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Perspectives on domestication research for sustainable seaweed aquaculture

Authors:
Myriam Valero at Roscoff Marine Station
Myriam Valero
Marie-Laure Guillemin at Universidad Austral de Chile
Marie-Laure Guillemin
Christophe Destombe at Sorbonne University
Christophe Destombe
Bertrand Jacquemin at MAARI (MacroAlgae Aquaculture Research & Innovation)
Bertrand Jacquemin
  • MAARI (MacroAlgae Aquaculture Research & Innovation)
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Abstract

In this paper, we address several issues related to seaweed domestication from an evolutionary and ecological perspective. We briefly cover the history of human interactions with seaweed and assess the importance of pre-domestication evolutionary processes. The various steps of the trajectory from wild to domesticated seaweeds are discussed for five crop seaweeds (i.e. Saccharina japonica (kombu), Pyropia sp. (nori), Undaria pinnatifida (wakame), Gracilaria chilensis (pellilo) and Kappaphycus sp.) to evaluate their domestication status. We show that seaweed domestication resulted from long-term interactions between humans, seaweeds, and environmental factors. This interplay has deeply modified the coastal ecosystem – sometimes with very detrimental effects (pests and invasions) – but was a key element in the evolutionary process leading to domestication. We then highlight the challenges for future research on seaweed domestication and show how better integration of knowledge on ecology and genetic diversity of wild populations and on the selective pressures exerted by cultivators can promote sustainable seaweed aquaculture.
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Perspectives in Phycology PrePub Article
Published online February 2017
© 2017 E. Schweizerbart’sche Verlagsbuchhandlung, 70176 Stuttgart, Germany www.schweizerbart.de
DOI: 10.1127/pip/2017/0066 10.1127/pip/2017/0066 $ 6.30
Perspectives on domestication research for sustainable seaweed aquaculture
Myriam Valero1,*, Marie-Laure Guillemin1,2, Christophe Destombe1, Bertrand Jacquemin1,
Claire M.M. Gachon3, Yacine Badis3, Alejandro H. Buschmann4, Carolina Camus4 and
Sylvain Faugeron1,5
1 CNRS, UMI 3614 Evolutionary Biology and Ecology of Algae, Sorbonne Universités, UPMC Univ Paris 6,
Ponticia Universidad Católica de Chile, Universidad Austral de Chile, Station Biologique de Roscoff, CS
90074, Place Georges Teissier, 29688 Roscoff cedex, France
2 Instituto de Ciencias Ambientales y Evolutivas, Universidad Austral de Chile, Casilla 567, Valdivia, Chile
3 Scottish Association for Marine Science, Scottish Marine Institute, Oban, PA37 1QA, United Kingdom
4 Centro i-mar and CeBiB, Universidad de los Lagos, Camino a Chinquihue km6, Puerto Montt, Chile
5 Centro de Conservación Marina, Departamento de Ecología, Facultad de Ciencias Biológicas, Ponticia
Universidad Católica de Chile, Casilla 114-D, Chile
* Corresponding author: valero@sb-roscoff.fr
With 3 gures and 1 table
Abstract: In this paper, we address several issues related to seaweed domestication from an evolutionary and ecological perspective. We
briey cover the history of human interactions with seaweed and assess the importance of pre-domestication evolutionary processes. The
various steps of the trajectory from wild to domesticated seaweeds are discussed for ve crop seaweeds (i.e. Saccharina japonica (kombu),
Pyropia sp. (nori), Undaria pinnatida (wakame), Gracilaria chilensis (pellilo) and Kappaphycus sp.) to evaluate their domestication
status. We show that seaweed domestication resulted from long-term interactions between humans, seaweeds, and environmental factors.
This interplay has deeply modied the coastal ecosystem – sometimes with very detrimental effects (pests and invasions) – but was a key
element in the evolutionary process leading to domestication. We then highlight the challenges for future research on seaweed domestica-
tion and show how better integration of knowledge on ecology and genetic diversity of wild populations and on the selective pressures
exerted by cultivators can promote sustainable seaweed aquaculture.
Keywords: Domestication, interaction, coevolution, algal resource management, genetic diversity, seaweed cultivation and aquaculture,
marine agronomy
Introduction
Domestication is considered a long and complex process
during which domesticators select and modify organisms
that can thrive in human eco-environments and express traits
of interest for human use (Tanno & Wilcox 2006, Larson et
al. 2014). Hence, domestication involves a multi-genera-
tional relationship between humans and the target organism.
Denitions of domestication vary depending on the nature
of this relationship and here we adopt the recent denition
by Zeder (2015): “a coevolutionary, mutualistic relationship
between domesticators and domesticates”. Interestingly,
Zeder (2015) draws attention to the fact that domestication
should be distinguished from resource management and
agriculture even if there is a continuum between these three
different but overlapping processes. Management is based
on enhancing the returns of the resource of interest, agricul-
ture is a provisioning system based on the production and
consumption of domesticates, whereas domestication is a
coevolving mutualism between the manager and the man-
aged resources. This evolutionary approach to domestication
focuses on the processes that intensify a species’ dependence
on humans for reproduction and dispersal (Milla et al. 2015).
Moreover, because the evolution of a species leads to evolu-
tion of its ecological niche (according to ecological niche
construction theory), domestication is also associated with
ecological changes in the environment driven by humans to
optimize the cultivation conditions of the domesticated spe-
cies (Smith 2016). “This close relationship between humans
and their domesticated plants and animals is precisely one
of the aspects that makes the study of domestication such a
fascinating area of study” (Gepts 2010). Full understanding
of the domestication process can only be achieved within a
cross-disciplinary framework that brings together genetics,
evolutionary biology, ecology, and anthropology (Larson
... Few seaweed species, like other marine fishes and invertebrates, are within the more recent groups of domesticated organisms (Duarte et al. 2007;Valero et al. 2017). In these crops that have been under human selection for much fewer generations than the traditional terrestrial ones, the use of new methods, such as marker-assisted selection (MAS), could help to accelerate crop improvement. ...
... However, even without a clear strategy for crop improvement, other crops have been influenced by cultivation techniques applied on farms. For example, in G. chilensis, it has been proposed that inconsistent selection by algal farmers for fast-growing genotypes has led to crops mostly dominated by highly heterozygous diploid tetrasporophytes (Guillemin et al. 2008b;Valero et al. 2017) that invert very few of their resources in sexual reproduction (Guillemin et al. 2008b;Usandizaga et al. 2021). Laboratory and field experiments have also proposed that Chilean farmers have selected general-purpose genotypes able to maintain high constant fitness across a range of abiotic conditions (Gallegos Sanchez et al. 2018;Usandizaga et al. 2019Usandizaga et al. , 2021. ...
... Laboratory and field experiments have also proposed that Chilean farmers have selected general-purpose genotypes able to maintain high constant fitness across a range of abiotic conditions (Gallegos Sanchez et al. 2018;Usandizaga et al. 2019Usandizaga et al. , 2021. Inconscient selection over a few decades can have profound repercussions for Gracilaria farming as it could lead to the uncoupling of the sexual haploiddiploid life cycle (i.e., one phase is lost in the farming environment) and a loss of fertility (Guillemin et al. 2008b;Valero et al. 2017). Because it affects the capacity to use crop-selected strains for breeding, these changes could ultimately impede future crop improvement, as has already been observed in other mostly asexually maintained crops (Zohary 2004;McKey et al. 2010). ...
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... Transitioning to aquaculture produces high-quality biomass on a large scale, safeguarding wild populations while supporting blue economy industries [21,23]. Also, cultivating indigenous seaweed species, rather than introducing non-native varieties, is essential to protect ecosystem integrity and prevent potential invasions that can disrupt native biodiversity and marine habitats [24,25]. However, the main commercial sources of carrageenan are the Asian species Eucheuma and Supplementary Materials: The following supporting information can be downloaded at: https://www.mdpi.com/article/10.3390/app15020810/s1, ...
... Among marine organisms, seaweeds have traditionally been harvested from the wild for a variety of uses, including food, animal feed, and soil Kappaphycus species, which account for over 90% of global production [9]. As there are only a few cultivated species, it is important to find indigenous species that can be domesticated to increase the number of cultivated species and provide the market with a wide range of biological raw materials [25]. ...
... cultivating indigenous seaweed species, rather than introducing non-native varieties, is essential to protect ecosystem integrity and prevent potential invasions that can disrupt native biodiversity and marine habitats [24,25]. However, the main commercial sources of carrageenan are the Asian species Eucheuma and Kappaphycus species, which account for over 90% of global production [9]. ...
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... As seaweeds are domesticated, shifts in reproductive strategy are likely to occur. In red seaweeds cultivated globally, domesticated strains reproduce predominantly or solely vegetatively, in contrast to wild populations of the same species where sexual reproduction is common (Guillemin et al. 2008;Valero et al. 2017). Strictly clonal propagation facilitates strain selection and prevents farm to wild gene flow but restricts the potential for further breeding improvement (Valero et al. 2017). ...
... In red seaweeds cultivated globally, domesticated strains reproduce predominantly or solely vegetatively, in contrast to wild populations of the same species where sexual reproduction is common (Guillemin et al. 2008;Valero et al. 2017). Strictly clonal propagation facilitates strain selection and prevents farm to wild gene flow but restricts the potential for further breeding improvement (Valero et al. 2017). Clonally reproducing strains may still become pests and negatively impact wild stocks, e.g., if escaped fragments establish and outcompete local native strains (Loureiro et al. 2015;Brakel et al. 2021), such has occurred with Eucheuma denticulatum in Tanzania (Tano et al. 2015). ...
... Domestication of clonally propagated haplo-diploid red seaweeds with isomorphic phases has favoured selection of diploid phases (Guillemin et al. 2008;Valero et al. 2017 In cultivated seaweeds that are propagated sexually (brown seaweeds including wakame and kombu, red seaweeds including nori), inbreeding and selfing are common (Valero et al. 2017). ...
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... One of the main advantages of spore propagation is the enhancement of genetic diversity/validation in the cultivated population through the usage of sexually developed spores, and the detailed advantages of adopting spore-based seaweed cultivation over conventional cultivation are given in Table 12.1. This diversity can improve resilience against diseases and environmental stressors, making it potentially robust compared to vegetative means of propagation (Coelho et al. 2019a, b;Valero et al. 2017). Spore propagation enables large quantities of production from a single fertile frond which causes efficient scale-up for commercial seaweed farming to meet high demand compared to traditional methods through direct planting of mature seaweed fragments. ...
... We can address the problem through the selection and propagation of clonal lines derived from superior individuals. However, this method has its own challenges because clonal propagation reduces genetic diversity, and seaweed becomes more susceptible to diseases and environmental changes (Sahoo and Yarish 2005;Valero et al. 2017). Additionally, maintenance of clonal lines in tank-based systems requires careful attention to prevent contamination and maintain genetic integrity over multiple generations (Gachon et al. 2010a, b, c;Yarish et al. 2002). ...
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