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Rai, H.S., Reeves, P.A., Peakall, R

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Rai, H.S., Reeves, P.A., Peakall, R 658 Inference of higher-order conifer relationships from a multi-locus plastid data set1 Hardeep S. Rai, Patrick A. Reeves, Rod Peakall, Richard G. Olmstead, and Sean W. Graham Abstract: We reconstructed the broad backbone of conifer phylogeny from a survey of 15–17 plastid loci and associated noncoding regions from exemplar conifer species. Parsimony and likelihood analyses recover the same higher-order rela- tionships, and we find strong support for most of the deep splits in conifer phylogeny, including those within our two most heavily sampled families, Araucariaceae and Cupressaceae. Our findings are broadly congruent with other recent studies, and are inferred with comparable or improved bootstrap support. The deepest phylogenetic split in conifers is in- ferred to be between Pinaceae and all other conifers (Cupressophyta). Our current gene and taxon sampling does not sup- port a relationship between Pinaceae and Gnetales, observed in some published studies. Within the Cupressophyta clade, we infer well-supported relationships among Cephalotaxaceae, Cupressaceae, Sciadopityaceae, and Taxaceae. Our data support recent moves to recognize Cephalotaxus under Taxaceae, and we find strong support for a sister-group relationship between the two predominantly southern hemisphere conifer families, Araucariaceae and Podocarpaceae. A local hotspot of indel evolution shared by the latter two conifer families is identified in the coding portion of one of the plastid riboso- mal protein genes. The removal of the most rapidly evolving plastid characters, as defined using a likelihood-based classi- fication of substitution rates for the taxa considered here, is shown to have little to no effect on our inferences of higher- order conifer relationships. Key words: chloroplast genome, gymnosperms, microstructural mutations, rps7, seed-plant phylogeny, Wollemia. Re´sume´ : Les auteurs ont mis en place une large structure centrale pour la phyloge´nie des conife`res a` partir d’une e´tude sur 15–17 lieux de plastes et en associant des re´gions non-codantes pour des espe`ces de conife`res de re´fe´rence. Les analy- ses de parcimonie et de probabilite´ rame`nent la meˆme relation d’ordre supe´rieur, et on constate un fort support pour les di- visions marque´es dans la phyloge´nie des conife`res, incluant celles qu’on trouve dans les familles des Araucariaceae et des Cupressaceae, fortement e´chantillonne´es par les auteurs. Les re´sultats montrent une forte correspondance avec ceux d’autres e´tudes re´centes et en infe`rent avec un support bootstrap comparable ou ame´liore´.Onde´duit que la division phylo- ge´ne´tique la plus marque´e chez les conife`res se retrouve entre les Pinacea et tous les autres conife`res. Les e´chantillons de ge`nes et de taxons re´unis par les auteurs ne supportent aucune relation entre les Pinaceae et les Gne´tales, comme mention- ne´e dans certaines publications. Pour le clade des Cupressophyte, les auteurs de´duisent de fortes relations au sein des Ce- phalotaxaceae, Cupressaceae, Sciadopityaceae et Taxaceae. Les donne´es supportent la re´cente proposition pour reconnaıˆtre le Cephalotaxus comme Taxaceae, et on trouve un fort support pour une relation de groupe sœur entre deux familles pre´- dominantes dans l’he´misphe`re sud, les Araucariaceae et les Podocarpaceae. On a identifie´ un point chaud d’e´volution d’indels, commun aux deux familles de conife`res pre´cite´es, dans la portion codante d’un des ge`nes des prote´ines ribosomi- ques plastidiques. L’e´limination des caracte`res plastidiques e´voluant le plus rapidement, comme de´fini en utilisant une classification base´e sur la probabilite´ des taux de substitution chez les taxons conside´re´s, montre qu’elle a peu ou pas d’effet sur les de´ductions des auteurs concernant les relations d’ordre supe´rieur, chez les conife`res. Mots-cle´s:ge´nome chloroplastique, gymnospermes, mutations microstructurales, rps7, phyloge´nie des plantes a` graines, Wollemia. [Traduit par la Re´daction] Received 30 July 2007. Published on the NRC Research Press Web site at botany.nrc.ca on 12 June 2008. H.S. Rai2 and S.W. Graham.4 UBC Botanical Garden & Centre for Plant Research (Faculty of Land and Food Systems), and Department of Botany, 2357 Main Mall, University of British Columbia, Vancouver, BC V6T 1Z4, Canada. P.A. Reeves3 and R.G. Olmstead. Department of Biology, University of Washington, Seattle, WA 98195, USA. R. Peakall. School of Botany and Zoology, The Australian National University, Canberra, ACT 0200, Australia. 1This paper is one of a selection of papers published in the Special Issue on Systematics Research. 2Present address: The Arnold Arboretum of Harvard University, 22 Divinity Avenue, Cambridge, MA 02138, USA. 3Present address: Agricultural Research Service, National Center for Genetic Resources Preservation, United States Department of Agriculture, 1111 South Mason Street, Fort Collins, CO 80521-4500, USA. 4Corresponding author (e-mail: [email protected]). Botany 86: 658–669 (2008) doi:10.1139/B08-062 # 2008 NRC Canada Rai et al. 659 Introduction 2002), and more recently as Cupressophyta by Cantino et al. (2007). Conifers have a rich and deep fossil record, with taxa as- Within Cupressophyta, various molecular and morpholog- signable to extant families dating back to the Triassic (Yao ical phylogenetic studies support the existence of a clade et al. 1997; Stockey et al. 2005). Although angiosperms are consisting of members of Cephalotaxaceae and Taxaceae now the dominant group of seed plants in most terrestrial (e.g., Hart 1987; Cheng et al. 2000; Quinn et al. 2002), ecosystems, conifers are still ecologically significant in all although there is some uncertainty about the limits and continental floras (Enright and Hill 1995), and they domi- monophyly of Taxaceae (e.g., Page 1990d). For example, nate the northern boreal forests. Approximately 670 extant Quinn et al. (2002) proposed that Taxaceae should be cir- species are recognized in some 70 genera. Most conifer cumscribed to include Cephalotaxus Siebold & Zucc. ex systematists recognize seven families to accommodate their Endl., although this recommendation is not yet generally fol- diversity: Araucariaceae, Cephalotaxaceae, Cupressaceae, lowed. Most taxa formerly included in Taxodiaceae are now Pinaceae, Podocarpaceae, Sciadopityaceae, and Taxaceae recognized under a more broadly defined Cupressaceae, a (Phyllocladaceae are sometimes separated from Podocarpa- circumscription proposed by Eckenwalder (1976) on mor- ceae, while Taxodiaceae are now usually included in Cu- phological grounds, which has since been supported by nu- pressaceae). Considerable progress in our understanding of merous phylogenetic studies (e.g., Hart 1987; Brunsfeld et conifer classification and phylogenetics has been made using al. 1994; Stefanovic et al. 1998; Gadek et al. 2000; Kusumi multiple lines of evidence (e.g., Quinn et al. 2002). For ex- et al. 2000; Quinn et al. 2002; Rydin et al. 2002). The dis- ample, Taxaceae have sometimes been treated as an order tinctiveness of Sciadopitys verticillata (Thunb.) Siebold & distinct from other conifers (e.g., Florin 1951), but morpho- Zucc., traditionally considered to belong to Cupressaceae, logical and molecular data clearly support a nested phyloge- supports its recognition as a separate family, Sciadopitya- netic position for the family among the rest of the conifers ceae (e.g., Page 1990c). Morphological and molecular phy- (e.g., Hart 1987; Raubeson and Jansen 1992; Quinn et al. logenetic data confirm this view (e.g., Hart 1987; Brunsfeld 2002). et al. 1994). Both families are now recognized as part of the However, there are still points of weakness in our under- larger clade that includes Cephalotaxaceae and Taxaceae. standing of conifer higher-order phylogenetic relationships. Finally, the relative arrangement of Cephalotaxaceae, Cu- For example, it is still not clear whether extant conifers are pressaceae, Taxaceae, and Sciadopityaceae to each other is monophyletic (e.g., Burleigh and Mathews 2004, 2007a, incompletely understood (e.g., Stefanovic et al. 1998; Quinn 2007b). Some studies find the enigmatic Gnetales et al. 2002; Rydin et al. 2002). (Ephedra L., Gnetum L., and Welwitschia Hook. f.) to be The main goal of our study is to obtain well-supported re- the sister group of the pines and their relatives (Pinaceae) lationships for the deep branches of conifer phylogeny by with moderate to strong support (the ‘‘gnepine’’ hypothesis, surveying a large multigene plastid data set (15–17 plastid see Bowe et al. 2000; Chaw et al. 2000; Gugerli et al. 2001), genes and associated noncoding regions) for a broad range whereas others support the monophyly of extant conifers, of exemplar conifers. Increasing the amount of nucleotide with Gnetales being placed elsewhere in seed-plant phylog- data sampled per taxon has been shown to be an effective eny (e.g., Chaw et al. 1997; Rydin et al. 2002; Rai et al. way to clarify our understanding of deep phylogenetic rela- 2003). A placement of Gnetales as sister to Pinaceae is dif- tionships in various groups of plants, and to generally in- ficult to justify on morphological grounds (e.g., Donoghue crease support for phylogenetic inferences (for empirical and Doyle 2000), and may be a strong analytical artifact, examples using the current gene set see Graham and perhaps due to long-branch attraction (e.g., Burleigh and Olmstead 2000a; Rai et al. 2003; Graham et al. 2006; Mathews 2004). On the other hand, a sister-group relation-
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