Bayesian inference supports the host selection hypothesis in explaining adaptive host specificity by European bitterling

Generalist parasites have the capacity to infect multiple hosts. The temporal pattern of host specificity by generalist parasites is rarely studied, but is critical to understanding what variables underpin infection and thereby the impact of parasites on host species and the way they impose selection on hosts. Here, the temporal dynamics of infection of four species of freshwater mussel by European bitterling fish (Rhodeus amarus) was investigated over three spawning seasons. Bitterling lay their eggs in the gills of freshwater mussels, which suffer reduced growth, oxygen stress, gill damage and elevated mortality as a result of parasitism. The temporal pattern of infection of mussels by European bitterling in multiple populations was examined. Using a Bernoulli Generalized Additive Mixed Model with Bayesian inference it was demonstrated that one mussel species, Unio pictorum, was exploited over the entire bitterling spawning season. As the season progressed, bitterling showed a preference for other mussel species, which were inferior hosts. Temporal changes in host use reflected elevated density-dependent mortality in preferred hosts that were already infected. Plasticity in host specificity by bitterling conformed with the predictions of the host selection hypothesis. The relationship between bitterling and their host mussels differs qualitatively from that of avian brood parasites.     

The role of local adaptation in shaping fish‐mussel coevolution

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Interspecific comparison of movement patterns among bitterling species in an agricultural ditch system

Patterns of movement are related to life history and/or species traits. Understanding movement patterns of multiple species sharing the same niche may clarify coexistence mechanisms. Therefore, the movement patterns of three bitterling species, Acheilognathus tabira erythropterus, Acheilognathus melanogaster, and Rhodeus ocellatus ocellatus, were examined between June and November 2009 in an agricultural ditch system associated with Lake Kasumigaura in central Japan. The mark–recapture method was used with a fixed releasing point in an approximately 5.5 km-long ditch. Movement distances of A. t. erythropterus and A. melanogaster were longer than that of R. o. ocellatus, but the direction of movement was similar among the three species. However, R. o. ocellatus moved to locations with a low dissolved oxygen concentration and deeper water. These results suggest that R. o. ocellatus may adapt better to environmental fluctuations, because its tolerance to hypoxia is the highest of the three species. Compared with R. o. ocellatus, A. t. erythropterus and A. melanogaster may move relatively longer distances to search for suitable habitats following an environmental fluctuation.     

The endangered thick-shelled river mussel (<Emphasis Type="Italic">Unio crassus</Emphasis>): a new host species for the European bitterling (<Emphasis Type="Italic">Rhodeus amarus</Emphasis>)

Large freshwater mussels (Unionoida) are declining throughout the world. The European bitterling Rhodeus amarus (Bloch, 1782) female spawns its eggs inside the unionids’ shells, where fertilisation and further embryonic development take place; thus its reproduction depends fully on the presence of large freshwater mussels. Unio crassus, previously regarded as one of the most numerous unionids in Europe, is now listed in the IUCN Red Data List as being globally endangered. Despite its previous prevalence, it was never reported as a host for the bitterling. A large population of U. crassus was studied in small river at the ?wi?tokrzyskie Mts (Poland), where also electrofishing was conducted. In each bitterling territory located on the study plots, we found individuals of U. crassus, with the bitterling eggs or larvae developing on mussel’s gills. That proves that this species can be also used by the bitterling for reproduction. We suggest that this relationship has not been reported to date due to the mussels’ rarity and ongoing decline. However, it is also possible that the endangered mussel is a novel host for the bitterling, which is expanding its range throughout Europe.     

Mitochondrial and nuclear genetic structure in <Emphasis Type="Italic">Rhodeus ocellatus</Emphasis> (Teleostei: Cyprinidae) with approximate Bayesian computation

The rosy bitterling, Rhodeus ocellatus, is a small freshwater fish belonging to the family Cyprinidae. This species lives in ponds where freshwater mussels are abundant and female lays eggs inside mussels. To understand whether the reproduction mode influenced the phylogeography, our study examined the genetic structure of R. ocellatus using sequences from the mitochondrial DNA (cytochrome b gene and control region) and nuclear DNA (the first intron of ribosomal protein S7 gene). In total, 213 specimens were collected from twelve populations in south of Yangtze River, including Yangtze River, Taiwan and Hainan Islands. The phylogenetic analyses based on mitochondrial and nuclear sequences both showed the lack of a population genetic structure, but all results, including the approximate Bayesian computation approaches, showed that these two markers revealed incongruent historical signals. Our study found that (1) the discordance between these two markers were accounted for admixtures by introduced; (2) the phylogeographic pattern of R. ocellatus and that of other freshwater fish were identical; (3) the reproduction mode was due to that the gene flows among populations were limited; and (4) R. ocellatus colonized in south of the Yangtze River (including) after southeast coastal districts formed and before Taiwan Island reached its present shape by comparing our results with that of the previous studies.     

Direct impact of invasive bivalve (<Emphasis Type="Italic">Sinanodonta woodiana</Emphasis>) parasitism on freshwater fish physiology: evidence and implications

Direct and potentially damaging effects of invasive alien species can remain unnoticed or insufficiently quantified, resulting in a lack of stakeholder awareness. We report for the first time that parasitic larvae (glochidia) of the invasive freshwater mussel Sinanodonta (Anodonta) woodiana (Unionidae, Bivalvia) cause an unexpected reduction in the condition factor of parasitized native fish species. The reduction in the body mass and condition factor of experimentally infested European chub (Squalius cephalus) was associated with changes in several physiological parameters measured in host fish plasma. Ion concentrations (potassium, chloride) and enzymes activities (aspartate aminotransferase, alanine aminotransferase, lactate dehydrogenase, alkaline phosphatase) were significantly affected; hence, the results reveal the complex effects of non-native glochidia on the homeostasis of the individually tested fish. Changes in host physiology and condition status were recorded also in environmentally relevant infestation intensities (mean of 3.02 ± 0.51 glochidia g^?1). Despite intensive concern regarding the negative biodiversity and ecosystem impacts of the adult stage of S. woodiana among conservationists and natural resource managers, potential effects of its larval stage have been neglected until now. Because fish hosts are an obligatory part of the reproductive cycle of the mussel and the main vector for spreading, documentation of this direct and easily quantifiable impact on fish has great potential to influence the key community of stakeholders in fisheries and aquaculture sectors and to serve as a strong motivating factor for invasive species control. We argue for more careful consideration of potential multiple life-stage effects of S. woodiana and of other invasive alien species as well, as different life stages can have highly specific impacts and corresponding relevance for key stakeholder groups.     

Effects of Host Interspecific Interaction in the <Emphasis Type="Italic">Maculinea</Emphasis>–<Emphasis Type="Italic">Myrmica</Emphasis> Parasite–Host System

A model of interspecific host competition in a system with one parasite (butterfly—Maculinea) and multiple potential hosts (ants—Myrmica) is presented. Results indicate that host interspecific competition increases the occurrence of multiple host behaviour in Maculinea natural populations but decreases the ability of the parasite populations to adapt to the most abundant host species. These qualitative predictions were compared with data on host specificity, with good agreement. Analysis of the data also indicates that Maculinea teleius and Maculinea arion respond differently to changes in relative host abundances. Maculinea teleius shows a larger fraction of sites where it displays multiple host behaviour and a larger fraction of sites where the niches of the hosts overlap. In some instances, Maculinea teleius is adapted to Myrmica hosts that are present in lower frequencies. Maculinea arion is locally more host-specific and occurs at sites where host interspecific competition is unlikely and is more frequently adapted to the most abundant host species.     

Rare species of cyclostomata and fish in the Upper Oka basin and within Kaluga oblast

The species list of fish of the Upper Oka basin is verified. Data on biology of rare species are presented (western brook lamprey Lampetra planeri, sterlet Acipenser ruthenus, bystryanka Alburnoides bipunctatus rossicus, asp Aspius aspius, undermouth Chondrostoma variabile, bitterling Rhodeus sericeus, and fresh-water sculpin Cottus gobio koshewnikowi). Their morphological characters, distribution in the Upper Oka basin relative abundances of these species, and its changes during recent decades are also commented.     

Water clearance efficiency indicates potential filter-feeding interactions between invasive <Emphasis Type="Italic">Sinanodonta woodiana</Emphasis> and native freshwater mussels

The Chinese pond mussel (Sinanodonta woodiana Lea, 1834) is a benthic filter-feeder that prefers soft-bottomed freshwater habitats and has successfully spread into both tropical and temperate water bodies outside its natural Southeast Asian range. Due to its preference for nutrient-rich waters with high levels of suspended food particles, the capacity of S. woodiana to influence natural seston concentrations is thought to be relatively low in comparison to that of other invasive bivalves. The experimental quantification of seston removal efficiency reported here demonstrates that S. woodiana is able to reduce seston loads to levels comparable to those by the control native freshwater mussel species Unio tumidus Philipsson, 1788. Moreover, increasing food depletion did not cause detectable changes in the filtration regime of S. woodiana, although the activity of native U. tumidus was significantly reduced. The seston clearance rate (volume of water cleared of particles per unit time) of S. woodiana averaged 9.3 ± 4.0 mL g^?1 wet mass h^?1, which corresponds to the total daily volume of water filtered being up to several hundreds to thousands L m^?2 at the maximal S. woodiana population densities reported in the literature. The observed filtration capacity of S. woodiana and its current invasional spread into areas inhabited by endangered freshwater mussels call for more careful consideration of filter-feeding interactions with native mussels. The potential impacts of S. woodiana should be studied in more detail with respect to available food resources and long-term nutritional needs of native species and reflected in management strategies in the invaded range.     

Consequences of the arms race between <Emphasis Type="Italic">Maculinea teleius</Emphasis> social parasite and <Emphasis Type="Italic">Myrmica</Emphasis> host ants for myrmecophilous butterfly conservation

The arms race between Maculinea butterflies and Myrmica host ants leads to local host-parasite adaptations. In our study, we assessed whether sympatric and allopatric Myrmica scabrinodis populations exhibit behavioural differences towards Maculinea teleius larvae during the adoption-period when butterfly larvae need to be taken inside the Myrmica nest. The second aim was to assess the butterfly survival rate inside ant colonies from different populations. We used one sympatric host population and three allopatric populations: one infested by M. teleius and two uninfested populations. We found that ants from the sympatric population showed a higher number of positive behaviours toward M. teleius larvae during adoption than ants from the allopatric populations. There were no differences in the number of inspection or negative behaviour events. The survival of butterfly larvae was highest inside sympatric host colonies and differed from the survival of M. teleius reared by ants from the allopatric, uninfested populations. No difference was found for the survival rate of M. teleius raised by infested, allopatric host colonies compared to sympatric host populations. Our results suggest the lack of behavioural counter-adaptations of local hosts of M. teleius that more easily adopt and rear butterfly caterpillars compared to naive M. scabrinodis colonies. Our results may also have implications for Maculinea butterfly conservation, especially for reintroduction programmes. We suggest that the existence of behavioural host defences should be checked for the source host population, as well as for the Myrmica population from the reintroduction site. It may also be reasonable to introduce several Myrmica host colonies from the source butterfly host population.     

Lifting the curtain on the freshwater mussel diversity of the Italian Peninsula and Croatian Adriatic coast

Freshwater mussels of the order Unionida have been dramatically declining globally. Despite their ecological importance, conservation of these animals has been hindered by unresolved taxonomy and a lack of data on the distribution and status of populations, especially in southern Europe. Although the Italian Peninsula has been noted as a centre of endemism and one of the major refugia of the glacial ages for several taxa, few studies have been performed on the genetic diversity of Unionida. Most importantly, the taxonomic status of several freshwater mussel populations of the Italian Peninsula is still unresolved. Here we present the first comprehensive dataset for the Unionida of the region spanning Italy and the coastal Croatian region (west of the Dinaric Alps). In total, 191 specimens were collected (85 Anodonta, 64 Unio, 17 Microcondylaea bonellii and 25 Sinanodonta woodiana) from 34 sites across the Italian Peninsula and coastal Croatian river basins for molecular identification (COI, 16S and 28S). Genetic analyses were performed to understand major phylogenetic and phylogeographic patterns. Seven species were detected: three Anodonta species (A. anatina, A. cygnea and A. exulcerata), two Unio species (U. mancus and U. elongatulus), Microcondylaea bonellii, and the invasive Sinanodonta woodiana. The presence of three endemic species (A. exulcerata, U. elongatulus and M. bonellii) confirms the importance of the region as a centre of endemism for freshwater mussels. The Apennine Mountains act as an important biogeographic barrier.     

Rose bitterling (Rhodeus ocellatus) embryos parasitize freshwater mussels by competing for nutrients and oxygen

Spence, R. and Smith, C. 2011. Rose bitterling (Rhodeus ocellatus) embryos parasitize freshwater mussels by competing for nutrients and oxygen. —Acta Zoologica (Stockholm) 00 : 1–6. Understanding how parasites inflict fitness costs on their hosts is a key question in host–parasite biology. Rose bitterling (Rhodeus ocellatus) are small cyprinid fish that place their eggs in the gills of living freshwater mussels. The embryos complete their development inside the mussel gill and emerge as free‐swimming larvae after approximately 4 weeks. Bitterling show a range of specialized adaptations for using mussels as a spawning substrate, and the presence of bitterling embryos has been shown to retard the growth of mussels. We compared the development and survival of embryos incubated in either mussels or Petri dishes and exposed to either nutrient‐rich or nutrient‐poor pond water. Embryonic development rate was significantly faster in Petri dishes, probably as a result of oxygen limitation in mussel gills. Embryo survival rate was significantly higher in nutrient‐rich than filtered water, suggesting that the embryos obtained a nutritional benefit prior to emergence from the host. The results imply that bitterling embryos compete for oxygen and nutrients with their host mussel, as well as each other, and in this way, impose a growth cost on mussels.     

Population-specific responses to an invasive species

Predicting the impacts of non-native species remains a challenge. As populations of a species are genetically and phenotypically variable, the impact of non-native species on local taxa could crucially depend on population-specific traits and adaptations of both native and non-native species. Bitterling fishes are brood parasites of unionid mussels and unionid mussels produce larvae that parasitize fishes. We used common garden experiments to measure three key elements in the bitterling–mussel association among two populations of an invasive mussel (Anodonta woodiana) and four populations of European bitterling (Rhodeus amarus). The impact of the invasive mussel varied between geographically distinct R. amarus lineages and between local populations within lineages. The capacity of parasitic larvae of the invasive mussel to exploit R. amarus was higher in a Danubian than in a Baltic R. amarus lineage and in allopatric than in sympatric R. amarus populations. Maladaptive oviposition by R. amarus into A. woodiana varied among populations, with significant population-specific consequences for R. amarus recruitment. We suggest that variation in coevolutionary states may predispose different populations to divergent responses. Given that coevolutionary relationships are ubiquitous, population-specific attributes of invasive and native populations may play a critical role in the outcome of invasion. We argue for a shift from a species-centred to population-centred perspective of the impacts of invasions.     

The relationship between the freshwater pearl mussel (<Emphasis Type="Italic">Margaritifera margaritifera</Emphasis>) and its hosts

Endangered freshwater pearl mussels Margaritifera margaritifera reveal a complex life cycle with an obligate host-dependent phase. Only two species, Atlantic salmon Salmo salar and brown trout S. trutta, are important hosts in Europe, indicating a high degree of specialization. Whilst freshwater pearl mussels with their filtering activity can provide important ecosystem services and indirectly improve the habitat quality for their salmonid hosts, their direct effects on physiological stress, reduced swimming performance, and increased mortality at high rates of infestation all support a parasitic character of the mussel during its hostdependent phase. From an evolutionary perspective, both the much greater generation time of the parasite compared to the host, as well as the great distribution ranges of M. margaritifera and its hosts should favour local adaptation patterns. The variable suitability of different salmonid strains and species as hosts for M. margaritifera and the resulting differences in the performance of larvae during the host-dependent phase indicate that host-management strategies should focus on maintaining high quality hosts at a regional scale to avoid selection or genetic drift effects which could erode the genetic and evolutionary potential for adaptation to changing environmental conditions.     

Divergence in selection of host species and plant parts among populations of a phytophagous insect

The diversification of phytophagous insects is often attributed to diverging processes of host plant specialization onto different, often closely related, host plants. Some insect clades have diversified by specializing not only on different plant species but also on different plant parts of the same hosts. This is the case in Greya moths (Prodoxidae) where both Greya obscura and G. politella are tightly linked to host plants of the genus Lithophragma (Saxifragaceae). We assess how these species differ in their choice of plants and use of plant parts. Previous work showed that strong local host specialization in G. politella is mediated by floral scent variation among Lithophragma species. Here, we identify geographic variation in host plant use in the close relative G. obscura, relate the emerging patterns to previous studies of geographic variation in host use in G. politella and evaluate potential processes underlying the variation among and within species. First, we show that G. obscura also uses floral chemistry to locate hosts but that additional plant cues must be involved in deciding whether to oviposit on a plant, because females did not discriminate against chemically different host species in no-choice trials. We also found that, although all known populations of G. politella oviposit only in flowers, all G. obscura populations examined here distributed their eggs among both floral and scape tissues both in the field and in laboratory experiments. The distribution of eggs among plant parts, however, varied among moth populations, and also depended on the Lithophragma species they attacked. Together, these results show the potential for phytophagous insect species and populations to diverge in use of plant parts as part of the process of speciation and adaptation. These two layers of specialization enhance the potential for subsequent diversification in phytophagous insect lineages.     

Sex-specific effects of a parasite evolving in a female-biased host population

Background

Males and females differ in many ways and might present different opportunities and challenges to their parasites. In the same way that parasites adapt to the most common host type, they may adapt to the characteristics of the host sex they encounter most often. To explore this hypothesis, we characterized host sex-specific effects of the parasite Pasteuria ramosa, a bacterium evolving in naturally, strongly, female-biased populations of its host Daphnia magna.

Results

We show that the parasite proliferates more successfully in female hosts than in male hosts, even though males and females are genetically identical. In addition, when exposure occurred when hosts expressed a sexual dimorphism, females were more infected. In both host sexes, the parasite causes a similar reduction in longevity and leads to some level of castration. However, only in females does parasite-induced castration result in the gigantism that increases the carrying capacity for the proliferating parasite.

Conclusions

We show that mature male and female Daphnia represent different environments and reveal one parasite-induced symptom (host castration), which leads to increased carrying capacity for parasite proliferation in female but not male hosts. We propose that parasite induced host castration is a property of parasites that evolved as an adaptation to specifically exploit female hosts.

     

The populations of the freshwater pearl mussel, <Emphasis Type="Italic">Margaritifera margaritifera</Emphasis> (Linnaeus, 1758), and the thick shelled river mussel, <Emphasis Type="Italic">Unio crassus</Emphasis> Philipsson, 1788, in Latvia

The populations of two endangered species—the freshwater pearl mussel Margaritifera margaritifera and the thick shelled river mussel Unio crassus in Latvia were studied. The specimens were counted, measured, population density and age structure were calculated. The possible host fish presence was found.     

Spatial and genetic structure of directly-transmitted parasites reflects the distribution of their specific amphibian hosts

Parasite distributions depend on the local environment in which host infection occurs, and the surrounding landscape over which hosts move and transport their parasites. Although host and landscape effects on parasite prevalence and spatial distribution are difficult to observe directly, estimation of such relationships is necessary for understanding the spread of infections and parasite–habitat associations. Although parasite distributions are necessarily nested within host distributions, direct environmental influences on local infection or parasite effects on host dispersal could lead to distinct landscape or habitat relationships relative to their hosts. Our aim was to determine parasite spatial structure across a contiguous prairie by statistical modeling of parasite–landscape relationships combined with analysis of population genetic structure. We sampled northern leopard frogs (Lithobates pipiens) and wood frogs (L. sylvaticus) for host-specific lung nematodes (Rhabdias ranae and R. bakeri; respectively) across the Sheyenne National Grassland in southeastern North Dakota and developed primers for 13 microsatellite loci for Rhabdias. The two Rhabdias species exhibited different correlations with landscape characteristics that conformed with that of their hosts, indicating transmission is driven by host ecology, probably density, and not directly by the environment. There was evidence for localized, patchy spatial genetic structure, but no broader-scale geographic patterns, indicating no barriers to host and parasite dispersal. Nematodes cohabitating in an individual frog were most genetically similar. Worms within the same wetland were also genetically similar, indicating localized transmission and resulting wetland-scale patchiness are not completely obscured by broad-scale host–parasite dispersal. Beyond individual wetlands, we found no evidence of genetic isolation-by-distance or patchiness at the landscape-scale.     

Sleeping site ecology,but not sex,affect ecto- and hemoparasite risk,in sympatric,arboreal primates (<Emphasis Type="Italic">Avahi occidentalis</Emphasis> and <Emphasis Type="Italic">Lepilemur edwardsi</Emphasis>)

Background

A central question in evolutionary parasitology is to what extent ecology impacts patterns of parasitism in wild host populations. In this study, we aim to disentangle factors influencing the risk of parasite exposure by exploring the impact of sleeping site ecology on infection with ectoparasites and vector-borne hemoparasites in two sympatric primates endemic to Madagascar. Both species live in the same dry deciduous forest of northwestern Madagascar and cope with the same climatic constraints, they are arboreal, nocturnal, cat-sized and pair-living but differ prominently in sleeping site ecology. The Western woolly lemur (Avahi occidentalis) sleeps on open branches and frequently changes sleeping sites, whereas the Milne-Edward’s sportive lemur (Lepilemur edwardsi) uses tree holes, displaying strong sleeping site fidelity. Sleeping in tree holes should confer protection from mosquito-borne hemoparasites, but should enhance the risk for ectoparasite infestation with mites and nest-adapted ticks. Sex may affect parasite risk in both species comparably, with males bearing a higher risk than females due to an immunosuppressive effect of higher testosterone levels in males or to sex-specific behavior. To explore these hypotheses, ectoparasites and blood samples were collected from 22 individuals of A. occidentalis and 26 individuals of L. edwardsi during the dry and rainy season.

Results

L. edwardsi, but not A. occidentalis, harbored ectoparasites, namely ticks (Haemaphysalis lemuris [Ixodidae], Ornithodoros sp. [Argasidae]) and mites (Aetholaelaps trilyssa, [Laelapidae]), suggesting that sleeping in tree holes promotes infestation with ectoparasites. Interestingly, ectoparasites were found solely in the hot, rainy season with a prevalence of 75% (N = 16 animals). Blood smears were screened for the presence and infection intensity of hemoparasites. Microfilariae were detected in both species. Morphological characteristics suggested that each lemur species harbored two different filarial species. Prevalence of microfilarial infection was significantly lower in L. edwardsi than in A. occidentalis. No significant difference in infection intensity between the two host species, and no effect of season, daytime of sampling or sex on prevalence or infection intensity was found. In neither host species, parasite infection showed an influence on body weight as an indicator for body condition.

Conclusions

Our findings support that sleeping site ecology affects ectoparasite infestation in nocturnal, arboreal mammalian hosts in the tropics, whereas there is no significant effect of host sex. The influence of sleeping site ecology to vector-borne hemoparasite risk is less pronounced. The observed parasite infections did not affect body condition and thus may be of minor importance for shaping reproductive fitness. Findings provide first evidence for the specific relevance of sleeping site ecology on parasitism in arboreal and social mammals. Further, our results increase the sparse knowledge on ecological drivers of primate host-parasite interactions and transmission pathways in natural tropical environments.

     

Phylogenetic evidence for an ancestral coevolution between a major clade of coccidian parasites and elasmobranch hosts

Cartilaginous fishes are the oldest jawed vertebrates and are also reported to be the hosts of some of the most basal lineages of Cestoda and Aporocotylidae (Digenea) parasites. Recently a phylogenetic analysis of the coccidia (Apicomplexa) infecting marine vertebrates revealed that the lesser spotted dogfish harbours parasite lineages basal to Eimeria Schneider, 1875 and the group formed by Schellackia Reichenow, 1919, Lankesterella Ames, 1923, Caryospora Leger, 1904 and Isospora Schneider, 1881. In the present study we have found additional lineages of coccidian parasites infecting the cownose ray Rhinoptera bonasus Mitchill and the blue shark Prionace glauca Linnaeus. These lineages were also found as basal to species from the genera Lankesterella, Schellackia, Caryospora and Isospora infecting higher vertebrates. These results confirm previous phylogenetic assessments and suggest that these parasitic lineages first evolved in basal vertebrate hosts (i.e. Chondrichthyes), and that the more derived lineages infect higher vertebrates (e.g. birds and mammals) conforming to the evolution of their hosts. We hypothesise that elasmobranchs might host further ancestral parasite lineages harbouring unknown links of parasite evolution.