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Seascape Genetics of the Stalked Kelp Pterygophora Californica and Comparative Population Genetics in the Santa Barbara Channel1

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Seascape Genetics of the Stalked Kelp Pterygophora Californica and Comparative Population Genetics in the Santa Barbara Channel1 J. Phycol. 56, 110–120 (2020) © 2019 Phycological Society of America DOI: 10.1111/jpy.12918-19-050 SEASCAPE GENETICS OF THE STALKED KELP PTERYGOPHORA CALIFORNICA AND COMPARATIVE POPULATION GENETICS IN THE SANTA BARBARA CHANNEL1 Heidi L. Hargarten Tree Fruit Research Laboratory, US Department of Agriculture – Agricultural Research Service, Wenatchee, Washington 98801, USA Mattias L. Johansson Department of Biology, University of North Georgia, Oakwood, Georgia 30566, USA Daniel C. Reed Marine Science Institute, University of California, Santa Barbara, California 93106, USA Nelson C. Coelho Department of Computational and Systems Biology, School of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania 15261, USA David A. Siegel Earth Research Institute and Department of Geography, University of California, Santa Barbara, California 93106, USA and Filipe Alberto2 Department of Biological Sciences, University of Wisconsin – Milwaukee, Milwaukee, Wisconsin 53201, USA We conducted a population genetic analysis of the differentiation and pairwise differentiation were stalked kelp, Pterygophora californica, in the Santa similar among patches between the two kelp species, Barbara Channel, California, USA. The results were indicating that they have similar dispersal capabilities compared with previous work on the genetic despite their differences in rafting ability. These differentiation of giant kelp, Macrocystis pyrifera, in results suggest that rafting sporophytes do not play the same region. These two sympatric kelps not only a significant role in effective dispersal of share many life history and dispersal characteristics M. pyrifera at ecologically relevant spatial and but also differ in that dislodged P. californica does temporal scales. not produce floating rafts with buoyant fertile sporophytes, commonly observed for M. pyrifera.We Key index words: comparative population genetics; used a comparative population genetic approach with dispersal; genetic structure; giant kelp; marine con- these two species to test the hypothesis that nectivity; seascape genetics; stalked kelp the ability to produce floating rafts increases the Abbreviations: AB, Arroyo Burro; AH, Arroyo genetic connectivity among kelp patches in the Santa Hondo; AIC, Akaike information criterion is an esti- Barbara Channel. We quantified the association of mator of the relative quality of statistical models for habitat continuity and oceanographic distance with a given set of data; AQ, Arroyo Quemado; AR, Alle- the genetic differentiation observed in stalked kelp, lic richness standardized by sample size; B, Bullito; like previously conducted for giant kelp. We C, Carpinteria; CPG, Comparative population genet- compared both overall (across all patches) and ics; DEST, Estimator of genetic differentiation not pairwise (between patches) genetic differentiation. biased by the scale of genetic diversity (allelic rich- We found that oceanographic transit time, habitat ness or heterozygosity); FIS, Inbreeding coefficient; continuity, and geographic distance were all FST, Genetic differentiation or the proportion of associated with genetic connectivity in P. californica, the total genetic variance contained in a subpopula- supporting similar previous findings for M. pyrifera. tion relative to the total genetic variance; GeoDist, Controlling for differences in heterozygosity between Geographic distance; G, Goleta Bay; HabCont, kelp species using Jost’s DEST, we showed that global Habitat continuity; IBD, Isolation by distance model of genetic differentiation; IV, Isla Vista; M, 1Received 19 March 2019. Accepted 29 August 2019. First Pub- Mohawk; N, Naples Reef; TT, Minimum oceano- lished Online 12 September 2019. Published Online 6 November 2019, Wiley Online Library (wileyonlinelibrary.com). graphic transit time between two sites, the shortest 2Author for correspondence: e-mail [email protected]. transit time of the pair pop.i to pop.j or pop.j to Editorial Responsibility: M. Roleda (Associate Editor) popi 110 POPULATION GENETICS OF STALKED KELP 111 Dispersal is the universal mechanism that pro- Gene flow in kelps is intimately linked to their motes gene flow and population connectivity. heteromorphic life history characterized by a large Although several different dispersal mechanisms diploid sporophyte and a microscopic haploid have evolved in the ocean, the primary strategy gametophyte. Sporophytes produce haploid zoos- employed by species with sessile adult forms is the pores via meiosis that are released into the water production of planktonic propagules that are pas- column and disperse passively via oceanic currents sively dispersed locally or over long distances by over distances of meters to kilometers (Reed et al. ocean currents (Siegel et al. 2003, Sagarin et al. 1988, 1992, 2004, Gaylord et al. 2006, 2012). Upon 2006, Cowen and Sponaugle 2009, Selkoe et al. settling to the bottom zoospores germinate into ses- 2016, Padron et al. 2018, Xuereb et al. 2018). Con- sile, free-living male and female gametophytes that ventional theory predicts that organisms having produce gametes that disperse over distances of just long-lived planktonic stages have higher levels of a few millimeters (Muller 1981, Reed 1990). Thus, gene flow than those with short-lived planktonic genetic connectivity among kelp populations occurs stages (Siegel et al. 2003, Weersing and Toonen almost exclusively either through the dispersal of 2009, Selkoe et al. 2010). However, this is not always planktonic zoospores or reproductive sporophytes the case as cryptic ocean barriers, environmental that become dislodged and set adrift. The relative gradients, and temporal oscillations in oceano- importance of these two mechanisms in contribut- graphic circulation can create unexpected patterns ing to gene flow and population dynamics in kelps of connectivity and genetic structure across a range has been a topic of much discussion and debate of spatial scales (Gilg and Hilbish 2003, Johansson (Dayton 1985, Santelices 1990, Reed et al. 2004, et al. 2008, Treml et al. 2008, Alberto et al. 2011, 2006, Graham et al. 2007, Schiel and Foster 2015). DeFaveri et al. 2013, Liggins et al. 2013, Xuereb Integrating genetic studies of adult populations into et al. 2018). The effects of these factors on dispersal this discussion has the potential to provide addi- and gene flow depend on population history tional insight into the relative importance of these (Nesbo€ et al. 2000, Pelc et al. 2009), demography two mechanisms in promoting dispersal and gene (Dawson et al. 2002), life history (Shulman and Ber- flow in kelps (Alberto et al. 2010, 2011, Valero et al. mingham 1995, Sponaugle and Cowen 1997, Turner 2011, Robuchon et al. 2014, Evankow 2015). and Trexler 1998), and propagule behavior In the northeast Pacific, the kelps Pterygophora cali- (Pineda-Krch and Fagerstrom 1999, Paris et al. fornica and Macrocystis pyrifera commonly co-occur 2007, Pringle and Wares 2007, Woodson and McMa- in kelp forests from British Columbia, Canada to nus 2007, Cowen and Sponaugle 2009, Morgan and Baja California, Mexico (Abbott et al. 1992). The Fisher 2010, Pineda et al. 2010). As a result, com- stalked kelp P. californica grows 1–3 m in height and parisons of gene flow patterns between species or forms dense stands of ridged palm-like sporophytes, across different studies of the same species can be whereas the giant kelp M. pyrifera uses gas bladders challenging (Bird et al. 2007, Liggins et al. 2013, to extend through the water column to produce a Sexton et al. 2014). flexible floating canopy at the sea surface. The two Here, we use a comparative population genetics species co-occur in the same rocky habitat at similar (CPG) approach to examine the dispersal of two depths, experience many of the same biotic and abi- sympatric species of kelp (Order Laminariales). We otic pressures, and also share the same basic life his- define CPG as the study of genetic differentiation of tory. Moreover, the zoospores of both species are two or more taxa that share many life history traits released near the bottom, sink at similar rates, and and demographic history in a restricted geographic have similar planktonic durations (Reed et al. 1992, area. CPG has been used to examine the role of lar- Gaylord et al. 2002), which influence the distances val strategies (Lambert et al. 2003, Watts and over which they disperse (Norton 1992, Gaylord Thorpe 2006, Barbosa et al. 2013), life history char- et al. 2002). The primary difference in the dispersal acteristics (Criscione and Blouin 2004), and envi- potential of these two species is that unlike P. califor- ronmental gradients (White et al. 2011, DeFaveri nica, M. pyrifera is positively buoyant and intact et al. 2012) in understanding patterns of gene flow sporophytes that are dislodged by large waves create in a variety of marine and aquatic systems. More- floating rafts that are dispersed by winds and cur- over, comparing genetic differentiation between rents at the sea surface promote dispersal between populations of sympatric species with similar life his- populations that are tens or hundreds of kilometers tory traits over a limited geographic area has been apart from one another (Hobday 2000, Macaya used to make inferences about dispersal patterns for et al. 2005, Hernandez-Carmona et al. 2006, Gra- each species (Shulman and Bermingham 1995, ham et al. 2007, Gaylord et al. 2012). Sponaugle and Cowen 1997, Turner and Trexler For our CPG study, we performed a microsatel- 1998, Dawson et al. 2002, Nikula
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