Haseeb S. Randhawa

Evolution of parasitism along convergent lines: from ecology to genomics.

SUMMARY From hundreds of independent transitions from a free-living existence to a parasitic mode of life, separate parasite lineages have converged over evolutionary time to share traits and exploit their hosts in similar ways. Here, we first summarize the evidence that, at a phenotypic level, eukaryotic parasite lineages have all converged toward only six general parasitic strategies: parasitoid, parasitic castrator, directly transmitted parasite, trophically transmitted parasite, vector-transmitted parasite or micropredator. We argue that these strategies represent adaptive peaks, with the similarities among unrelated taxa within any strategy extending to all basic aspects of host exploitation and transmission among hosts and transcending phylogenetic boundaries. Then, we extend our examination of convergent patterns by looking at the evolution of parasite genomes. Despite the limited taxonomic coverage of sequenced parasite genomes currently available, we find some evidence of parallel evolution among unrelated parasite taxa with respect to genome reduction or compaction, and gene losses or gains. Matching such changes in parasite genomes with the broad phenotypic traits that define the convergence of parasites toward only six strategies of host exploitation is not possible at present. Nevertheless, as more parasite genomes become available, we may be able to detect clear trends in the evolution of parasitic genome architectures representing true convergent adaptive peaks, the genomic equivalents of the phenotypic strategies used by all parasites.

Monthly variation in the parasite communities of the intertidal fish Scartichthys viridis (Blenniidae) from central Chile: are there seasonal patterns?

Monthly variation in parasite populations and communities, from the blenniid fish Scartichthys viridis, were assessed during two consecutive years in order to examine monthly and seasonal temporal patterns. A total of 969 S. viridis was collected from September 2006 to August 2008 in central Chile. Sample size and fish total length (TL) varied among months. The S. viridis parasite community included 17 parasite taxa, of which five species were present throughout the year: a leech (Piscicolidae gen. sp.), two copepods (Lepeophtheirus zbigniewi and Colobomatus sp.), a monogenean (Microcotyle sp.) and a trematode (Lecithasteridae gen. sp.). The parasite prevalence, abundance and biovolume varied among months. More precisely, the leech and the copepod Colobomatus sp. were the most prevalent and abundant parasites, reaching their maxima between November and January (austral spring–summer). The parasite communities also showed seasonal patterns; prevalence, abundance and species richness of parasites were higher between October and January (spring–summer) than between March and May (autumn–winter). The population and community descriptors of parasites were significantly correlated with fish TL. Consequently, the variation in parasite populations and communities was associated with fish growth throughout the year. Postlarval settlement of S. viridis, in the intertidal rocky pools, occurs in autumn, with fish reaching larger body size in summer.

Determinants and consequences of interspecific body size variation in tetraphyllidean tapeworms

Tetraphyllidean cestodes are cosmopolitan, remarkably host specific, and form the most speciose and diverse group of helminths infecting elasmobranchs (sharks, skates and rays). They show substantial interspecific variation in a variety of morphological traits, including body size. Tetraphyllideans represent therefore, an ideal group in which to examine the relationship between parasite body size and abundance. The individual and combined effects of host size, environmental temperature, host habitat, host environment, host physiology, and host type (all likely correlates of parasite body size) on parasite length were assessed using general linear model analyses using data from 515 tetraphyllidean cestode species (182 species were included in analyses). The relationships between tetraphyllidean cestode length and intensity and abundance of infection were assessed using simple linear regression analyses. Due to the contrasting morphologies between shark and batoid hosts, and contrasting physiologies between sharks of the Lamnidae family and other sharks, analyses were repeated in different subsets based on host morphology and physiologies (“sharks” vs. batoids) to determine the influence of these variables on adult tetraphyllidean tapeworm body size. Results presented herein indicate that host body size, environmental temperature and host habitat are relatively important variables in models explaining interspecific variations in tetraphyllidean tapeworm length. In addition, a negative relationship between tetraphyllidean body size and intensity of infection was apparent. These results suggest that space constraints and ambient temperature, via their effects on metabolism and growth, determine adult tetraphyllidean cestode size. Consequently, a trade-off between size and numbers is possibly imposed by external forces influencing host size, hence limiting physical space or other resources available to the parasites.

Insights Using a Molecular Approach Into the Life Cycle of a Tapeworm Infecting Great White Sharks

Abstract The great white shark Carcharodon carcharias Linnaeus, 1758 is a versatile and fierce predator (and responsible for many shark attacks on humans). This apex predator feeds on a wide range of organisms including teleosts, other elasmobranchs, cephalopods, pinnipeds, and cetaceans. Although much is known about its diet, no trophic links have been empirically identified as being involved in the transmission of its tapeworm parasites. Recently, the use of molecular tools combined with phylogenetics has proven useful to identify larval and immature stages of marine tapeworms; utilization of the technique has been increasing rapidly. However, the usefulness of this approach remains limited by the availability of molecular data. Here, I employed gene sequence data from the D2 region of the large subunit of ribosomal DNA to link adults of the tapeworm Clistobothrium carcharodoni Dailey and Vogelbein, 1990 (Cestoda: Tetraphyllidea) to larvae for which sequence data for this gene are available. The sequences from the adult tapeworms were genetically identical (0% sequence divergence) to those available on GenBank for “SP” ‘small’ Scolex pleuronectis recovered from the striped dolphin (Stenella coeruleoalba) and Rissos dolphin (Grampus griseus). This study is the first to provide empirical evidence linking the trophic interaction between great white sharks and cetaceans as a definitive route for the successful transmission of a tetraphyllidean tapeworm. Using the intensity of infection data from this shark and from cetaceans as proxies for the extent of predation, I estimate that this individual shark would have consumed between 9 to 83 G. griseus, fresh, dead, or both, in its lifetime.

Missing links: testing the completeness of host-parasite checklists.

Host-parasite checklists are essential resources in ecological parasitology, and are regularly used as sources of data in comparative studies of parasite species richness across host species, or of host specificity among parasite species. However, checklists are only useful datasets if they are relatively complete, that is, close to capturing all host-parasite associations occurring in a particular region. Here, we use three approaches to assess the completeness of 25 checklists of metazoan parasites in vertebrate hosts from various geographic regions. First, treating checklists as interaction networks between a set of parasite species and a set of host species, we identify networks with a greater connectance (proportion of realized host-parasite associations) than expected for their size. Second, assuming that the cumulative rise over time in the number of known host-parasite associations in a region tends toward an asymptote as their discovery progresses, we attempt to extrapolate the estimated total number of existing associations. Third, we test for a positive correlation between the number of published reports mentioning an association and the time since its first record, which is expected because observing and reporting host-parasite associations are frequency-dependent processes. Overall, no checklist fared well in all three tests, and only three of 25 passed two of the tests. These results suggest that most checklists, despite being useful syntheses of regional host-parasite associations, cannot be used as reliable sources of data for comparative analyses.

Genetic and phenotypic influences on clone-level success and host specialization in a generalist parasite

Studying resource specialization at the individual level can identify factors constraining the evolution of generalism. We quantified genotypic and phenotypic variability among infective stages of 20 clones of the parasitic trematode Maritrema novaezealandensis and measured their infection success and post‐infection fitness (growth, egg output) in several crabs and amphipods. First, different clones varied in their infection success of different crustaceans. Second, neither genetic nor phenotypic traits had consistent effects on infection success across all host species. Although the results suggest a relationship between infection success and phenotypic variability, phenotypically variable clones were not better at infecting more host species than less variable ones. Third, genetic and phenotypic traits also showed no consistent correlations with post‐infection fitness measures. Overall, we found no consistent clone‐level specialization, with some clones acting as specialists and others, generalists. The trematode population therefore maintains an overall generalist strategy by comprising a mixture of clone‐level specialists and generalists.

Determinants of Host Specificity and Comments on Attachment Site Specificity of Tetraphyllidean Cestodes Infecting Rajid Skates from the Northwest Atlantic

The objectives of this study were to (1) describe the host range for 6 tetraphyllidean species and quantify their host specificity using 5 specificity indices; (2) determine the role of morphological determinants in the host specificity of tetraphyllideans by comparing villar and bothridial measurements of species examined herein; and (3) determine the role of a physiological component in the host specificity of tetraphyllideans by exposing tetraphyllideans to blood sera from different fish species and other solutions. Our results indicate that Echeneibothrium dubium abyssorum (ex Amblyraja radiata), Echeneibothrium canadensis (ex A. radiata), and Zyxibothrium kamienae (ex Malacoraja senta) exhibit the highest degree of specificity, followed by Echeneibothrium vernetae (ex Leucoraja erinacea and Leucoraja ocellata), Pseudanthobothrium hanseni (ex A. radiata and M. senta), and Pseudanthobothrium purtoni (ex Leucoraja erinacea and L. ocellata). However, these results vary based on the specificity index used. Compatible bothridial and villar measurements indicate that there is no morphological determinant of host specificity but that there is a morphological determinant to attachment site specificity. Our data indicate that attachment site specificity may also be phylogenetically determined. Additionally, the exposure of parasites to blood sera from various hosts confirms that host specificity in this system has a physiological determinant. Therefore, host specificity in this system is determined, at least in part, by physiological factors, whereas attachment site specificity is an extension of host specificity and is phylogenetically determined.

Parasites of polychaetes and their impact on host survival in Otago Harbour, New Zealand

Parasitism is increasingly recognized as an important determinant of population dynamics, productivity and community structure in intertidal ecosystems, and yet there is very little known about the effect of parasites on polychaetes, which represent a major component of the benthic fauna. We surveyed 11 polychaete species from a mudflat in Otago Harbour, New Zealand, and found that seven of these were infected by five parasite species: four trematodes and one apicomplexan gregarine. The gregarine found in Spirobranchus cariniferus and a strigeid trematode using Streblosoma toddae as its first intermediate host are both likely to have negative fitness impacts on their hosts. Other trematodes found were at the metacercarial stage and thus use polychaetes as second intermediate hosts. The most common, an opecoelid, infected the polychaetes Heteromastus filiformis and Abarenicola affinis at relatively high abundance. There was no indication of parasite-induced mortality in these two hosts based on the relationship between host size and infection intensity. However, a comparison of intact H. filiformis individuals with those that fragmented during collection revealed a significantly higher number of opecoelid metacercariae per segment in the fragments than in the complete individuals, suggesting that infection may compromise the structural integrity of the polychaetes. These results suggest that there exists a great diversity of both trematodes and host– trematode associations within the polychaete fauna, whose ecological impact remains to be quantified.

Student peer review: enhancing formative feedback with a rebuttal

Abstract This study examines the use of peer review in an undergraduate ecology programme, in which students write a research proposal as a grant application, prior to carrying out the research project. Using a theoretical feedback model, we compared teacher and student peer reviews in a double blind exercise, and show how students responded to feedback given by each group. In addition, students wrote a rebuttal for every feedback point before re-drafting and submission. Despite students claiming they could tell if the reviewer was a teacher or student, this was not always the case, and both student and teacher feedback was accepted on merit. Analysis of feedback types and rebuttal actions showed similar patterns between students and teachers. Where teachers differed slightly was in the use of questions and giving direction. Interviews with students showed the rebuttal was a novel experience, because it required a consideration of each comment and justification as to why it was accepted, partially accepted or rejected. Being a reviewer helped students to learn about their own work, and it changed the way they understood the scientific literature. In addition, some students transferred their new peer review skills to help others outside of the ecology programme.

Factors influencing spatial variation and abundance of a mermithid parasite in sand hoppers

The impact of parasites on host population dynamics depends on local abundance of the parasites, which may vary considerably across spatial scales. In sand hopper populations, mermithid parasites have major impacts on host dynamics, which may vary among spatially separated populations due to the sand hopper’s wide, patchy distribution. The present study compared the abundance and biomass of a mermithid parasite (Thaumamermis zealandica Poinar et al., 2002) in sand hoppers (Bellorchestia quoyana (Milne-Edwards)) both within and among disconnected beaches. In addition, several variables were measured and tested as potentially important predictors of the parasite abundance and biomass. It was found that geographic isolation may only be responsible for minor differences in parasite populations compared with other factors. Host size was identified as the most important predictor of mermithid parasite abundance, but epibiont abundance, kelp patch mass and host density were poor predictors of abundance. These factors were also poor predictors of parasite biomass in hosts. This study further supports the notion that studies aiming to elucidate population dynamics or patterns should sample thoroughly across both spatial and temporal scales.