Harnessing the Power of Genomics to Secure the Future of Seafood
Authors: Louis Bernatchez, Maren Wellenreuther, Cristián Araneda, David T. Ashton, Julia M.I. Barth, Terry D. Beacham, Gregory E. Maes, Jann T. Martinsohn, Kristina M. Miller, Kerry A. Naish, Jennifer R. Ovenden, Craig R. Primmer, Ho Young Suk, Nina O. Therkildsen, Ruth E. Withler
Journal: Trends in Ecology & Evolution (2017)

Advancements of genetic technologies now allow the collection of genome-wide data in nonmodel species in a cost -effective manner. These genomic-informed technologies allow addressing a comprehensive spectrum of needs and applications relevant to fisheries, aquaculture , and biosecurity. Genomics tools also improve our understanding of how aquatic organisms adapt and respond to the environment, and improve our ability to monitor environmental variation and exploited species. Genomic approaches are now rapidly replacing traditional genetic markers, but their application in fisheries and aquaculture management has stagnated when compared to agriculture where they have long been used for improved production. There is no reason to further delay the application of genomic tools in fisheries management and aquaculture production. Best use of scientific knowledge is required to maintain the fundamental role of seafood in human nutrition. While it is acknowledged that genomic-based methods allow the collection of powerful data, their value to inform fisheries management, aquaculture , and biosecurity applications remains underestimated. We review genomic applications of relevance to the sustainable management of seafood resources, illustrate the benefits of, and identify barriers to their integration. We conclude that the value of genomic information towards securing the future of seafood does not need to be further demonstrated. Instead, we need immediate efforts to remove structural roadblocks and focus on ways that support integration of genomic-informed methods into management and production practices. We propose solutions to pave the way forward. Best use of scientific knowledge is required to maintain the fundamental role of seafood in human nutrition. While it is acknowledged that genomic-based methods allow the collection of powerful data, their value to inform fisheries management, aquaculture , and biosecurity applications remains underestimated. We review genomic applications of relevance to the sustainable management of seafood resources, illustrate the benefits of, and identify barriers to their integration. We conclude that the value of genomic information towards securing the future of seafood does not need to be further demonstrated. Instead, we need immediate efforts to remove structural roadblocks and focus on ways that support integration of genomic-informed methods into management and production practices. We propose solutions to pave the way forward. Seafood plays a fundamental role in meeting current and future food needs [1Béné C. et al.Contribution of fisheries and aquaculture to food security and poverty reduction: assessing the current evidence.World Dev. 2016; 79: 177-196Crossref Scopus (409) Google Scholar]. Capture fisheries use the only remaining wild animal protein source, and aquaculture is the fastest growing food production sector in the world. Together they provide 4.5 billion people with at least 15% of their animal protein [2Béné C. Small-scale fisheries: assessing their contribution to rural livelihoods in developing countries.FAO Fisheries Circular. FAO, 2006Google Scholar, 3McIntyre P.B. et al.Linking freshwater fishery management to global food security and biodiversity conservation.Proc. Nat. Acad. Sci. U. S. A. 2016; 113: 12880-12885Crossref Scopus (139) Google Scholar]. The human population may exceed 9 billion by 2050, so a pressing question is whether fisheries and aquaculture can help to alleviate food security issues [3McIntyre P.B. et al.Linking freshwater fishery management to global food security and biodiversity conservation.Proc. Nat. Acad. Sci. U. S. A. 2016; 113: 12880-12885Crossref Scopus (139) Google Scholar]. The answer to this remains unknown. Seafood needs of some developed countries can no longer be sustained from local fish stocks and are increasingly supplemented from elsewhere [4Pauly D. Zeller D. Catch reconstructions reveal that global marine fisheries catches are higher than reported and declining.Nat. Commun. 2016; 7: 10244Crossref PubMed Scopus (707) Google Scholar]. This trend will probably remain or increase over time, as several stocks are near or above sustainable limits [5Hilborn R. Stokes K. Defining overfished stocks: have we lost the plot?.Fisheries. 2010; 35: 113-120Crossref Scopus (61) Google Scholar, 6Rose G.A. Rowe S. Northern cod comeback.Can. J. Fish. Aquat. Sci. 2015; 72: 1789-1798Crossref Scopus (69) Google Scholar], and many fisheries remain overexploited or near collapse [4Pauly D. Zeller D. Catch reconstructions reveal that global marine fisheries catches are higher than reported and declining.Nat. 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While finfish production from aquaculture has reached the volume of wild fisheries [10Béné C. et al.Feeding 9 billion by 2050–Putting fish back on the menu.Food Secur. 2015; 7: 261-274Crossref Scopus (424) Google Scholar], growth is expected to decelerate in response to freshwater shortage, lack of suitable locations, and increasing feed costs [11Food and Agriculture Organization The State of World Fisheries and Aquaculture 2016. Contributing to food security and nutrition for all.STECF: Scientific, Technical and Economic Committee for Fisheries. Publications Office of the European Union, 2016Google Scholar]. Moreover, other aquaculture industries (e.g., shellfish) are suffering production setbacks due to disease outbreaks and ocean acidification [12S et al.An Updated Synthesis of the Impacts of Ocean Acidification on Marine Biodiversity. Secretariat of the Convention on Biological Diversity, 2014Google Scholar]. Careful management and production strategies are required to maintain a sustainable future for the seafood industry, making it critical that the best scientific knowledge informs decision-making [3McIntyre P.B. et al.Linking freshwater fishery management to global food security and biodiversity conservation.Proc. Nat. Acad. Sci. U. S. A. 2016; 113: 12880-12885Crossref Scopus (139) Google Scholar, 4Pauly D. Zeller D. Catch reconstructions reveal that global marine fisheries catches are higher than reported and declining.Nat. Commun. 2016; 7: 10244Crossref PubMed Scopus (707) Google Scholar, 13Melnychuk M.C. et al.Fisheries management impacts on target species status.Proc. Nat. Acad. Sci. U. S. A. 2017; 114: 178-183Crossref PubMed Scopus (100) Google Scholar]. Traditional scientific fisheries management relies on stock assessment models to predict variability in stock–recruitment relationships to determine sustainable catch limits [7Worm B. et al.Rebuilding global fisheries.Science. 2009; 325: 578-585Crossref PubMed Scopus (1578) Google Scholar, 14Myers R.A. Stock and recruitment: generalizations about maximum reproductive rate, density dependence, and variability using meta-analytic approaches.ICES J. Mar. Sci. 2001; 58: 937-951Crossref Scopus (208) Google Scholar, 15Beddington J.R. et al.Current problems in the management of marine fisheries.Science. 2007; 316: 1713-1716Crossref PubMed Scopus (457) Google Scholar]. Genetic methods can also provide fundamental data to inform fisheries management and aquaculture production [16Waples R.S. et al.Integrating genetic data into management of marine resources: how can we do it better?.Fish Fish. 2008; 9: 423-449Crossref Scopus (235) Google Scholar], however, the integration of genetic data has stagnated (Box 1). Consequently, and despite the demonstrated ability of genetic data to delineate populations accurately (see section below), management units are predominantly based on administrative units, which are often not closely connected with population biology [8Osio G.C. et al.Assessing the vulnerability of Mediterranean demersal stocks and predicting exploitation status of un-assessed stocks.Fish. Res. 2015; 171: 110-121Crossref Scopus (35) Google Scholar, 17Borja A. et al.Overview of integrative assessment of marine systems: the ecosystem approach in practice.Front. Mar. Sci. 2016; 3: 20Crossref Scopus (180) Google Scholar]. This contradicts the basis of fisheries science whereby the Maximum Sustainable Yield (MSY) can only be achieved by the efficient management of distinct populations [8Osio G.C. et al.Assessing the vulnerability of Mediterranean demersal stocks and predicting exploitation status of un-assessed stocks.Fish. Res. 2015; 171: 110-121Crossref Scopus (35) Google Scholar, 16Waples R.S. et al.Integrating genetic data into management of marine resources: how can we do it better?.Fish Fish. 2008; 9: 423-449Crossref Scopus (235) Google Scholar, 18Utter F.M. Biochemical genetics and fishery management: an historical perspective.J. Fish Biol. 1991; 39: 1-20Crossref Scopus (147) Google Scholar].Box 1Why Genetic Data Has Seldom Been Incorporated into Fisheries Management, and What to Do about itThe fisheries genetics explosion began in the 1980 s propelled by the allelic interpretation of the electrophoretic mobility of proteins and accelerated now by the genomics revolution 9Snapper9 [49Ryman N. Utter F. Genetics and fisheries management: past, present and future.in: Ryman N. Utter F. Population genetics and fisheries management. University of Washington, 1987: 1-20Google Scholar]. Sadly, exclamations of the practical value of population genetics for management and conservation have largely fallen on deaf ears. Despite trouble-shooting by experts [16Waples R.S. et al.Integrating genetic data into management of marine resources: how can we do it better?.Fish Fish. 2008; 9: 423-449Crossref Scopus (235) Google Scholar, 50Hauser L. Carvalho G.R. Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts.Fish Fish. 2008; 9: 333-362Crossref Scopus (449) Google Scholar], impediments to the downstream use of genetics in seafood production still remain.To systematically address this, three user groups were consulted in one-to-one structured interviews [51Dichmont, C.M. et al. (2012) Scoping current and future genetic tools, their limitations and their applications for wild fisheries management. Final Report. Australian Fisheries Research & Development Corporation Project 2011/035.Google Scholar]. The groups were fisheries scientists (n = 26), fisheries managers (n = 24), and fishing industry representatives (n = 12) in Australia, Europe, North and South America, Western Pacific, South Africa , and New Zealand. The purpose was to qualitatively assess attitudes and perceptions on the use of genetics in a fisheries management context to determine if there were barriers to the uptake of genetic information and how this might be improved. Over 90% of interviewees were familiar with the use of genetics for fisheries stock structure (Theme II in [52Ovenden J.R. et al.Ocean's eleven: a critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries.Fish Fish. 2015; 16: 125-159Crossref Scopus (113) Google Scholar]). The awareness of the remaining ten genetic themes was poor to moderate. Industry and management representatives viewed the role of genetics in fisheries more positively than fisheries scientists. The basis for positive attitudes was the recognition of the general usefulness of genetics, in particular for defining the spatial structure of populations. Where there was a negative perception by interviewees, several reasons were provided:•A general lack of understanding of the potential value of genetic information,•A perception that genetic studies are expensive,•A perception that genetic results are often 'oversold',•A lack of consistency in interpretations of results by geneticists,•The importance of genetic information was far outweighed by other inputs to management decisions.All interviewees agreed that the role and effectiveness of genetic information in fisheries management could be improved. The suggestions were grouped into two categories: communication and technical. Improvements to communication strategies (around 70% of suggestions) were considered essential. Specific suggestions included: improved communication of results across user groups using plain language; greater communication among fishery scientists, geneticists, fishery managers , and industry; a need for greater understanding of the utility of genetic methods by user groups; and greater accessibility to genetic research and geneticists. Technical suggestions for improvement included reducing cost of genetic projects; more robust and reliable genetic techniques; and more robust sampling designs.Unhappily, communication challenges are still a roadblock for the uptake of genetic data, which is a wake-up call for those involved in genomics for seafood security. There are glimmers of hope that attitudes are changing. The survey showed that most understand its power for defining fisheries stocks and are sympathetic, if not knowledgeable, about the role of genetics. Thus, the judicious use of genomics is likely to be well received, but its application needs to be carefully tailored to provide solutions for management and policy issues (Ovenden and Moore, S11). The onus is on geneticists and end-users to reach mutual understanding (Figure I), or else the improvement in the perceived value of genetics to the seafood industry will be not be sustained. The fisheries genetics explosion began in the 1980 s propelled by the allelic interpretation of the electrophoretic mobility of proteins and accelerated now by the genomics revolution 9Snapper9 [49Ryman N. Utter F. Genetics and fisheries management: past, present and future.in: Ryman N. Utter F. Population genetics and fisheries management. University of Washington, 1987: 1-20Google Scholar]. Sadly, exclamations of the practical value of population genetics for management and conservation have largely fallen on deaf ears. Despite trouble-shooting by experts [16Waples R.S. et al.Integrating genetic data into management of marine resources: how can we do it better?.Fish Fish. 2008; 9: 423-449Crossref Scopus (235) Google Scholar, 50Hauser L. Carvalho G.R. Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts.Fish Fish. 2008; 9: 333-362Crossref Scopus (449) Google Scholar], impediments to the downstream use of genetics in seafood production still remain. To systematically address this, three user groups were consulted in one-to-one structured interviews [51Dichmont, C.M. et al. (2012) Scoping current and future genetic tools, their limitations and their applications for wild fisheries management. Final Report. Australian Fisheries Research & Development Corporation Project 2011/035.Google Scholar]. The groups were fisheries scientists (n = 26), fisheries managers (n = 24), and fishing industry representatives (n = 12) in Australia, Europe, North and South America, Western Pacific, South Africa , and New Zealand. The purpose was to qualitatively assess attitudes and perceptions on the use of genetics in a fisheries management context to determine if there were barriers to the uptake of genetic information and how this might be improved. Over 90% of interviewees were familiar with the use of genetics for fisheries stock structure (Theme II in [52Ovenden J.R. et al.Ocean's eleven: a critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries.Fish Fish. 2015; 16: 125-159Crossref Scopus (113) Google Scholar]). The awareness of the remaining ten genetic themes was poor to moderate. Industry and management representatives viewed the role of genetics in fisheries more positively than fisheries scientists. The basis for positive attitudes was the recognition of the general usefulness of genetics, in particular for defining the spatial structure of populations. Where there was a negative perception by interviewees, several reasons were provided:•A general lack of understanding of the potential value of genetic information,•A perception that genetic studies are expensive,•A perception that genetic results are often 'oversold',•A lack of consistency in interpretations of results by geneticists,•The importance of genetic information was far outweighed by other inputs to management decisions. All interviewees agreed that the role and effectiveness of genetic information in fisheries management could be improved. The suggestions were grouped into two categories: communication and technical. Improvements to communication strategies (around 70% of suggestions) were considered essential. Specific suggestions included: improved communication of results across user groups using plain language; greater communication among fishery scientists, geneticists, fishery managers , and industry; a need for greater understanding of the utility of genetic methods by user groups; and greater accessibility to genetic research and geneticists. Technical suggestions for improvement included reducing cost of genetic projects; more robust and reliable genetic techniques; and more robust sampling designs. Unhappily, communication challenges are still a roadblock for the uptake of genetic data, which is a wake-up call for those involved in genomics for seafood security. There are glimmers of hope that attitudes are changing. The survey showed that most understand its power for defining fisheries stocks and are sympathetic, if not knowledgeable, about the role of genetics. Thus, the judicious use of genomics is likely to be well received, but its application needs to be carefully tailored to provide solutions for management and policy issues (Ovenden and Moore, S11). The onus is on geneticists and end-users to reach mutual understanding (Figure I), or else the improvement in the perceived value of genetics to the seafood industry will be not be sustained. Novel technologies now allow the collection of genome-wide data to better inform fisheries management, biosecurity, and aquaculture applications [19Willette D. et al.So, you want to use next-generation sequencing in marine systems? Insight from the Pan-Pacific Advanced Studies Institute.Bull. Mar. Sci. 2014; 90: 79-122Crossref Scopus (45) Google Scholar, 20da Fonseca R.R. et al.Next-generation biology: sequencing and data analysis approaches for non-model organisms.Mar. Genom. 2016; 30: 3-13Crossref PubMed Scopus (97) Google Scholar]. Genomic approaches are now rapidly replacing traditional genetic markers (e.g., microsatellite DNA), but as with genetic data, little is used when developing management policies (Box 1). Genomics refers to approaches relating to the complete genome of an organism [21Pearse D. Saving the spandrels? Adaptive genomic variation in conservation and fisheries management.J. Fish Biol. 2016; 89: 2697-2716Crossref PubMed Scopus (37) Google Scholar]. In population genetics, the term genomics is typically used as a shorthand to describe studies applying large and genome-wide datasets; with a typical, yet arbitrary, threshold of >1000s versus 10s–100s of markers to distinguish between genomic and genetic studies, respectively. For decades, only low-resolution genetic methods were available to address issues pertaining to fisheries management and aquaculture. Indeed the first genome sequence of a key seafood production species was published in 2011 [22Star B. et al.The genome sequence of Atlantic cod reveals a unique immune system.Nature. 2011; 477: 207-210Crossref PubMed Scopus (570) Google Scholar]. While the limited incorporation of genetic information into fisheries and aquaculture management is not a new problem [16Waples R.S. et al.Integrating genetic data into management of marine resources: how can we do it better?.Fish Fish. 2008; 9: 423-449Crossref Scopus (235) Google Scholar], genomics makes the situation qualitatively different. This is because genomic-informed technologies allow for the first time the development and application of cost-effective genetic tools that can address a comprehensive spectrum of needs and applications relevant to fisheries and aquaculture management, biosecurity, and traceability in the supply chain [23Kelley J.L. et al.The life aquatic: advances in marine vertebrate genomics.Nat. Rev. Genet. 2016; 4: 523-534Crossref Scopus (52) Google Scholar] (Figure 1). Specifically for fisheries management, genomics defines management units, quantifies the extent of adaptive divergence and connectivity between them, and allows performing mixed-stock analysis with substantially increased resolution. Genomic tools also have the potential to advance aquaculture production by means of genomic selection for growth or disease resistance, and identifying wild populations with the greatest potential for domestication [24Yáñez J.M. et al.Genomics in aquaculture to better understand species biology and accelerate genetic progress.Front. Genet. 2015; 6https://doi.org/10.3389/fgene.2015.00128Crossref PubMed Scopus (76) Google Scholar]. Genomics can also increase biosecurity, for example, by identifying escapees from fish farms. A small to moderate number of markers may sometimes provide sufficient power to address the question at hand [19Willette D. et al.So, you want to use next-generation sequencing in marine systems? Insight from the Pan-Pacific Advanced Studies Institute.Bull. Mar. Sci. 2014; 90: 79-122Crossref Scopus (45) Google Scholar, 25Ovenden J.R. et al.Ocean's eleven: a critical evaluation of the role of population, evolutionary and molecular genetics in the management of wild fisheries.Fish Fish. 2015; 16: 125-159Crossref Scopus (31) Google Scholar], yet genomic-informed approaches often provide a necessary first step for identifying the best set of markers to be used in subsequent surveys. Tools derived from genomics can also improve our understanding of how aquatic organisms adapt and respond to their environments from the species to the community level, and improve our ability to monitor biological environmental variation or exploited species, for instance, as provided by the exponential development of environmental DNA (eDNA) and metabarcoding methods [26Rees H.C. et al.REVIEW: The detection of aquatic animal species using environmental DNA – a review of eDNA as a survey tool in ecology.J. Appl. Ecol. 2014; 51: 1450-1459Crossref Scopus (596) Google Scholar]. The following outlines representative examples of genomic applications of direct relevance to fisheries management, aquaculture, and the conservation of exploited species, as well as for food quality and safety purposes. Details for each of these case studies are presented in 14 short papers (S1–S14) in the Supplementary Material that summarise the presentations of invited speakers during a symposium entitled: "Genomics for improved fisheries management and conservation: have the promises been fulfilled?" Accurate identification of fisheries management units and species is mandatory to enable proactive population management. Bernatchez (S6) reported how using several thousands of single nucleotide polymorphism (SNP) markers allowed the refinement of management units of the American lobster, documenting the degree of overlap between biological and current management units, while also providing evidence for local adaptation. Regional patterns of recruitment in the American eel are affected by selection imposed by the local environment, which has been shown to recur in every generation following dispersal from a single spawning area (Bernatchez, S6). This finding may influence both global and local restoration strategies. Species identification for improved conservation practices can also be aided by genomic-based approaches. For example, Lee et al. (S7) showed that adaptive and neutral markers have considerable potential to discriminate cryptic species of sympatric freshwater fishes on the Korean peninsula. Similarly, Araneda and Larraín (S1) demonstrated the usefulness of a moderate number of markers derived from genomic methods for the management and traceability of seafood species (Box 2).Box 2Genomic Approaches for Seafood TraceabilityTraceability of marine or aquacultured products like finfish and shellfish throughout the food chain ('from the ocean to the fork ') with high certainty about their origin and identity is crucial for their sustainable utilisation, the conservation of exploited stocks , and to prevent food fraud [53Stawitz C.C. et al.Financial and Ecological Implications of Global Seafood Mislabeling.Conserv. Lett. 2016; https://doi.org/10.1111/conl.12328Crossref Scopus (28) Google Scholar]. In general, species and their origin may be identified by external traits; however, phenotypic tracing becomes unusable once the species has entered food processing. Genetics and genomics resources provide powerful tools, with high reproducibility and reliability, for tracing and identifying marine products; they can easily be combined and compared with reference materials [54Martinshohn J. et al.Tracing fish and fish products from ocean to fork using advanced molecular technologies. Woodhead Publishing, 2011Google Scholar] to determine authenticity , and to verify labelling information. Traceability can be applied on three broad levels: species, population , and individual identification. Hitherto, the first two levels have been explored using either genetics or genomics derived methods.Two objectives of the species level include preventing food fraud by the substitution of a valuable species with lower value species and marketing of potentially harmful to the consumer or protected species [55Abbadi M. et al.Species identification of bivalve molluscs by pyrosequencing.J. Sci. Food Agr. Discipl. 2017; 97: 512-519Crossref PubMed Scopus (19) Google Scholar, 56Wong E.H.-K. Hanner R.H. DNA barcoding detects market substitution in North American seafood.Food Res. Int. 2008; 41: 828-837Crossref Scopus (351) Google Scholar, 57Miller D. et al.Seafood mislabelling: comparisons of two western European case studies assist in defining influencing factors, mechanisms and motives.Fish Fish. 2012; 13: 345-358Crossref Scopus (68) Google Scholar, 58Filonzi L. et al.Molecular barcoding reveals mislabelling of commercial fish products in Italy.Food Res. Int. 2010; 43: 1383-1388Crossref Scopus (151) Google Scholar]. Many examples of mislabelling have been detected through analysis of the cytochrome oxidase I gene (COI) and by comparing this with the database of DNA barcoding (FISH-BOL) [59Ward R.D. et al.The campaign to DNA barcode all fishes, FISH-BOL.J. Fish Biol. 2009; 74: 329-356Crossref PubMed Scopus (656) Google Scholar, 60Becker S. et al.Five years of FISH-BOL: brief status report.Mitochondrial DNA. 2011; 22: 3-9Crossref PubMed Scopus (98) Google Scholar, 61Oliveira L. et al.Assembling and auditing a comprehensive DNA barcode reference library for European marine fishes.J. Fish Biol. 2016; 89: 2741-2754Crossref PubMed Scopus (21) Google Scholar]. DNA barcoding is less developed in shellfish because species identification often requires the development and applications of different mitochondrial and nuclear molecular markers as well as SNP panels [62Zbawicka M. et al.Identification and validation of novel SNP markers in European populations of marine Mytilus mussels.Mar. Biol. 2012; 159: 1347-1362Crossref Scopus (43) Google Scholar] depending on taxa [63Kijewski T. et al.Distribution of Mytilus taxa in European coastal areas as inferred from molecular markers.J. Sea Res. 2011; 65: 224-234Crossref Scopus (53) Google Scholar]. Examples include, separation of Mediterranean mussel, common blue mussel, Baltic mussel , and Chilean mussel with high accuracy using a panel of 49 SNPs (Larraín et al. in preparation) and the separation of Chilean and Mediterranean mussels with a subpanel of 19 SNPs (Araneda and Larraín, S1).The objectives for the second (population) level include preventing the sale of products from illegal, unreported , and unregulated fisheries, and protecting consumers from seafood products collected in areas affected by threats to public health (for example, harmful algal blooms). Assignments based on a moderate number of non-neutral SNP markers identified using genomics have been successful at differentiating among fish species (Atlantic cod, Atlantic herring, sole, and European hake) from different geographical areas in Europe [31Nielsen E.E. et al.Gene-associated markers provide tools for tackling illegal fishing and false eco-certification.Nat. Commun. 2012; 3: 851Crossref PubMed Scopus (178) Google Scholar]. In Chilean mussel, this approach allowed to differentiate populations from three different environments [64Araneda C. et al.Adaptive genetic variation distinguishes Chilean blue mussels (Mytilus chilensis) from different marine environments.Ecol. Evol. 2016; 6: 3632-3644Crossref PubMed Scopus (38) Google Scholar], two of which were affected by the red tide in 2016, thus permitting physical traceability (records, labels). Such small panels of informative SNPs usually perform better