Regional Variation in Parasite Species Richness and Abundance in the Introduced Range of the Invasive Lionfish,Pterois volitans

Parasites can play an important role in biological invasions. While introduced species often lose parasites from their native range, they can also accumulate novel parasites in their new range. The accumulation of parasites by introduced species likely varies spatially, and more parasites may shift to new hosts where parasite diversity is high. Considering that parasitism and disease are generally more prevalent at lower latitudes, the accumulation of parasites by introduced hosts may be greater in tropical regions. The Indo-Pacific lionfish (Pterois volitans) has become widely distributed across the Western Atlantic. In this study, we compared parasitism across thirteen locations in four regions, spanning seventeen degrees of latitude in the lionfish''s introduced range to examine potential spatial variation in parasitism. In addition, as an initial step to explore how indirect effects of parasitism might influence interactions between lionfish and ecologically similar native hosts, we also compared parasitism in lionfish and two co-occurring native fish species, the graysby grouper, Cephalopholis cruentata, and the lizardfish, Synodus intermedius, in the southernmost region, Panama. Our results show that accumulation of native parasites on lionfish varies across broad spatial scales, and that colonization by ectoparasites was highest in Panama, relative to the other study sites. Endoparasite richness and abundance, on the other hand, were highest in Belize where lionfish were infected by twice as many endoparasite species as lionfish in other regions. The prevalence of all but two parasite species infecting lionfish was below 25%, and we did not detect an association between parasite abundance and host condition, suggesting a limited direct effect of parasites on lionfish, even where parasitism was highest. Further, parasite species richness and abundance were significantly higher in both native fishes compared to lionfish, and parasite abundance was negatively associated with the condition index of the native grouper but not that of the lionfish or lizardfish. While two co-occurring native fishes were more heavily parasitized compared to lionfish in Panama any indirect benefits of differential parasitism requires further investigation. Future parasitological surveys of lionfish across the eastern coast of North America and the Lesser Antilles would further resolve geographic patterns of parasitism in invasive lionfish.     

Specific association between the mites Androlaelaps fahrenholzi (Acari: Laelapidae) and birds Premnoplex brunnescens in Costa Rica: possible evidence of a recent host switch

Androlaelaps fahrenholzi is a common, cosmopolitan mite constituting a species complex. This mite is found in nests or on mammal hosts and occasionally on birds. The specific host association between A. fahrenholzi-like mites and Premnoplex brunnescens in Costa Rica is reported here. Adults (females and males), deutonymphs and protonymphs were found on 14 P. brunnescens examined (prevalence was 100 %) with mean abundance 42 (2–222). The nest environment plays an important role in the evolution of parasites and could explain the evolutionary path of Laelapinae towards parasitism. We hypothesize that the colonization of P. brunnescens took place in this context quite recently, from sympatrically living rodents. Morphology and ecology of A. fahrenholzi from P. brunnescens may constitute at least a new variation of A. fahrenholzi, and possibly a new species.     

The evolution of acceptance and tolerance in hosts of avian brood parasites

Avian brood parasites lay their eggs in the nests of their hosts, which rear the parasite's progeny. The costs of parasitism have selected for the evolution of defence strategies in many host species. Most research has focused on resistance strategies, where hosts minimize the number of successful parasitism events using defences such as mobbing of adult brood parasites or rejection of parasite eggs. However, many hosts do not exhibit resistance. Here we explore why some hosts accept parasite eggs in their nests and how this is related to the virulence of the parasite. We also explore the extent to which acceptance of parasites can be explained by the evolution of tolerance; a strategy in which the host accepts the parasite but adjusts its life history or other traits to minimize the costs of parasitism. We review examples of tolerance in hosts of brood parasites (such as modifications to clutch size and multi‐broodedness), and utilize the literature on host–pathogen interactions and plant herbivory to analyse the prevalence of each type of defence (tolerance or resistance) and their evolution. We conclude that (i) the interactions between brood parasites and their hosts provide a highly tractable system for studying the evolution of tolerance, (ii) studies of host defences against brood parasites should investigate both resistance and tolerance, and (iii) tolerance and resistance can lead to contrasting evolutionary scenarios.     

The evolution of bacterial mutation rates under simultaneous selection by interspecific and social parasitism

Many bacterial populations harbour substantial numbers of hypermutable bacteria, in spite of hypermutation being associated with deleterious mutations. One reason for the persistence of hypermutators is the provision of novel mutations, enabling rapid adaptation to continually changing environments, for example coevolving virulent parasites. However, hypermutation also increases the rate at which intraspecific parasites (social cheats) are generated. Interspecific and intraspecific parasitism are therefore likely to impose conflicting selection pressure on mutation rate. Here, we combine theory and experiments to investigate how simultaneous selection from inter- and intraspecific parasitism affects the evolution of bacterial mutation rates in the plant-colonizing bacterium Pseudomonas fluorescens. Both our theoretical and experimental results suggest that phage presence increases and selection for public goods cooperation (the production of iron-scavenging siderophores) decreases selection for mutator bacteria. Moreover, phages imposed a much greater growth cost than social cheating, and when both selection pressures were imposed simultaneously, selection for cooperation did not affect mutation rate evolution. Given the ubiquity of infectious phages in the natural environment and clinical infections, our results suggest that phages are likely to be more important than social interactions in determining mutation rate evolution.     

Higher parasite richness, abundance and impact in native versus introduced cichlid fishes

Empirical studies suggest that most exotic species have fewer parasite species in their introduced range relative to their native range. However, it is less clear how, ecologically, the loss of parasite species translates into a measurable advantage for invaders relative to native species in the new community. We compared parasitism at three levels (species richness, abundance and impact) for a pair of native and introduced cichlid fishes which compete for resources in the Panama Canal watershed. The introduced Nile tilapia, Oreochromis niloticus, was infected by a single parasite species from its native range, but shared eight native parasite species with the native Vieja maculicauda. Despite acquiring new parasites in its introduced range, O. niloticus had both lower parasite species richness and lower parasite abundance compared with its native competitor. There was also a significant negative association between parasite load (abundance per individual fish) and host condition for the native fish, but no such association for the invader. The effects of parasites on the native fish varied across sites and types of parasites, suggesting that release from parasites may benefit the invader, but that the magnitude of release may depend upon interactions between the host, parasites and the environment.     

Recovery of two exotic parasites,Trichogramma brasiliensis [Hym.: Trichogrammatidae] andEucelatoria bryani [Dip.: Tachinidae] fromHeliothis armigera [Lep.: Noctuidae] in tomato fields

Heliothis armigera (Hübner) is a major pest of several crops especially tomato and pulses in India. Indigenous natural enemies likeCarcelia illota Curr.,Campoletis chlorideae Uchida,Trichogramma chilonis Ishii andHexamermis sp are unable to exert adequate control ofH. armigera in tomato. Field trials were conducted with 2 exotic parasites,Trichogramma brasiliensis (Ashmead) andEucelatoria bryani Sabrosky in tomato fields around Bangalore. Both the parasites were recovered fromH. armigera in tomato fields. Field parasitism inH. armigera byT. brasiliensis ranged from 34.6 to 51.3%. WithE. bryani, the parasitism ranged from 0.0 to 8.0%.     

Natural occurrence of fungal egg parasites of root-knot nematodes, Meloidogyne spp. in organic and integrated vegetable production systems in Spain

A survey was conducted to assess the biodiversity and frequency of infection of fungal egg parasites of Meloidogyne spp. and relate results to soil properties in organic and integrated vegetable production in Spain. Forty sites were sampled at the end of the cropping cycle, 30 under integrated and ten under organic production. Fungal egg parasites were isolated from all organically managed sites and from 73 % sites under integrated production. Species richness and Shannon–Wiener index did not differ between production systems but the percentage of fungal egg parasitism did, as well as soil properties. Percentages of egg parasitism higher than 40 % were found in five and three sites under organic and integrated production, respectively. In all these sites, Pochonia chlamydosporia was present alone or co-occurring with other fungal species. The relative frequency of P. chlamydosporia was positively related to the percentage of parasitism in both production systems.     

Collective defence portfolios of ant hosts shift with social parasite pressure

Host defences become increasingly costly as parasites breach successive lines of defence. Because selection favours hosts that successfully resist parasitism at the lowest possible cost, escalating coevolutionary arms races are likely to drive host defence portfolios towards ever more expensive strategies. We investigated the interplay between host defence portfolios and social parasite pressure by comparing 17 populations of two Temnothorax ant species. When successful, collective aggression not only prevents parasitation but also spares host colonies the cost of searching for and moving to a new nest site. However, once parasites breach the host''s nest defence, host colonies should resort to flight as the more beneficial resistance strategy. We show that under low parasite pressure, host colonies more likely responded to an intruding Protomognathus americanus slavemaker with collective aggression, which prevented the slavemaker from escaping and potentially recruiting nest-mates. However, as parasite pressure increased, ant colonies of both host species became more likely to flee rather than to fight. We conclude that host defence portfolios shift consistently with social parasite pressure, which is in accordance with the degeneration of frontline defences and the evolution of subsequent anti-parasite strategies often invoked in hosts of brood parasites.     

A double-edged sword: parental care increases risk of offspring infection by a maternally vectored parasite

Parental care can protect offspring from predators but can also create opportunities for parents to vector parasites to their offspring. We hypothesized that the risk of infection by maternally vectored parasites would increase with the frequency of mother–offspring contact. Ammophila spp. wasps (Hymenoptera: Sphecidae) build nests in which they rear a single offspring. Ammophila species exhibit varied offspring provisioning behaviours: some species enter the nest once to provision a single, large caterpillar, whereas others enter the nest repeatedly to provision with many smaller caterpillars. We hypothesized that each nest visit increases the risk of offspring parasitism by Paraxenos lugubris (Strepsiptera: Xenidae), whose infectious stages ride on the mother wasp (phoresy) to reach the vulnerable Ammophila offspring. We quantified parasitism risk by external examination of museum-curated Ammophila specimens—the anterior portion of P. lugubris protrudes between the adult host''s abdominal sclerites and reflects infection during the larval stage. As predicted, Ammophila species that receive larger numbers of provisions incur greater risks of parasitism, with nest provisioning behaviour explaining ca 90% of the interspecific variation in mean parasitism. These findings demonstrate that parental care can augment, rather than reduce, the risk of parasite transmission to offspring.     

Facultative social parasitism in the allodapine bee Macrogalea berentyensis

Previous research on social parasitism has largely ignored allodapine social parasites, which is surprising given the huge potential of these bees to provide a better understanding of social parasitism. Macrogalea berentyensis, a species that was previously suggested to be a social parasite, was collected in nests of M. ellioti, and also in nests consisting of only M. berentyensis. These f＇mdings, along with morphological and phylogenetic evidence, show that this species is a facultative social parasite. In the independently living M. berentyensis nests, brood were present that had been reared to an advanced stage, suggesting that： （i） these parasites may be effective at foraging and caring for their brood; or （ii） these nests may be colonies where all the hosts had died, and these parasites had yet to disperse. Macrogalea berentyensis is the closest relative of the facultative social parasite, M. antanosy, and both these species represent the most recent evolutionary origin of social parasitism within the allodapines. Further behavioral research on both these parasitic species would therefore have important implications for the understanding of the evolution of social parasitism.     

Unveiling the Intracellular Survival Gene Kit of Trypanosomatid Parasites

Trypanosomatids are unicellular protozoans of medical and economical relevance since they are the etiologic agents of infectious diseases in humans as well as livestock. Whereas Trypanosoma cruzi and different species of Leishmania are obligate intracellular parasites, Trypanosoma brucei and other trypanosomatids develop extracellularly throughout their entire life cycle. After their genomes have been sequenced, various comparative genomic studies aimed at identifying sequences involved with host cell invasion and intracellular survival have been described. However, for only a handful of genes, most of them present exclusively in the T. cruzi or Leishmania genomes, has there been any experimental evidence associating them with intracellular parasitism. With the increasing number of published complete genome sequences of members of the trypanosomatid family, including not only different Trypanosoma and Leishmania strains and subspecies but also trypanosomatids that do not infect humans or other mammals, we may now be able to contemplate a slightly better picture regarding the specific set of parasite factors that defines each organism''s mode of living and the associated disease phenotypes. Here, we review the studies concerning T. cruzi and Leishmania genes that have been implicated with cell invasion and intracellular parasitism and also summarize the wealth of new information regarding the mode of living of intracellular parasites that is resulting from comparative genome studies that are based on increasingly larger trypanosomatid genome datasets.     

Influence of crucifer cropping system on the parasitism ofPlutella xylostella (Lep., Yponomeutidae) byCotesia plutellae (Hym., Braconidae) andDiadegma semiclausum (Hym., Ichneumonidae)

Field experiments were conducted to study the influence of cabbage monoculture and mixed cropping on the parasitism of diamondback moth,Plutella xylostella (L.), a destructive pest of all crucifers, by 2 larval parasites,Diadegma semiclausum Hellén andCotesia plutellae Kurdjumov. There was no significant difference in parasitism by either species whether cabbage was planted in insecticide-free monoculture or in mixed cropping with 8 noncrucifers which were sprayed twice a week with chemical insecticides mevinphos, methamidophos and permethrin. Population ofP. xylostella increased as the cabbage plants grew older. Parasitism byC. plutellae was higher soon after cabbage transplanting but decreased as the plants grew older. Parasitism byD. semiclausum was very low soon after cabbage planting but increased as the plants grew older. A significant negative correlation was found betwen parasitism byC. plutellae andD. semiclausum. In a caged field study where only one parasite species was used in an individual cage, parasitism ofP. xylostella by both species decreased as theP. xylostella population increased. This is believed to be due to the absence of competition between the two parasites inside the cage. There was no relationship between host-plant age and parasitism ofP. xylostella larvae by either parasite species.     

Parasitism of orangestriped oakworm (Lepidoptera: Saturniidae) eggs in the urban landscape

Orangestriped oakworm, Anisota senatoria (J. E. Smith), has caused widespread defoliation of oak trees in the urban landscape of southeastern Virginia since 1985. Egg masses were collected from 1988 to 1990 to determine the impact of native egg parasites on A. senatoria populations. The most abundant egg parasite was Aprostocetus new sp. and mean egg mass parasitism was 24.6%. The eupelmid Anastatus hirtus (Ashmead), a new host record, parasitized a mean of 11.7% of A. senatoria egg masses. The encyrtid Ooencytrus sp., a new host record, had a mean egg mass parasitism of 0.09%. Inundative releases of Trichogramma minutum (Riley) in 1989 and 1990 did not increase parasitism rates and mean egg mass parasitism was 2.3%. Parasitism of first generation A. senatoria egg masses was higher compared with second generation. The four egg parasites collected in this study parasitized 30% of A. senatoria egg masses and within egg mass parasitism was 7.9%. These relatively low parasitism rates may partially explain the presence of consistently high A. senatoria populations in southeastern Virginia.     

Lack of Phenotypic and Evolutionary Cross-Resistance against Parasitoids and Pathogens in Drosophila melanogaster

Background

When organisms are attacked by multiple natural enemies, the evolution of a resistance mechanism to one natural enemy will be influenced by the degree of cross-resistance to another natural enemy. Cross-resistance can be positive, when a resistance mechanism against one natural enemy also offers resistance to another; or negative, in the form of a trade-off, when an increase in resistance against one natural enemy results in a decrease in resistance against another. Using Drosophila melanogaster, an important model system for the evolution of invertebrate immunity, we test for the existence of cross-resistance against parasites and pathogens, at both a phenotypic and evolutionary level.

Methods

We used a field strain of D. melanogaster to test whether surviving parasitism by the parasitoid Asobara tabida has an effect on the resistance against Beauveria bassiana, an entomopathogenic fungus; and whether infection with the microsporidian Tubulinosema kingi has an effect on the resistance against A. tabida. We used lines selected for increased resistance to A. tabida to test whether increased parasitoid resistance has an effect on resistance against B. bassiana and T. kingi. We used lines selected for increased tolerance against B. bassiana to test whether increased fungal resistance has an effect on resistance against A. tabida.

Results/Conclusions

We found no positive cross-resistance or trade-offs in the resistance to parasites and pathogens. This is an important finding, given the use of D. melanogaster as a model system for the evolution of invertebrate immunity. The lack of any cross-resistance to parasites and pathogens, at both the phenotypic and the evolutionary level, suggests that evolution of resistance against one class of natural enemies is largely independent of evolution of resistance against the other.     

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.     

Differential Water Mite Parasitism,Phenoloxidase Activity,and Resistance to Mites Are Unrelated across Pairs of Related Damselfly Species

Related host species often demonstrate differences in prevalence and/or intensity of infection by particular parasite species, as well as different levels of resistance to those parasites. The mechanisms underlying this interspecific variation in parasitism and resistance expression are not well understood. Surprisingly, few researchers have assessed relations between actual levels of parasitism and resistance to parasites seen in nature across multiple host species. The main goal of this study was to determine whether interspecific variation in resistance against ectoparasitic larval water mites either was predictive of interspecific variation in parasitism for ten closely related species of damselflies (grouped into five “species pairs”), or was predicted by interspecific variation in a commonly used measure of innate immunity (total Phenoloxidase or potential PO activity). Two of five species pairs had interspecific differences in proportions of individuals resisting larval Arrenurus water mites, only one of five species pairs had species differences in prevalence of larval Arrenurus water mites, and another two of five species pairs showed species differences in mean PO activity. Within the two species pairs where species differed in proportion of individuals resisting mites the species with the higher proportion did not have correspondingly higher PO activity levels. Furthermore, the proportion of individuals resisting mites mirrored prevalence of parasitism in only one species pair. There was no interspecific variation in median intensity of mite infestation within any species pair. We conclude that a species’ relative ability to resist particular parasites does not explain interspecific variation in parasitism within species pairs and that neither resistance nor parasitism is reflected by interspecific variation in total PO or potential PO activity.     

Introduced species: domestic mammals are more significant transmitters of parasites to native mammals than are feral mammals

The study of parasitism related to biological invasion has focused on attributes and impacts of parasites as invaders and the impact of introduced hosts on endemic parasitism. Thus, there is currently no study of the attributes of hosts which influence the invasiveness of parasites. We aimed to determine whether the degree of domestication of introduced mammalian species – feral introduced mammals, livestock or pets, hereafter ‘D’ – is important in the spillover of introduced parasites. The literature on introduced parasites of mammals in Chile was reviewed. We designed an index for estimating the relevance of the introduced host species to parasite spillover and determined whether the D of introduced mammals predicted this index. A total of 223 introduced parasite species were found. Our results indicate that domestic mammals have a higher number of introduced parasites and spillover parasites, and the index indicates that these mammals, particularly pets, are more relevant introducers than introduced feral mammals. Further analyses indicated that the higher impact is due to higher parasite richness, a longer time since introduction and wider dispersal, as well as how these mammals are maintained. The greater relevance of domestic mammals is important given that they are basically the same species distributed worldwide and can become the main transmitters of parasites to native mammals elsewhere. This finding also underlines the feasibility of management in order to reduce the transmission of parasites to native fauna through anti-parasitic treatment of domestic mammals, animal-ownership education and the prevention of importing new parasite species.     

Sequencing of the smallest Apicomplexan genome from the human pathogen Babesia microti

We have sequenced the genome of the emerging human pathogen Babesia microti and compared it with that of other protozoa. B. microti has the smallest nuclear genome among all Apicomplexan parasites sequenced to date with three chromosomes encoding ∼3500 polypeptides, several of which are species specific. Genome-wide phylogenetic analyses indicate that B. microti is significantly distant from all species of Babesidae and Theileridae and defines a new clade in the phylum Apicomplexa. Furthermore, unlike all other Apicomplexa, its mitochondrial genome is circular. Genome-scale reconstruction of functional networks revealed that B. microti has the minimal metabolic requirement for intraerythrocytic protozoan parasitism. B. microti multigene families differ from those of other protozoa in both the copy number and organization. Two lateral transfer events with significant metabolic implications occurred during the evolution of this parasite. The genomic sequencing of B. microti identified several targets suitable for the development of diagnostic assays and novel therapies for human babesiosis.     

On the extent and origins of genic novelty in the phylum Nematoda

Background

The phylum Nematoda is biologically diverse, including parasites of plants and animals as well as free-living taxa. Underpinning this diversity will be commensurate diversity in expressed genes, including gene sets associated specifically with evolution of parasitism.

Methods and Findings

Here we have analyzed the extensive expressed sequence tag data (available for 37 nematode species, most of which are parasites) and define over 120,000 distinct putative genes from which we have derived robust protein translations. Combined with the complete proteomes of Caenorhabditis elegans and Caenorhabditis briggsae, these proteins have been grouped into 65,000 protein families that in turn contain 40,000 distinct protein domains. We have mapped the occurrence of domains and families across the Nematoda and compared the nematode data to that available for other phyla. Gene loss is common, and in particular we identify nearly 5,000 genes that may have been lost from the lineage leading to the model nematode C. elegans. We find a preponderance of novelty, including 56,000 nematode-restricted protein families and 26,000 nematode-restricted domains. Mapping of the latest time-of-origin of these new families and domains across the nematode phylogeny revealed ongoing evolution of novelty. A number of genes from parasitic species had signatures of horizontal transfer from their host organisms, and parasitic species had a greater proportion of novel, secreted proteins than did free-living ones.

Conclusions

These classes of genes may underpin parasitic phenotypes, and thus may be targets for development of effective control measures.     

Temporary parasitism of Coriolus spp. by Lenzites betulina: A strategy for domain capture in wood decay fungi

Temporary parasitism by individual of the wood-decaying basidiomycete Lenzites betulina allows them to gain selective access to wood occupied by populations of pioneer basidiomycete colonisers in the genus Coriolus. Pseudotrametes gibbosa is similarly temporarily parasitic on species of Bjerkandera. This strategy facilitates possession by the parasites of a large mycelial domain, which in turn allows them to produce large sporophores with a high reproductive output. This behaviour strongly resembles that of strangler figs and temporary social parasitism in ants.