Host ecology and biogeography drive parasite community composition in Atlantic killifishes.

Understanding the mechanisms of parasite community assembly can be confounded by phylogenetic distance among host species. Addressing this requires focusing on parasite communities within closely related taxa. Thus, we took a macroecological approach to examining parasite community structure within Killifish species in the genus Fundulus to disentangle the effects of host phylogeny and ecological variables. We constructed a database of parasite communities within Fundulus species from 15 published and unpublished surveys covering the Atlantic coast of the US and Canada. The database was expanded by sampling sites in underrepresented provinces and states, totaling 10 Fundulus species from 57 unique geographic sites. Univariate analysis of observed parasite species richness among Fundulus populations in the dataset found that latitude, climate type, and salinity were the dominant factors determining parasite species richness. Multivariate analysis found that host species and landscape type were the most important factors in determining the similarity of parasite assemblages. Unexpectedly, parasite species richness decreased in low latitudes, and host phylogenetic distance was not found to be a significant factor in the similarity of parasite communities. These results indicate that commonly reported large-scale drivers of parasite community structure, such as latitude and phylogeny, could have diminished significance at the host genus level relative to host ecology, biogeography, and local landscape factors.

Mysterious microsporidians: springtime outbreaks of disease in Daphnia communities in shallow pond ecosystems.

Parasites can play key roles in ecosystems, especially when they infect common hosts that play important ecological roles. Daphnia are critical grazers in many lentic freshwater ecosystems and typically reach peak densities in early spring. Daphnia have also become prominent model host organisms for the field of disease ecology, although most well-studied parasites infect them in summer or fall. Here, we report field patterns of virulent microsporidian parasites that consistently infect Daphnia in springtime, in a set of seven shallow ponds in Georgia, USA, sampled every 3-4 weeks for 18 months. We detected two distinct parasite taxa, closely matching sequences of Pseudoberwaldia daphniae and Conglomerata obtusa, both infecting all three resident species of Daphnia: D. ambigua, D. laevis, and D. parvula. To our knowledge, neither parasite has been previously reported in any of these host species or anywhere in North America. Infection prevalence peaked consistently in February-May, but the severity of these outbreaks differed substantially among ponds. Moreover, host species differed markedly in terms of their maximum infection prevalence (5% [D. parvula] to 72% [D. laevis]), mean reduction of fecundity when infected (70.6% [D. ambigua] to 99.8% [D. laevis]), mean spore yield (62,000 [D. parvula] to 377,000 [D. laevis] per host), and likelihood of being infected by each parasite. The timing and severity of the outbreaks suggests that these parasites could be impactful members of these shallow freshwater ecosystems, and that the strength of their effects is likely to hinge on the composition of ponds' zooplankton communities.

Within-host and external environments differentially shape ß-diversity across parasite life stages.

Uncovering drivers of community assembly is a key aspect of learning how biological communities function. Drivers of community similarity can be especially useful in this task as they affect assemblage-level changes that lead to differences in species diversity between habitats. Concepts of ß-diversity originally developed for use in free-living communities have been widely applied to parasite communities to gain insight into how infection risk changes with local conditions by comparing parasite communities across abiotic and biotic gradients. Factors shaping ß-diversity in communities of immature parasites, such as larvae, are largely unknown. This is a key knowledge gap as larvae are frequently the infective life-stage and understanding variation in these larval communities is thus key for disease prevention. Our goal was to uncover links between ß-diversity of parasite communities at different life stages; therefore, we used gastrointestinal nematodes infecting African buffalo in Kruger National Park, South Africa, to investigate within-host and extra-host drivers of adult and larval parasite community similarity. We employed a cross-sectional approach using PERMANOVA that examined each worm community at a single time point to assess independent drivers of ß-diversity in larvae and adults as well as a longitudinal approach with path analysis where adult and larval communities from the same host were compared to better link drivers of ß-diversity between these two life stages. Using the cross-sectional approach, we generally found that intrinsic, within-host traits had significant effects on ß-diversity of adult nematode communities, while extrinsic, extra-host variables had significant effects on ß-diversity of larval nematode communities. However, the longitudinal approach provided evidence that intrinsic, within-host factors affected the larval community indirectly via the adult community. Our results provide key data for the comparison of community-level processes where adult and immature stages inhabit vastly different habitats (i.e. within-host vs. abiotic environment). In the context of parasitism, this helps elucidate host infection risk via larval stages and the drivers that shape persistence of adult parasite assemblages, both of which are useful for predicting and preventing infectious disease.

Life in the margins: host-parasite relationships in ecological edges.

Transitional zones, such as edge habitat, are key landscapes for investigating biodiversity. "Soft edges" are permeable corridors that hosts can cross, while "hard edges" are impermeable borders that hosts cannot pass. Although pathogen transmission in the context of edges is vital to species conservation, drivers of host-parasite relationships in ecological edges remain poorly understood. Thus, we defined a framework for testing hypotheses of host-parasite interactions in hard and soft edges by (1) characterizing hard and soft edges from both the host and parasite perspectives, (2) predicting the types of parasites that would be successful in each type of edge, and (3) applying our framework to species invasion fronts as an example of host-parasite relationships in a soft edge. Generally, we posited that parasites in soft edges are more likely to be negatively affected by habitat fragmentation than their hosts because they occupy higher trophic levels but parasite transmission would benefit from increased host connectivity. Parasites along hard edges, however, are at higher risk of local extinction due to host population perturbations with limited opportunity for parasite recolonization. We then used these characteristics to predict functional traits that would lead to parasite success along soft and hard edges. Finally, we applied our framework to invasive species fronts to highlight predictions regarding host connectivity and parasite traits in soft edges. We anticipate that our work will promote a more complete discussion of habitat connectivity using a common framework and stimulate empirical research into host-parasite relationships within ecological edges and transitional zones.

Colonization of a novel host by fleas: changes in egg production and egg size.

We studied the success of fleas, Synosternus cleopatrae and Xenopsylla ramesis, in switching to a novel host by establishing experimental lines maintained on different hosts for 18 generations. Fleas fed on principal (P-line) or novel hosts, either sympatric with (S-line) or allopatric to (A-line) a flea and its principal host, then we assessed their reproductive performance via the number and size of eggs. We compared reproductive performance between hosts within a line and between lines within a host asking: (a) whether fleas adapt to a novel host species after multiple generations; (b) if yes, whether the pattern of adaptation differs between novel host species sympatric with or allopatric to a flea and its principal host; and (c) adaptation to a novel host is accompanied with a loss of success in exploitation of an original host. Fleas from the S- and A-lines increased their egg production on a novel host (except X. ramesis from the S-line). S. cleopatrae from the S-line but not the A-line increased egg size on a novel host, whereas X. ramesis from the A-line but not the S-line produced larger eggs from a novel host. We found no indication of a loss of reproductive performance on the original host while adapting to a novel host. We conclude that fleas are able to switch rapidly to a new host with the pattern of a switch to either sympatric or an allopatric host depending on the identities of both flea and host species.

Feeding performance on a novel host: no adaptation over generations and differential patterns in two flea species.

To model the colonization of a novel host by fleas, Synosternus cleopatrae and Xenopsylla ramesis, we established experimental lines maintained for 15 generations on a principal or a novel host (either co-occurring with a flea or not). We compared the blood meal size and the energy expended for digestion by fleas from the 15th generation of each line on these hosts between hosts within a line and between lines within a host asking (a) whether fleas adapt to a novel host (increased blood consumption/decreased energy expended for digestion); (b) if yes, whether this adaptation leads to the loss of ability to exploit an original host, and (c) whether the success of adaptation to a novel host depends on its ecological co-occurrence with a flea. The blood consumption and digestion energetics of fleas fed on the principal host differed from those on other hosts. The effect of the principal host on feeding performance differed between fleas, with S. cleopatrae consuming less blood and expending more energy for digestion on the principal than on any other host, whereas the opposite was true for X. ramesis. No changes in feeding performance on a novel host over generations were found. We propose several explanations for the lack of adaptation to a novel host over time. We explain the poor performance of S. cleopatrae on its principal host via its immune response mounting pattern. We argue that the principal host of a parasite is not necessarily the host on which the parasite demonstrates the best performance.

Flea infestation, social contact, and stress in a gregarious rodent species: minimizing the potential parasitic costs of group-living.

Both parasitism and social contact are common sources of stress that many gregarious species encounter in nature. Upon encountering such stressors, individuals secrete glucocorticoids and although short-term elevation of glucocorticoids is adaptive, long-term increases are correlated with higher mortality and deleterious reproductive effects. Here, we used an experimental host-parasite system, social rodents Acomys cahirinus and their characteristic fleas Parapulex chephrenis, in a fully-crossed design to test the effects of social contact and parasitism on stress during pregnancy. By analysing faecal glucocorticoid metabolites, we found that social hierarchy did not have a significant effect on glucocorticoid concentration. Rather, solitary females had significantly higher glucocorticoid levels than females housed in pairs. We found a significant interaction between the stressors of parasitism and social contact with solitary, uninfested females having the highest faecal glucocorticoid metabolite levels suggesting that both social contact and infestation mitigate allostatic load in pregnant rodents. Therefore, the increased risk of infestation that accompanies group-living could be outweighed by positive aspects of social contact within A. cahirinus colonies in nature.

Species and site contributions to ß-diversity in fleas parasitic on the Palearctic small mammals: ecology, geography and host species composition matter the most.

The ß-diversity of fleas parasitic on small mammals in 45 regions of the Palearctic was partitioned into species [species contributions to ß-diversity (SCBD)] and site ( = assemblage) contributions [local contributions to ß-diversity (LCBD)]. We asked what are the factors affecting SCBD and LCBD and tested whether (a) variation in ecological, morphological, life history and geographic traits of fleas can predict SCBD and (b) variation in flea and host community metrics, off-host environmental factors, host species composition of flea assemblages can predict LCBD. We used spatial variables to describe geographic distribution of flea assemblages with various LCBD values. SCBD significantly increased with an increase in abundance and a decrease in phylogenetic host specificity of a flea as well as with size and latitude of its geographic range, but was not associated with any morphological/life history trait. LCBD of flea assemblages did not depend on either flea or host species richness or environmental predictors, but was significantly affected by compositional uniqueness ( = LCBD) of regional host assemblages and variables describing their species composition. In addition, variation in LCBD was also explained by broad-to-moderate-scale spatial variables. We conclude that SCBD of fleas could be predicted via their ecological and geographic traits, whereas LCBD of their assemblages could be predicted via host composition.

Reproductive performance in generalist haematophagous ectoparasites: maternal environment, rearing conditions or both?

We tested whether and how the maternal environment (i.e. host species exploited by a mother), rearing conditions (i.e. host species exploited by her offspring) or both (i.e. matches and mismatches in host species exploited by a mother and her offspring) affect reproductive performance in the offspring. We experimentally manipulated maternal and rearing environments in two generalist fleas (Xenopsylla conformis and Xenopsylla ramesis) implementing a factorial cross-rearing design. Mothers exploited either the principal host (PH) or auxiliary hosts that were either closely (CAH) or distantly related (DAH) to the PH. After six generations of infesting a given host species, we cross-reared fleas within and between host species. These fleas reproduced and we measured their reproductive performance both quantitatively (i.e. egg number) and qualitatively (i.e. egg size, development time, body size of the next generation). We found that identity of the host a flea was reared on (=actual host) had the strongest effect on its performance. Individuals reared on the PH performed considerably better than those reared on either auxiliary host. Moreover, fleas reared on a CAH performed better than those reared on a DAH. Actual host identity also had a stronger effect on reproductive performance in X. ramesis than in X. conformis. Nevertheless, there was no difference in performance between match and mismatch maternal and actual host identities. We conclude that rearing environment has the strongest effect on fitness in generalist parasites. Moreover, phylogenetic distance between an auxiliary host and the PH determines the level of suitability of the former.

The effects of environment, hosts and space on compositional, phylogenetic and functional beta-diversity in two taxa of arthropod ectoparasites.

We studied the effects of variation in environmental, host-associated and spatial factors on variation in compositional, phylogenetic/taxonomic and functional facets of beta-diversity in fleas and gamasid mites parasitic on small mammals and asked whether (a) the importance of these factors as drivers of beta-diversity differs among its multiple facets and (b) the effects of variation in environment, hosts and space on beta-diversity variation differ between the two ectoparasite taxa. To understand the relative effects of each group of predictors, we used a distance-based redundancy analysis and variation partitioning. The greatest portions of variation in the compositional beta-diversity of fleas were equally explained by host-associated and spatial predictors, whereas variation in host species composition contributed the most to variation in the compositional beta-diversity of mites. Variation in the phylogenetic (i.e. based on phylogenetic tree) beta-diversity of fleas was mainly due to variation in the phylogenetic composition of host communities, while the taxonomic (i.e. based on Linnean taxonomy) beta-diversity of mites was influenced by environmental variation. Unique contributions of spatial and environmental variation explained most of the variation in functional beta-diversity and its species replacement (= turnover) component (i.e. beta-diversity explained by replacement of species alone) in fleas and mites, respectively. Variation in the richness difference component (i.e. beta-diversity explained by species loss/gain alone) of functional beta-diversity was mainly affected by either variation in the functional composition of host assemblages (fleas) or its joint action with environmental variables (mites). We conclude that the pattern of the relative effects of environmental, host-associated and spatial factors on beta-diversity is context-dependent and may differ among different facets of beta-diversity, among different beta-diversity components and also among taxa dependent on biological affinities.

Do the pattern and strength of species associations in ectoparasite communities conform to biogeographic rules?

We tested whether biogeographic patterns characteristic of species diversity and composition may also apply to community assembly by investigating geographic variation in the pattern (PSA) (aggregation versus segregation) and strength of species associations (SSA) in flea and mite communities harbored by small mammalian hosts in Western Siberia. We asked whether (a) there is a relationship between latitude and PSA or SSA and (b) similarities in PSA or SSA follow a distance decay pattern or if they are better explained by variation in environmental factors (altitude, amount of vegetation, precipitation, and air temperature). We used a sign of a co-occurrence metric (the C-score) as an indicator of PSA and its absolute standardized value as a measure of SSA. We analyzed data using logistic and linear models, generalized dissimilarity modeling (GDM), and a logistic version of the multiple regression on distance matrices (MRM). The majority of the C-scores of the observed presence/absence matrices indicated a tendency to species aggregation rather than segregation. No effect of latitude on PSA or SSA was found. The dissimilarity in PSA was affected by environmental dissimilarity in mite compound communities only. A relatively large proportion of the deviance of spatial variation in SSA was explained by the GDMs in infracommunities, but not component communities, and in only three (of seven) and two (of eight) host species of fleas and mites, respectively. The best predictors of dissimilarity in SSA in fleas differed between host species, whereas the same factor (precipitation) was the best predictor of dissimilarity in SSA in mites. We conclude that PSA and SSA in parasite communities rarely conform to biogeographic rules. However, when a biogeographic pattern is detected, its manifestation differs among hosts and between ectoparasite taxa.

Body size and ecological traits in fleas parasitic on small mammals in the Palearctic: larger species attain higher abundance.

We studied the relationships between body size and (a) abundance and (b) host specificity in fleas parasitic on small mammals (rodents and shrews) in the Palearctic taking into account the confounding effect of phylogeny. We tested these relationships both across 127 flea species and within separate phylogenetic clades, predicting higher abundance and lower host specificity (in terms of the number or diversity of hosts used by a flea) in smaller species. We also tested for the relationships between body size and abundance separately for species that spend most of their lives on a host's body (the "body" fleas) and species that spend most of their lives in a host's burrow or nest (the "nest" fleas). A significant phylogenetic signal in body size was detected across all fleas, as well as in five of six separate clades. Across all fleas and in majority of phylogenetic clades, mean abundance significantly increased with an increase in body size. The same pattern was found for both the "body" and the "nest" fleas, although the slope of the relationship appeared to be steeper in the former than in the latter. Neither measure of host specificity demonstrated a significant correlation with body size regardless of the subset of flea species analysed. We explain higher abundance attained by larger flea species by higher fecundity and/or competitive advantage upon smaller species at larval stage. We conclude that the macroecological patterns reported to date in parasites are far from being universal.

Phylogenetic heritability of geographic range size in haematophagous ectoparasites: time of divergence and variation among continents.

To understand existence, patterns and mechanisms behind phylogenetic heritability in the geographic range size (GRS) of parasites, we measured phylogenetic signal (PS) in the sizes of both regional (within a region) and continental (within a continent) geographic ranges of fleas in five regions. We asked whether (a) GRS is phylogenetically heritable and (b) the manifestation of PS varies between regions. We also asked whether geographic variation in PS reflects the effects of the environment's spatiotemporal stability (e.g. glaciation disrupting geographic ranges) or is associated with time since divergence (accumulation differences among species over time). Support for the former hypothesis would be indicated by stronger PS in southern than in northern regions, whereas support for the latter hypothesis would be shown by stronger PS in regions with a large proportion of species belonging to the derived lineages than in regions with a large proportion of species belonging to the basal lineages. We detected significant PS in both regional and continental GRSs of fleas from Canada and in continental GRS of fleas from Mongolia. No PS was found in the GRS of fleas from Australia and Southern Africa. Venezuelan fleas demonstrated significant PS in regional GRS only. Local Indicators of Phylogenetic Association detected significant local positive autocorrelations of GRS in some clades even in regions in which PS has not been detected across the entire phylogeny. This was mainly characteristic of younger taxa.

Nestedness in assemblages of helminth parasites of bats: a function of geography, environment, or host nestedness?

Nested subsets occur in ecological communities when species-poor communities are subsets of larger, species-rich communities. Understanding this pattern can help elucidate species colonization abilities, extinction risks, and general structuring of biological communities. Here, we evaluate nestedness in a poorly studied host-parasite system, bats and their helminths, across the Japanese archipelago and within its different bioclimatic regions. We hypothesized that (1) if helminth communities are nested across geographic sites at the level of the archipelago, then broad-scale processes, like colonization-extinction dynamics, mainly structure parasite assemblages; (2) if helminth communities are nested across geographic sites at the level of the bioclimatic region, then fine-scale environmental variation plays a significant role in species nestedness; (3) if helminth community nestedness mirrors host species nestedness, then communities are nested because the habitats they occupy are nested; and (4) if nestedness does not occur or if it is not correlated with any geographical or host data, then passive sampling could be responsible for the patterns of parasite assemblage in our sample. We found that helminth communities were nested across host species throughout the archipelago but, when considering each bioclimatic region, helminths in only one region were significantly more nested than the null model. Helminth communities were also nested across sites within all four bioclimatic regions. These results suggest that helminths form nested subsets across the archipelago due to broad-scale processes that reflect the overall lineages of their mammalian hosts; however, at the regional scale, environmental processes related to nestedness of their habitats drive parasite community nestedness.

Can we predict the success of a parasite to colonise an invasive host?

To understand whether a parasite can exploit a novel invasive host species, we measured reproductive performance (number of eggs per female per day, egg size, development rate and size of new imagoes) of fleas from the Negev desert in Israel (two host generalists, Synosternus cleopatrae and Xenopsylla ramesis, and a host specialist, Parapulex chephrenis) when they exploited either a local murid host (Gerbillus andersoni, Meriones crassus and Acomys cahirinus) or two alien hosts (North American heteromyids, Chaetodipus penicillatus and Dipodomys merriami). We asked whether (1) reproductive performance of a flea differs between an alien and a characteristic hosts and (2) this difference is greater in a host specialist than in host generalists. The three fleas performed poorly on alien hosts as compared to local hosts, but the pattern of performance differed both among fleas and within fleas between alien hosts. The response to alien hosts did not depend on the degree of host specificity of a flea. We conclude that successful parasite colonisation of an invasive host is determined by some physiological, immunological and/or behavioural compatibility between a host and a parasite. This compatibility is unique for each host-parasite association, so that the success of a parasite to colonise an invasive host is unpredictable.

Morphological asymmetry and habitat quality: using fleas and their rodent hosts as a novel experimental system.

Morphological asymmetry is widely used to measure developmental instability and higher levels of asymmetry often correlate with decreased mating success, increased inbreeding, increased stress and decreased habitat quality. We studied asymmetry and relationships between asymmetry and host identity in two flea species, host generalist Xenopsylla ramesis and host specialist Parapulex chephrenis, and asked: (1) what the level of asymmetry was in their femurs and tibiae; (2) which type of asymmetry predominates; and (3) whether fleas that fed on host species distantly related to their principal host species produced offspring that exhibited greater asymmetry compared with offspring of fleas that fed on their principal host species. We found fluctuating asymmetry in femurs and tibiae of X. ramesis and in the tibiae of P. chephrenis as well as significantly left-handed directional asymmetry in the femurs of P. chephrenis Host species identity significantly impacted asymmetry in leg segments of P. chephrenis but not in those of X. ramesis Offspring asymmetry increased when mother fleas fed on a host that was distantly related to the principal host. Fleas parasitizing multiple host species might compensate for developmental instability when utilizing a novel host species; therefore, host-switching events in host-specific parasites could be constrained by the relatedness between a novel and a principal host species.

Beta-diversity of ectoparasites at two spatial scales: nested hierarchy, geography and habitat type.

Beta-diversity of biological communities can be decomposed into (a) dissimilarity of communities among units of finer scale within units of broader scale and (b) dissimilarity of communities among units of broader scale. We investigated compositional, phylogenetic/taxonomic and functional beta-diversity of compound communities of fleas and gamasid mites parasitic on small Palearctic mammals in a nested hierarchy at two spatial scales: (a) continental scale (across the Palearctic) and (b) regional scale (across sites within Slovakia). At each scale, we analyzed beta-diversity among smaller units within larger units and among larger units with partitioning based on either geography or ecology. We asked (a) whether compositional, phylogenetic/taxonomic and functional dissimilarities of flea and mite assemblages are scale dependent; (b) how geographical (partitioning of sites according to geographic position) or ecological (partitioning of sites according to habitat type) characteristics affect phylogenetic/taxonomic and functional components of dissimilarity of ectoparasite assemblages and (c) whether assemblages of fleas and gamasid mites differ in their degree of dissimilarity, all else being equal. We found that compositional, phylogenetic/taxonomic, or functional beta-diversity was greater on a continental rather than a regional scale. Compositional and phylogenetic/taxonomic components of beta-diversity were greater among larger units than among smaller units within larger units, whereas functional beta-diversity did not exhibit any consistent trend regarding site partitioning. Geographic partitioning resulted in higher values of beta-diversity of ectoparasites than ecological partitioning. Compositional and phylogenetic components of beta-diversity were higher in fleas than mites but the opposite was true for functional beta-diversity in some, but not all, traits.

Revisiting the role of dissimilarity of host communities in driving dissimilarity of ectoparasite assemblages: non-linear vs linear approach.

We revisited the role of dissimilarity of host assemblages in shaping dissimilarity of flea assemblages using a non-linear approach. Generalized dissimilarity models (GDMs) were applied using data from regional surveys of fleas parasitic on small mammals in four biogeographical realms. We compared (1) model fit, (2) the relative effects of host compositional and phylogenetic turnover and geographic distance on flea compositional and phylogenetic turnover, and (3) the rate of flea turnover along gradients of host turnover and geographic distance with those from earlier application of a linear approach. GDMs outperformed linear models in explaining variation in flea species turnover and host dissimilarity was the best predictor of flea dissimilarity, irrespective of scale. The shape of the relationships between flea compositional turnovers along host compositional turnover was similar in all realms, whereas turnover along geographic distance differed among realms. In contrast, the rate of flea phylogenetic turnover along gradients of host phylogenetic turnover differed among realms, whereas flea phylogenetic turnover did not depend on geographic distance in any realm. We demonstrated that a non-linear approach (a) explained spatial variation in parasite community composition better than and (b) revealed patterns that were obscured by earlier linear analyses.