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1.  Identification of candidate mimicry proteins involved in parasite-driven phenotypic changes 
Parasites & Vectors  2015;8:225.
Endoparasites with complex life cycles are faced with several biological challenges, as they need to occupy various ecological niches throughout their development. Host phenotypes that increase the parasite’s transmission rate to the next host have been extensively described, but few mechanistic explanations have been proposed to describe their proximate causes. In this study we explore the possibility that host phenotypic changes are triggered by the production of mimicry proteins from the parasite by using an ecological model system consisting of the infection of the threespine stickleback (Gasterosteus aculeatus) by the cestode Schistocephalus solidus.
Using RNA-seq data, we assembled 9,093 protein-coding genes from which ORFs were predicted to generate a reference proteome. Based on a previously published method, we built two complementary analysis pipelines to i) establish a general classification of protein similarity among various species (pipeline A) and ii) identify candidate mimicry proteins showing specific host-parasite similarities (pipeline B), a key feature underlying the possibility of molecular mimicry.
Ninety-four tapeworm proteins showed high local sequence homology with stickleback proteins. Four of these candidates correspond to secreted or membrane proteins that could be produced by the parasite and eventually be released in or be in contact with the host to modulate physiological pathways involved in various phenotypes (e.g. behaviors). One of these candidates belongs to the Wnt family, a large group of signaling molecules involved in cell-to-cell interactions and various developmental pathways. The three other candidates are involved in ion transport and post-translational protein modifications. We further confirmed that these four candidates are expressed in three different developmental stages of the cestode by RT-PCR, including the stages found in the host.
In this study, we identified mimicry candidate peptides from a behavior-altering cestode showing specific sequence similarity with host proteins. Despite their potential role in modulating host pathways that could lead to parasite-induced phenotypic changes and despite our confirmation that they are expressed in the developmental stage corresponding to the altered host behavior, further investigations will be needed to confirm their mechanistic role in the molecular cross-talk taking place between S. solidus and the threespine stickleback.
Electronic supplementary material
The online version of this article (doi:10.1186/s13071-015-0834-1) contains supplementary material, which is available to authorized users.
PMCID: PMC4407394  PMID: 25888917
Parasites; Schistocephalus solidus; Cestodes; Ecological genomics; Genomics/proteomics; Molecular mimicry; Host-parasite interactions; Wnt; RT-PCR
2.  Extensive Behavioural Divergence following Colonisation of the Freshwater Environment in Threespine Sticklebacks 
PLoS ONE  2014;9(6):e98980.
Colonisation of novel environments means facing new ecological challenges often resulting in the evolution of striking divergence in phenotypes. However, little is known about behavioural divergence following colonisation, despite the predicted importance of the role of behavioural phenotype-environment associations in adaptive divergence. We studied the threespine stickleback (Gasterosteus aculeatus), a model system for postglacial colonisation of freshwater habitats largely differing in ecological conditions from the ones faced by the descendants of the marine ancestor. We found that common-environment reared freshwater juveniles were less social, more active and more aggressive than their marine counterparts. This behavioural divergence could represent the result of natural selection that acted on individuals following freshwater colonisation, with predation as a key selection agent. Alternatively, the behavioural profile of freshwater juveniles could represent the characteristics of individuals that preferentially invaded freshwater after the glacial retreat, drawn from the standing variation present in the marine population.
PMCID: PMC4051677  PMID: 24914554
3.  Stable reprogramming of brain transcription profiles by the early social environment in a cooperatively breeding fish 
Adult social behaviour can be persistently modified by early-life social experience. In rodents, such effects are induced by tactile maternal stimulation resulting in neuroendocrine modifications of the hypothalamic–pituitary–adrenal axis involved in stress responsiveness. Whether similar long-term alterations can occur in the hypothalamic–pituitary–interrenal (HPI) axis of poikilothermic vertebrates is unknown. We compared the expression of four genes of the HPI axis in adults of the cooperatively breeding cichlid Neolamprologus pulcher, which had been exposed to two early-life social treatments 1.5 years prior to brain sampling. Fish reared with parents and siblings had less brain expression of corticotropin-releasing factor and of the functional homologue of the mammalian glucocorticoid receptor (GR1) than individuals reared with same-age siblings only. Expression of the mineralocorticoid receptors (MR) did not differ between treatments, but the MR/GR1 expression ratio was markedly higher in fish reared with parents and siblings. Thus, we show here that early social experience can alter the programming of the stress axis in poikilothermic vertebrates, suggesting that this mechanism is deeply conserved within vertebrates. Moreover, we show for the first time that reprogramming of the stress axis of a vertebrate can be induced without tactile stimulation by parents.
PMCID: PMC3574353  PMID: 23269853
early social environment; gene expression; stress response; glucocorticoid receptor; corticotropin-releasing factor; fish
4.  Fish & Chips: Functional Genomics of Social Plasticity in an African Cichlid Fish 
The Journal of experimental biology  2008;211(0 18):3041-3056.
Behaviour and physiology are regulated by both environment and social context. A central goal in the study of the social control of behaviour is to determine the underlying physiological, cellular and molecular mechanisms in the brain. The African cichlid fish Astatotilapia burtoni has long been used as a model system to study how social interactions regulate neural and behavioural plasticity. In this species, males are either socially dominant and reproductively active or subordinate and reproductively suppressed. This phenotypic difference is reversible. Using an integrative approach that combines quantitative behavioural measurements, functional genomics and bioinformatic analyses, we examine neural gene expression in dominant and subordinate males as well as brooding females. We confirm the role of numerous candidate genes that are part of neuroendocrine pathways and show that specific co-regulated gene sets (modules), as well as specific functional Gene Ontology categories, are significantly associated with dominance or reproductive state. Finally, even though the dominant and subordinate phenotypes are robustly defined, we find a surprisingly high degree of individual variation in the transcript levels of the very genes that are differentially regulated between these phenotypes. Our results demonstrate the molecular complexity in the brain underlying social behaviour, identify novel targets for future studies, validate many candidate genes, and exploit individual variation in order to gain biological insights.
PMCID: PMC3728697  PMID: 18775941
cichlid; microarray; social behaviour; behavior
5.  Females of an African Cichlid Fish Display Male-Typical Social Dominance Behavior and Elevated Androgens in the Absence of Males 
Hormones and Behavior  2012;61(4):496-503.
Social environment can affect the expression of sex-typical behavior in both males and females. Males of the African cichlid species Astatotilapia burtoni have long served as a model system to study the neural, endocrine, and molecular basis of socially plastic dominance behavior. Here we show that in all-female communities of A. burtoni, some individuals acquire a male-typical dominance phenotype, including aggressive territorial defense, distinctive color patterns, and courtship behavior. Furthermore, dominant females have higher levels of circulating androgens than either subordinate females or females in mixed-sex communities. These male-typical traits do not involve sex change, nor do the social phenotypes in all-female communities differ in relative ovarian size, suggesting that factors other than gonadal physiology underlie much of the observed variation. In contrast to the well-studied situation in males, dominant and subordinate females do not differ in the rate of somatic growth. Dominant females are not any more likely than subordinates to spawn with an introduced male, although they do so sooner. These results extend the well known extraordinary behavioral plasticity of A. burtoni to the females of this species and provide a foundation for uncovering the neural and molecular basis of social dominance behavior while controlling for factors such as sex, gonadal state and growth.
PMCID: PMC3319202  PMID: 22285646
Aggression; social dominance; sex steroid hormones; reproduction; growth
6.  What can whole genome expression data tell us about the ecology and evolution of personality? 
Consistent individual differences in behaviour, aka personality, pose several evolutionary questions. For example, it is difficult to explain within-individual consistency in behaviour because behavioural plasticity is often advantageous. In addition, selection erodes heritable behavioural variation that is related to fitness, therefore we wish to know the mechanisms that can maintain between-individual variation in behaviour. In this paper, we argue that whole genome expression data can reveal new insights into the proximate mechanisms underlying personality, as well as its evolutionary consequences. After introducing the basics of whole genome expression analysis, we show how whole genome expression data can be used to understand whether behaviours in different contexts are affected by the same molecular mechanisms. We suggest strategies for using the power of genomics to understand what maintains behavioural variation, to study the evolution of behavioural correlations and to compare personality traits across diverse organisms.
PMCID: PMC2992745  PMID: 21078652
gene expression; consistency; individual variation; genetics; behavioural syndrome
7.  Gene-expression signatures of Atlantic salmon’s plastic life cycle 
How genomic expression differs as a function of life history variation is largely unknown. Atlantic salmon exhibits extreme alternative life histories. We defined the gene-expression signatures of wild-caught salmon at two different life stages by comparing the brain expression profiles of mature sneaker males and immature males, and early migrants and late migrants. In addition to life-stage-specific signatures, we discovered a surprisingly large gene set that was differentially regulated - at similar magnitudes, yet in opposite direction - in both life history transitions. We suggest that this co-variation is not a consequence of many independent cellular and molecular switches in the same direction but rather represents the molecular equivalent of a physiological shift orchestrated by one or very few master regulators.
PMCID: PMC2706306  PMID: 19401203
Life history; alternative reproductive tactics; migration; microarrays; gene expression; gene-expression signature; ecological genomics; module
8.  Alternative life histories shape brain gene expression profiles in males of the same population 
Atlantic salmon (Salmo salar) undergo spectacular marine migrations before homing to spawn in natal rivers. However, males that grow fastest early in life can adopt an alternative ‘sneaker’ tactic by maturing earlier at greatly reduced size without leaving freshwater. While the ultimate evolutionary causes have been well studied, virtually nothing is known about the molecular bases of this developmental plasticity. We investigate the nature and extent of coordinated molecular changes that accompany such a fundamental transformation by comparing the brain transcription profiles of wild mature sneaker males to age-matched immature males (future large anadromous males) and immature females. Of the ca. 3000 genes surveyed, 15% are differentially expressed in the brains of the two male types. These genes are involved in a wide range of processes, including growth, reproduction and neural plasticity. Interestingly, despite the potential for wide variation in gene expression profiles among individuals sampled in nature, consistent patterns of gene expression were found for individuals of the same reproductive tactic. Notably, gene expression patterns in immature males were different both from immature females and sneakers, indicating that delayed maturation and sea migration by immature males, the ‘default’ life cycle, may actually result from an active inhibition of development into a sneaker.
PMCID: PMC1559854  PMID: 16087419
microarray; gene expression; plasticity; behaviour; reproduction; brain
9.  Large-scale genetic variation of the symbiosis-required megaplasmid pSymA revealed by comparative genomic analysis of Sinorhizobium meliloti natural strains 
BMC Genomics  2005;6:158.
Sinorhizobium meliloti is a soil bacterium that forms nitrogen-fixing nodules on the roots of leguminous plants such as alfalfa (Medicago sativa). This species occupies different ecological niches, being present as a free-living soil bacterium and as a symbiont of plant root nodules. The genome of the type strain Rm 1021 contains one chromosome and two megaplasmids for a total genome size of 6 Mb. We applied comparative genomic hybridisation (CGH) on an oligonucleotide microarrays to estimate genetic variation at the genomic level in four natural strains, two isolated from Italian agricultural soil and two from desert soil in the Aral Sea region.
From 4.6 to 5.7 percent of the genes showed a pattern of hybridisation concordant with deletion, nucleotide divergence or ORF duplication when compared to the type strain Rm 1021. A large number of these polymorphisms were confirmed by sequencing and Southern blot. A statistically significant fraction of these variable genes was found on the pSymA megaplasmid and grouped in clusters. These variable genes were found to be mainly transposases or genes with unknown function.
The obtained results allow to conclude that the symbiosis-required megaplasmid pSymA can be considered the major hot-spot for intra-specific differentiation in S. meliloti.
PMCID: PMC1298293  PMID: 16283928
10.  Biologically meaningful expression profiling across species using heterologous hybridization to a cDNA microarray 
BMC Genomics  2004;5:42.
Unravelling the path from genotype to phenotype, as it is influenced by an organism's environment, is one of the central goals in biology. Gene expression profiling by means of microarrays has become very prominent in this endeavour, although resources exist only for relatively few model systems. As genomics has matured into a comparative research program, expression profiling now also provides a powerful tool for non-traditional model systems to elucidate the molecular basis of complex traits.
Here we present a microarray constructed with ~4500 features, derived from a brain-specific cDNA library for the African cichlid fish Astatotilapia burtoni (Perciformes). Heterologous hybridization, targeting RNA to an array constructed for a different species, is used for eight different fish species. We quantified the concordance in gene expression profiles across these species (number of genes and fold-changes). Although most robust when target RNA is derived from closely related species (<10 MA divergence time), our results showed consistent profiles for other closely related taxa (~65 MA divergence time) and, to a lesser extent, even very distantly related species (>200 MA divergence time).
This strategy overcomes some of the restrictions imposed on model systems that are of importance for evolutionary and ecological studies, but for which only limited sequence information is available. Our work validates the use of expression profiling for functional genomics within a comparative framework and provides a foundation for the molecular and cellular analysis of complex traits in a wide range of organisms.
PMCID: PMC471549  PMID: 15238158

Results 1-10 (10)