Phylogeny and Evolution of the Brown Algae Trevor Bringloe, Samuel Starko, Rachael Wade, Christophe Vieira, Hiroshi Kawai, Olivier De Clerck, J
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Phylogeny and Evolution of the Brown Algae Trevor Bringloe, Samuel Starko, Rachael Wade, Christophe Vieira, Hiroshi Kawai, Olivier de Clerck, J. Mark Cock, Susana Coelho, Christophe Destombe, Myriam Valero, et al. To cite this version: Trevor Bringloe, Samuel Starko, Rachael Wade, Christophe Vieira, Hiroshi Kawai, et al.. Phylogeny and Evolution of the Brown Algae. Critical Reviews in Plant Sciences, Taylor & Francis, 2020, 39, pp.281 - 321. 10.1080/07352689.2020.1787679. hal-02995644 HAL Id: hal-02995644 https://hal-cnrs.archives-ouvertes.fr/hal-02995644 Submitted on 9 Nov 2020 HAL is a multi-disciplinary open access L’archive ouverte pluridisciplinaire HAL, est archive for the deposit and dissemination of sci- destinée au dépôt et à la diffusion de documents entific research documents, whether they are pub- scientifiques de niveau recherche, publiés ou non, lished or not. The documents may come from émanant des établissements d’enseignement et de teaching and research institutions in France or recherche français ou étrangers, des laboratoires abroad, or from public or private research centers. publics ou privés. CRITICAL REVIEWS IN PLANT SCIENCES https://doi.org/10.1080/07352689.2020.1787679 Phylogeny and Evolution of the Brown Algae Trevor T. Bringloea , Samuel Starkob, Rachael M. Wadec, Christophe Vieirad, Hiroshi Kawaid, Olivier De Clercke , J. Mark Cockf , Susana M. Coelhof, Christophe Destombeg , Myriam Valerog , Jo~ao Neivah , Gareth A. Pearsonh , Sylvain Faugerong,i , Ester A. Serr~aoh, and Heroen Verbruggena aSchool of BioSciences, University of Melbourne, Victoria, Australia; bDepartment of Biology, University of Victoria, Victoria, Canada; cDepartment of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, USA; dKobe University Research Center for Inland Seas, Rokkodai, Kobe, Japan; eDepartment of Biology, Phycology Research Group, Ghent University, Ghent, Belgium; fAlgal Genetics Group, CNRS, Sorbonne Universite, UMR 8227, Integrative Biology of Marine Models, Station Biologique de Roscoff, Roscoff, France; gEvolutionary Biology and Ecology of Algae, CNRS, Sorbonne Universite, Pontificia Universidad Catolica de Chile, Universidad Austral de Chile, UMI 3614, Station Biologique de Roscoff, Roscoff, France; hCentre for Marine Sciences (CCMAR), University of Algarve, Faro, Portugal; iFacultad de Ciencias Biologicas, Pontificia Universidad Catolica de Chile, Santiago, Chile ABSTRACT KEYWORDS The brown algae (Phaeophyceae) are a group of multicellular heterokonts that are ubiqui- Biogeography; complex life tous in today’s oceans. Large brown algae from multiple orders are the foundation to tem- cycles; diversity; genomics; perate coastal ecosystems globally, a role that extends into arctic and tropical regions, seaweed; speciation providing services indirectly through increased coastal productivity and habitat provisioning, and directly as a source of food and commercially important extracts. Recent multi-locus and genome-scale analyses have revolutionized our understanding of the brown algal phyl- ogeny, providing a robust framework to test evolutionary hypotheses and interpret genomic variation across diverse brown algal lineages. Here, we review recent developments in our understanding of brown algal evolution based on modern advances in phylogenetics and functional genomics. We begin by summarizing modern phylogenetic hypotheses, illuminat- ing the timescales over which the various brown algal orders diversified. We then discuss key insights on our understanding of brown algal life cycle variation and sexual reproduc- tion systems derived from modern genomic techniques. We also review brown algal speci- ation mechanisms and the associated biogeographic patterns that have emerged globally. We conclude our review by discussing promising avenues for future research opened by genomic datasets, directions that are expected to reveal critical insights into brown algal evolution in past, present, and future oceans. I. The nature and origin of brown algae dimensional growth (Fritsch, 1935; Starko and The brown algae (Phaeophyceae) comprise approxi- Martone, 2016a). These features have contributed to mately 2000 described species, and are one of few the emergence and diversification of the world’s larg- eukaryotic lineages to have evolved complex multicel- est marine autotrophs (e.g. Laminariales, Fucales) lularity (Charrier et al., 2008; Knoll, 2011; Cock et al., besides clonal plants (e.g. Arnaud-Haond et al., 2012), 2014). Along with other multicellular groups such as and have restructured the dynamics of coastal marine metazoans, fungi and green plants, brown algae pos- ecosystems around the world (Steinberg et al., 1995; sess several key characteristics that have enabled them Steneck et al., 2002; Pyenson and Vermeij, 2016; to thrive as macroscopic organisms (Charrier et al., Starko et al., 2019; Vermeij et al., 2019). Brown algae 2008), including cell-to-cell adhesion and communica- also exhibit striking morphological variation across tion (Charrier et al., 2008; Cock et al., 2010; 2014; species, differing substantially in their level of com- Deniaud-Bou€et et al., 2014), tissue differentiation plexity at the levels of cells, tissues and organs (Fritsch, 1935; Kloareg and Quatrano, 1988), internal (Fritsch, 1935). A thorough understanding of brown transport of sugars (Fritsch, 1935; Schmitz and algal evolution and systematics is essential for disen- Srivastava, 1976) and the capacity for three tangling the processes underlying the evolution of CONTACT Trevor T. Bringloe [email protected] School of BioSciences, University of Melbourne, Victoria, Australia Supplemental data for this article is available online at at publisher’s website. ß 2020 Taylor & Francis Group, LLC 2 T. T. BRINGLOE ET AL. complexity in this group and its implications for $500,000–1,000,000 per year per km of coastline coastal ecosystems globally. (Filbee-Dexter and Wernberg, 2018). Given that for- Brown algae play fundamental roles in the func- ests of large brown algae dominate approximately 25% tioning of coastal marine ecosystems. Large brown of the world’s coastlines (Wernberg et al., 2019), the algae, particularly those in the orders Laminariales, global value of ecosystem services provided by brown Tilopteridales, Fucales, and Desmarestiales, act as eco- algae is likely to be in the hundreds of billions of system engineers (Bruno and Bertness, 2001; Schiel USD per year. and Foster, 2006; Mineur et al., 2015, Teagle et al., In addition to the indirect benefits that they pro- 2017) and are dominant members of intertidal and vide to humans by maintaining ecosystem functioning shallow subtidal ecosystems worldwide (Steneck et al., in nearshore marine environments, brown algae hold 2002; Schiel and Foster, 2006; Teagle et al., 2017). direct economic value through food harvests and Large brown algae form complex underwater forests commercial extracts (Mautner, 1954;Vasquez et al., that dramatically increase the structural complexity of 2014; Bennett et al., 2016; Milledge et al., 2016). marine ecosystems (Steneck et al., 2002; Teagle et al., Brown algae have long been used as a food source by 2017) and alter environmental factors such as light human communities with coastal access (Tseng, 1981; (Gerard, 1984; Connell, 2003a; Gattuso et al., 2006), Druehl, 1988; McHugh, 2003). Today, brown algae are fluid dynamics (Hurd and Stevens, 1997; Stephens harvested from the wild and through aquaculture and Hepburn, 2014), sedimentation (Connell, 2003b; operations around the world (Fleurence et al., 2012; Filbee-Dexter et al., 2016) and food availability Charrier et al., 2017; Bennion et al., 2019). The global (Duggins et al., 1989; Estes et al., 2016). Large brown harvest of brown macroalgae from wild stocks is esti- algae also provide habitat for a wide range of other mated at more than half a million tonnes per year taxa (Steneck et al., 2002; Graham, 2004; Teagle et al., and has been increasing in recent decades (Mac 2017; Hind et al., 2019), including many commercially Monagail et al., 2017). The polysaccharide metabolism important animals (Bologna and Steneck, 1993; Smale of brown algae is unique among photoautotrophs et al., 2013; Markel et al., 2017), and serve as essential (including red and green algae) and many of these nursery grounds for many species (Holbrook et al., polysaccharides are desirable for their bioactive prop- 1990; Kitada et al., 2019). Besides habitat provision, erties. For example, fucose-containing sulfated poly- brown algae are a key source of productivity along the saccharides (FCSPs), found in the cell wall and coast (Mann, 1973; Pfister et al., 2019) and can sig- extracellular matrices of brown algae (Deniaud-Bouet nificantly increase secondary productivity in nearshore et al., 2014; Kloareg and Quatrano, 1988), can have ecosystems through direct herbivory and increased anti-inflammatory, anti-viral, anti-biotic, anti-oxidant, detrital production (Duggins et al., 1989; Krumhansl anti-coagulant, and anti-adhesive properties (Li et al., and Scheibling, 2012). This energy input plays an 2008; Morya et al., 2012), and are widely used in important role in maintaining food security for many medicine and cosmetics (Li et al., 2008; Fitton, 2011). large mammals (Estes et al., 2016; Pyenson and Alginates, carbohydrate polymers made up of man- Vermeij, 2016; Vermeij et al., 2019), including nuronic and guluronic acids (Kloareg and Quatrano, humans, and is believed to have facilitated