Genomics for monitoring and understanding species responses to global climate change.

All life forms across the globe are experiencing drastic changes in environmental conditions as a result of global climate change. These environmental changes are happening rapidly, incur substantial socioeconomic costs, pose threats to biodiversity and diminish a species' potential to adapt to future environments. Understanding and monitoring how organisms respond to human-driven climate change is therefore a major priority for the conservation of biodiversity in a rapidly changing environment. Recent developments in genomic, transcriptomic and epigenomic technologies are enabling unprecedented insights into the evolutionary processes and molecular bases of adaptation. This Review summarizes methods that apply and integrate omics tools to experimentally investigate, monitor and predict how species and communities in the wild cope with global climate change, which is by genetically adapting to new environmental conditions, through range shifts or through phenotypic plasticity. We identify advantages and limitations of each method and discuss future research avenues that would improve our understanding of species' evolutionary responses to global climate change, highlighting the need for holistic, multi-omics approaches to ecosystem monitoring during global climate change.

A qPCR-based method to detect the eel parasitic nematode Anguillicola crassus in intermediate and final hosts.

Being able to systematically detect parasitic infection, even when no visual signs of infection are present, is crucial to the establishment of accurate conservation policies. The nematode Anguillicola crassus infects the swimbladder of anguillid species and is a potential threat for eel populations. In North America, naïve hosts such as the American eel Anguilla rostrata are affected by this infection. The accidental introduction of A. crassus following restocking programs may contribute to the actual decline of the American eel in Canada. We present a quantitative real time PCR-based method to detect A. crassus infection in final and intermediate hosts. We tested two protocols on samples from different geographical origins in Canada: 1) a general detection of A. crassus DNA in pools of young final hosts (glass eels) or crustacean intermediate hosts 2) a detection at the individual scale by analyzing swim bladders from elvers, or from adult yellow and silver eels. The DNA of A. crassus was detected in one pool of zooplankton (intermediate host) from the Richelieu River (Montérégie-Québec), as well as in individual swim bladders of 13 elvers from Grande and Petite Trinité rivers (Côte-Nord-Québec). We suggest that our qPCR approach could be used in a quantitative way to estimate the parasitic burden in individual swim bladders of elvers. Our method, which goes beyond most of previous developed protocols that restricted the diagnosis of A. crassus to the moment when it was fully established in its final host, should help to detect early A. crassus infection in nature.

The parasite Schistocephalus solidus secretes proteins with putative host manipulation functions.

BACKGROUND: Manipulative parasites are thought to liberate molecules in their external environment, acting as manipulation factors with biological functions implicated in their host's physiological and behavioural alterations. These manipulation factors are part of a complex mixture called the secretome. While the secretomes of various parasites have been described, there is very little data for a putative manipulative parasite. It is necessary to study the molecular interaction between a manipulative parasite and its host to better understand how such alterations evolve. METHODS: Here, we used proteomics to characterize the secretome of a model cestode with a complex life cycle based on trophic transmission. We studied Schistocephalus solidus during the life stage in which behavioural changes take place in its obligatory intermediate fish host, the threespine stickleback (Gasterosteus aculeatus). We produced a novel genome sequence and assembly of S. solidus to improve protein coding gene prediction and annotation for this parasite. We then described the whole worm's proteome and its secretome during fish host infection using LC-MS/MS. RESULTS: A total of 2290 proteins were detected in the proteome of S. solidus, and 30 additional proteins were detected specifically in the secretome. We found that the secretome contains proteases, proteins with neural and immune functions, as well as proteins involved in cell communication. We detected receptor-type tyrosine-protein phosphatases, which were reported in other parasitic systems to be manipulation factors. We also detected 12 S. solidus-specific proteins in the secretome that may play important roles in host-parasite interactions. CONCLUSIONS: Our results suggest that S. solidus liberates molecules with putative host manipulation functions in the host and that many of them are species-specific.

The secretome of a parasite alters its host's behaviour but does not recapitulate the behavioural response to infection.

Parasites with complex life cycles have been proposed to manipulate the behaviour of their intermediate hosts to increase the probability of reaching their final host. The cause of these drastic behavioural changes could be manipulation factors released by the parasite in its environment (the secretome), but this has rarely been assessed. We studied a non-cerebral parasite, the cestode Schistocephalus solidus, and its intermediate host, the threespine stickleback (Gasterosteus aculeatus), whose response to danger becomes significantly diminished when infected. These altered behaviours appear only during late infection, when the worm is ready to reproduce in its final avian host. Sympatric host-parasite pairs show higher infection success for parasites, suggesting that the secretome effects could differ for allopatric host-parasite pairs with independent evolutionary histories. We tested the effects of secretome exposure on behaviour by using secretions from the early and late infection of S. solidus and by injecting them in healthy sticklebacks from a sympatric and allopatric population. Contrary to our prediction, secretome from late infection worms did not result in more risky behaviours, but secretome from early infection resulted in more cautious hosts, only in fish from the allopatric population. Our results suggest that the secretome of S. solidus contains molecules that can affect host behaviour, that the causes underlying the behavioural changes in infected sticklebacks are multifactorial and that local adaptation between host-parasite pairs may extend to the response to the parasite's secretome content.

An eDNA-qPCR assay to detect the presence of the parasite Schistocephalus solidus inside its threespine stickleback host.

Detecting the presence of a parasite within its host is crucial to the study of host-parasite interactions. The Schistocephalus solidus-threespine stickleback pair has been studied extensively to investigate host phenotypic alterations associated with a parasite with a complex life cycle. This cestode is localized inside the stickleback's abdominal cavity and can be visually detected only once it passes a mass threshold. We present a non-lethal quantitative PCR (qPCR) approach based on detection of environmental DNA from the worm (eDNA), sampled in the fish abdominal cavity. Using this approach on two fish populations (n=151), 98% of fish were correctly assigned to their S. solidus infection status. There was a significant correlation between eDNA concentration and total parasitic mass. We also assessed ventilation rate as a complementary mean to detect infection. Our eDNA detection method gives a reliable presence/absence response and its future use for quantitative assessment of infection is promising.

Can the behaviour of threespine stickleback parasitized with Schistocephalus solidus be replicated by manipulating host physiology?

Sticklebacks infected by the parasitic flatworm Schistocephalus solidus show dramatic changes in phenotype, including a loss of species-typical behavioural responses to predators. The timing of host behaviour change coincides with the development of infectivity of the parasite to the final host (a piscivorous bird), making it an ideal model for studying the mechanisms of infection-induced behavioural modification. However, whether the loss of host anti-predator behaviour results from direct manipulation by the parasite, or is a by-product (e.g. host immune response) or side effect of infection (e.g. energetic loss), remains controversial. To understand the physiological mechanisms that generate these behavioural changes, we quantified the behavioural profiles of experimentally infected fish and attempted to replicate these in non-parasitized fish by exposing them to treatments including immunity activation and fasting, or by pharmacologically inhibiting the stress axis. All fish were screened for the following behaviours: activity, water depth preference, sociability, phototaxis, anti-predator response and latency to feed. We were able to change individual behaviours with certain treatments. Our results suggest that the impact of S. solidus on the stickleback might be of a multifactorial nature. The behaviour changes observed in infected fish might result from the combined effects of modifying the serotonergic axis, lack of energy and activation of the immune system.

Evolutionary impact of transposable elements on genomic diversity and lineage-specific innovation in vertebrates.

Since their discovery, a growing body of evidence has emerged demonstrating that transposable elements are important drivers of species diversity. These mobile elements exhibit a great variety in structure, size and mechanisms of transposition, making them important putative actors in organism evolution. The vertebrates represent a highly diverse and successful lineage that has adapted to a wide range of different environments. These animals also possess a rich repertoire of transposable elements, with highly diverse content between lineages and even between species. Here, we review how transposable elements are driving genomic diversity and lineage-specific innovation within vertebrates. We discuss the large differences in TE content between different vertebrate groups and then go on to look at how they affect organisms at a variety of levels: from the structure of chromosomes to their involvement in the regulation of gene expression, as well as in the formation and evolution of non-coding RNAs and protein-coding genes. In the process of doing this, we highlight how transposable elements have been involved in the evolution of some of the key innovations observed within the vertebrate lineage, driving the group's diversity and success.