve an optimal combination of transmission and virulence. Human‐induced changes in parasite ecology, such as intensive farming of hosts, might not only favour increased parasite abundances, but also alter the selection acting on parasites and lead to life‐history evolution. The trade‐off between transmission and virulence could be affected by intensive farming practices such as high host density and the use of antiparasitic drugs, which might lead to increased virulence in some host–parasite systems. To test this, we therefore infected Atlantic salmon (Salmo salar) smolts with salmon lice (Lepeophtheirus salmonis) sampled either from wild or farmed hosts in a laboratory experiment. We compared growth and skin damage (i.e. proxies for virulence) of hosts infected with either wild or farmed lice and found that, compared to lice sampled from wild hosts in unfarmed areas, those originating from farmed fish were more harmful; they inflicted more skin damage to their hosts and reduced relative host weight gain to a greater extent. We advocate that more evolutionary studies should be carried out using farmed animals as study species, given the current increase in intensive food production practices that might be compared to a global experiment in parasite evolution.     

Louse flies of Eleonora’s falcons that also feed on their prey are evolutionary dead‐end hosts for blood parasites

Host shifts are widespread among avian haemosporidians, although the success of transmission depends upon parasite‐host and parasite‐vector compatibility. Insular avifaunas are typically characterized by a low prevalence and diversity of haemosporidians, although the underlying ecological and evolutionary processes remain unclear. We investigated the parasite transmission network in an insular system formed by Eleonora's falcons (the avian host), louse flies that parasitize the falcons (the potential vector), and haemosporidians (the parasites). We found a great diversity of parasites in louse flies (16 Haemoproteus and 6 Plasmodium lineages) that did not match with lineages previously found infecting adult falcons (only one shared lineage). Because Eleonora's falcon feeds on migratory passerines hunted over the ocean, we sampled falcon kills in search of the origin of parasites found in louse flies. Surprisingly, louse flies shared 10 of the 18 different parasite lineages infecting falcon kills. Phylogenetic analyses revealed that all lineages found in louse flies (including five new lineages) corresponded to Haemoproteus and Plasmodium parasites infecting Passeriformes. We found molecular evidence of louse flies feeding on passerines hunted by falcons. The lack of infection in nestlings and the mismatch between the lineages isolated in adult falcons and louse flies suggest that despite louse flies’ contact with a diverse array of parasites, no successful transmission to Eleonora's falcon occurs. This could be due to the falcons’ resistance to infection, the inability of parasites to develop in these phylogenetically distant species, or the inability of haemosporidian lineages to complete their development in louse flies.     

Infection with Haemoproteus iwa affects vector movement in a hippoboscid fly—frigatebird system

Haemosporidian parasites, which require both a vertebrate and invertebrate host, are most commonly studied in the life stages occurring in the vertebrate. However, aspects of the vector's behaviour and biology can have profound effects on parasite dynamics. We explored the effects of a haemosporidian parasite, Haemoproteus iwa, on a hippoboscid fly vector, Olfersia spinifera. Olfersia spinifera is an obligate ectoparasite of the great frigatebird, Fregata minor, living among bird feathers for all of its adult life. This study examined the movements of O. spinifera between great frigatebird hosts. Movement, or host switching, was inferred by identifying host (frigatebird) microsatellite genotypes from fly bloodmeals that did not match the host from which the fly was collected. Such host switches were analysed using a logistic regression model, and the best‐fit model included the H. iwa infection status of the fly and the bird host sex. Uninfected flies were more likely to have a bird genotype in their bloodmeal that was different from their current host's genotype (i.e. to have switched hosts) than infected flies. Flies collected from female birds were more likely to have switched hosts than those collected on males. Reduced movement of infected flies suggests that there may be a cost of parasitism for the fly. The effect of host sex is probably driven by differences in the sex ratio of bird hosts available to moving flies.     

Life history and virulence are linked in the ectoparasitic salmon louse Lepeophtheirus salmonis

Models of virulence evolution for horizontally transmitted parasites often assume that transmission rate (the probability that an infected host infects a susceptible host) and virulence (the increase in host mortality due to infection) are positively correlated, because higher rates of production of propagules may cause more damages to the host. However, empirical support for this assumption is scant and limited to microparasites. To fill this gap, we explored the relationships between parasite life history and virulence in the salmon louse, Lepeophtheirus salmonis, a horizontally transmitted copepod ectoparasite on Atlantic salmon Salmo salar. In the laboratory, we infected juvenile salmon hosts with equal doses of infective L. salmonis larvae and monitored parasite age at first reproduction, parasite fecundity, area of damage caused on the skin of the host, and host weight and length gain. We found that earlier onset of parasite reproduction was associated with higher parasite fecundity. Moreover, higher parasite fecundity (a proxy for transmission rate, as infection probability increases with higher numbers of parasite larvae released to the water) was associated with lower host weight gain (correlated with lower survival in juvenile salmon), supporting the presence of a virulence–transmission trade‐off. Our results are relevant in the context of increasing intensive farming, where frequent anti‐parasite drug use and increased host density may have selected for faster production of parasite transmission stages, via earlier reproduction and increased early fecundity. Our study highlights that salmon lice, therefore, are a good model for studying how human activity may affect the evolution of parasite virulence.     

Predators can influence the host‐parasite dynamics of their prey via nonconsumptive effects

Ecological communities are partly structured by indirect interactions, where one species can indirectly affect another by altering its interactions with a third species. In the absence of direct predation, nonconsumptive effects of predators on prey have important implications for subsequent community interactions. To better understand these interactions, we used a Daphnia‐parasite‐predator cue system to evaluate if predation risk affects Daphnia responses to a parasite. We investigated the effects of predator cues on two aspects of host–parasite interactions (susceptibility to infection and infection intensity), and whether or not these effects differed between sexes. Our results show that changes in response to predator cues caused an increase in the prevalence and intensity of parasite infections in female predator‐exposed Daphnia. Importantly, the magnitude of infection risk depended on how long Daphnia were exposed to the cues. Additionally, heavily infected Daphnia that were constantly exposed to cues produced relatively more offspring. While males were ~5× less likely to become infected compared to females, we were unable to detect effects of predator cues on male Daphnia–parasite interactions. In sum, predators, prey, and their parasites can form complex subnetworks in food webs, necessitating a nuanced understanding of how nonconsumptive effects may mediate these interactions.     

A parasite's modification of host behavior reduces predation on its host

Parasite modification of host behavior is common, and the literature is dominated by demonstrations of enhanced predation on parasitized prey resulting in transmission of parasites to their next host. We present a case in which predation on parasitized prey is reduced. Despite theoretical modeling suggesting that this phenomenon should be common, it has been reported in only a few host–parasite–predator systems. Using a system of gregarine endosymbionts in host mosquitoes, we designed experiments to compare the vulnerability of parasitized and unparasitized mosquito larvae to predation by obligate predatory mosquito larvae and then compared behavioral features known to change in the presence of predatory cues. We exposed Aedes triseriatus larvae to the parasite Ascogregarina barretti and the predator Toxohrynchites rutilus and assessed larval mortality rate under each treatment condition. Further, we assessed behavioral differences in larvae due to infection and predation stimuli by recording larvae and scoring behaviors and positions within microcosms. Infection with gregarines reduced cohort mortality in the presence of the predator, but the parasite did not affect mortality alone. Further, infection by parasites altered behavior such that infected hosts thrashed less frequently than uninfected hosts and were found more frequently on or in a refuge within the microcosm. By reducing predation on their host, gregarines may be acting as mutualists in the presence of predation on their hosts. These results illustrate a higher‐order interaction, in which a relationship between a species pair (host–endosymbiont or predator–prey) is altered by the presence of a third species.     

Global warming will reshuffle the areas of high prevalence and richness of three genera of avian blood parasites

The importance of parasitism for host populations depends on local parasite richness and prevalence: usually host individuals face higher infection risk in areas where parasites are most diverse, and host dispersal to or from these areas may have fitness consequences. Knowing how parasites are and will be distributed in space and time (in a context of global change) is thus crucial from both an ecological and a biological conservation perspective. Nevertheless, most research articles focus just on elaborating models of parasite distribution instead of parasite diversity. We produced distribution models of the areas where haemosporidian parasites are currently highly diverse (both at community and at within‐host levels) and prevalent among Iberian populations of a model passerine host: the blackcap Sylvia atricapilla; and how these areas are expected to vary according to three scenarios of climate change. On the basis of these models, we analysed whether variation among populations in parasite richness or prevalence are expected to remain the same or change in the future, thereby reshuffling the geographic mosaic of host‐parasite interactions as we observe it today. Our models predict a rearrangement of areas of high prevalence and richness of parasites in the future, with Haemoproteus and Leucocytozoon parasites (today the most diverse genera in blackcaps) losing areas of high diversity and Plasmodium parasites (the most virulent ones) gaining them. Likewise, the prevalence of multiple infections and parasite infracommunity richness would be reduced. Importantly, differences among populations in the prevalence and richness of parasites are expected to decrease in the future, creating a more homogeneous parasitic landscape. This predicts an altered geographic mosaic of host‐parasite relationships, which will modify the interaction arena in which parasite virulence evolves.     

Vertically transmitted symbiont reduces host fitness along temperature gradient

Parasites with exclusive vertical transmission from host parent to offspring are an evolutionary puzzle. With parasite fitness entirely linked to host reproduction, any fitness cost for infected hosts risks their selective elimination. Environmental conditions likely influence parasite impact and thereby the success of purely vertical transmission strategies. We tested for temperature‐dependent virulence of Caedibacter taeniospiralis, a vertically transmitted bacterial symbiont of the protozoan Paramecium tetraurelia. We compared growth of infected and cured host populations at five temperatures (16–32 °C). Infection reduced host density at all temperatures, with a peak of ?30% at 28 °C. These patterns were largely consistent across five infected Paramecium strains. Similar to Wolbachia symbionts, C. taeniospiralis may compensate fitness costs by conferring to the host a ‘killer trait’, targeting uninfected competitors. Considerable loss of infection at 32 °C suggests that killer efficacy is not universal and that limited heat tolerance restricts the conditions for persistence of C. taeniospiralis.     

Elevated atmospheric concentrations of carbon dioxide reduce monarch tolerance and increase parasite virulence by altering the medicinal properties of milkweeds

Hosts combat their parasites using mechanisms of resistance and tolerance, which together determine parasite virulence. Environmental factors, including diet, mediate the impact of parasites on hosts, with diet providing nutritional and medicinal properties. Here, we present the first evidence that ongoing environmental change decreases host tolerance and increases parasite virulence through a loss of dietary medicinal quality. Monarch butterflies use dietary toxins (cardenolides) to reduce the deleterious impacts of a protozoan parasite. We fed monarch larvae foliage from four milkweed species grown under either elevated or ambient CO₂, and measured changes in resistance, tolerance, and virulence. The most high‐cardenolide milkweed species lost its medicinal properties under elevated CO₂; monarch tolerance to infection decreased, and parasite virulence increased. Declines in medicinal quality were associated with declines in foliar concentrations of lipophilic cardenolides. Our results emphasize that global environmental change may influence parasite–host interactions through changes in the medicinal properties of plants.     

Predation and disease: understanding the effects of predators at several trophic levels on pathogen transmission

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Genetic structure and host–parasite co‐divergence: evidence for trait‐specific local adaptation

Host–parasite co‐evolution can lead to genetic differentiation among isolated host–parasite populations and local adaptation between parasites and their hosts. However, tests of local adaptation rarely consider multiple fitness‐related traits although focus on a single component of fitness can be misleading. Here, we concomitantly examined genetic structure and co‐divergence patterns of the trematode Coitocaecum parvum and its crustacean host Paracalliope fluviatilis among isolated populations using the mitochondrial cytochrome oxidase I gene (COI). We then performed experimental cross‐infections between two genetically divergent host–parasite populations. Both hosts and parasites displayed genetic differentiation among populations, although genetic structure was less pronounced in the parasite. Data also supported a co‐divergence scenario between C. parvum and P. fluviatilis potentially related to local co‐adaptation. Results from cross‐infections indicated that some parasite lineages seemed to be locally adapted to their sympatric (home) hosts in which they achieved higher infection and survival rates than in allopatric (away) amphipods. However, local, intrinsic host and parasite characteristics (host behavioural or immunological resistance to infections, parasite infectivity or growth rate) also influenced patterns of host–parasite interactions. For example, overall host vulnerability to C. parvum varied between populations, regardless of parasite origin (local vs. foreign), potentially swamping apparent local co‐adaptation effects. Furthermore, local adaptation effects seemed trait specific; different components of parasite fitness (infection and survival rates, growth) responded differently to cross‐infections. Overall, data show that genetic differentiation is not inevitably coupled with local adaptation, and that the latter must be interpreted with caution in a multi‐trait context.     

Apparent vector‐mediated parent‐to‐offspring transmission in an avian malaria‐like parasite

Parasite transmission strategies strongly impact host–parasite co‐evolution and virulence. However, studies of vector‐borne parasites such as avian malaria have neglected the potential effects of host relatedness on the exchange of parasites. To test whether extended parental care in the presence of vectors increases the probability of transmission from parents to offspring, we used high‐throughput sequencing to develop microsatellites for malaria‐like Leucocytozoon parasites of a wild raptor population. We show that host siblings carry genetically more similar parasites than unrelated chicks both within and across years. Moreover, chicks of mothers of the same plumage morph carried more similar parasites than nestlings whose mothers were of different morphs, consistent with matrilineal transmission of morph‐specific parasite strains. Ours is the first evidence of an association between host relatedness and parasite genetic similarity, consistent with vector‐mediated parent‐to‐offspring transmission. The conditions for such ‘quasi‐vertical’ transmission may be common and could suppress the evolution of pathogen virulence.     

Parasite preferences for large host body size can drive overdispersion in a fly-mite association

Body size generally correlates intraspecifically with insect fitness but can also correlate with parasite abundance (number of parasites). Host preferences by parasites, and variation in host immunity, could contribute to this trend. We investigated the effect of host size on mite-fly interactions (Macrocheles subbadius and Drosophila nigrospiracula). Mites strongly preferred to infect larger flies in pair-wise choices, and larger flies were more likely to be infected and acquired more mites in infection microcosms. Preferences of parasites resulted in size-biased infection outcomes. We discuss the implications of this heterogeneity in infection on parasite overdispersion and fly populations.     

Of mice and worms: are co-infections with unrelated parasite strains more damaging to definitive hosts?

Intraspecific competition between co-infecting parasites can influence the amount of virulence, or damage, they do to their host. Kin selection theory dictates that infections with related parasite individuals should have lower virulence than infections with unrelated individuals, because they benefit from inclusive fitness and increased host longevity. These predictions have been tested in a variety of microparasite systems, and in larval stage macroparasites within intermediate hosts, but the influence of adult macroparasite relatedness on virulence has not been investigated in definitive hosts. This study used the human parasite Schistosoma mansoni to determine whether definitive hosts infected with related parasites experience lower virulence than hosts infected with unrelated parasites, and to compare the results from intermediate host studies in this system. The presence of unrelated parasites in an infection decreased parasite infectivity, the ability of a parasite to infect a definitive host, and total worm establishment in hosts, impacting the less virulent parasite strain more severely. Unrelated parasite co-infections had similar virulence to the more virulent of the two parasite strains. We combine these findings with complementary studies of the intermediate snail host and describe trade-offs in virulence and selection within the life cycle. Damage to the host by the dominant strain was muted by the presence of a competitor in the intermediate host, but was largely unaffected in the definitive host. Our results in this host–parasite system suggest that unrelated infections may select for higher virulence in definitive hosts while selecting for lower virulence in intermediate hosts.     

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.     

VARIATION BETWEEN POPULATIONS AND LOCAL ADAPTATION IN ACANTHOCEPHALAN‐INDUCED PARASITE MANIPULATION

Many trophically transmitted parasites manipulate their intermediate host phenotype, resulting in higher transmission to the final host. However, it is not known if manipulation is a fixed adaptation of the parasite or a dynamic process upon which selection still acts. In particular, local adaptation has never been tested in manipulating parasites. In this study, using experimental infections between six populations of the acanthocephalan parasite Pomphorhynchus laevis and its amphipod host Gammarus pulex, we investigated whether a manipulative parasite may be locally adapted to its host. We compared adaptation patterns for infectivity and manipulative ability. We first found a negative effect of all parasite infections on host survival. Both parasite and host origins influenced infection success. We found a tendency for higher infectivity in sympatric versus allopatric combinations, but detailed analyses revealed significant differences for two populations only. Conversely, no pattern of local adaptation was found for behavioral manipulation, but manipulation ability varied among parasite origins. This suggests that parasites may adapt their investment in behavioral manipulation according to some of their host's characteristics. In addition, all naturally infected host populations were less sensitive to parasite manipulation compared to a naive host population, suggesting that hosts may evolve a general resistance to manipulation.