Parasite mediated homogenizing selection at the MHC in guppies

Understanding the selective forces influencing genetic diversity is a fundamental goal of evolutionary ecology. The genes of the major histocompatibility complex (MHC) play a key role in the adaptive immune response of vertebrates and thus provide an excellent opportunity to examine the agents of selection on a functionally important gene. Here we examine the genetic architecture of the MHC class IIB genes in 10 wild populations of guppies (Poecilia reticulata) in Northern Trinidad. We have previously shown that these populations are significantly less diverged at the class IIB locus than expected based on neutral (microsatellite) loci. We now survey infection by Gyrodactylus turnbulli and G. bullatarudis, common parasitic worms that infect guppies, as a potential agent of homogenizing selection. We used a genetic algorithm to partition both additive and non-additive genetic effects of the five most common MHC allele types as well as a rare allele category. Although we found no evidence for non-additive effects, across the populations we found that one allele type (the a-type) had a significant negative additive effect on parasite load. Thus, individuals who had more copies of the a-type allele were infected with fewer gyrodactylus than individuals with fewer copies of the allele. These results not only link parasite infection with MHC genotype, they provide a mechanism of homogenizing selection across these otherwise disparate populations.     

Parasite predators exhibit a rapid numerical response to increased parasite abundance and reduce transmission to hosts

Predators of parasites have recently gained attention as important parts of food webs and ecosystems. In aquatic systems, many taxa consume free‐living stages of parasites, and can thus reduce parasite transmission to hosts. However, the importance of the functional and numerical responses of parasite predators to disease dynamics is not well understood. We collected host–parasite–predator cooccurrence data from the field, and then experimentally manipulated predator abundance, parasite abundance, and the presence of alternative prey to determine the consequences for parasite transmission. The parasite predator of interest was a ubiquitous symbiotic oligochaete of mollusks, Chaetogaster limnaei limnaei, which inhabits host shells and consumes larval trematode parasites. Predators exhibited a rapid numerical response, where predator populations increased or decreased by as much as 60% in just 5 days, depending on the parasite:predator ratio. Furthermore, snail infection decreased substantially with increasing parasite predator densities, where the highest predator densities reduced infection by up to 89%. Predators of parasites can play an important role in regulating parasite transmission, even when infection risk is high, and especially when predators can rapidly respond numerically to resource pulses. We suggest that these types of interactions might have cascading effects on entire disease systems, and emphasize the importance of considering disease dynamics at the community level.     

Sex-specific differences in shoaling affect parasite transmission in guppies

Background

Individuals have to trade-off the costs and benefits of group membership during shoaling behaviour. Shoaling can increase the risk of parasite transmission, but this cost has rarely been quantified experimentally. Guppies (Poecilia reticulata) are a model system for behavioural studies, and they are commonly infected by gyrodactylid parasites, notorious fish pathogens that are directly transmitted between guppy hosts.

Methodology/Principal Findings

Parasite transmission in single sex shoals of male and female guppies were observed using an experimental infection of Gyrodactylus turnbulli. Parasite transmission was affected by sex-specific differences in host behaviour, and significantly more parasites were transmitted when fish had more frequent and more prolonged contact with each other. Females shoaled significantly more than males and had a four times higher risk to contract an infection.

Conclusions/Significance

Intersexual differences in host behaviours such as shoaling are driven by differences in natural and sexual selection experienced by both sexes. Here we show that the potential benefits of an increased shoaling tendency are traded off against increased risks of contracting an infectious parasite in a group-living species.     

Parasite prevalence in intermediate hosts increases with waterbody age and abundance of final hosts

Oecologia - Prevalence of a parasite may be influenced by age of the habitat (= time available for hosts and parasites to colonize habitats), assemblage composition of host and non-host...     

Quality matters: resource quality for hosts and the timing of epidemics

Epidemiologists increasingly realize that species interactions (e.g. selective predation) can determine when epidemics start and end. We hypothesize here that resource quality can also strongly influence disease dynamics: epidemics can be inhibited when resource quality for hosts is too poor and too good. In three lakes, resource quality for the zooplankton host ( Daphnia dentifera ) was poor when fungal epidemics ( Metschnikowia bicuspidata ) commenced and increased as epidemics waned. Experiments using variation in algal food showed that resource quality had conflicting effects on underlying epidemiology: high-quality food induced large production of infective propagules (spores) and high birth rate but also reduced transmission. A model then illustrated how these underlying correlations can inhibit the start of epidemics (when spore production/birth rate are too low) but also catalyse their end (when transmission becomes too low). This resource quality mechanism is likely to interface with other ones controlling disease dynamics and warrants closer evaluation.     

Schistosoma transmission: scaling-up competence from hosts to ecosystems

In a One-Health context, it is urgent to establish the links between environmental degradation, biodiversity loss, and the circulation of pathogens. Here we review and literally draw a general vision of aquatic environmental factors that interface with Schistosoma species, agents of schistosomiasis, and ultimately modulate their transmission at the ecosystem scale. From this synthesis, we introduce the concept of ecosystem competence defined as ‘the propensity of an ecosystem to amplify or mitigate an incoming quantity of a given pathogen that can be ultimately transmitted to their definitive hosts’. Ecosystem competence integrates all mechanisms at the ecosystem scale underlying the transmission risk of a given pathogen and offers a promising measure for operationalizing the One-Health concept.     

Parasite biodiversity and host defenses: chewing lice and immune response of their avian hosts

Antagonistic host-parasite interactions lead to coevolution of host defenses and parasite virulence. Such adaptation by parasites to host defenses may occur to the detriment of the ability of parasites to exploit alternative hosts, causing parasite specialization and speciation. We investigated the relationship between level of anti-parasite defense in hosts and taxonomic richness of two chewing louse suborders (Phthiraptera: Amblycera, Ischnocera) on birds. While Amblyceran lice tend to occur in contact with host skin, feed on host skin and chew emerging tips of developing feathers to obtain blood, Ischnoceran lice live on feathers and feed on the non-living keratin of feather barbules. We hypothesized that Amblyceran abundance and richness would have evolved in response to interaction with the immune system of the host, while Ischnoceran taxonomic richness would have evolved independently of immunological constraints. In an interspecific comparison, the abundance of Ischnocerans was positively related to host body size, while host body mass and Ischnoceran taxonomic richness accounted for the abundance of Amblycerans. Amblyceran taxonomic richness was predicted by the intensity of T-cell mediated immune response of nestling hosts, while the T-cell response of adults had no significant effect. In contrast, Ischnoceran taxonomic richness was not predicted by host T-cell responses. These results suggest that the taxonomic richness of different parasite taxa is influenced by different host defenses, and they are consistent with the hypothesis that increasing host allocation to immune defense increases Amblyceran biodiversity.Electronic Supplementary Material Supplementary material is available for this article at     

Parasite transmission and cannibalism in an amphipod (Crustacea)

In its freshwater amphipod host Gammarus duebeni celticus, the microsporidian parasite Pleistophora mulleri showed 23% transmission efficiency when uninfected individuals were fed infected tissue, but 0% transmission by water-borne and coprophagous routes. Cannibalism between unparasitised and parasitised individuals was significantly in favour of the former (37% compared to 0%). In addition, cannibalism between parasitised individuals was significantly higher than between unparasitised individuals (27% compared to 0%). Thus, parasitised individuals were more likely to be cannibalised by both unparasitised and parasitised individuals. We discuss the conflicting selective forces within this host/parasite relationship, the implications of parasite mediated cannibalism for host population structure and the impacts this may have on the wider aquatic community.     

Influencing random transmission is a neutral character in hosts

This study introduces an individual-based model on a host-parasite assemblage to investigate whether hosts are necessarily selected for obstructing the transmission of virulent parasites to conspecifics. Contrary to the widespread notion, a host's ability to influence parasite transmission within the host population is a neutral character provided that parasite transmission routes are random, with no reference to genetic relatedness. Due to a lack of selection pressure under such circumstances, hosts may fail to evolve counteradaptations against manipulations by parasites to enhance transmission. However, vertically biased transmission (biased toward kin) selects hosts for a decrease of parasite transmission, while it is also known to select parasites to decrease virulence. Horizontally biased transmission routes (biased toward nonrelated conspecifics) select hosts to increase parasite transmission. In this case, their interests coincide with that of their virulent parasites in enhancing transmission to conspecifics. This finding yields the predictions that hosts infected by virulent pathogens, but unable to recover from disease, should be prone to emigrate from their natal territories and also to enhance transmission at a distance from their natal ranges. These results may considerably improve our understanding of the epidemiology of contagious pathogens and the evolution of social and sexual behavior in host species.     

Cleaner fish become hosts: a novel form of parasite transmission

Adult bucephalid trematodes (Digenea) generally only occur in piscivorous fish. Within labrid fishes they are very rare, however, we have found them in labrid cleaner fish that feed on the ectoparasites of fish. We surveyed 969 labrid fishes from the tropical Pacific and found bucephalids only in cleaners (Labroides dimidiatus, L. bicolor, and Bodianus axillaris) and none in piscivores. The prevalences of bucephalids in L. dimidiatus at Lizard Island, Heron Island, Orpheus Island (all on the Great Barrier Reef), New Caledonia, and Moorea (French Polynesia) were 51, 47, 67, 56, and 67%, respectively. All of the L. bicolor examined from Moorea were infected. Bucephalids were highly prevalent in all size classes of L. dimidiatus from Lizard Island. Bucephalids were found in a 1.6-cm long juvenile L. dimidiatus, in which, piscivory is highly unlikely. We examined the literature on the worldwide bucephalid fauna in labrids and all hosts were found to be cleaners (Symphodus tinca, S. mediterraneus, L. dimidiatus, L. bicolor, and Bodianus axillaris) except Notolabrus parilus, whose ecology is unknown. We suggest that cleaners eat bucephalid metacercariae directly from the exterior surface of client fish during cleaning interactions. This is the first evidence of digeneans in the diet of L. dimidiatus, and the first study to show this novel form of parasite transmission where infective stages are eaten as a result of cleaning behaviour. Cleaning-mediated parasite transmission may result in behavioural modification of second intermediate hosts because clients and parasites both benefit from transmission. If the infection is costly to cleaners and acquired during cheating behaviour, then this parasite might regulate mutualism. Alternatively, if infective stages are targeted, infection by these bucephalids may be a negative consequence of an honest foraging strategy.Communicated by: P. F. Sale     

Parasite transmission risk from geophagic and foraging behavior in chacma baboons

Numerous behavioral and ecological factors are associated with parasite transmission. One factor explored in human research, but absent from nonhuman primate research, is parasite transmission from soil ingestion. Human studies suggest geophagy, the regular and deliberate consumption of soil, increases risk of soil‐transmitted helminth (STH) infection. Geophagy, which is prevalent in nonhuman primates, has several positive associations: gastrointestinal distress alleviation, possible mineral supplementation, and bacterial infection prevention. Our objective was to determine whether STH transmission was possible from deliberate or accidental soil ingestion, in a troop of chacma baboons (Papio hamadryas ursinus) that engaged in geophagy, foraged on the terrestrial substrata, and had a Trichuris sp. sample prevalence of 100%. We collected and analyzed 80 soil samples from geophagy and ground foraging sites on and around Wildcliff Nature Reserve, South Africa. Forty soil samples were collected from sites where soil was consumed, and 40 were collected from sites where soil was not consumed. At geophagy sites, the number of Trichuris sp. eggs recovered varied significantly between areas used and unused by the baboons, suggesting behavior is an important factor. In contrast, at foraging sites, there was only a tendency to recover more eggs at used than unused areas, and we propose egg recovery was influenced by fecal contamination that occurred throughout foraging stands. The difference in egg recovery between used areas at geophagy sites and used areas at foraging sites was not significant. These preliminary findings suggest both geophagy and foraging sites are a potential source of STH infection for this troop. Whether geophagy benefits outweigh the potential cost of parasite reinfection for this baboon troop is unknown, so we encourage future research on the influence that host foraging behavior may have on parasite reinfection. Am. J. Primatol. 74:940‐947, 2012. © 2012 Wiley Periodicals, Inc.     

Wolbachia infection in crustaceans: novel hosts and potential routes for horizontal transmission

Thirty‐five percent of isopods are estimated to be infected by Wolbachia, an intracellular maternally inherited α‐Proteobacterium. Previous studies have indicated that horizontal transfer of Wolbachia strains may occur, although the mechanisms are unclear. The wsp gene was sequenced from 17 Wolbachia strains harboured by crustacean host species and three from their associated predators and parasites. Two major clades of Wolbachia were found in crustacean, with relatives also found in insects, the other restricted to crustaceans. Highly divergent Wolbachia strains were found in a woodlouse‐eating spider and its prey, suggesting no intertaxon bacterial exchange via the predator–prey route. The phylogenetic proximity of Wolbachia from parasitoid flies or phoretic mites to those from isopods suggests that horizontal symbiont transmission may have occurred between those taxa. Two distant Wolbachia strains were detected in two intertidal amphipods; these strains were closely related to different coastal isopod symbionts, suggesting Wolbachia transmission may occur between distantly related crustacean hosts living under the same ecological conditions.     

Detecting social transmission in networks

In recent years researchers have drawn attention to a need for new methods with which to identify the spread of behavioural innovations through social transmission in animal populations. Network-based analyses seek to recognise diffusions mediated by social learning by detecting a correspondence between patterns of association and the flow of information through groups. Here we introduce a new order of acquisition diffusion analysis (OADA) and develop established time of acquisition diffusion analysis (TADA) methods further. Through simulation we compare the merits of these and other approaches, demonstrating that OADA and TADA have greater power and lower Type I error rates than available alternatives, and specifying when each approach should be deployed. We illustrate the new methods by applying them to reanalyse an established dataset corresponding to the diffusion of foraging innovations in starlings, where OADA and TADA detect social transmission that hitherto had been missed. The methods are potentially widely applicable by researchers wishing to detect social learning in natural and captive populations of animals, and to facilitate this we provide code to implement OADA and TADA in the statistical package R.     

Phylogenetic relationships among monogenean gill parasites (Dactylogyridea, Ancyrocephalidae) infesting tilapiine hosts (Cichlidae): systematic and evolutionary implications

We studied the systematics of 14 species of monogenean (Ancyrocephalidae) gill parasites from West African tilapiine hosts (Cichlidae) using both morphological and genetic data. With these tools, we were able to: (i) confirm the validity of the previously described morphological parasite species and of the genus Scutogyrus; (ii) propose that some stenoxenous species (i.e., parasite species with more than one host) may be composed of sister species (e.g., Cichlidogyrus tilapiae); (iii) state that the use of the morphology of the haptoral sclerites is more suitable to infer phylogenetic relationships than the morphology of the genitalia (which seems to be more useful to resolve species-level identifications, presumably because of its faster rate of change). These results imply that: (i) the specificity of these monogenean parasites is greater than initially supposed (what were thought to be stenoxenous species may be assemblages of oïoxenous sister species); (ii) related species groups (i.e., “tilapiae,” “halli,” and “tiberianus”) have to be, as genus Scutogyrus, validated within the 54 ancyrocephalid species described from 18 species of tilapiine hosts in West Africa, (iii) the group “tilapiae,” due to its morphology and host range, have to be considered as being the most primitive; (iv) the occurrence of lateral transfers and parallel speciation processes are necessary to describe the repartition of the newly described parasite groups on the three host genera studied (Tilapia, Oreochromis, and Sarotherodon).     

Epizootiology of Eustrongylides ignotus in Florida: transmission and development of larvae in intermediate hosts

Under laboratory conditions, 2 modes of transmission of Eustrongylides ignotus (Nematoda: Dioctophymatoidea) to fish were identified. Eastern mosquitofish (Gambusia holbrooki) became infected after ingestion of either eggs of E. ignotus containing first-stage larvae or aquatic oligochaetes (Limnodrilus hoffmeisteri) containing third-stage larvae of E. ignotus. After removal from the uterus of gravid E. ignotus females and incubation for 17-28 days, depending on temperature, it was found that parasite eggs contained first-stage larvae that were infective to fish and oligochaetes. Larvae developed to the third stage in oligochaetes and were infective to fish 35-77 days postinfection (PI) and when fed to fish, developed to the fourth stage between 127 and 184 days PI. Eggs containing first-stage larvae fed directly to fish developed to the fourth stage between 84 and 105 days PI. The amount of time for development from the undifferentiated egg to the fourth-stage larva was 78-156 days shorter when fish ingested eggs containing first-stage larvae than when fish ingested oligochaetes containing third-stage larvae. Three species of large piscivorous fish, including black crappie (Pomoxis nigromaculatus), largemouth bass (Micropterus salmoides), and warmouth (Lepomis gulosus), were fed mosquitofish containing fourth-stage larvae. At necropsy, live E. ignotus larvae were recovered from all 3 species. Several fish had multiple infections after ingesting > 1 larva, indicating that bioaccumulation of the parasite in the food chain may occur.     

Life-history evolution in guppies viii: the demographics of density regulation in guppies (poecilia reticulata)

In prior research, we found the way guppy life histories evolve in response to living in environments with a high or low risk of predation is consistent with life-history theory that assumes no density dependence. We later found that guppies from high-predation environments experience higher mortality rates than those from low-predation environments, but the increased risk was evenly distributed across all age/size classes. Life-history theory that assumes density-independent population growth predicts that life histories will not evolve under such circumstances, yet we have shown with field introduction experiments that they do evolve. However, theory that incorporates density regulation predicts this pattern of mortality can result in the patterns of life-history evolution we had observed. Here we report on density manipulation experiments performed in populations of guppies from low-predation environments to ask whether natural populations normally experience density regulation and, if so, to characterize the short-term demographic changes that underlie density regulation. Our experiments reveal that these populations are density regulated. Decreased density resulted in higher juvenile growth, decreased juvenile mortality rates, and increased reproductive investment by adult females. Increased density causes reduced offspring size, decreased fat storage by adult females, and increased adult mortality.     

Different transmission strategies of a parasite in male and female hosts

We investigated whether a parasite with two routes of transmission responds to the different transmission opportunities offered by male and female hosts by using different transmission strategies in the two sexes. The parasite Ascogregarina culicis, which infects the mosquito Aedes aegypti, can be transmitted as its host’s pupa transforms into an adult or when a female lays its eggs. As the latter transmission route is missing in males, we expected, and found, that the parasite releases a greater proportion of its infectious forms during emergence when it is within a male than when it infects a female. The transmission route, which influences the parasite’s dispersal and the evolution of its virulence, was also affected by the dose of infection and the parasite’s previous transmission route. Our results emphasize the complexity underlying the development of parasites and show their ability to tune their strategy to their environment.