Ecdysteroids in helminths and annelids

Summary

This review focuses on recent research developments in the past three years concerning ecdysteroid biochemistry in helminths and annelids, with emphasis on results reported at the IXth Ecdysone Workshop in Paris, France, in September 1989. During the past three years, most of the research in this area has been concentrated on nematodes, in several species of which the occurrence of ecdysteroids has been demonstrated. Interesting biological effects of exogenously applied ecdysteroids have been discovered on meiotic reinitiation in oocytes of the dog heartworm, Dirofilaria immitis, and on microfilarial production by Brugia pahangi. These effects, together with previous discoveries, demonstrate the feasibility of affecting nematode physiology with exogenously applied ecdysteroids. However, experiments with four species of nematodes in three separate laboratories have failed to demonstrate that nematodes biosynthesize ecdysteroids from cholesterol. Therefore, it remains to be proven whether ecdysteroids are truly endogenous nematode hormones or are merely compounds with strong biological activity. Research with cestodes and trematodes has similarly revealed that ecdysteroids occur in these organisms and that the compounds have possible regulatory roles, but experiments demonstrating endogenous biosynthesis have yet to be performed. Annelids, which are more closely related to insects than helminths, also contain ecdysteroids; recent research has demonstrated the C-20 hydroxylation of ecdysone to 20-hydroxyecdysone, the active moulting hormone of most insects. Experiments to demonstrate this metabolic step in helminths have failed.     

Life history, ecology and parasite community structure in Soviet birds

The paper describes an investigation of parasite richness in relation to host life history and ecology using data from an extensive survey of helminth parasites (cestodes, trematodes and nematodes) in Soviet birds. Correlates of parasite richness (number of parasite species per host species) were sought among 13 life-history variables, 13 ecological variables and one non-biological variable (number of host individuals examined) across a sample of 158 species of host. A statistical method to control for the effects of phylogenetic association was adopted throughout. Parasite richness correlates positively with the number of hosts examined (sample size) in all three parasite groups. Positive correlations (after controlling for the effects of sample size) were also found between host body weight and parasite richness for trematodes and nematodes, but not for cestodes.
A number of ecological variables were associated with parasite richness. However, when the effects of sample size and body weight were controlled for, only a single significant correlation (an association between trematode richness and aquatic habitat) remained. Similarly, a number of significant correlates of parasite richness were found among the life-history variables examined. Though several of these were robust to the confounding effects of sample size, all could be explained by the co-variation between life-history traits and body weight among the host species under investigation.     

Intestinal helminths infection of rats (Ratus norvegicus) in the Belgrade area (Serbia): the effect of sex, age and habitat

SUMMARY: Gastrointestinal helminths of Norway rat (Rattus norvegicus) from the Belgrade area were studied as a part of a wider ecological research of rats in Serbia (data on the distribution, population ecology, economic and epizoothiological-epidemiological importance, and density control). Rats were captured from May 2005 to July 2009 at both urban and suburban-rural sites. Of a total of 302 trapped rats 48% were males and 52% females, with 36.5% and 38.8% of juvenile-subadult individuals, per sex respectively. Intestinal helminth infection was noted in 68.5% of rats, with a higher prevalence in male hosts and in adult individuals. Higher numbers of infected juveniles-subadults were noted in suburban-rural habitats, while an opposite tendency was noted in adult rats. Seven helminth species were recovered, of which five were nematode (Heterakis spumosa, Nippostrongylus brasiliensis, Capillaria sp., Trichuris muns and Syphacia muris) and two cestode species (Hymenolepis diminuta and Rodentolepis fraterna). The most prevalent parasites were Heterakis spumosa (36.7%) and Hymenolepis diminuta (30.5 %). Sex and habitat-related differences were noted in the prevalence of infection with Capillaria sp. and Trichuris muris, while there were no age-related differences in the prevalence of infection with any individual helminth species. Significantly higher prevalence of infection was noted in summer as compared to spring or winter, with a tendency to be higher in autumn as compared to spring. The only significant difference in the prevalence of infection between habitat-related was noted during spring. H. spumosa was most prevalent in summer, while H. diminuta and N. brasiliensis in autumn. The mean intensity of infection with H. spumosa, R. fraterna, S. muris and T muris was higher in autumn than in the other seasons, while N. brasiliensis and Capillaria sp. occured in winter. No more than four helminth species were found in one host.     

Divergence of ovipositor length and egg shape in a brood parasitic bitterling fish through the use of different mussel hosts

Bitterling fishes deposit their eggs on the gills of living mussels using a long ovipositor. We examined whether ovipositor length (OL) and egg shape correlated with differences in host mussel species in the family Unionidae among populations of the tabira bitterling (Acheilognathus tabira) in Japan. Bitterling populations that use mussels in the sub-family Anodontinae possessed longer ovipositors and more elongated eggs than those using mussels of Unioninae, as expected from the difference in host size between the sub-families (anodontine mussels are larger than unionine mussels). Based on a robust phylogeny of A. tabira populations, we demonstrated that the evolution of both OL and egg shape were correlated with host differences, but not with each other, suggesting that these traits have been selected for independently. Our study demonstrates how adaptive traits for brood parasitism may diverge with host shift due to different host availability and/or interspecific competition for hosts.     

Quantifying shape and ecology in avian pedal claws: The relationship between the bony core and keratinous sheath

Terrestrial tetrapods use their claws to interact with their environments in a plethora of ways. Birds in particular have developed a diversity of claw shapes since they are often not bound to terrestrial locomotion and have heterogeneous body masses ranging several orders of magnitude. Numerous previous studies have hypothesized a connection between pedal claw shape and ecological mode in birds, yet have generated conflicting results, spanning from clear ecological groupings based on claw shape to a complete overlap of ecological modes. The majority of these studies have relied on traditional morphometric arc measurements of keratinous sheaths and have variably accounted for likely confounding factors such as body mass and phylogenetic relatedness. To better address the hypothesized relationship between ecology and claw shape in birds, we collected 580 radiographs allowing visualization of the bony core and keratinous sheath shape in 21 avian orders. Geometric morphometrics was used to quantify bony core and keratinous sheath shape and was compared to results using traditional arc measurements. Neither approach significantly separates bird claws into coarse ecological categories after integrating body size and phylogenetic relatedness; however, some separation between ecological groups is evident and we find a gradual shift from the claw shape of ground‐dwelling birds to those of predatory birds. Further, the bony claw core and keratinous sheath are significantly correlated, and the degree of functional integration does not differ across ecological groups. Therefore, it is likely possible to compare fossil bony cores with extant keratinous sheaths after applying corrections. Finally, traditional metrics and geometric morphometric shape are significantly, yet loosely correlated. Based on these results, future workers are encouraged to use geometric morphometric approaches to study claw geometry and account for confounding factors such as body size, phylogeny, and individual variation prior to predicting ecology in fossil taxa.     

Parasites and invasions: a biogeographic examination of parasites and hosts in native and introduced ranges

Aim To use a comparative approach to understand parasite demographic patterns in native versus introduced populations, evaluating the potential roles of host invasion history and parasite life history. Location North American east and west coasts with a focus on San Francisco Bay (SFB). Methods Species richness and prevalence of trematode parasites were examined in the native and introduced ranges of two gastropod host species, Ilyanassa obsoleta and Littorina saxatilis. We divided the native range into the putative source area for introduction and areas to the north and south; we also sampled the overlapping introduced range in SFB. We dissected 14,781 snails from 103 populations and recorded the prevalence and identity of trematode parasites. We compared trematode species richness and prevalence across the hosts’ introduced and native ranges, and evaluated the influence of host availability on observed patterns. Results Relative to the native range, both I. obsoleta and L. saxatilis have escaped (lost) parasites in SFB, and L. saxatilis demonstrated a greater reduction of trematode diversity and infection prevalence than I. obsoleta. This was not due to sampling inequalities between the hosts. Instead, rarefaction curves suggested complete capture of trematode species in native source and SFB subregions, except for L. saxatilis in SFB, where infection was extremely rare. For I. obsoleta, infection prevalence of trematodes using fish definitive hosts was significantly lower in SFB compared to the native range, unlike those using bird hosts. Host availability partly explained the presence of introduced trematodes in SFB. Main conclusions Differential losses of parasite richness and prevalence for the two gastropod host species in their introduced range is probably the result of several mechanistic factors: time since introduction, propagule pressure, vector of introduction, and host availability. Moreover, the recent occurrence of L. saxatilis’ invasion and its active introduction vector suggest that its parasite diversity and distribution will probably increase over time. Our study suggests that host invasion history and parasite life history play key roles in the extent and diversity of trematodes transferred to introduced populations. Our results also provide vital information for understanding community‐level influences of parasite introductions, as well as for disease ecology in general.     

Nippostrongylus brasiliensis: effects of immunity on the pre-intestinal and intestinal larval stages of the parasite

Nippostrongylus brasiliensis: effects of immunity on the pre-intestinal and intestinal larval stages of the parasite. International journal for Parasitology4: 183–191. Migration of the pre-intestinal larval stages of N. brasiliensis was studied in rats undergoing either primary or challenge infections. In rats undergoing a primary infection, more than 67 percent of larvae successfully migrated from the skin to the oesophagus by 70 h after infection, and subsequently over 90 per cent of these larvae became established in the small intestine as sexually mature adults. In immune rats undergoing a second infection, 46 per cent of larvae completed migration to the oesophagus by 70 h and of these, only 1·6 per cent became established in the intestine to produce eggs. These inhibitory effects on the pre-intestinal and intestinal larval stages were even more pronounced in immune rats undergoing a third or fourth infection and in addition, there was a prolonged sojourn and substantial retention of larvae in their lungs. There was no evidence that the immune response had an adverse effect on oesophageal fourth stags larvae as these organisms (obtained from immune donors) were able to establish and develop to maturity when transferred per os to normal animals.Syngeneic transfer of immune mesenteric lymph node cells to normal recipients, caused expulsion of parasites from the intestine but failed to effect migration of pre-intestinal larval stages. The implications of these findings are discussed in the context of current knowledge of the mechanisms of immunity to helminths.     

Evolution and determinants of host specificity in the genus Lamellodiscus (Monogenea)

The evolution and determinants of host specificity in Lamellodiscus species (Monogenea, Diplectanidae) were investigated. The 20 known Mediterranean species were studied, all parasites of fishes from the family Sparidae (Teleostei). An index of specificity, which takes into account the phylogenetic relationships of their fish host species, was defined. The link between specificity and its potential determinants was investigated in a phylogenetic context using the method of independent contrasts. Host specificity in Lamellodiscus species appeared to be highly constrained by phylogeny, but also linked to host size. Mapping specificity onto the parasite phylogenetic tree suggests that specialist species do not represent an evolutionary dead end, and that specialization is not a derived condition. It is hypothesized that the ability to be generalist or specialist in Lamellodiscus is controlled by intrinsic, phylogenetically-related characteristics, and that specialist species tend to use large hosts, which may be more predictable.  © 2002 The Linnean Society of London, Biological Journal of the Linnean Society , 2002, 77, 431−443.     

Parasites on an intertidal Corophium-bed: factors determining the phenology of microphallid trematodes in the intermediate host populations of the mud-snail Hydrobia ulvae and the amphipod Corophium volutator

The phenology of microphallid trematodes within their intermediate hostpopulations has been studied on an intertidal mud flat. The parasites usethe mud snail Hydrobia ulvae and the infaunal amphipod Corophium volutatoras first and secondary intermediate host, respectively. Migratory shorebirdsact as final hosts. Our results show a general trend of decline in thedensity of infected intermediate hosts during both spring and autumn, whichcould mainly be ascribed to shorebird predation. During summer the densityof both infected snails and infected amphipods increased considerably, witha culmination in June within the snail population (1000 infectedm-² and in August within the amphipod population (40 000infected m-². This time lag in parasite occurrence could berelated to (1) the development time of larval trematodes within the snails,(2) higher ambient temperatures in late summer increasing parasitetransmission between snails and amphipods during this period, and (3) ageneral increase in the Corophium population during late summer. Fromsamples collected between 1990 and 1995 it is shown that microphallidtrematodes occasionally may give rise to mass mortality in the amphipodpopulation. The prerequisites for such an event are a high parasiteprevalence within the first intermediate host population and unusually highambient temperatures, facilitating parasite transmission to the secondaryintermediate host, C. volutator.     

Phylogenetic eigenvectors and nonstationarity in the evolution of theropod dinosaur skulls

Despite the long‐standing interest in nonstationarity of both phenotypic evolution and diversification rates, only recently have methods been developed to study this property. Here, we propose a methodological expansion of the phylogenetic signal‐representation (PSR) curve based on phylogenetic eigenvectors to test for nonstationarity. The PSR curve is built by plotting the coefficients of determination R² from phylogenetic eigenvector regression (PVR) models increasing the number of phylogenetic eigenvectors against the accumulated eigenvalues. The PSR curve is linear under a stationary model of trait evolution (i.e. the Brownian motion model). Here we describe the distribution of shifts in the models R² and used a randomization procedure to compare observed and simulated shifts along the PSR curve, which allowed detecting nonstationarity in trait evolution. As an applied example, we show that the main evolutionary pattern of variation in the theropod dinosaur skull was nonstationary, with a significant shift in evolutionary rates in derived oviraptorosaurs, an aberrant group of mostly toothless, crested, birdlike theropods. This result is also supported by a recently proposed Bayesian‐based method (AUTEUR). A significant deviation between Ceratosaurus and Limusaurus terminal branches was also detected. We purport that our new approach is a valuable tool for evolutionary biologists, owing to its simplicity, flexibility and comprehensiveness.     

The evolution of cranial form and function in theropod dinosaurs: insights from geometric morphometrics

Theropod dinosaurs, an iconic clade of fossil species including Tyrannosaurus and Velociraptor, developed a great diversity of body size, skull form and feeding habits over their 160+ million year evolutionary history. Here, we utilize geometric morphometrics to study broad patterns in theropod skull shape variation and compare the distribution of taxa in cranial morphospace (form) to both phylogeny and quantitative metrics of biting behaviour (function). We find that theropod skulls primarily differ in relative anteroposterior length and snout depth and to a lesser extent in orbit size and depth of the cheek region, and oviraptorosaurs deviate most strongly from the "typical" and ancestral theropod morphologies. Noncarnivorous taxa generally fall out in distinct regions of morphospace and exhibit greater overall disparity than carnivorous taxa, whereas large-bodied carnivores independently converge on the same region of morphospace. The distribution of taxa in morphospace is strongly correlated with phylogeny but only weakly correlated with functional biting behaviour. These results imply that phylogeny, not biting function, was the major determinant of theropod skull shape.     

Phylogenetically structured variance in felid bite force: the role of phylogeny in the evolution of biting performance

A key question in evolution is the degree to which morphofunctional complexes are constrained by phylogeny. We investigated the role of phylogeny in the evolution of biting performance, quantified as bite forces, using phylogenetic eigenvector regression. Results indicate that there are strong phylogenetic signals in both absolute and size‐adjusted bite forces, although it is weaker in the latter. This indicates that elimination of size influences reduces the level of phylogenetic inertia and that the majority of the phylogenetic constraint is a result of size. Tracing the evolution of bite force through phylogeny by character optimization also supports this notion, in that relative bite force is randomly distributed across phylogeny whereas absolute bite force diverges according to clade. The nonphylogenetically structured variance in bite force could not be sufficiently explained by species‐unique morphology or by ecology. This study demonstrates the difficulties in identifying causes of nonphylogenetically structured variance in morphofunctional character complexes.     

Trophic Structure of One Deep-sea Benthic Fish Community in the Eastern Canadian Arctic: Application of Food, Parasites and Multivariate Analysis

Synopsis As new arctic marine fisheries develop there is need for a comprehensive ecosystem approach to long-term management. This approach recognizes the importance of community interactions such as food web structure and trophic patterns. We determined whether hierarchical clustering (guild formation) is an effective method of trophic evaluation in deep-sea Artic fish communities using stomach content and parasite data with size class, and evaluated the application of endohelminth communities (parasite species transmitted in the food) as indicators of trophic status. Cluster analysis using food group abundance with size class of fish revealed the presence of 11 guilds within the community, however the same analysis using parasite data showed little correlation between food and parasites. Redundancy analysis (RDA) within the 11 guilds also revealed no significant correlations between food group and parasite abundance suggesting that this type of ordination is not suited for environments containing mainly generalist feeders. RDA of individual taxa without a priori guild designation found that taxa in benthic deep-sea communities are defined by their ability to exploit prey species in more than one habitat zone. Benthic fish species were significantly correlated with benthic food groups and parasites that utilize benthic intermediate hosts whereas benthopelagic–pelagic species fed on a higher diversity of prey species and were infected by a larger number of non-host specific parasites. Eigenanalysis and Monte Carlo results showed that parasites and food groups are highly correlated, indicating that parasite community analysis is an effective tool for predicting feeding strategies in Arctic marine environments. It also suggests that in most cases endoparasite infections alone could be used for trophic evaluation in the absence of stomach content data.     

phylosignal: an R package to measure,test, and explore the phylogenetic signal

Phylogenetic signal is the tendency for closely related species to display similar trait values as a consequence of their phylogenetic proximity. Ecologists and evolutionary biologists are becoming increasingly interested in studying the phylogenetic signal and the processes which drive patterns of trait values in the phylogeny. Here, we present a new R package, phylosignal which provides a collection of tools to explore the phylogenetic signal for continuous biological traits. These tools are mainly based on the concept of autocorrelation and have been first developed in the field of spatial statistics. To illustrate the use of the package, we analyze the phylogenetic signal in pollution sensitivity for 17 species of diatoms.     

Parasites and deleterious mutations: interactions influencing the evolutionary maintenance of sex

The restrictive assumptions associated with purely genetic and purely ecological mechanisms suggest that neither of the two forces, in isolation, can offer a general explanation for the evolutionary maintenance of sex. Consequently, attention has turned to pluralistic models (i.e. models that apply both ecological and genetic mechanisms). Existing research has shown that combining mutation accumulation and parasitism allows restrictive assumptions about genetic and parasite parameter values to be relaxed while still predicting the maintenance of sex. However, several empirical studies have shown that deleterious mutations and parasitism can reduce fitness to a greater extent than would be expected if the two acted independently. We show how interactions between these genetic and ecological forces can completely reverse predictions about the evolution of reproductive modes. Moreover, we demonstrate that synergistic interactions between infection and deleterious mutations can render sex evolutionarily stable even when there is antagonistic epistasis among deleterious mutations, thereby widening the conditions for the evolutionary maintenance of sex.     

Impacts of the swimbladder nematode Anguillicola crassus on Anguilla anguilla: variations in liver and spleen masses

Variations in the liver and spleen masses of the eel Anguilla anguilla were analysed in relation to the parasite load of Anguillicola crassus at autopsy (current infection by swimbladder lumen worms) and in relation to the severity of damage observed in the swimbladder (a way of assessing the intensity of past infections). None of these measures of parasite pressure were shown to account for variation in the relative liver mass, either when controlling for somatic mass or eel age. In marked contrast, a significant increase in spleen size was revealed in eels harbouring many lumen worms and also in eels with severe damage in the swimbladder. Splenic enlargement was nearly two‐fold higher among severely affected eels (harbouring more than seven lumen parasites and showing severe damage in the swimbladder) than among infection‐free eels (no lumen parasites and no pathological signs in the swimbladder). Several possible hypotheses are reviewed before arguing for an adaptive host response involving the haematological and immunological functions of the spleen. Indeed, among eels with no pathological signs in the swimbladder, the relative spleen mass was positively associated with the mass of lumen parasites, which suggests a hyper‐synthesis of blood cells by the spleen in response to the bloodsucking activity of lumen worms. Nevertheless, among eels with no lumen parasites at autopsy, there was still an increase in spleen size in relation to the severity of the swimbladder damage, which also suggests a hyper‐synthesis of splenic immune cells (lymphocytes and macrophages) in reaction to damaged tissues and particularly to larvae in the swimbladder wall.     

Assessing current adaptation and phylogenetic inertia as explanations of trait evolution: the need for controlled comparisons

The determination of whether the pattern of trait evolution observed in a comparative analysis of species data is due to adaptation to current environments, to phylogenetic inertia, or to both of these forces requires that one control for the effects of either force when making an assessment of the evolutionary role of the other. Orzack and Sober (2001) developed the method of controlled comparisons to make such assessments; their implementation of the method focussed on a discretely varying trait. Here, we show that the method of controlled comparisons can be viewed as a meta-method, which can be implemented in many ways. We discuss which recent methods for the comparative analysis of continuously distributed traits can generate controlled comparisons and can thereby be used to properly assess whether current adaptation and/or phylogenetic inertia have influenced a trait's evolution. The implementation of controlled comparisons is illustrated by an analysis of sex-ratio data for fig wasps. This analysis suggests that current adaptation and phylogenetic inertia influence this trait.     

Parasites as biological markers: evolutionary relationships in the heterospecific combination of helminths (monogeneans) and teleosts (Gadidae)

Analysis of the genetic structure (11 loci) of helminth populations (Monogenea, Diclidophora ), parasites of two teleost species (Gadidae, Trisopterus luscus and T. minutus minulus ) which are sympatric in the Atlantic, revealed the existence of two species which were specific to each of the two hosts. A strong genetic similitude was found between one of these species ( Diclidophora luscae ), a parasite of T. luscus and a monogenean population parasitizing a third Gadidae ( Trisopterus minutus capelanus ) in the Mediterranean. These results led to a re-examinination of the evolutionary systematics of the three host taxa of the genus Trisopterus. Genetic analysis showed differences between the two subspecies T. minutus minutus (Atlantic) and T. minutus capelanus (Mediterranean) at eight of the 16 loci studied. However, there was no significant genetic divergence between T. luscus and T.m. capelanus. A new phyletic structure in the genus Trisopterus is proposed and the evolutionary trends within the Gadidae/Monogenea system are discussed.