Pathogen interactions, population cycles, and phase shifts

Interspecific pathogen interactions can profoundly affect pathogen population dynamics and the efficacy of control strategies. However, many pathogens exhibit cyclic abundance patterns (e.g., seasonality), and temporal asynchrony between interacting pathogens could reduce the impact of those interactions. Here we use an extension of our previously published model to investigate the effects of cycles on pathogen interaction. We demonstrate that host immune memory can maintain the impact of an interaction, even when the effector pathogen abundance is low or the pathogen is absent. Paradoxically, immune memory can result in pathogens interacting more strongly when temporally out of phase. We find that interactions between species can result in changes to the temporal pattern of the affected species. We further demonstrate that this may be observed in a natural host-pathogen system. Given the continuing debate regarding the relevance of pathogen interactions in natural systems and increasing concern about treatment strategies for coinfections, both the discovery of a shift in cycle in empirical data and the mechanism by which we identified it are important. Finally, because the model structure used here is analogous to models of a simple predator-prey system, we also consider the consequences of these findings in the context of that system.     

Experimental evaluation of the relationship between lethal or non-lethal virulence and transmission success in malaria parasite infections

Background  

Evolutionary theory suggests that the selection pressure on parasites to maximize their transmission determines their optimal host exploitation strategies and thus their virulence. Establishing the adaptive basis to parasite life history traits has important consequences for predicting parasite responses to public health interventions. In this study we examine the extent to which malaria parasites conform to the predicted adaptive trade-off between transmission and virulence, as defined by mortality. The majority of natural infections, however, result in sub-lethal virulent effects (e.g. anaemia) and are often composed of many strains. Both sub-lethal effects and pathogen population structure have been theoretically shown to have important consequences for virulence evolution. Thus, we additionally examine the relationship between anaemia and transmission in single and mixed clone infections.     

The potential role of habitat on intestinal helminths of mountain hares, Lepus timidus

Over the last century in the uplands of Scotland, the extent of heather moorland which supports high densities of mountain hares Lepus timidus has diminished and has gradually been replaced by large-scale commercial forestry plantations or expanding natural woodlands. The potential impact of such a change in land use on host-parasite interactions was investigated by comparing the intensity and prevalence of infection of hares by parasites in two separate habitats: a large hare-fenced young forestry plantation and the adjacent open moorland. Carcasses were collected in November 1990 from within both habitats and after the woodland had been enclosed for nine months. Age, sex, fatness (kidney fat index) and degree of infection of hares were noted. Two parasites were recorded: the nematode Trichostrongylus retortaeformis and the cestode Mosgovoyia pectinata. Clear differences in the intensity of infection of adults occupying the different habitats had occurred in the nine months since woodland enclosure. Adult mountain hares in the woodland had levels of infections approaching four times that observed in hares occupying the open moorland and although not significant, the prevalence of infection was greater in hosts inhabiting the woodland than the open moorland. It is suggested that the parasite-host relationship differs between the two habitats and as heather-dominated moorland landscapes become more fragmented with the increasing establishment of woodlands, the impact of parasites on the life history strategies of mountain hares needs to be reconsidered.     

Patterns of parasite aggregation in the wild European rabbit (Oryctolagus cuniculus)

Understanding the factors controlling the distribution of parasites within their host population is fundamental to the wider understanding of parasite epidemiology and ecology. To explore changes in parasite aggregation, Taylor's power law was used to examine the distributions of five gut helminths of the wild rabbit. Aggregation was found to be a dynamic process that varied with year, season, host sex, age class, and myxomatosis. Yearly and seasonal changes are thought, in the main, to be the result of variations in weather conditions acting upon infectious stages (or intermediate hosts). Evidence in support of this was the comparatively low degree of fluctuation in the aggregation of the pinworm, Passalurus ambiguus, as the infectious stage of this parasite is likely to be less susceptible to environmental variation. Host age had a marked effect on the level of aggregation of all parasites, but this effect varied between parasite species. P. ambiguus, Trichostrongylus retortaeformis and Cittotaenia denticulata aggregation were lower in adult than juvenile rabbits whilst Graphidium strigosum and Mosgovoyia pectinata aggregation tended to increase with age. Host immunity is thought to be responsible for these differences. Differences in aggregation for different parasites were also seen when the rabbit population was split into males and females. Myxomatosis had a marked effect on helminth distribution with substantially less aggregation in rabbits showing clinical signs of the disease.     

Discordant temporal and geographic patterns in maternal lineages of eastern North American frogs, Rana catesbeiana (Ranidae) and Pseudacris crucifer (Hylidae)

Whether the Pleistocene has had a disproportionate impact on the recent diversification of temperate species, or played a lesser role in a more protracted process, has been a prominent evolutionary debate for the past decade. We used cytochrome b sequences to reconstruct the evolutionary histories of two widely co-distributed, and ecologically divergent frogs (Rana catesbeiana and Pseudacris crucifer) to examine the role of the Pleistocene in structuring these species. Results for R. catesbeiana reflect a pattern of allopatric fragmentation, likely in Coastal Plain refugia on either side of the Mississippi River dating to the mid to early Pleistocene. In contrast, P. crucifer contains numerous divergent lineages, including one west of the Mississippi River in the Interior Highlands, and in the east, multiple lineages that likely expanded from a number of southern Appalachian refugia with lineage sundering originating in the late Pliocene. Large-scale phylogeographic comparisons between these and other eastern North American species reflect both congruent and independent patterns of diversification, possibly reflecting the relative importance of dispersal ability and habitat associations. Although intra-lineage diversification has been structured by repeated Pleistocene glaciations, lineage sundering likely dates at least to the Pliocene in most (but not all) northern temperate amphibian and reptile species studied to date.     

Appraisal of the consequences of the DDT-induced bottleneck on the level and geographic distribution of neutral genetic variation in Canadian peregrine falcons, Falco peregrinus

Peregrine falcon populations underwent devastating declines in the mid-20th century due to the bioaccumulation of organochlorine contaminants, becoming essentially extirpated east of the Great Plains and significantly reduced elsewhere in North America. Extensive re-introduction programs and restrictions on pesticide use in Canada and the United States have returned many populations to predecline sizes. A proper population genetic appraisal of the consequences of this decline requires an appropriate context defined by (i) meaningful demographic entities; and (ii) suitable reference populations. Here we explore the validity of currently recognized subspecies designations using data from the mitochondrial control region and 11 polymorphic microsatellite loci taken from 184 contemporary individuals from across the breeding range, and compare patterns of population genetic structure with historical patterns inferred from 95 museum specimens. Of the three North American subspecies, the west coast marine subspecies Falco peregrinus pealei is well differentiated genetically in both time periods using nuclear loci. In contrast, the partitioning of continental Falco peregrinus anatum and arctic Falco peregrinus tundrius subspecies is not substantiated, as individuals from these subspecies are historically indistinguishable genetically. Bayesian clustering analyses demonstrate that contemporary genetic differentiation between these two subspecies is mainly due to changes within F. p. anatum (specifically the southern F. p. anatum populations). Despite expectations and a variety of tests, no genetic bottleneck signature is found in the identified populations; in fact, many contemporary indices of diversity are higher than historical values. These results are rationalized by the promptness of the recovery and the possible introduction of new genetic material.     

The effect of single and concomitant pathogen infections on condition and fecundity of the wild rabbit (Oryctolagus cuniculus)

We assessed the effect of two pathogens (myxoma virus and Eimeria stiedae) and five macroparasites (gastrointestinal helminth species) of the wild rabbit (Oryctolagus cuniculus) upon total host body mass and abdominal fat level. Additionally, we assessed the effects of these organisms on the number of foetuses in adult females during the peak breeding period. Both mass of abdominal fat and total body mass of the rabbit were negatively associated with myxoma virus infection and increasing helminth species richness. Total body mass was also negatively associated with the protozoan parasite E. steidae. No relationship was found between any of the parasites/pathogens and the number of foetuses in adult females, although only relatively small sample sizes were available for this section of the analysis. Increasing host body mass was positively associated with number of foetuses and we propose that mass reduction caused by the pathogen and parasite species could also have the consequence of reducing foetal number.     

Male-biased mutation rates and the overestimation of extrapair paternity: problem, solution, and illustration using thick-billed murres (Uria lomvia, Alcidae)

The widespread utility of hypervariable loci in genetic studies derives from the high mutation rate, and thus the high polymorphism, of these loci. Recent evidence suggests that mutation rates can be extremely high and may be male biased (occurring in the male germ-line). These two factors combined may result in erroneous overestimates of extrapair paternity, since legitimate offspring with novel alleles will have more mismatches with respect to the biological father than the biological mother. As mutations are male driven, increasing the number of hypervariable loci screened may simply increase the number of mismatches between fathers and their legitimate offspring. Here we describe a simple statistic, the probability of resemblance (PR), to distinguish between mismatches due to parental misassignment versus mutation in either sex or null alleles. We apply this method to parentage data on thick-billed murres (Uria lomvia), and demonstrate that, without considering either mutations or male-biased mutation rates, cases of extrapair paternity (7% in this study) would be grossly overestimated (14.5%-22%). The probability of resemblance can be utilized in parentage studies of any sexually reproducing species when allele or haplotype frequency data are available for putative parents and offspring. We suggest calculating this probability to correctly categorize legitimate offspring when mutations and null alleles may cause mismatches.