Exploring the microbial ecology and energetics of wild and domesticated Atlantic salmon (Salmo salar)
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Date
2023
Authors
Schaal, Patrick Daniel
Journal Title
Journal ISSN
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Publisher
University College Cork
Published Version
Abstract
Since the inception of Atlantic salmon (Salmo salar) aquaculture in the 1970s, millions of domesticated fish have escaped from aquaculture facilities into the wild. This phenomenon raises concerns about the ecological and genetic consequences of farmed fish interbreeding with their wild counterparts. The fitness of hybrid offspring from such interactions has long been recognised as diminished compared to pure wild salmon populations, thereby posing a substantial threat to the overall health and robustness of Atlantic salmon populations.
This study takes a comprehensive approach to investigate the impact of domestication on two vital aspects of Atlantic salmon biology: gut microbial communities and metabolism. Both traits have been identified as critical determinants of fish health and well-being. To disentangle the genetic effects from confounding environmental factors, this study employed common garden experiments. These experiments involved rearing fish with diverse genetic backgrounds, including wild, domesticated and reciprocal hybrids, together from the eyed-egg stage through both freshwater and marine phases. This design allowed us to simulate farmed escape and hybridisation events that naturally occur in the wild.
The first data chapter examines the drivers and sources that shape gut microbial assembly over time in juvenile Atlantic salmon in a natural river system. The study shows that the major contributors to the salmon intestine's microbial taxa come from macroinvertebrates, a potential food source, rather than the water column. Moreover, results suggest a possible role of host genetics in driving inter-individual differences in gut microbial community composition, leading to distinct microbiota assemblages between farmed, wild and hybrid fish. Neutral modelling further revealed that the majority of gut taxa are transient, underscoring the dynamic nature of these microbial communities and emphasizing the need to distinguish between transient and resident taxa within the gut environment.
The second data chapter examines the seasonal dynamics of gut microbial communities and energetics in juvenile Atlantic salmon, considering potential variations among farmed, wild and hybrid fish. The study unveils genetic factors as significant influencers of metabolic flexibility in Atlantic salmon. Wild fish exhibit lower metabolic rates in winter and higher rates in summer compared to farmed salmon, indicating their adaptability to seasonal environmental changes. This metabolic flexibility potentially enhances their chances of survival in variable wild environments compared to their farmed counterparts, which might exhibit less adaptability due to artificial selection for commercially favoured traits. Furthermore, our research unveils shifts in gut microbial communities during the winter months, particularly among the offspring of wild fish, possibly attributable to reduced feeding activity. This reduced activity, in turn, might be associated with their generally lower metabolic demands in winter.
The third data chapter assesses whether survivability, gut microbial structure and metabolic rate of Atlantic salmon reared in marine sea pens are affected by amoebic gill disease (AGD), a parasitic infection that poses a significant challenge to Atlantic salmon reared in aquaculture facilities, and if those effects vary between fish from farmed, wild and hybrid origins. Wild fish exhibited substantially higher mortality rates compared to their farmed counterparts, while hybrids fell in between. All fish, regardless of genetic origin, showed significantly lower metabolic rates with increased AGD infection rates. In addition, gut microbial diversity significantly declined in AGD-infected fish.
In summary, our study significantly contributes to our understanding of the complex interactions between host genetics, environmental factors and gut microbiota in Atlantic salmon. It offers indications that the domestication process in Atlantic salmon has influenced both host-associated microbiota and metabolism. As aquaculture continues to expand, these findings underscore the need for comprehensive conservation strategies to safeguard the ecological integrity of wild Atlantic salmon populations in the face of evolving aquaculture practices and the potential consequences of farmed fish escape events.
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Keywords
Atlantic salmon , Gut microbiota , Metabolism , Amoebic gill disease , Hybridisation , Farmed escapes , Aquaculture , Domestication , Common garden experiments , Salmon population fitness
Citation
Schaal, P. D. 2023. Exploring the microbial ecology and energetics of wild and domesticated Atlantic salmon (Salmo salar). PhD Thesis, University College Cork.