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Patterns of Population Structure and Complex Haplotype Sharing Among Field Isolates of the Green Alga Chlamydomonas Reinhardtii

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Patterns of Population Structure and Complex Haplotype Sharing Among Field Isolates of the Green Alga Chlamydomonas Reinhardtii Received: 1 April 2019 | Revised: 5 July 2019 | Accepted: 17 July 2019 DOI: 10.1111/mec.15193 ORIGINAL ARTICLE Patterns of population structure and complex haplotype sharing among field isolates of the green alga Chlamydomonas reinhardtii Rory J. Craig1,2 | Katharina B. Böndel1,3 | Kazuharu Arakawa4,5 | Takashi Nakada4,5,6 | Takuro Ito4,5 | Graham Bell7 | Nick Colegrave1 | Peter D. Keightley1 | Rob W. Ness2 1Institute of Evolutionary Biology, School of Biological Sciences, University of Edinburgh, Abstract Edinburgh, UK The nature of population structure in microbial eukaryotes has long been debated. 2 Department of Biology, University of Competing models have argued that microbial species are either ubiquitous, with Toronto Mississauga, Mississauga, ON, Canada high dispersal and low rates of speciation, or that for many species gene flow be- 3Institute of Plant Breeding, Seed Science tween populations is limited, resulting in evolutionary histories similar to those of and Population Genetics, University of Hohenheim, Stuttgart, Germany macroorganisms. However, population genomic approaches have seldom been ap- 4Institute for Advanced Biosciences, Keio plied to this question. Here, we analyse whole‐genome resequencing data for all University, Tsuruoka, Japan 36 confirmed field isolates of the green alga Chlamydomonas reinhardtii. At a con- 5Systems Biology Program, Graduate School tinental scale, we report evidence for putative allopatric divergence, between both of Media and Governance, Keio University, Fujisawa, Japan North American and Japanese isolates, and two highly differentiated lineages within 6 Faculty of Environment and Information N. America. Conversely, at a local scale within the most densely sampled lineage, Sciences, Yokohama National University, Yokohama, Japan we find little evidence for either spatial or temporal structure. Taken together with 7Department of Biology, McGill University, evidence for ongoing admixture between the two N. American lineages, this lack of Montreal, QC, Canada structure supports a role for substantial dispersal in C. reinhardtii and implies that Correspondence between‐lineage differentiation may be maintained by reproductive isolation and/ Rory J. Craig and Rob W. Ness, Department or local adaptation. Our results therefore support a role for allopatric divergence in of Biology, University of Toronto Mississauga, Mississauga, ON L5L 1C6, microbial eukaryotes, while also indicating that species may be ubiquitous at local Canada. scales. Despite the high genetic diversity observed within the most well‐sampled Emails: [email protected] and rob.ness@ utoronto.ca lineage, we find that pairs of isolates share on average ~9% of their genomes in long haplotypes, even when isolates were sampled decades apart and from different loca- Funding information Yamagata Prefectural Government/ tions. This proportion is several orders of magnitude higher than the Wright–Fisher Tsuruoka City; European Research Council expectation, raising many further questions concerning the evolutionary genetics of under the European Union's Horizon 2020 Research and Innovation Programme, Grant/ C. reinhardtii and microbial eukaryotes generally. Award Number: 694212; Biotechnology and Biological Sciences Research Council; KEYWORDS Canada Foundation for Innovation JELF; Natural Sciences and Engineering Research admixture, Chlamydomonas reinhardtii, genetic differentiation, identity by descent, microbial Council of Canada eukaryotes, population structure Molecular Ecology. 2019;28:3977–3993. wileyonlinelibrary.com/journal/mec © 2019 John Wiley & Sons Ltd | 3977 3978 | CRAIG ET AL. 1 | INTRODUCTION abundance and phylogenetic diversity (Pawlowski et al., 2012), and very few population genomic data sets currently exist for free‐living ‘Everything is everywhere: but the environment selects’ (Baas species (Johri et al., 2017). Such data sets are required to fully cap- Becking, 1934) has been a long‐standing tenet of microbiology ture patterns of genetic diversity within and between populations, (O'Malley, 2008). Under this paradigm, dispersal is considered to be to reveal complex patterns of migration and gene flow, and to iden- effectively unlimited, and the biogeography and evolutionary histo- tify loci putatively contributing to local adaptation and speciation. ries of microbial species should therefore be determined by ecol- Here, we analyse whole‐genome resequencing data for all ogy, rather than geography. For microbial eukaryotes (i.e. protists currently available Chlamydomonas reinhardtii field isolates. C. re‐ and other unicellular/colonial eukaryotes), this has been extended inhardtii is a soil‐dwelling unicellular green alga that is used ex- to the ubiquity model (Fenchel & Finlay, 2004; Finlay, 2002; Finlay & tensively as a model organism for plant physiology, molecular and Fenchel, 1999), which predicts both cosmopolitan distributions and cell biology (Blaby et al., 2014; Harris, 2001, 2008), experimental low rates of speciation, due to the extremely large population sizes evolution (Bell, 1997; Colegrave, 2002; Collins & Bell, 2004), and and high dispersal of species. This view has been countered by the biofuel research (Scranton, Ostrand, Fields, & Mayfield, 2015). moderate endemicity model (Foissner, 1999, 2006, 2008), which pos- Despite its importance as a model system, very little is known its that dispersal is limited for many species, and as such, the taxo- about the ecology and evolutionary history of the species (Sasso, nomic diversity, biogeography and evolution of microbial eukaryotes Stibor, Mittag, & Grossman, 2018). For many years, C. reinhardtii are generally expected to be more similar to that of macroorganisms. had only been isolated from eastern North America, suggesting Exploring the validity of these opposing models is thus crucial for that the species may be endemic (Pröschold, Harris, & Coleman, determining microbial eukaryotic biodiversity, for understanding the 2005). However, isolates that are interfertile with N. American rate and mode of speciation in understudied lineages, and for pro- laboratory strains have since been discovered in Japan, imply- viding insights into the ecology and evolutionary histories of individ- ing a more cosmopolitan distribution (Nakada, Shinkawa, Ito, & ual species of interest. Tomita, 2010; Nakada, Tsuchida, Arakawa, Ito, & Tomita, 2014). Empirical tests of the two competing models have, however, Two previous studies have reported evidence for population largely been based on morphology, and their interpretation has been structure in field isolates of C. reinhardtii (Flowers et al., 2015; highly dependent on the species concept employed (Caron, 2009). Jang & Ehrenreich, 2012), but sampling was limited to N. America, DNA sequence‐based studies of microbial eukaryotes are therefore and between the studies, a total of only 12 isolates were anal- of great importance, primarily to broadly delineate species (due to ysed, limiting the inferences that could be drawn. Furthermore, the prevalence of cryptic speciation; Lahr, Laughinghouse, Oliverio, although there are excellent genomic resources available for C. re‐ Gao, & Katz, 2014), but more specifically to characterize the nature inhardtii (Blaby et al., 2014; Merchant et al., 2007), the low number of population structure within species. Genetic structure can arise as of sequenced isolates has hindered the study of the population a result of barriers to gene flow formed by limited dispersal (allopatry genetics of the species. C. reinhardtii has several attributes that or isolation by distance), reduced establishment of migrants (‘isola- make it a particularly interesting model for population genetics. tion by adaptation’) or more complex patterns caused by founder Synonymous genetic diversity (~3%) and the estimated effective events (‘isolation by colonization’; Orsini, Vanoverbeke, Swillen, population size (~108) are amongst the highest reported in eukary- Mergeay, & De Meester, 2013). Exploring the extent of population otes (Flowers et al., 2015), and its haploid state makes it highly structure and its causes can be used to test between the ubiquity amenable to studying recombination and evolutionary phenomena and moderate endemicity models, as the former predicts a lack of di- that would otherwise require haplotype phasing. vergence in allopatry or isolation by distance, and little evidence for In this study, we explore patterns of population structure in- recent speciation events, in contrast to what is observed in many ferred from 36 C. reinhardtii isolates sampled at three scales: (a) plants and animals. Evidence for genetically structured populations local, both between and within sites and time points in Quebec; (b) has recently been reported across a variety of taxa and habitats, within continent, between N. American isolates; and (c) between including examples from ciliates (Zufall, Dimond, & Doerder, 2013), continent, specifically between N. American and Japanese isolates. amoebae (Douglas, Kronforst, Queller, & Strassmann, 2011; Heger, Overall, we report evidence for allopatric divergence, both between Mitchell, & Leander, 2013), diatoms (Casteleyn et al., 2010; Sjöqvist, N. American and Japanese isolates, and putatively between two Godhe, Jonsson, Sundqvist, & Kremp, 2015; Vanormelingen et al., highly differentiated lineages in N. America, supporting the moder‐ 2015; Whittaker & Rynearson, 2017), dinoflagellates (Lowe, Martin, ate endemicity model for the species. We find evidence for substan-
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