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Linking Ecology to Genetics to Better Understand Adaptation and Evolution: a Review in Marine Macrophytes

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Linking Ecology to Genetics to Better Understand Adaptation and Evolution: a Review in Marine Macrophytes fmars-07-545102 November 9, 2020 Time: 17:23 # 1 REVIEW published: 13 November 2020 doi: 10.3389/fmars.2020.545102 Linking Ecology to Genetics to Better Understand Adaptation and Evolution: A Review in Marine Macrophytes Zi-Min Hu1,2*, Kai-Le Zhong1,3, Florian Weinberger4, De-Lin Duan1,2, Stefano G. A. Draisma5 and Ester A. Serrão6 1 Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, China, 2 Laboratory for Marine Biology and Biotechnology, Qingdao National Laboratory for Marine Science and Technology, Qingdao, China, 3 College of Earth Science, University of Chinese Academy of Sciences, Beijing, China, 4 Department of Benthic Ecology, GEOMAR Helmholtz-Zentrum für Ozeanforschung Kiel, Kiel, Germany, 5 Excellence Center for Biodiversity of Peninsular Thailand, Faculty of Science, Prince of Songkla University, Hat Yai, Thailand, 6 Center of Marine Sciences, Faculty of Sciences and Technology, University of Algarve, Faro, Portugal Edited by: Ecological processes and intra-specific genetic diversity reciprocally affect each other. Christos Dimitrios Arvanitidis, While the importance of uniting ecological variables and genetic variation to understand Hellenic Centre for Marine Research species’ plasticity, adaptation, and evolution is increasingly recognized, only few studies (HCMR), Greece have attempted to address the intersection of population ecology and genetics using Reviewed by: Anne Chenuil, marine macrophyte as models. Representative empirical case studies on genetic Centre National de la Recherche diversity are reviewed that explore ecological and evolutionary processes in marine Scientifique (CNRS), France Francisco Arenas, macrophytes. These include studies on environment-induced phenotypic plasticity and University of Porto, Portugal associated ecological adaptation; population genetic variation and structuring driven *Correspondence: by ecological variation; and ecological consequences mediated by intraspecific and Zi-Min Hu interspecific diversity. Knowledge gaps are also discussed that impede the connection of [email protected] ecology and genetics in macrophytes and possible approaches to address these issues. Specialty section: Finally, an eco-evolutionary perspective is advocated, by incorporating structural-to- This article was submitted to functional genomics and life cycle complexity, to increase the understanding of the Marine Ecosystem Ecology, a section of the journal adaptation and evolution of macrophytes in response to environmental heterogeneity. Frontiers in Marine Science Keywords: adaptive genetic variation, divergent selection, ecological processes, phenotypic plasticity, ploidy Received: 23 April 2020 diversity, genetic consequences Accepted: 21 October 2020 Published: 13 November 2020 Citation: INTRODUCTION Hu Z-M, Zhong K-L, Weinberger F, Duan D-L, Local adaptive evolution (see explanation in Box 1, other terms are also explained in the Draisma SGA and Serrão EA (2020) same Box) and the evolution of phenotypic plasticity are both vital processes enabling Linking Ecology to Genetics to Better Understand Adaptation and Evolution: organisms in a population to obtain maximum fitness in response to heterogeneous A Review in Marine Macrophytes. environments. In the marine environment, migratory connectivity via genetic exchange of Front. Mar. Sci. 7:545102. adults, spores or propagules, is a salient difference compared with terrestrial ecosystem doi: 10.3389/fmars.2020.545102 (Palumbi, 1994). Marine connectivity counteracts local adaptation on one hand (so it may Frontiers in Marine Science| www.frontiersin.org 1 November 2020| Volume 7| Article 545102 fmars-07-545102 November 9, 2020 Time: 17:23 # 2 Hu et al. Ecological Genetics of Macrophyte decrease fitness locally), but by increasing gene flow (N M) e BOX 1 | Glossary of terms, defined in the context to link Ecology and it allows recolonization, reduces consanguinity, and may Genetics in marine macrophytes. increase effective size at the global (species or metapopulation) Acclimation: A phenotypic/physiological/metabolic change during an level (Bolnick and Nosil, 2007). Therefore, whether selection individual’s lifetime. favors phenotypic plasticity or local adaptation will depend Adaptation: A trans-generational fixed change at population level. Adaptive evolution: A kind of evolutionary change that is adaptive to a on the balance between spatial environmental heterogeneity particular environment, which enables an organism to cope with the and dispersal-mediated gene flow (van Tienderen, 1991). environment. Classic ecological genetic studies usually combined field (e.g., Adaptive genetic variation: The variation found in the genomes that has reciprocal transplant) and laboratory (e.g., common garden) evolved to help an organism to increase its fitness. approaches to investigate how natural selection generated Clonal propagation: Producing units derived from the same original reproductive cell that have the capacity for independent life, e.g., ramets adaptive variability among populations along different ecological (fronds). gradients (Schmidt et al., 2008). In recent years, the emergence Co-dominant: A locus where all its alleles are expressed, and heterozygotes of ecological/landscape genomics based on next-generation can therefore be discriminated from homozygotes. sequencing has provided more comprehensive insights into the Cryptic genetic variation: Unexpressed, bottled-up genetic variation that ways in which species respond to their changing environments may become expressed in a new environment. Divergent selection: The accumulation of differences between closely and into the limitations of their potential to adapt (Savolainen related populations within a species, which eventually may lead to speciation. et al., 2013). All these types of evidence hint at how genotype, Fitness: The ability of a phenotype–more rarely, population or species–to phenotype, and environment interact as a whole to ultimately survive and reproduce in an environment it inhabits. influence adaptive capability and evolvability (Figure 1). Genetic assimilation: A process whereby environmentally induced Seaweeds (macroalgae) and seagrasses, collectively termed phenotypes become genetically fixed and no longer require the original environmental stimulus. marine macrophytes, are ecologically important primary Introgression: The transfer of genetic information from one species to producers, carbon sinks, and ecosystem engineers, and highly another as a result of hybridization between them and repeated backcrossing. adaptive to environmental shifts (Reusch et al., 2005; Harley Landscape genetics: A scientific field aiming to study how landscape et al., 2012). Ecology and genetics can each influence diversity, features interact with microevolutionary processes (e.g., gene flow, genetic drift, and selection). plasticity, adaptation, and evolution of marine macrophytes Landscape genomics: Combines genomic concepts and technologies with (Pereyra et al., 2009; Padilla and Savedo, 2013; Duarte et al., landscape genetics approaches. 2018; Wernberg et al., 2018; Figure 1). Ecological factors, such NeM: The average number of effective migrants exchanged per generation. as habitat preferences, species interactions, and environmental Ne is the product of the effective population size, and M is the migration rate. gradients, can generate variable allelic frequencies in macrophyte Neutral genetic variation: A gene or locus that has no effect on fitness or may be subject to various constraints; large parts of an organism’s DNA are populations at specific genetic loci that are associated with effectively neutral. differentiated phenotypes (Schmidt et al., 2008), enabling them Outlier: An observation (or statistical measurement) that has an extreme value ∼ to adapt to different environments (e.g., Bergström and Kautsky, compared with the distribution of other FST D 1/(4NmC1) observations. 2006; Hays, 2007). In turn, genetic variation/diversity can alter or Phenotypic plasticity: The ability of one genotype to generate more than modify the fitness and evolvability of organisms, and hence the one phenotype when exposed to different environmental conditions by modifying phenotypic traits during an individual’s lifetime (Bradshaw, 1965). way species metabolize, grow and survive, and ultimately interact Quantitative Trait Loci: Sections of the genome that correlate with a with a changing ecosystem (e.g., Bracken et al., 2008; Hughes particular phenotypic trait of a population or an organism. et al., 2008). Unraveling the link between adaptive genetic Seascape genetics: A scientific field aiming to study how spatially variable variation, ecological adaptation, and phenotypic alteration is structural and environmental features affect genetic profiles of marine also a major goal in evolutionary biology and conservation organisms. biogeography of macrophytes under climate change (Harley et al., 2012; Hu and Fraser, 2016). There is a widespread conceptual recognition that ecological 2013). Here we summarize the major findings and challenges and genetic methods should be united to study adaptation, associated either with ecological processes or genetic diversity speciation, and morphological diversity of marine macrophytes in macrophytes responding to environmental shifts. We choose (Serrão et al., 1996; Gabrielsen et al., 2002; Leskinen et al., representative studies to illustrate how typical ecological factors 2004; Reusch et al.,
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