Specificity and specialization of congeneric monogeneans parasitizing cyprinid fish

Patterns and likely processes connected with evolution of host specificity in congeneric monogeneans parasitizing fish species of the Cyprinidae were investigated. A total of 51 Dactylogyrus species was included. We investigated (1) the link between host specificity and parasite phylogeny; (2) the morphometric correlates of host specificity, parasite body size, and variables of attachment organs important for host specificity; (3) the evolution of morphological adaptation, that is, attachment organ; (4) the determinants of host specificity following the hypothesis of specialization on more predictable resources considering maximal body size, maximal longevity, and abundance as measures of host predictability; and (5) the potential link between host specificity and parasite diversification. Host specificity, expressed as an index of host specificity including phylogenetic and taxonomic relatedness of hosts, was partially associated with parasite phylogeny, but no significant contribution of host phylogeny was found. The mapping of host specificity into the phylogenetic tree suggests that being specialist is not a derived condition for Dactylogyrus species. The different morphometric traits of the attachment apparatus seem to be selected in connection with specialization of specialist parasites and other traits favored as adaptations in generalist parasites. Parasites widespread on several host species reach higher abundance within hosts, which supports the hypothesis of ecological specialization. When separating specialists and generalists, we confirmed the hypothesis of specialization on a predictable resource; that is, specialists with larger anchors tend to live on fish species with larger body size and greater longevity, which could be also interpreted as a mechanism for optimizing morphological adaptation. We demonstrated that ecology of host species could also be recognized as an important determinant of host specificity. The mapping of morphological characters of the attachment organ onto the parasite phylogenetic tree reveals that morphological evolution of the attachment organ is connected with host specificity in the context of fish relatedness, especially at the level of host subfamilies. Finally, we did not find that host specificity leads to parasite diversification in congeneric monogeneans.     

Evolutionary relationships, cospeciation, and host switching in avian malaria parasites

We used phylogenetic analyses of cytochrome b sequences of malaria parasites and their avian hosts to assess the coevolutionary relationships between host and parasite lineages. Many lineages of avian malaria parasites have broad host distributions, which tend to obscure cospeciation events. The hosts of a single parasite or of closely related parasites were nonetheless most frequently recovered from members of the same host taxonomic family, more so than expected by chance. However, global assessments of the relationship between parasite and host phylogenetic trees, using Component and ParaFit, failed to detect significant cospeciation. The event-based approach employed by TreeFitter revealed significant cospeciation and duplication with certain cost assignments for these events, but host switching was consistently more prominent in matching the parasite tree to the host tree. The absence of a global cospeciation signal despite conservative host distribution most likely reflects relatively frequent acquisition of new hosts by individual parasite lineages. Understanding these processes will require a more refined species concept for malaria parasites and more extensive sampling of parasite distributions across hosts. If parasites can disperse between allopatric host populations through alternative hosts, cospeciation may not have a strong influence on the architecture of host-parasite relationships. Rather, parasite speciation may happen more often in conjunction with the acquisition of new hosts followed by divergent selection between host lineages in sympatry. Detailed studies of the phylogeographic distributions of hosts and parasites are needed to characterize these events.     

Diversification and host switching in avian malaria parasites

The switching of parasitic organisms to novel hosts, in which they may cause the emergence of new diseases, is of great concern to human health and the management of wild and domesticated populations of animals. We used a phylogenetic approach to develop a better statistical assessment of host switching in a large sample of vector-borne malaria parasites of birds (Plasmodium and Haemoproteus) over their history of parasite-host relations. Even with sparse sampling, the number of parasite lineages was almost equal to the number of avian hosts. We found that strongly supported sister lineages of parasites, averaging 1.2% sequence divergence, exhibited highly significant host and geographical fidelity. Event-based matching of host and parasite phylogenetic trees revealed significant cospeciation. However, the accumulated effects of host switching and long distance dispersal cause these signals to disappear before 4% sequence divergence is achieved. Mitochondrial DNA nucleotide substitution appears to occur about three times faster in hosts than in parasites, contrary to findings on other parasite-host systems. Using this mutual calibration, the phylogenies of the parasites and their hosts appear to be similar in age, suggesting that avian malaria parasites diversified along with their modern avian hosts. Although host switching has been a prominent feature over the evolutionary history of avian malaria parasites, it is infrequent and unpredictable on time scales germane to public health and wildlife management.     

Coevolution of resource trade-offs driving species interactions in a host–parasite network: an exploratory model

Patterns of specialization asymmetry, where specialist species interact mainly with generalists while generalists interact with both generalists and specialists, are often observed in mutualistic and antagonistic bipartite ecological networks. These have been explained in terms of the relative abundance of species, using a null model that assigns links in proportion to abundance, but doubts have been raised as to whether this offers a complete explanation. In particular, host–parasite networks offer a variety of examples in which the reverse patterns are observed. We propose that the link between specificity and species richness may also be driven by the coevolution of hosts and parasites, as hosts allocate resources to optimize defense against parasites, and parasites to optimize attack on hosts. In this hypothesis, species interactions are a result of resource allocations. This novel concept, linking together many different arguments for network structures, is introduced through the adaptive dynamics of a simple ecological toy system of two hosts and two parasites. We analyze the toy model and its functionality, demonstrating that coevolution leads to specialization asymmetry in networks with closely related parasites or fast host mutation rates, but not in networks with more distantly related species. Having constructed the toy model and tested its applicability, our model can now be expanded to the full problem of a larger system.     

Big bang in the evolution of extant malaria parasites

Malaria parasites (genus Plasmodium) infect all classes of terrestrial vertebrates and display host specificity in their infections. It is therefore assumed that malaria parasites coevolved intimately with their hosts. Here, we propose a novel scenario of malaria parasite-host coevolution. A phylogenetic tree constructed using the malaria parasite mitochondrial genome reveals that the extant primate, rodent, bird, and reptile parasite lineages rapidly diverged from a common ancestor during an evolutionary short time period. This rapid diversification occurred long after the establishment of the primate, rodent, bird, and reptile host lineages, which implies that host-switch events contributed to the rapid diversification of extant malaria parasite lineages. Interestingly, the rapid diversification coincides with the radiation of the mammalian genera, suggesting that adaptive radiation to new mammalian hosts triggered the rapid diversification of extant malaria parasite lineages.     

Diversification by host switching and dispersal shaped the diversity and distribution of avian malaria parasites in Amazonia

Understanding how pathogens and parasites diversify through time and space is fundamental to predicting emerging infectious diseases. Here, we use biogeographic, coevolutionary and phylogenetic analyses to describe the origin, diversity, and distribution of avian malaria parasites in the most diverse avifauna on Earth. We first performed phylogenetic analyses using the mitochondrial cytochrome b (cyt b) gene to determine relationships among parasite lineages. Then, we estimated divergence times and reconstructed ancestral areas to uncover how landscape evolution has shaped the diversification of Parahaemoproteus and Plasmodium in Amazonia. Finally, we assessed the coevolutionary patterns of diversification in this host–parasite system to determine how coevolution may have influenced the contemporary diversity of avian malaria parasites and their distribution among Amazonian birds. Biogeographic analysis of 324 haemosporidian parasite lineages recovered from 4178 individual birds provided strong evidence that these parasites readily disperse across major Amazonian rivers and this has occurred with increasing frequency over the last five million years. We also recovered many duplication events within areas of endemism in Amazonia. Cophylogenetic analyses of these blood parasites and their avian hosts support a diversification history dominated by host switching. The ability of avian malaria parasites to disperse geographically and shift among avian hosts has played a major role in their radiation and has shaped the current distribution and diversity of these parasites across Amazonia.     

Loss of forest cover and host functional diversity increases prevalence of avian malaria parasites in the Atlantic Forest

Host phylogenetic relatedness and ecological similarity are thought to contribute to parasite community assembly and infection rates. However, recent landscape level anthropogenic changes may disrupt host-parasite systems by impacting functional and phylogenetic diversity of host communities. We examined whether changes in host functional and phylogenetic diversity, forest cover, and minimum temperature influence the prevalence, diversity, and distributions of avian haemosporidian parasites (genera Haemoproteus and Plasmodium) across 18 avian communities in the Atlantic Forest. To explore spatial patterns in avian haemosporidian prevalence and taxonomic and phylogenetic diversity, we surveyed 2241 individuals belonging to 233 avian species across a deforestation gradient. Mean prevalence and parasite diversity varied considerably across avian communities and parasites responded differently to host attributes and anthropogenic changes. Avian malaria prevalence (termed herein as an infection caused by Plasmodium parasites) was higher in deforested sites, and both Plasmodium prevalence and taxonomic diversity were negatively related to host functional diversity. Increased diversity of avian hosts increased local taxonomic diversity of Plasmodium lineages but decreased phylogenetic diversity of this parasite genus. Temperature and host phylogenetic diversity did not influence prevalence and diversity of haemosporidian parasites. Variation in the diversity of avian host traits that promote parasite encounter and vector exposure (host functional diversity) partially explained the variation in avian malaria prevalence and diversity. Recent anthropogenic landscape transformation (reduced proportion of native forest cover) had a major influence on avian malaria occurrence across the Atlantic Forest. This suggests that, for Plasmodium, host phylogenetic diversity was not a biotic filter to parasite transmission as prevalence was largely explained by host ecological attributes and recent anthropogenic factors. Our results demonstrate that, similar to human malaria and other vector-transmitted pathogens, prevalence of avian malaria parasites will likely increase with deforestation.     

Ectoparasitic "jacks-of-all-trades": relationship between abundance and host specificity in fleas (Siphonaptera) parasitic on small mammals

Animal species with larger local populations tend to be widespread across many localities, whereas species with smaller local populations occur in fewer localities. This pattern is well documented for free-living species and can be explained by the resource breadth hypothesis: the attributes that enable a species to exploit a diversity of resources allow it to attain a broad distribution and high local density. In contrast, for parasitic organisms, the trade-off hypothesis predicts that parasites exploiting many host species will achieve lower mean abundance on those hosts than more host-specific parasites because of the costs of adaptations against multiple defense systems. We test these alternative hypotheses with data on host specificity and abundance of fleas parasitic on small mammals from 20 different regions. Our analyses controlled for phylogenetic influences, differences in host body surface area, and sampling effort. In most regions, we found significant positive relationships between flea abundance and either the number of host species they exploited or the average taxonomic distance among those host species. This was true whether we used mean flea abundance or the maximum abundance they achieved on their optimal host. Although fleas tended to exploit more host species in regions with either larger number of available hosts or more taxonomically diverse host faunas, differences in host faunas between regions had no clear effect on the abundance-host specificity relationship. Overall, the results support the resource breadth hypothesis: fleas exploiting many host species or taxonomically unrelated hosts achieve higher abundance than specialist fleas. We conclude that generalist parasites achieve higher abundance because of a combination of resource availability and stability.     

Specificity and host predictability: a comparative analysis among monogenean parasites of fish

1. This article compares generalist (parasite species found on two or more host species) and specialist (found on only one host species) monogenean parasite species of fish. The reduction of the host range – that is an increase in host specificity – may correspond with a better adaptation of the parasite to a more predictable host environment. A more predictable environment may allow the parasite species to develop specific adaptations.
2. We assume that the more predictable host environment can be evaluated by host body size, since numerous life-traits, such as longevity, are positively correlated with size.
3. We found that specialist parasites parasitize larger hosts species than generalist parasites. We also found a good relationship between host body size and parasite body size for specialist parasite species.
4. An adaptation to the mechanical problems encountered in the host's gill chamber may lead to an increase in parasite body size. The infection of a larger part of the host population in order to decrease the chances of local extinction due to fluctuations of host abundance may be another adaptive mechanism.
5. We found a negative correlation between parasite body size and prevalence for generalist parasite species. This relationship disappeared when using the comparative method controlling for phylogeny, which proved that it was a phylogenetic effect.     

Determinants of distribution and prevalence of avian malaria in blue tit populations across Europe: separating host and parasite effects

Although avian malarial parasites are globally distributed, the factors that affect the geographical distribution and local prevalence of different parasite lineages across host populations or species are still poorly understood. Based on the intense screening of avian malarial parasites in nine European blue tit populations, we studied whether distribution ranges as well as local adaptation, host specialization and phylogenetic relationships can determine the observed prevalences within populations. We found that prevalence differed consistently between parasite lineages and host populations, indicating that the transmission success of parasites is lineage specific but is partly shaped by locality-specific effects. We also found that the lineage-specific estimate of prevalence was related to the distribution range of parasites: lineages found in more host populations were generally more prevalent within these populations. Additionally, parasites with high prevalence that were also widely distributed among blue tit populations were also found to infect more host species. These findings suggest that parasites reaching high local prevalence can also realize wide distribution at a global scale that can have further consequences for host specialization. Although phylogenetic relationships among parasites did not predict prevalence, we detected a close match between a tree based on the geographic distance of the host populations and the parasite phylogenetic tree, implying that neighbouring host populations shared a related parasite fauna.     

Biogeography of avian blood parasites (Leucocytozoon spp.) in two resident hosts across Europe: phylogeographic structuring or the abundance–occupancy relationship?

Relationships between hosts and parasites represent complex co-evolving systems that can vary both temporally and spatially. This variation may result in different phylogeographic outcomes, ranging from highly geographically structured parasite populations comprised of specialist lineages that are locally abundant but have restricted global occupancy to geographically unstructured parasite populations consisting of widespread parasites. Here, we present results from a large biogeographic study of the Leucocytozoon blood parasites of two nonmigrant bird species, conducted at nine sites across Europe. The aim was to determine whether the parasite lineages of the two hosts were phylogeographically structured across Europe. Employing molecular methods, we found a large diversity of parasites, and although overall prevalence varied greatly, the parasites were not genetically structured. Several measures of local parasite abundance were associated with the number of sites that the lineage occurred in, which is consistent with the macroecological phenomenon of the abundance-occupancy relationship. Taken together, our results show that parasite dispersal is somewhat uncoupled to that of the host in this system: we suggest that broad host and/or vector preference may play an important role in determining the distribution of these parasites and in affecting host-parasite coevolution in this system.     

Host and habitat specialization of avian malaria in Africa

Studies of both vertebrates and invertebrates have suggested that specialists, as compared to generalists, are likely to suffer more serious declines in response to environmental change. Less is known about the effects of environmental conditions on specialist versus generalist parasites. Here, we study the evolutionary strategies of malaria parasites (Plasmodium spp.) among different bird host communities. We determined the parasite diversity and prevalence of avian malaria in three bird communities in the lowland forests in Cameroon, highland forests in East Africa and fynbos in South Africa. We calculated the host specificity index of parasites to examine the range of hosts parasitized as a function of the habitat and investigated the phylogenetic relationships of parasites. First, using phylogenetic and ancestral reconstruction analyses, we found an evolutionary tendency for generalist malaria parasites to become specialists. The transition rate at which generalists become specialists was nearly four times as great as the rate at which specialists become generalists. We also found more specialist parasites and greater parasite diversity in African lowland rainforests as compared to the more climatically variable habitats of the fynbos and the highland forests. Thus, with environmental changes, we anticipate a change in the distribution of both specialist and generalist parasites with potential impacts on bird communities.     

Competition promotes the evolution of host generalists in obligate parasites

Ecological theory traditionally predicts that interspecific competition selects for an increase in ecological specialization. Specialization, in turn, is often thought to be an evolutionary ‘dead end,’ with specialist lineages unlikely to evolve into generalist lineages. In host–parasite systems, this specialization can take the form of host specificity, with more specialized parasites using fewer hosts. We tested the hypothesis that specialists are evolutionarily more derived, and whether competition favours specialization, using the ectoparasitic feather lice of doves. Phylogenetic analyses revealed that complete host specificity is actually the ancestral condition, with generalists repeatedly evolving from specialist ancestors. These multiple origins of generalists are correlated with the presence of potentially competing species of the same genus. A competition experiment with captive doves and lice confirmed that congeneric species of lice do, in fact, have the potential to compete in ecological time. Taken together, these results suggest that interspecific competition can favour the evolution of host generalists, not specialists, over macroevolutionary time.     

The evolution of virulence and host specialization in malaria parasites of primates

Parasite virulence, i.e. the damage done to the host, may be a by-product of the parasite's effort to maximize its fitness. Accordingly, several life-history trade-offs may explain interspecific differences in virulence, but such constraints remain little tested in an evolutionary context. In this phylogenetic study of primate malarias, I investigated the relationship between virulence and other parasite life-history traits. I used peak parasitaemia as a proxy for virulence, because it reflected parasite reproductive success and parasite-induced mortality. Peak parasitaemia was higher in specialist than in generalist species, even when confounding life-history traits were controlled. While there was a significant phylogenetic relationship between the number of competitors per host and host specialization, peak parasitaemia was unrelated to within-host competition. Therefore, the key evolutionary factor that favours virulence is host specialization, and the evolutionary success of virulent parasites, such as Plasmodium falciparum , may be better understood when the trade-off in virulence between different hosts is considered. Such phylogenetic results may help us design better protection programmes against malaria.     

Integrating phylogenetic and ecological distances reveals new insights into parasite host specificity

The range of hosts a pathogen infects (host specificity) is a key element of disease risk that may be influenced by both shared phylogenetic history and shared ecological attributes of prospective hosts. Phylospecificity indices quantify host specificity in terms of host relatedness, but can fail to capture ecological attributes that increase susceptibility. For instance, similarity in habitat niche may expose phylogenetically unrelated host species to similar pathogen assemblages. Using a recently proposed method that integrates multiple distances, we assess the relative contributions of host phylogenetic and functional distances to pathogen host specificity (functional–phylogenetic host specificity). We apply this index to a data set of avian malaria parasite (Plasmodium and Haemoproteus spp.) infections from Melanesian birds to show that multihost parasites generally use hosts that are closely related, not hosts with similar habitat niches. We also show that host community phylogenetic ß‐diversity (Pßd) predicts parasite Pßd and that individual host species carry phylogenetically clustered Haemoproteus parasite assemblages. Our findings were robust to phylogenetic uncertainty, and suggest that phylogenetic ancestry of both hosts and parasites plays important roles in driving avian malaria host specificity and community assembly. However, restricting host specificity analyses to either recent or historical timescales identified notable exceptions, including a ‘habitat specialist’ parasite that infects a diversity of unrelated host species with similar habitat niches. This work highlights that integrating ecological and phylogenetic distances provides a powerful approach to better understand drivers of pathogen host specificity and community assembly.     

Plasmodium relictum infection and MHC diversity in the house sparrow (Passer domesticus)

Antagonistic coevolution between hosts and parasites has been proposed as a mechanism maintaining genetic diversity in both host and parasite populations. In particular, the high level of genetic diversity usually observed at the major histocompatibility complex (MHC) is generally thought to be maintained by parasite-driven selection. Among the possible ways through which parasites can maintain MHC diversity, diversifying selection has received relatively less attention. This hypothesis is based on the idea that parasites exert spatially variable selection pressures because of heterogeneity in parasite genetic structure, abundance or virulence. Variable selection pressures should select for different host allelic lineages resulting in population-specific associations between MHC alleles and risk of infection. In this study, we took advantage of a large survey of avian malaria in 13 populations of the house sparrow (Passer domesticus) to test this hypothesis. We found that (i) several MHC alleles were either associated with increased or decreased risk to be infected with Plasmodium relictum, (ii) the effects were population specific, and (iii) some alleles had antagonistic effects across populations. Overall, these results support the hypothesis that diversifying selection in space can maintain MHC variation and suggest a pattern of local adaptation where MHC alleles are selected at the local host population level.     

Diversity and host assemblage of avian haemosporidians in different terrestrial ecoregions of Peru

Characterizing the diversity and structure of host–parasite communities is crucial to understanding their eco-evolutionary dynamics. Malaria and related haemosporidian parasites are responsible for fitness loss and mortality in bird species worldwide. However, despite exhibiting the greatest ornithological biodiversity, avian haemosporidians from Neotropical regions are quite unexplored. Here, we analyze the genetic diversity of bird haemosporidian parasites (Plasmodium and Haemoproteus) in 1,336 individuals belonging to 206 bird species to explore for differences in diversity of parasite lineages and bird species across 5 well-differentiated Peruvian ecoregions. We detected 70 different haemosporidian lineages infecting 74 bird species. We showed that 25 out of the 70 haplotypes had not been previously recorded. Moreover, we also identified 81 new host–parasite interactions representing new host records for these haemosporidian parasites. Our outcomes revealed that the effective diversity (as well as the richness, abundance, and Shannon–Weaver index) for both birds and parasite lineages was higher in Amazon basin ecoregions. Furthermore, we also showed that ecoregions with greater diversity of bird species also had high parasite richness, hence suggesting that host community is crucial in explaining parasite richness. Generalist parasites were found in ecoregions with lower bird diversity, implying that the abundance and richness of hosts may shape the exploitation strategy followed by haemosporidian parasites. These outcomes reveal that Neotropical region is a major reservoir of unidentified haemosporidian lineages. Further studies analyzing host distribution and specificity of these parasites in the tropics will provide important knowledge about phylogenetic relationships, phylogeography, and patterns of evolution and distribution of haemosporidian parasites.     

Specialized avian Haemosporida trade reduced host breadth for increased prevalence

Parasite specialization on one or a few host species leads to a reduction in the total number of available host individuals, which may decrease transmission. However, specialists are thought to be able to compensate by increased prevalence in the host population and increased success in each individual host. Here, we use variation in host breadth among a community of avian Haemosporida to investigate consequences of generalist and specialist strategies on prevalence across hosts. We show that specialist parasites are more prevalent than generalist parasites in host populations that are shared between them. Moreover, the total number of infections of generalist and specialist parasites within the study area did not vary significantly with host breadth. This suggests that specialists can infect a similar number of host individuals as generalists, thus compensating for a reduction in host availability by achieving higher prevalence in a single host species. Specialist parasites also tended to infect older hosts, whereas infections by generalists were biased towards younger hosts. We suggest that this reflects different abilities of generalists and specialists to persist in hosts following infection. Higher abundance and increased persistence in hosts suggest that specialists are more effective parasites than generalists, supporting the existence of a trade‐off between host breadth and average host use among these parasites.     

Host-parasite associations and host-specificity in haemoparasites of reed bed passerines

The host specificity and host sharing of avian haemoparasites (genera Haemoproteus and Plasmodium) is still poorly known, although they infect a large proportion of several studied bird populations. This study used molecular techniques to detect haemoparasites in marsh warblers and in other passerines that feed in reed beds, at 4 sites in Portugal. The host-specificity of the parasite lineages was analysed and compared with other cases described in the literature to assess whether apparent host specificity changes according to the studied system. Nine lineages of Haemoproteus and 15 of Plasmodium were found, of which only 10 Plasmodium were proven to have local transmission. Each lineage was confined to a distinct set of host species. The distribution of parasites in the host species was non-nested, meaning that specialist lineages did not always share hosts with generalists. The most prevalent lineages were those with a wider host range, indicating that the ability to infect more hosts will enhance a parasite's prevalence in its entire host range. We also found that in our areas, a specialist parasite (H. MW1) appears to have a more generalist character than described in the literature, suggesting that a parasite's apparent specialization can depend on the type of host species sampled.     

Host specificity in spinturnicid mites: do parasites share a long evolutionary history with their host?

Host specificity in parasites can be explained by spatial isolation from other potential hosts or by specialization and speciation of specific parasite species. The first assertion is based on allopatric speciation, the latter on differential lifetime reproductive success on different available hosts. We investigated the host specificity and cophylogenetic histories of four sympatric European bat species of the genus Myotis and their ectoparasitic wing mites of the genus Spinturnix. We sampled >40 parasite specimens from each bat species and reconstructed their phylogenetic COI trees to assess host specificity. To test for cospeciation, we compared host and parasite trees for congruencies in tree topologies. Corresponding divergence events in host and parasite trees were dated using the molecular clock approach. We found two species of wing mites to be host specific and one species to occur on two unrelated hosts. Host specificity cannot be explained by isolation of host species, because we found individual parasites on other species than their native hosts. Furthermore, we found no evidence for cospeciation, but for one host switch and one sorting event. Host‐specific wing mites were several million years younger than their hosts. Speciation of hosts did not cause speciation in their respective parasites, but we found that diversification of recent host lineages coincided with a lineage split in some parasites.