Evidence for gene flow in parasitic nematodes between two host species of shrews

We describe the genetic structure of populations of the intestinal nematode Longistriata caudabullata (Trichostrongyloidea: Heligmosomidae), a common parasite of short-tailed shrews (genus Blarina, Insectivora: Soricidae). Parasites and hosts were collected from a transect across a contact zone between two species of hosts, Blarina brevicauda and B. hylophaga, in central North America. An 800-base pairs (bp) fragment of the ND4 mitochondrial DNA (mtDNA) gene was sequenced for 28 worms and a 783-bp fragment of the mtDNA control region was analysed for 16 shrews. Phylogenetic analyses of mtDNA sequences revealed reciprocal monophyly for the shrew species, concordant with morphological diagnosis, and supported the idea that the transect cuts through a secondary contact zone between well-differentiated B. brevicauda and B. hylophaga. In contrast to this pattern, the parasitic nematode mtDNA phylogeny was not subdivided according to host affiliation. Genealogical discordance between parasite and host phylogenies suggests extensive gene flow among parasites across the host species boundary.     

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.     

The trophic vacuum and the evolution of complex life cycles in trophically transmitted helminths

Parasitic worms (helminths) frequently have complex life cycles in which they are transmitted trophically between two or more successive hosts. Sexual reproduction often takes place in high trophic-level (TL) vertebrates, where parasites can grow to large sizes with high fecundity. Direct infection of high TL hosts, while advantageous, may be unachievable for parasites constrained to transmit trophically, because helminth propagules are unlikely to be ingested by large predators. Lack of niche overlap between propagule and definitive host (the trophic transmission vacuum) may explain the origin and/or maintenance of intermediate hosts, which overcome this transmission barrier. We show that nematodes infecting high TL definitive hosts tend to have more successive hosts in their life cycles. This relationship was modest, though, driven mainly by the minimum TL of hosts, suggesting that the shortest trophic chains leading to a host define the boundaries of the transmission vacuum. We also show that alternative modes of transmission, like host penetration, allow nematodes to reach high TLs without intermediate hosts. We suggest that widespread omnivory as well as parasite adaptations to increase transmission probably reduce, but do not eliminate, the barriers to the transmission of helminths through the food web.     

Nematode transmission patterns

The transmission of nematode parasites of vertebrates is reviewed with special reference to the phenomena of monoxeny, heteroxeny, paratenesis, and precocity. Monoxeny is divided into 2 types. Primary monoxeny assumes that there was never an intermediate host in the transmission. Secondary monoxeny assumes the loss of an intermediate host during the course of evolution and its replacement by a tissue phase in the final host. Heteroxeny, or the use of intermediate hosts, is a common feature of many nematode groups. The Spirurida utilize arthropods, the Metastrongyloidea molluscs, and Ascaridida arthropods and vertebrates. Paratenesis, or the use of transport hosts, is a common feature of the transmission of nematode parasites of carnivores. It is postulated that in some instances paratenic hosts have become intermediate hosts and replaced the original intermediate host. Precocity in the development of nematodes in intermediate hosts (including what may have been paratenic hosts) is defined as growth and/or development beyond the expected. Its occurrence among the nematode parasites of vertebrates is reviewed. It is regarded as a transmission strategy which accelerates gamete production in the final host. Precocity could also provide the mechanism for the transfer of a parasite from a predator final host to a prey final host.     

Origin and higher-level relationships of psoroptidian mites (Acari: Astigmata: Psoroptidia): evidence from three nuclear genes

Phylogenic relationships of the Psoroptidia, a group of primarily parasitic mites of vertebrates, were investigated based on sequences from three nuclear genes (4.2 kb aligned) sampled from 126 taxa. Several morphological classification schemes and a recent molecular analysis, suggesting that the group may not be monophyletic were statistically rejected by newly generated molecular data, and the results are robust under a range of analytical and partition strategies. Six families Psoroptidae, Lobalgidae (mammalian parasites), Pyroglyphidae (house dust mites and parasites inside feather calamus), Turbinoptidae (upper respiratory track parasites of birds), Psoroptoididae (downy feather mites), and Epidermoptidae (skin parasites of birds) form a well-supported monophyletic group (the epidermoptid-psoroptid complex). These relationships, recovered by combined and separate analyses of all gene partitions, were previously suspected based on some morphological evidence, but evidence has been dismissed as resulting from convergence based on similar parasitic ecologies. The existence of the epidermoptid-psoroptid complex and the statistical rejection of Sarcoptoidea (the morphology-based group joining all mammal-associated mites) indicate that current classification criteria, influenced as they are by host preferences, need to be reassessed for non-pterolichoid superfamilies. However, two of our findings remain sensitive to analytical methods and assumptions: (i) the families Heterocoptidae and Hypoderatidae as the first and second closest outgroups of Psoroptidia, respectively, and (ii) the superfamily Pterolichoidea (including Freyanoidea) forming a sister clade to the remaining psoroptidian superfamilies. Our findings suggest that (i) house dust mites (Pyroglyphidae: Dermatophagoidinae) originated from a parasitic ancestor within the core of Psoroptidia, violating a basic principle of evolution that it is virtually impossible for a permanent parasite to become free-living, and (ii) there were at least two shifts from presumably avian to mammalian hosts.     

Fossils of parasites: what can the fossil record tell us about the evolution of parasitism?

Parasites are common in many ecosystems, yet because of their nature, they do not fossilise readily and are very rare in the geological record. This makes it challenging to study the evolutionary transition that led to the evolution of parasitism in different taxa. Most studies on the evolution of parasites are based on phylogenies of extant species that were constructed based on morphological and molecular data, but they give us an incomplete picture and offer little information on many important details of parasite–host interactions. The lack of fossil parasites also means we know very little about the roles that parasites played in ecosystems of the past even though it is known that parasites have significant influences on many ecosystems. The goal of this review is to bring attention to known fossils of parasites and parasitism, and provide a conceptual framework for how research on fossil parasites can develop in the future. Despite their rarity, there are some fossil parasites which have been described from different geological eras. These fossils include the free‐living stage of parasites, parasites which became fossilised with their hosts, parasite eggs and propagules in coprolites, and traces of pathology inflicted by parasites on the host's body. Judging from the fossil record, while there were some parasite–host relationships which no longer exist in the present day, many parasite taxa which are known from the fossil record seem to have remained relatively unchanged in their general morphology and their patterns of host association over tens or even hundreds of millions of years. It also appears that major evolutionary and ecological transitions throughout the history of life on Earth coincided with the appearance of certain parasite taxa, as the appearance of new host groups also provided new niches for potential parasites. As such, fossil parasites can provide additional data regarding the ecology of their extinct hosts, since many parasites have specific life cycles and transmission modes which reflect certain aspects of the host's ecology. The study of fossil parasites can be conducted using existing techniques in palaeontology and palaeoecology, and microscopic examination of potential material such as coprolites may uncover more fossil evidence of parasitism. However, I also urge caution when interpreting fossils as examples of parasites or parasitism‐induced traces. I point out a number of cases where parasitism has been spuriously attributed to some fossil specimens which, upon re‐examination, display traits which are just as (if not more) likely to be found in free‐living taxa. The study of parasite fossils can provide a more complete picture of the ecosystems and evolution of life throughout Earth's history.     

Are Cuckoos Maximizing Egg Mimicry by Selecting Host Individuals with Better Matching Egg Phenotypes?

Background

Avian brood parasites and their hosts are involved in complex offence-defense coevolutionary arms races. The most common pair of reciprocal adaptations in these systems is egg discrimination by hosts and egg mimicry by parasites. As mimicry improves, more advanced host adaptations evolve such as decreased intra- and increased interclutch variation in egg appearance to facilitate detection of parasitic eggs. As interclutch variation increases, parasites able to choose hosts matching best their own egg phenotype should be selected, but this requires that parasites know their own egg phenotype and select host nests correspondingly.

Methodology/Principal Findings

We compared egg mimicry of common cuckoo Cuculus canorus eggs in naturally parasitized marsh warbler Acrocephalus palustris nests and their nearest unparasitized conspecific neighbors having similar laying dates and nest-site characteristics. Modeling of avian vision and image analyses revealed no evidence that cuckoos parasitize nests where their eggs better match the host eggs. Cuckoo eggs were as good mimics, in terms of background and spot color, background luminance, spotting pattern and egg size, of host eggs in the nests actually exploited as those in the neighboring unparasitized nests.

Conclusions/Significance

We reviewed the evidence for brood parasites selecting better-matching host egg phenotypes from several relevant studies and argue that such selection probably cannot exist in host-parasite systems where host interclutch variation is continuous and overall low or moderate. To date there is also no evidence that parasites prefer certain egg phenotypes in systems where it should be most advantageous, i.e., when both hosts and parasites lay polymorphic eggs. Hence, the existence of an ability to select host nests to maximize mimicry by brood parasites appears unlikely, but this possibility should be further explored in cuckoo-host systems where the host has evolved discrete egg phenotypes.     

Parasites as Drivers and Passengers of Human-Mediated Biological Invasions

We provide an overview of the current state of knowledge of parasites in biological invasions by alien species. Parasites have frequently been invoked as drivers of invasions, but have received less attention as invasion passengers. The evidence to date that parasites drive invasions by hosts is weak: while there is abundant evidence that parasites have effects in the context of alien invasions, there is little evidence to suggest that parasites have differential effects on alien species that succeed versus fail in the invasion process. Particular case studies are suggestive but not yet informative about general effects. What evidence there is for parasites as aliens suggests that the same kind of factors determine their success as for non-parasites. Thus, availability is likely to be an important determinant of the probability of translocation. Establishment and spread are likely to depend on propagule pressure and on the environment being suitable (all necessary hosts and vectors are present); the likelihood of both of these dependencies being favourable will be affected by traits relating to parasite life history and demography. The added complication for the success of parasites as aliens is that often this will depend on the success of their hosts. We discuss how these conclusions help us to understand the likely effects of parasites on the success of establishing host populations (alien or native).

     

Parasites as Drivers and Passengers of Human-Mediated Biological Invasions

We provide an overview of the current state of knowledge of parasites in biological invasions by alien species. Parasites have frequently been invoked as drivers of invasions, but have received less attention as invasion passengers. The evidence to date that parasites drive invasions by hosts is weak: while there is abundant evidence that parasites have effects in the context of alien invasions, there is little evidence to suggest that parasites have differential effects on alien species that succeed versus fail in the invasion process. Particular case studies are suggestive but not yet informative about general effects. What evidence there is for parasites as aliens suggests that the same kind of factors determine their success as for non-parasites. Thus, availability is likely to be an important determinant of the probability of translocation. Establishment and spread are likely to depend on propagule pressure and on the environment being suitable (all necessary hosts and vectors are present); the likelihood of both of these dependencies being favourable will be affected by traits relating to parasite life history and demography. The added complication for the success of parasites as aliens is that often this will depend on the success of their hosts. We discuss how these conclusions help us to understand the likely effects of parasites on the success of establishing host populations (alien or native).     

Strong density-dependent competition and acquired immunity constrain parasite establishment: implications for parasite aggregation

The vast majority of parasites exhibit an aggregated frequency distribution within their host population, such that most hosts have few or no parasites while only a minority of hosts are heavily infected. One exception to this rule is the trophically transmitted parasite Pterygodermatites peromysci of the white-footed mouse (Peromyscus leucopus), which is randomly distributed within its host population. Here, we ask: what are the factors generating the random distribution of parasites in this system when the majority of macroparasites exhibit non-random patterns? We hypothesise that tight density-dependent processes constrain parasite establishment and survival, preventing the build-up of parasites within individual hosts, and preclude aggregation within the host population. We first conducted primary infections in a laboratory experiment using white-footed mice to test for density-dependent parasite establishment and survival of adult worms. Secondary or challenge infection experiments were then conducted to investigate underlying mechanisms, including intra-specific competition and host-mediated restrictions (i.e. acquired immunity). The results of our experimental infections show a dose-dependent constraint on within-host-parasite establishment, such that the proportion of mice infected rose initially with exposure, and then dropped off at the highest dose. Additional evidence of density-dependent competition comes from the decrease in worm length with increasing levels of exposure. In the challenge infection experiment, previous exposure to parasites resulted in a lower prevalence and intensity of infection compared with primary infection of naïve mice; the magnitude of this effect was also density-dependent. Host immune response (IgG levels) increased with the level of exposure, but decreased with the number of worms established. Our results suggest that strong intra-specific competition and acquired host immunity operate in a density-dependent manner to constrain parasite establishment, driving down aggregation and ultimately accounting for the observed random distribution of parasites.     

Age of the last common ancestor of extant Plasmodium parasite lineages

Parasites of the genus Plasmodium infect all classes of amniotes (mammals, birds and reptiles) and display host specificity in their infections. It is therefore generally believed that Plasmodium parasites co-evolved intimately with their hosts. Here, we report that based on an evolutionary analysis using 22 genes in the nuclear genome, extant lineages of Plasmodium parasites originated roughly in the Oligocene epoch after the emergence of their hosts. This timing on the age of the common ancestor of extant Plasmodium parasites suggest the importance of host switches and lends support to the evolutionary scenario of a "malaria big bang" that was proposed based on the evolutionary analysis using the mitochondrial genome.     

Does timing matter? How priority effects influence the outcome of parasite interactions within hosts

In nature, hosts are exposed to an assemblage of parasite species that collectively form a complex community within the host. To date, however, our understanding of how within-host–parasite communities assemble and interact remains limited. Using a larval amphibian host (Pacific chorus frog, Pseudacris regilla) and two common trematode parasites (Ribeiroia ondatrae and Echinostoma trivolvis), we experimentally examined how the sequence of host exposure influenced parasite interactions within hosts. While there was no evidence that the parasites interacted when hosts were exposed to both parasites simultaneously, we detected evidence of both intraspecific and interspecific competition when exposures were temporally staggered. However, the strength and outcome of these priority effects depended on the sequence of addition, even after accounting for the fact that parasites added early in host development were more likely to encyst compared to parasites added later. Ribeiroia infection success was reduced by 14 % when Echinostoma was added prior to Ribeiroia, whereas no such effect was noted for Echinostoma when Ribeiroia was added first. Using a novel fluorescent-labeling technique that allowed us to track Ribeiroia infections from different exposure events, we also discovered that, similar to the interspecific interactions, early encysting parasites reduced the encystment success of later arriving parasites by 41 %, which could be mediated by host immune responses and/or competition for space. These results suggest that parasite identity interacts with host immune responses to mediate parasite interactions within the host, such that priority effects may play an important role in structuring parasite communities within hosts. This knowledge can be used to assess host–parasite interactions within natural communities in which environmental conditions can lead to heterogeneity in the timing and composition of host exposure to parasites.     

Evolution of host egg mimicry in a brood parasite, the great spotted cuckoo

Brood parasitism in birds is one of the best examples of coevolutionary interactions in vertebrates. Coevolution between hosts and parasites is assumed to occur because the parasite imposes strong selection pressures on its hosts, reducing their fitness and thereby favouring counter-adaptations (e.g. egg rejection) which, in turn, select for parasite resistance (e.g. egg mimicry). Great spotted cuckoos ( Clamator glandarius ) are usually considered a brood parasite with eggs almost perfectly mimicking those of their host, the magpie ( Pica pica ). However, Cl. glandarius also exploits South African hosts with very different eggs, both in colour and size, while the Cl. glandarius eggs are similar to those laid in nests of European hosts. Here, we used spectrophotometric techniques for the first time to quantify mimicry of parasitic eggs for eight different host species. We found: (1) non-significant differences in appearance of Cl. glandarius eggs laid in nests of different host species, although eggs laid in South Africa and Europe differed significantly; (2) contrary to the general assumption that Cl. glandarius eggs better mimic those of the main host in Europe ( P. pica ), Cl. glandarius eggs more closely resembled those of the azure-winged magpie ( Cyanopica cyana ), a potential host in which there is no evidence of recent parasitism; (3) the appearance of Cl. glandarius eggs was not significantly related to the appearance of host eggs. We discuss three possible reasons why Cl. glandarius eggs resemble eggs of some of their hosts. We suggest that colouration of Cl. glandarius eggs is an apomorphic trait, and that variation between eggs laid in South African and European host nests is due to genetic isolation among these populations and not due to variation in colouration of host eggs.  © 2003 The Linnean Society of London, Biological Journal of the Linnean Society , 2003, 79 , 551–563.     

Morphometric and genetic variability of Rodentolepis asymmetrica (Hymenolepididae) from the Pyrenean mountains

Rodentolepis asymmetrica (Janicki, 1904), is a common hymenolepidid cestode recorded in several vole species (rodents) in the Palearctic. Here, we report a detailed analysis of this species, which includes metrical features and multilocus enzyme electrophoresis. Worms isolated from 4 species of arvicolid hosts in 3 localities in Spain and France from 1994 to 1997 were studied. All the worms used in the morphological study ranged between I and 5 individuals per host. Furthermore, all individuals were analyzed electrophoretically. Statistical analysis of metrical features in scolex, sexual segments, and eggs was carried out, and significant differences were detected only in sexual structures of mature segments. These differences were found in worms from each host species in different localities and in the same host species in 2 localities. Multivariate statistical analysis shows correct classification of worms in all cases. Surprisingly, we observed a lack of genetic variability at the 11 enzymatic loci analyzed, which could be explained by 2 nonexclusive hypotheses: (1) a preferential selfing mode of reproduction for these parasites, and (2) a weak effective size of parasite populations.     

Parasite diversity declines with host evolutionary distinctiveness: A global analysis of carnivores

Evolutionarily distinctive host lineages might harbor fewer parasite species because they have fewer opportunities for parasite sharing than hosts having extant close relatives, or because diverse parasite assemblages promote host diversification. We evaluate these hypotheses using data from 930 species of parasites reported to infect free‐living carnivores. We applied nonparametric richness estimators to estimate parasite diversity among well‐sampled carnivore species and assessed how well host evolutionary distinctiveness, relative to other biological and environmental factors, explained variation in estimated parasite diversity. Species richness estimates indicate that the current published literature captures less than 50% of the true parasite diversity for most carnivores. Parasite species richness declined with evolutionary distinctiveness of carnivore hosts (i.e., length of terminal ranches of the phylogeny) and increased with host species body mass and geographic range area. We found no support for the hypothesis that hosts from more diverse lineages support a higher number of generalist parasites, but we did find evidence that parasite assemblages might have driven host lineage diversification through mechanisms linked to sexual selection. Collectively, this work provides strong support for host evolutionary history being an essential predictor of parasite diversity, and offers a simple model for predicting parasite diversity in understudied carnivore species.     

Species-specific prevalence of mermithid parasites in populations of six congeneric host caddisflies of Ecnomus McLachlan, 1864 (Trichoptera: Ecnomidae)

Mermithid nematodes are entomophagous parasites and, despite being present in diverse aquatic insects, studies of caddisflies acting as definitive hosts are few and the ecological impacts on host populations are largely unknown. During a four-year study in a stream in southeastern Australia, parasitic mermithid worms were commonly found inside adult caddisflies, but only species of the genus Ecnomus McLachlan, 1864 (Ecnomidae). Ecnomus were the definitive host and parasite prevalence ranged from <1% to nearly 50% across six species. Species-specific prevalence varied little between years and was typically higher in males than in females. Parasite intensity ranged from 1 to 6 (median = 1), but did not vary between species or sexes. Infected hosts could fly, but were castrated and died when worms emerged. High prevalence and virulence (reproductive failure and death of the host) suggests that these parasites could potentially play a role in the population dynamics of some Ecnomus spp.     

Malaria parasites (Apicomplexa,Haematozoea) and their relationships with their hosts: is there an evolutionary cost for the specialization?

Parasite–host specialization is frequently considered to be a derived state such that it represents an 'evolutionary dead end' that strongly limits further evolution. In this study, it was tested whether this theory is applicable to the relationship of malaria parasites and their vertebrate hosts. For this, we revisited Perkins and Schall (2002) analysis of the phylogenetic relationships of the malaria parasites (belonging to the genera Plasmodium , Haemoproteus and Hepatocystis ) based on the mitochondrial Cytochrome b gene sequence, and inferred, using a maximum likelihood (ML) approach, the putative ancestral vertebrate hosts. As the topology in this study presents several unresolved branches and is slightly different from that of Perkins and Schall, a Shimodaira and Hasegawa (SH; 1999) test has been performed in order to properly consider several alternative topologies. The results of this study suggest that the common ancestor of all these malaria parasites was a reptile (more specific of the order Squamata), and that the host switches from Squamata to Aves and vice versa were quite frequent along the evolution of these parasites. On the contrary, a strong evidence that the host shift from Squamata to Mammalia had occurred only once during the evolution of these organisms was found. This evidence (added to the current knowledge about the association of the malaria parasites with their vertebrate hosts) allows us to suggest, at least considering the species included in this study, that the adaptation in mammals had required a high level of specialization. Hence, the acquisition of this host class had culminated in an evolutionary dead end for the mammalian malaria parasites.     

Infection success in novel hosts: an experimental and phylogenetic study of Drosophila-parasitic nematodes

Surprisingly little is known about what determines a parasite's host range, which is essential in enabling us to predict the fate of novel infections. In this study, we evaluate the importance of both host and parasite phylogeny in determining the ability of parasites to infect novel host species. Using experimental lab assays, we infected 24 taxonomically diverse species of Drosophila flies (Diptera: Drosophilidae) with five different nematode species (Tylenchida: Allantonematidae: Howardula, Parasitylenchus), and measured parasite infection success, growth, and effects on female host fecundity (i.e., virulence). These nematodes are obligate parasites of mushroom-feeding Drosophila, particularly quinaria and testacca group species, often with severe fitness consequences on their hosts. We show that the potential host ranges of the nematodes are much larger than their actual ranges, even for parasites with only one known host species in nature. Novel hosts that are distantly related from the native host are much less likely to be infected, but among more closely related hosts, there is much variation in susceptibility. Potential host ranges differ greatly between the related parasite species. All nematode species that successfully infected novel hosts produced infective juveniles in these hosts. Most novel infections did not result in significant reductions in the fecundity of female hosts, with one exception: the host specialist Parasitylenchus nearcticus sterilized all quinaria group hosts, only one of which is a host in nature. The large potential host ranges of these parasites, in combination with the high potential for host colonization due to shared mushroom breeding sites, explain the widespread host switching observed in comparisons of nematode and Drosophila phylogenies.     

Host resistance and tolerance of parasitic gut worms depend on resource availability

Resource availability can significantly alter host–parasite dynamics. Abundant food can provide more resources for hosts to resist infections, but also increase host tolerance of infections by reducing competition between hosts and parasites for food. Whether abundant food favors host resistance or tolerance (or both) might depend on the type of resource that the parasite exploits (e.g., host tissue vs. food), which can vary based on the stage of infection. In our study, we evaluated how low and high resource diets affect Cuban tree frog (Osteopilus septentrionalis) resistance and tolerance of a skin-penetrating, gut nematode Aplectana sp. at each stage of the infection. Compared to a low resource diet, a high resource diet enhanced frog resistance to worm penetration and tolerance while worms traveled to the gut. In contrast, a low resource diet increased resistance to establishment of the infection. After the infection established and worms could access food resources in the gut, a high resource diet enhanced host tolerance of parasites. On a high resource diet, parasitized frogs consumed significantly more food than non-parasitized frogs; when food was then restricted, mass of non-parasitized frogs did not change, whereas mass of parasitized frogs decreased significantly. Thus, a high resource diet increased frog tolerance of established worms because frogs could fully compensate for energy lost to the parasites. Our study shows that host–parasite dynamics are influenced by the effect of resource availability on host resistance and tolerance, which depends on when parasites have access to food and the stage of infection.