Leslie R. Noble

Environmental context explains Lévy and Brownian movement patterns of marine predators.

An optimal search theory, the so-called Lévy-flight foraging hypothesis, predicts that predators should adopt search strategies known as Lévy flights where prey is sparse and distributed unpredictably, but that Brownian movement is sufficiently efficient for locating abundant prey. Empirical studies have generated controversy because the accuracy of statistical methods that have been used to identify Lévy behaviour has recently been questioned. Consequently, whether foragers exhibit Lévy flights in the wild remains unclear. Crucially, moreover, it has not been tested whether observed movement patterns across natural landscapes having different expected resource distributions conform to the theory’s central predictions. Here we use maximum-likelihood methods to test for Lévy patterns in relation to environmental gradients in the largest animal movement data set assembled for this purpose. Strong support was found for Lévy search patterns across 14 species of open-ocean predatory fish (sharks, tuna, billfish and ocean sunfish), with some individuals switching between Lévy and Brownian movement as they traversed different habitat types. We tested the spatial occurrence of these two principal patterns and found Lévy behaviour to be associated with less productive waters (sparser prey) and Brownian movements to be associated with productive shelf or convergence-front habitats (abundant prey). These results are consistent with the Lévy-flight foraging hypothesis, supporting the contention that organism search strategies naturally evolved in such a way that they exploit optimal Lévy patterns.

Sex-biased dispersal of great white sharks

In some respects, these sharks behave more like whales and dolphins than other fish.

Assignment of paternity groups without access to parental genotypes: multiple mating and developmental plasticity in squid

We present a novel approach to investigating sibling relationships and reconstructing parental genotypes from a progeny array. The Bayesian method we have employed is flexible and may be applicable to a variety of situations in addition to the one presented here. While mutation rates and breeding population allele frequencies can be taken into account, the model requires relatively few loci and makes few assumptions. Paternity of 270 veined squid (Loligo forbesi) hatchlings from three egg strings collected from one location was assigned using five microsatellite loci. Paternal and maternal genotypes reconstructed for each of the three strings were identical, strongly indicating that a single female produced the strings that were fertilized by the same four males. The proportion of eggs fertilized was not equal between males in all three strings, with male 1 siring most offspring (up to 68% in string 1), through to male 4 siring the least (as low as 2.4% in string 1). Although temperature had a profound effect on incubation time, paternity did not affect this trait at 12 °C or 8 °C.

Female control of paternity in the internally fertilizing compound ascidian Diplosoma listerianum. II. Investigation of male mating success using RAPD markers

Randomly amplified polymorphic DNA paternity markers were used to assess male success during simultaneous, three-way mating opportunities between cultured clones of the hermaphroditic protochordate Diplosoma listerianum. The previously reported blockage of sperm movement in the oviduct, barring access to the site of fertilization in the ovary, was shown to prevent cross-fertilization between two particular clones. The same mechanism prevents selfing. Direct observation of pairings within a more extensive set of laboratory clones derived from the same natural population indicated that failure of one or both partners of a pair to produce brooded progeny was relatively common. A weak negative correlation was found between the mating success of pairs and their overall genetic similarity estimated from RAPD fingerprints from several primers. The data suggest the operation of a somatic-gametic incompatibility mechanism regulating mating in D. listerianum. This may involve differential phagocytic removal, in the oviduct, of sperm that share self-recognition markers with maternal tissue.

Biomphalaria glabrata transcriptome: cDNA microarray profiling identifies resistant- and susceptible-specific gene expression in haemocytes from snail strains exposed to Schistosoma mansoni

BackgroundBiomphalaria glabrata is an intermediate snail host for Schistosoma mansoni, one of the important schistosomes infecting man. B. glabrata/S. mansoni provides a useful model system for investigating the intimate interactions between host and parasite. Examining differential gene expression between S. mansoni-exposed schistosome-resistant and susceptible snail lines will identify genes and pathways that may be involved in snail defences.ResultsWe have developed a 2053 element cDNA microarray for B. glabrata containing clones from ORESTES (Open Reading frame ESTs) libraries, suppression subtractive hybridization (SSH) libraries and clones identified in previous expression studies. Snail haemocyte RNA, extracted from parasite-challenged resistant and susceptible snails, 2 to 24 h post-exposure to S. mansoni, was hybridized to the custom made cDNA microarray and 98 differentially expressed genes or gene clusters were identified, 94 resistant-associated and 4 susceptible-associated. Quantitative PCR analysis verified the cDNA microarray results for representative transcripts. Differentially expressed genes were annotated and clustered using gene ontology (GO) terminology and Kyoto Encyclopaedia of Genes and Genomes (KEGG) pathway analysis. 61% of the identified differentially expressed genes have no known function including the 4 susceptible strain-specific transcripts. Resistant strain-specific expression of genes implicated in innate immunity of invertebrates was identified, including hydrolytic enzymes such as cathepsin L, a cysteine proteinase involved in lysis of phagocytosed particles; metabolic enzymes such as ornithine decarboxylase, the rate-limiting enzyme in the production of polyamines, important in inflammation and infection processes, as well as scavenging damaging free radicals produced during production of reactive oxygen species; stress response genes such as HSP70; proteins involved in signalling, such as importin 7 and copine 1, cytoplasmic intermediate filament (IF) protein and transcription enzymes such as elongation factor 1α and EF-2.ConclusionProduction of the first cDNA microarray for profiling gene expression in B. glabrata provides a foundation for expanding our understanding of pathways and genes involved in the snail internal defence system (IDS). We demonstrate resistant strain-specific expression of genes potentially associated with the snail IDS, ranging from signalling and inflammation responses through to lysis of proteinacous products (encapsulated sporocysts or phagocytosed parasite components) and processing/degradation of these targeted products by ubiquitination.

Molecular evidence supports an African affinity of the Neotropical freshwater gastropod, Biomphalaria glabrata, Say 1818, an intermediate host for Schistosoma mansoni

Freshwater snails of the genus Biomphalaria, Preston 1910, are the most important and widely distributed intermediate hosts of Schistosoma mansoni, the blood fluke responsible for human intestinal schistosomiasis, in Africa and the Neotropics. S. mansoni is thought to have been imported repeatedly into the Americas during the last 500 years with the African slave trade. Surprisingly, considering that the New and Old World separated 95–106 million years (Myr) ago, the disease rapidly became established due to the presence of endemic susceptible hosts. Reconstructing the phylogenetic relationships within Biomphalaria may provide insights into the successful intercontinental spread of S. mansoni. Parsimony and distance analyses of mitochondrial and nuclear sequences show African taxa to be monophyletic and Neotropical speciesparaphyletic, with Biomphalaria glabrata forming a separate clade from other Neotropical Biomphalaria, and ancestral to the African taxa. A west to east trans–Atlantic dispersal of a B. glabrata–like taxon, possibly as recently as the Plio–Pleistocene (1.8–3.6 Myr ago) according to a general mitochondrial clock, would fit these observations. Vicariance or an African origin for B. glabrata followed by multiple introductions to South America over the past 500 years with the African slave trade seem unlikely explanations. Knowledge of the phylogenetic relationships among important intermediate host species may prove useful in furthering control measures which exploit genetic differences in susceptibility to parasites, and in elucidating the evolution of schistosome resistance.

The expression of immune-regulatory genes in rainbow trout, Oncorhynchus mykiss , during a natural outbreak of proliferative kidney disease (PKD)

Proliferative kidney disease (PKD) is a parasitic infection of salmonid fish characterized by an apparently abnormal immune response to the presence of the myxozoan parasite, Tetracapsuloides bryosalmonae. In order to examine the nature of the immune response at the molecular level, the expression of a range of immune regulatory genes, including cytokines and cyclooxygenase (COX)-2 was examined in naive unexposed fish and in naive fish exposed to parasite-infected water at three points during the course of a natural outbreak of PKD. Since fish with advanced PKD pathology generally exhibit increased susceptibility to secondary infections which is typical of stress/cortisol-mediated immune suppression, a further aim of this work was to examine in vitro the influence of the glucocorticoid cortisol on the bacterial lipopolysaccharide (LPS)-induced expression of the trout cytokine genes studied. Two weeks after the initial sampling, naive exposed fish showed a specific profile of up-regulated tumor necrosis factor (TNF)-alpha2, COX-2 and, to a lesser extent, transforming growth factor (TGF)-beta1 expression. As the disease pathology increased, TNF-alpha2 and COX-2 expression returned to normal levels. Stress levels of cortisol suppressed the LPS inducibility of pro-inflammatory cytokine genes, although TGF-beta1 and TNF-alpha2 appeared to be refractory. These data demonstrate that specific immune responses at the molecular level are affected during PKD infection, with the cortisol suppression of cytokine expression in vitro providing a possible link to PKD-mediated cytokine down-regulation and immune suppression.

Spatial dynamics and expanded vertical niche of blue sharks in oceanographic fronts reveal habitat targets for conservation

Dramatic population declines among species of pelagic shark as a result of overfishing have been reported, with some species now at a fraction of their historical biomass. Advanced telemetry techniques enable tracking of spatial dynamics and behaviour, providing fundamental information on habitat preferences of threatened species to aid conservation. We tracked movements of the highest pelagic fisheries by-catch species, the blue shark Prionace glauca, in the North-east Atlantic using pop-off satellite-linked archival tags to determine the degree of space use linked to habitat and to examine vertical niche. Overall, blue sharks moved south-west of tagging sites (English Channel; southern Portugal), exhibiting pronounced site fidelity correlated with localized productive frontal areas, with estimated space-use patterns being significantly different from that of random walks. Tracked female sharks displayed behavioural variability in diel depth preferences, both within and between individuals. Diel depth use ranged from normal DVM (nDVM; dawn descent, dusk ascent), to reverse DVM (rDVM; dawn ascent, dusk descent), to behavioural patterns where no diel differences were apparent. Results showed that blue sharks occupy some of the most productive marine zones for extended periods and structure diel activity patterns across multiple spatio-temporal scales in response to particular habitat types. In so doing, sharks occupied an extraordinarily broad vertical depth range for their size (1.0–2.0 m fork length), from the surface into the bathypelagic realm (max. dive depth, 1160 m). The space-use patterns of blue sharks indicated they spend much of the time in areas where pelagic longlining activities are often highest, and in depth zones where these fisheries particularly target other species, which could account for the rapid declines recently reported for blue sharks in many parts of the worlds oceans. Our results provide habitat targets for blue shark conservation that may also be relevant to other pelagic species.

Population introgression and differentiation in the great cormorant Phalacrocorax carbo in Europe

Seven hypervariable microsatellite markers were used to genotype individuals from 21 European populations of great cormorant (Phalacrocorax carbo) with the aim of: (i) evaluating levels of pan-European population structuring; and (ii) determining the genetic provenance of birds present in newly formed colonies in southeast England. Significant population differentiation was detected overall, with populations of the ‘North Atlantic’ cormorant subspecies (P.c. carbo) showing greater levels of divergence than populations of the ‘Eurasian’ subspecies (P.c. sinensis). The populations from southeast England, which are of unknown racial origin but within the geographical distribution of the P.c. carbo subspecies, clustered with P.c. sinensis populations in phylogenetic topologies, highlighting the fact that P.c. sinensis individuals were present at these sites. Multivariate analyses (principal component analysis, principal coordinate analysis and discriminant function analysis) indicated that these inland colonies were not comprised solely of P.c. sinensis, but that both subspecies were living sympatrically and were probably hybridizing. The implications for cormorant management and conservation of P.c. sinensis breeding in the UK and of population introgression with P.c. carbo are considerable, and are discussed.

Conservation of a dinucleotide simple sequence repeat locus in sharks

Recent studies indicate that the flanking region and repeat motif structure of conserved microsatellite loci are useful for phylogenetic inference. Most comparative studies of microsatellite loci involve relatively closely related species, however, primarily because primers developed for one species often amplify only related species. We describe an analysis of a microsatellite locus in lamniform sharks that we estimate has been conserved for a billion years. Combined analysis of the flanking sequence and repeat motif structure resulted in a gene tree comparable to those reported from similar analyses of other genes. The conservation of the simple sequence repeat (SSR), and of the sequence flanking the SSR, is explained by a low substitution rate in sharks coupled with the possibility that mutations which interrupt perfect repeats are lost by replication slippage.