School of BioSciences - Research Publications

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    A metapopulation model reveals connectivity-driven hotspots in treatment resistance evolution in a marine parasite
    Coates, A ; Robinson, N ; Dempster, T ; Samsing, F ; Johnsen, I ; Phillips, BL ; Miller-Saunders, K (Oxford University Press, 2022-11-30)
    In salmon aquaculture, the sustainable management of salmon lice (Lepeophtheirus salmonis) is limited by the adaptive capacity of the parasite. This is evident in the repeated evolution of pesticide resistance in the salmon louse population. To better prepare for resistance, we constructed a numerical metapopulation model that predicts the evolutionary dynamics of lice across an interconnected farm network. This model integrates within-farm population dynamics and between-farm louse dispersal, the latter using outputs from a state-of-the-art particle-tracking model. Distinct from previous metapopulation models, it also simulates spatial and temporal genetic variation arising from selection. The model was parameterized to simulate the evolution of resistance to the pesticide azamethiphos on farms in southern Norway. It successfully reproduced the rapid (within 10 years) evolution of azamethiphos resistance following extensive delousing treatments. It also identified strong spatial patterns in resistance, with regions of high farm connectivity being potential hotspots of louse adaptation. Rates of infestation and evolution were significantly reduced when highly connected farms were excluded from the simulation, compared to when low-connectivity or random sites were excluded. This model can be a valuable tool for coordinating pest management at a regional scale, in a way that slows or prevents the spread of resistance.
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    Applying genetic technologies to combat infectious diseases in aquaculture
    Robinson, NA ; Robledo, D ; Sveen, L ; Daniels, RR ; Krasnov, A ; Coates, A ; Jin, YH ; Barrett, LT ; Lillehammer, M ; Kettunen, AH ; Phillips, BL ; Dempster, T ; Doeschl-Wilson, A ; Samsing, F ; Difford, G ; Salisbury, S ; Gjerde, B ; Haugen, J-E ; Burgerhout, E ; Dagnachew, BS ; Kurian, D ; Fast, MD ; Rye, M ; Salazar, M ; Bron, JE ; Monaghan, SJ ; Jacq, C ; Birkett, M ; Browman, HI ; Skiftesvik, AB ; Fields, DM ; Selander, E ; Bui, S ; Sonesson, A ; Skugor, S ; Ostbye, T-KK ; Houston, RD (WILEY, 2023-03)
    Disease and parasitism cause major welfare, environmental and economic concerns for global aquaculture. In this review, we examine the status and potential of technologies that exploit genetic variation in host resistance to tackle this problem. We argue that there is an urgent need to improve understanding of the genetic mechanisms involved, leading to the development of tools that can be applied to boost host resistance and reduce the disease burden. We draw on two pressing global disease problems as case studies-sea lice infestations in salmonids and white spot syndrome in shrimp. We review how the latest genetic technologies can be capitalised upon to determine the mechanisms underlying inter- and intra-species variation in pathogen/parasite resistance, and how the derived knowledge could be applied to boost disease resistance using selective breeding, gene editing and/or with targeted feed treatments and vaccines. Gene editing brings novel opportunities, but also implementation and dissemination challenges, and necessitates new protocols to integrate the technology into aquaculture breeding programmes. There is also an ongoing need to minimise risks of disease agents evolving to overcome genetic improvements to host resistance, and insights from epidemiological and evolutionary models of pathogen infestation in wild and cultured host populations are explored. Ethical issues around the different approaches for achieving genetic resistance are discussed. Application of genetic technologies and approaches has potential to improve fundamental knowledge of mechanisms affecting genetic resistance and provide effective pathways for implementation that could lead to more resistant aquaculture stocks, transforming global aquaculture.
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    Skin and bone development in Atlantic salmon (Salmo salar) influenced by hatchery environment
    Robinson, N ; Karlsen, C ; Ytteborg, E ; Krasnov, A ; Gerwins, J ; Johnsen, H ; Kolarevic, J (ELSEVIER, 2021-11-15)
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    Genetic Connectivity of Seamount Populations of Bluenose Warehou (Hyperoglyphe antarctica)
    Heyworth, SM ; Bell, JB ; Wade, CM ; Cavalcante, G ; Robinson, N ; Young, E ; Glass, J ; Feary, DA (FRONTIERS MEDIA SA, 2021-09-09)
    Quantifying the level of population connectivity within and between geographically separated single-species deep-water fisheries stocks will be vital for designing effective management plans to preserve such populations. Despite this, stock structure in many fisheries is still poorly described and, at best, subject to precautionary management. Here we use rapidly evolving mitochondrial genes and microsatellite markers to investigate population connectivity patterns in commercially targeted Hyperoglyphe antarctica populations between four seamounts within the Tristan da Cunha Exclusive Economic Zone (EEZ). We find little evidence of population genetic structure between fished populations, with both mtDNA and microsatellite markers showing that there is low genetic population diversity (reflecting substantial gene flow) across the four seamounts. We also find little genetic differentiation between H. antarctica across the wider Southern Hemisphere. Such results support the role for coordinated management of all four populations across the seamounts, and potentially including stocks associated with Australia and New Zealand, with expansion of the fishery clearly having the potential to substantially impact the source of recruits and therefore wider population sustainability.
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    Seascape genomics reveals adaptive divergence in a connected and commercially important mollusc, the greenlip abalone (Haliotis laevigata), along a longitudinal environmental gradient
    Sandoval-Castillo, J ; Robinson, NA ; Hart, AM ; Strain, LWS ; Beheregaray, LB (WILEY, 2018-04)
    Populations of broadcast spawning marine organisms often have large sizes and are exposed to reduced genetic drift. Under such scenarios, strong selection associated with spatial environmental heterogeneity is expected to drive localized adaptive divergence, even in the face of connectivity. We tested this hypothesis using a seascape genomics approach in the commercially important greenlip abalone (Haliotis laevigata). We assessed how its population structure has been influenced by environmental heterogeneity along a zonal coastal boundary in southern Australia linked by strong oceanographic connectivity. Our data sets include 9,109 filtered SNPs for 371 abalones from 13 localities and environmental mapping across ~800 km. Genotype-environment association analyses and outlier tests defined 8,786 putatively neutral and 323 candidate adaptive loci. From a neutral perspective, the species is better represented by a metapopulation with very low differentiation (global FST  = 0.0081) and weak isolation by distance following a stepping-stone model. For the candidate adaptive loci, however, model-based and model-free approaches indicated five divergent population clusters. After controlling for spatial distance, the distribution of putatively adaptive variation was strongly correlated to selection linked to minimum sea surface temperature and oxygen concentration. Around 80 candidates were annotated to genes with functions related to high temperature and/or low oxygen tolerance, including genes that influence the resilience of abalone species found in other biogeographic regions. Our study includes a documented example about the uptake of genomic information in fisheries management and supports the hypothesis of adaptive divergence due to coastal environmental heterogeneity in a connected metapopulation of a broadcast spawner.
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    Prevention not cure: a review of methods to avoid sea lice infestations in salmon aquaculture
    Barrett, LT ; Oppedal, F ; Robinson, N ; Dempster, T (WILEY, 2020-11-01)
    The Atlantic salmon aquaculture industry still struggles with ectoparasitic sea lice despite decades of research and development invested into louse removal methods. In contrast, methods to prevent infestations before they occur have received relatively little research effort, yet may offer key benefits over treatment‐focused methods. Here, we summarise the range of potential and existing preventative methods, conduct a meta‐analysis of studies trialling the efficacy of existing preventative methods and discuss the rationale for a shift to the prevention‐focused louse management paradigm. Barrier technologies that minimise host–parasite encounter rates provide the greatest protection against lice, with a weighted median 76% reduction in infestation density in cages with plankton mesh ‘snorkels’ or ‘skirts’, and up to a 100% reduction for fully enclosed cages. Other methods such as geographic spatiotemporal management, manipulation of swimming depth, functional feeds, repellents and host cue masking can drive smaller reductions that may be additive when used in combination with barrier technologies. Finally, ongoing development of louse‐resistant salmon lineages may lead to long‐term improvements if genetic gain is maintained, while the development of an effective vaccine remains a key target. Preventative methods emphasise host resistance traits while simultaneously reducing host–parasite encounters. Effective implementation has the potential to dramatically reduce the need for delousing and thus improve fish welfare, productivity and sustainability in louse‐prone salmon farming regions.
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    Evolution of salmon lice in response to management strategies: a review
    Coates, A ; Phillips, BL ; Bui, S ; Oppedal, F ; Robinson, NA ; Dempster, T (WILEY, 2021-06)
    Abstract Ectoparasitic salmon lice (Lepeophtheirus salmonis) present a major challenge to Atlantic salmon (Salmo salar) aquaculture. The demand for effective louse control has produced diverse management strategies. These strategies essentially impose novel selection pressures on parasite populations, driving the evolution of resistance. Here we assess the potential for salmon lice to adapt to current prevention and control methods. Lice have evolved resistance to at least four of five chemical therapeutants, and use of these chemicals has declined significantly in recent years. The industry has shifted to alternative non‐chemical approaches, yet lice may adapt to these as well. Early research suggests that phenotypic variation exists in the louse population upon which non‐chemical selection pressures could act and that this variation may have a genetic basis. From the existing evidence, as well as an examination of evolutionary processes in other relevant parasite and pest systems, we conclude that the evolution of non‐chemical resistance is an emergent concern that must be considered by the industry. We recommend areas for focused research to better assess this risk. It is also important to determine whether phenotypic shifts in response to non‐chemical selection may shift the ecological niche of the parasite, as this may have cascading effects on wild salmon populations. We also recommend further research to identify strategy combinations that have antagonistic selective effects that slow louse evolution and those with synergistic effects that should be avoided. Greater understanding of evolutionary processes can inform aquaculture policies that counteract the rise of resistant parasite populations.
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    Training the salmon's genes: influence of aerobic exercise, swimming performance and selection on gene expression in Atlantic salmon
    Robinson, NA ; Timmerhaus, G ; Baranski, M ; Andersen, O ; Takle, H ; Krasnov, A (BMC, 2017-12-15)
    BACKGROUND: Farmed and wild Atlantic salmon are exposed to many infectious and non-infectious challenges that can cause mortality when they enter the sea. Exercise before transfer promotes growth, health and survival in the sea. Swimming performance in juveniles at the freshwater parr stage is positively associated with resistance to some diseases. Genetic variation is likely to affect response to exercise. In this study we map genetic differences associated with aerobic exercise, swimming performance and genetic origin. Eggs from the selectively bred Bolaks salmon and wild Lærdal River salmon strains were reared until parr in a common environment. Swimming performance was assessed by subjecting the fish to either continuous hard exercise or control conditions for 18 days. Heart was sampled for examination of gene expression using RNA-seq (~60 fish/treatment). RESULTS: Lower expression of genes affecting immune function was found in domesticated than wild parr. Among wild parr under control exercise the expression of a large number of genes involved in general metabolism, stress and immune response was lower in superior swimmers suggesting that minimisation of energy expenditure during periods of low activity makes parr better able to sustain bursts of swimming for predator avoidance. A similar set of genes were down-regulated with training among wild parr with inferior swimming performance. These parr react to training in a way that their cardiac expression patterns become like the superior performing wild parr under control exercise conditions. Diversifying selection caused by breeding of domesticated stock, and adaptive pressures in wild stock, has affected the expression and frequency of single nucleotide polymorphisms (SNPs) for multiple functional groups of genes affecting diverse processes. SNPs associated with swimming performance in wild parr map to genes involved in energetic processes, coding for contractile filaments in the muscle and controlling cell proliferation. CONCLUSIONS: Domesticated parr have less phenotypic plasticity in response to training and lower expression of genes with functions affecting immune response. The genetic response to training is complex and depends on the background of parr and their swimming ability. Exercise should be tailored to the genetics and swimming performance of fish.
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    The Development of a High Density Linkage Map for Black Tiger Shrimp (Penaeus monodon) Based on cSNPs
    Baranski, M ; Gopikrishna, G ; Robinson, NA ; Katneni, VK ; Shekhar, MS ; Shanmugakarthik, J ; Jothivel, S ; Gopal, C ; Ravichandran, P ; Kent, M ; Arnyasi, M ; Ponniah, AG ; Jiravanichpaisal, P (PUBLIC LIBRARY SCIENCE, 2014-01-17)
    Transcriptome sequencing using Illumina RNA-seq was performed on populations of black tiger shrimp from India. Samples were collected from (i) four landing centres around the east coastline (EC) of India, (ii) survivors of a severe WSSV infection during pond culture (SUR) and (iii) the Andaman Islands (AI) in the Bay of Bengal. Equal quantities of purified total RNA from homogenates of hepatopancreas, muscle, nervous tissue, intestinal tract, heart, gonad, gills, pleopod and lymphoid organs were combined to create AI, EC and SUR pools for RNA sequencing. De novo transcriptome assembly resulted in 136,223 contigs (minimum size 100 base pairs, bp) with a total length 61 Mb, an average length of 446 bp and an average coverage of 163× across all pools. Approximately 16% of contigs were annotated with BLAST hit information and gene ontology annotations. A total of 473,620 putative SNPs/indels were identified. An Illumina iSelect genotyping array containing 6,000 SNPs was developed and used to genotype 1024 offspring belonging to seven full-sibling families. A total of 3959 SNPs were mapped to 44 linkage groups. The linkage groups consisted of between 16-129 and 13-130 markers, of length between 139-10.8 and 109.1-10.5 cM and with intervals averaging between 1.2 and 0.9 cM for the female and male maps respectively. The female map was 28% longer than the male map (4060 and 2917 cM respectively) with a 1.6 higher recombination rate observed for female compared to male meioses. This approach has substantially increased expressed sequence and DNA marker resources for tiger shrimp and is a useful resource for QTL mapping and association studies for evolutionarily and commercially important traits.
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    QTL for white spot syndrome virus resistance and the sex-determining locus in the Indian black tiger shrimp (Penaeus monodon)
    Robinson, NA ; Gopikrishna, G ; Baranski, M ; Katneni, VK ; Shekhar, MS ; Shanmugakarthik, J ; Jothivel, S ; Gopal, C ; Ravichandran, P ; Gitterle, T ; Ponniah, AG (BIOMED CENTRAL LTD, 2014-08-28)
    BACKGROUND: Shrimp culture is a fast growing aquaculture sector, but in recent years there has been a shift away from tiger shrimp Penaeus monodon to other species. This is largely due to the susceptibility of P. monodon to white spot syndrome virus disease (Whispovirus sp.) which has impacted production around the world. As female penaeid shrimp grow more rapidly than males, mono-sex production would be advantageous, however little is known about genes controlling or markers associated with sex determination in shrimp. In this study, a mapped set of 3959 transcribed single nucleotide polymorphisms were used to scan the P. monodon genome for loci associated with resistance to white-spot syndrome virus and sex in seven full-sibling tiger shrimp families challenged with white spot syndrome virus. RESULTS: Linkage groups 2, 3, 5, 6, 17, 18, 19, 22, 27 and 43 were found to contain quantitative trait loci significantly associated with hours of survival after white spot syndrome virus infection (P < 0.05 after Bonferroni correction). Nine QTL were significantly associated with hours of survival. Of the SNPs mapping to these and other regions with suggestive associations, many were found to occur in transcripts showing homology to genes with putative immune functions of interest, including genes affecting the action of the ubiquitin-proteasome pathway, lymphocyte-cell function, heat shock proteins, the TOLL pathway, protein kinase signal transduction pathways, mRNA binding proteins, lectins and genes affecting the development and differentiation of the immune system (eg. RUNT protein 1A). Several SNPs significantly associated with sex were mapped to linkage group 30, the strongest associations (P < 0.001 after Bonferroni correction) for 3 SNPs located in a 0.8 cM stretch between positions 43.5 and 44.3 cM where the feminisation gene (FEM-1, affecting sexual differentiation in Caenorhabditis elegans) mapped. CONCLUSIONS: The markers for disease resistance and sexual differentiation identified by this study could be useful for marker assisted selection to improve resistance to WSSV and for identifying homogametic female individuals for mono-sex (all female) production. The genes with putative functions affecting immunity and sexual differentiation that were found to closely map to these loci provide leads about the mechanisms affecting these important economic traits in shrimp.