Phylogenetic History and Geography As Joint Predictors of Oak Plastome Phylogeny1 Kasey K
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720 ARTICLE A time and a place for everything: phylogenetic history and geography as joint predictors of oak plastome phylogeny1 Kasey K. Pham, Andrew L. Hipp, Paul S. Manos, and Richard C. Cronn Abstract: Owing to high rates of introgressive hybridization, the plastid genome is poorly suited to fine-scale DNA barcoding and phylogenetic studies of the oak genus (Quercus, Fagaceae). At the tips of the oak plastome phylogeny, recent gene migration and reticulation generally cause topology to reflect geographic structure, while deeper branches reflect lineage divergence. In this study, we quantify the simple and partial effects of geographic proximity and nucleome-inferred phylogenetic history on oak plastome phylogeny at different evolutionary scales. Our study compares pairwise phylogenetic distances based on complete plastome sequences, pairwise phylogenetic distances from nuclear restriction site-associated DNA sequences (RADseq), and pairwise geographic distances for 34 individuals of the white oak clade representing 24 North American and Eurasian species. Within the North American white oak clade alone, phylogenetic history has essentially no effect on plastome variation, while geography explains 11%–21% of plastome phylogenetic variance. However, across multiple continents and clades, phylogeny predicts 30%–41% of plastome variation, geography 3%–41%. Tipwise attenuation of phylogenetic informativeness in the plas- tome means that in practical terms, plastome data has little use in solving phylogenetic questions, but can still be a useful barcoding or phylogenetic marker for resolving questions among major clades. Key words: gene flow, hybridization, partial Mantel test, plastome sequencing, restriction-site associated DNA (RADseq). Résumé : En raison de l’abondance d’hybridation introgressive, le génome plastidique convient peu a` des études fines de codage a` barres de l’ADN et aux études phylogénétiques chez les chênes (genre Quercus, Fagacées). Aux extrémités de la phylogénie du plastome du chêne, des événements récents de migration génique et de réticulation font généralement en sorte que la topologie reflète la structure géographique, tandis que les branches ancrées plus profondément reflètent davantage la divergence des lignées. Dans ce travail, les auteurs ont quantifié les effets simples et partiels de la proximité géographique et de l’historique phylogénétique, déduit en étudiant le génome nucléaire, sur la phylogénie du plastome du chêne a` différentes échelles évolu- tives. Ce travail compare les distances phylogénétiques basées sur les séquences complètes des plastomes, les distances calculées sur la base de séquences RADseq nucléaires et les distances géographiques chez 34 individus du clade du chêne blanc représent- ant 24 espèces nord-américaines et eurasiennes. Au sein du seul clade du chêne blanc nord-américain, l’historique phylogéné- For personal use only. tique n’avait essentiellement aucun effet sur la variation observée au sein du plastome, tandis que la géographie expliquait entre 11 et 21 % de la variance génétique du plastome. Cependant, a` l’échelle de plusieurs continents et clades, la phylogénie permettait d’expliquer entre 30 et 41 % de la variation plastomique et la géographie entre 3 et 41 %. L’atténuation de la valeur informative de la phylogénie aux extrémités de l’arbre signifie qu’en termes pratiques les données du plastome sont peu utiles pour répondre a` des questions phylogénétiques, mais qu’elles demeurent utiles comme marqueurs, en tant que codes a` barres ou en phylogé- nie, pour résoudre des questions au sein de principaux clades. [Traduit par la Rédaction] Mots-clés : flux génique, hybridation, test de Mantel partiel, séquençage du plastome, séquençage de l’ADN associé aux sites de restriction (RADseq). Introduction cies with overlapping ranges exchange alleles through introgres- Oaks have long been notorious among biologists for both high sive hybridization (Whittemore and Schaal 1991; Cavender-Bares intraspecific morphological variation and low reproductive barri- and Pahlich 2009; Peñaloza-Ramírez et al. 2010), these events are Genome Downloaded from www.nrcresearchpress.com by USDANALBF on 04/03/18 ers (e.g., Wiegand 1935; Muller 1952; Burger 1975; Hardin 1975). rare relative to the rate of intraspecific gene flow (Muir et al. 2000; Van Valen (1976) famously wrote, “It may well be that Quercus Hipp and Weber 2008; Cavender-Bares and Pahlich 2009; Gerber macrocarpa in Quebec exchanges many more genes with local et al. 2014). This asymmetry of rates helps to maintain species Q. bicolor than it does with Q. macrocarpa in Texas” (Van Valen 1976, boundaries even in sympatry and the genetic coherence of oak pg. 235). Other studies have since confirmed that while oak spe- species over large geographic ranges. It appears that high rates of Received 24 October 2016. Accepted 21 March 2017. Corresponding Editor: Juan P. Jaramillo-Correa. K.K. Pham. The Morton Arboretum, 4100 Illinois Route 53, Lisle, IL 60532-1293, USA; Department of Plant Biology, Michigan State University, East Lansing, MI 48824-1312, USA. A.L. Hipp.* The Morton Arboretum, 4100 Illinois Route 53, Lisle, IL 60532-1293, USA; The Field Museum, 1400 S Lake Shore Drive, Chicago, IL 60605, USA. P.S. Manos. Department of Biology, Duke University, Durham, NC 27708-0338, USA. R.C. Cronn. Pacific Northwest Research Station, 3200 SW Jefferson Way, Corvallis, OR 97331-4401, USA. Corresponding authors: K.K. Pham (email: [email protected]); A.L. Hipp (email: [email protected]). *Andrew L. Hipp currently serves as a Guest Editor; peer review and editorial decisions regarding this manuscript were handled by Juan P. Jaramillo-Correa. 1This paper is part of a Special Issue entitled The Evolution of Tree Diversity. Copyright remains with the author(s) or their institution(s). Permission for reuse (free in most cases) can be obtained from RightsLink. Genome 60: 720–732 (2017) dx.doi.org/10.1139/gen-2016-0191 Published at www.nrcresearchpress.com/gen on 26 April 2017. Pham et al. 721 intraspecific gene exchange ensure that introgressant alleles re- logeographic structure at a continental scale; 33 of these samples main at low frequencies (Petit and Excoffier 2009), increasing overlapped between datasets. Three Eurasian white oak species their chance of loss through drift. Thus gene flow among conspe- (Quercus mongolica Fisch. ex. Ledeb.; Q. petraea (Mattuschka) Libel.; cific populations counterbalances the homogenizing effect of Q. robur L.) were included for both datasets to assess geographic hybridization in the oak nuclear genome, making nuclear DNA a and phylogenetic structure between North America and Eurasia reliable source of phylogenetic data (Eaton et al. 2015; Hipp 2015). based on RADseq and plastome data. An additional 51 white oak The plastid genome, long the workhorse of angiosperm phylo- samples focused predominantly on four Eurasian white oak spe- genetics (Chase et al. 1993; Ruhfel et al. 2014; Shaw et al. 2014 and cies (the three aforementioned, plus Q. dentata Thunb.) were also references therein), is haploid and non-recombinant, and it has a surveyed for plastome variation to more exhaustively assess plas- smaller effective population size than nuclear alleles. These fac- tome phylogenetic and geographically structured genetic varia- tors increase the rate of fixation of haplotypes within populations tion among North American, European, and Asian white oaks. and species via drift. Moreover, maternally inherited plastids typ- The total number of plastome sequences reported here is 91. A ically have lower rates of among-population migration, reducing previously published red oak plastid genome (Q. rubra L.; NCBI their effectiveness in maintaining species cohesion (Petit and NC_020152) was included as an outgroup, and one RADseq sample Excoffier 2009). For these reasons, the plastome often tracks pat- from a different individual was added as the RADseq outgroup. terns of geographically structured interspecific gene flow that Thus the total number of RADseq samples presented in this paper dominates in lineages at recent phylogenetic scales (e.g., Rieseberg is 47. Geographic coordinates (latitude and longitude) were col- and Soltis 1991; Rieseberg et al. 1991; Whittemore and Schaal 1991; lected for source trees using GPS. Sang et al. 1997; Petit and Excoffier 2009) and can reveal evidence of hybridization history at even deep phylogenetic scales (Folk Restriction-site associated DNA sequencing (RADseq) et al. 2016). These and related studies demonstrate that while RADseq DNA extraction, library preparation, and sequencing phylogeny frequently tracks geography at broad scales, localized were conducted as presented previously by A. Hipp and colleagues interspecific gene flow is often detectable at finer scales through (Hipp et al. 2014; Eaton et al. 2015; Cavender-Bares et al. 2015). conflict between plastomic and genomic phylogenies. Briefly, DNA for all RADseq samples was extracted from fresh or Forest trees in particular frequently demonstrate plastome di- frozen material using the DNeasy plant extraction protocol vergence patterns that conflict with known lineage divergence (DNeasy, Qiagen, Valencia, Calif.). DNA extractions were gel quan- history (phylogeny), reflecting either the sorting of plastome lin- tified in agarose by visual comparison with the New England eages in large populations across large geographic regions or con- BioLabs 100 bp DNA Ladder (NEB, Ipswich, Mass.). Extraction temporary hybridization among interfertile species