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Widespread Genealogical Nonmonophyly in Species of Pinus Subgenus Strobus

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Widespread Genealogical Nonmonophyly in Species of Pinus Subgenus Strobus Syst. Biol. 56(2):163-181,2007 Copyright © Society of Systematic Biologists ISSN: 1063-5157 print / 1076-836X online DOI: 10.1080/10635150701258787 Widespread Genealogical Nonmonophyly in Species of Pinus Subgenus Strobus JOHN SYRING,1* KATHLEEN FARRELL,2 ROMAN BUSINSKY,3 RICHARD CRONN,4 AND AARON LISTON2 department of Biological and Physical Sciences, Montana State University-Billings, Billings, Montana 59101, USA ^•Department of Botany and Plant Pathology, Oregon State University, Corvallis, Oregon 97331, USA; E-mail: [email protected] (A.L.) 3Silva Tarouca Research Institute for Landscape and Ornamental Gardening, Pruhonice, Czech Republic ^Pacific Northwest Research Station, USDA Forest Service, 3200 SW Jefferson Way, Corvallis, Oregon 97331, USA *Corresponding author: John Syring. E-mail: [email protected] Abstract.—Phylogenetic relationships among Pinus species from subgenus Strobus remain unresolved despite combined efforts based on nrFTS and cpDNA. To provide greater resolution among these taxa, a 900-bp intron from a late embryogenesis abundant (LEA)-like gene (IFG8612) was sequenced from 39 pine species, with two or more alleles representing 33 species. Downloaded from https://academic.oup.com/sysbio/article/56/2/163/1685319 by guest on 28 September 2021 Nineteen of 33 species exhibited allelic nonmonphyly in the strict consensus tree, and 10 deviated significantly from allelic monophyly based on topology incongruence tests. Intraspecific nucleotide diversity ranged from 0.0 to 0.0211, and analysis of variance shows that nucleotide diversity was strongly associated (P < 0.0001) with the degree of species monophyly. Although species nonmonophyly complicates phylogenetic interpretations, this nuclear locus offers greater topological support than previously observed for cpDNA or nrlTS. Lacking evidence for hybridization, recombination, or imperfect taxonomy, we feel that incomplete lineage sorting remains the best explanation for the polymorphisms shared among species. Depending on the species, coalescent expectations indicate that reciprocal monophyly will be more likely than paraphyly in 1.71 to 24.0 x 106 years, and that complete genome-wide coalescence in these species may require up to 76.3 x 106 years. The absence of allelic coalescence is a severe constraint in the application of phylogenetic methods in Pinus, and taxa sharing similar life history traits with Pinus are likely to show species nonmonophyly using nuclear markers. [Lineage sorting; monophyly; nonmonophyly; nuclear genes; pinaceae; Pinus; phylogeny.] Whenever a phylogenetic study uses a single individ- species; Miiller and Borsch, 2005), Solanum (14 included ual to represent a species, an implicit assumption is made species; Levin et al., 2005), Viburnum (41 included species; that the species is monophyletic (Funk and Omland, Winkworth and Donoghue, 2005), Silene (16 included 2003; Shaw and Small, 2005). To the extent that complicat- species; Popp and Oxelman, 2004), and Dioscorea (67 in- ing factors (e.g., reticulation) are rare in the divergence cluded species; Wilkin et al., 2005). history of terminal taxa, this assumption offers a con- Although many examples of species nonmonophyly venient simplification for sampling. However, sampling are the direct result of inadequate phylogenetic sig- a single individual per species provides no opportunity nal (Cross et al., 2002; Roalson and Friar, 2004; Levin to test the hypothesis of allelic monophyly (coalescence) and Miller, 2005; Shaw and Small, 2005), recent pub- within species. In molecular phylogenetics, this issue can lications across the plant kingdom have demonstrated become acute, because gene trees are used to infer or- that species-level paraphyly and polyphyly can be well ganismal phylogenies. These gene trees are subject to supported (Roalson and Friar, 2004; Alvarez et al., 2005; processes that can result in the nonmonophyly of se- Church and Taylor, 2005; Kamiya et al., 2005; Oh and quences sampled from a single species (lineage sorting, Potter, 2005; Yuan et al., 2005). Causative factors respon- reticulate evolution; Nei, 1987; Wendel and Doyle, 1998). sible for species nonmonophyly are often difficult to es- Errors in phylogenetic estimation can occur when gene tablish. Factors commonly cited include introgressive tree/species tree incongruence exists, but species sam- hybridization (Roalson and Friar, 2004; Kamiya et al., pling is insufficient to detect the responsible phenomena. 2005; Mason-Gamer, 2005; Shaw and Small, 2005), in- Many species remain poorly known, and the presence of complete lineage sorting (Chiang et al., 2004; Bouill£ and cryptic taxa or an inadequate taxonomic treatment can Bousquet, 2005; Kamiya et al., 2005), unrecognized am- be recognized when nonmonophyletic species are dis- plification of a paralogous locus (Roalson and Friar, 2004; covered in a phylogenetic analysis. Alvarez et al., 2005), recombination among divergent al- Awareness of the existence and complications aris- leles (Schierup and Hein, 2000), and imperfect taxonomy ing from intraspecific polymorphism is growing. This is including the occurrence of cryptic species (Goodwillie illustrated by recently published plant molecular phy- and Stiller, 2001; Treutlein et al., 2003; Roalson and logenetic studies (Appendix 1) that increasingly in- Friar, 2004; Shaw and Small, 2005). Further, paraphyletic clude sampling to evaluate species level monophyly. species may be the direct result of certain evolutionary Not surprisingly, varying levels of nonmonophyly are processes, as suggested for recent progenitor-derivative encountered as more intensive population-level sam- speciation (Rieseberg and Brouillet, 1994; Rosenberg, pling is included in phylogenetic analyses (Appendix 1). 2003). Despite the prevalence of nonmonophyly, many recent Funk and Omland (2003) reported a common trend studies in plants do not include multiple samples per of species-level coalescence failure from mitochondrial species, even in the species-rich genera Rhododendron (86 DNA studies in animals. Their survey of 584 stud- included species; Goetsch et al., 2005), Aconitum (54 in- ies and 2319 species found that 23.1% of the studies cluded species; Luo et al., 2005), Utricularia (31 included showed species-level paraphyly or polyphyly. Bouill6 163 164 SYSTEMATIC BIOLOGY VOL. 56 and Bousquet (2005) recently demonstrated a striking large effective population sizes (Ne; Ledig, 1998) makes case of trans-species allelic polymorphism in three low- it likely that mutations have spread and become fixed copy nuclear genes in different species of spruce (Picea). slowly across a species' range. This presents the poten- Allelic coalescence times between randomly selected al- tial for long-lived allelic diversity that spans one or more leles from these spruce species were estimated at 10 to speciation events. 18 million years ago, values that overlapped with esti- Pinus subg. Strobus has a long history of systematic mated divergence times (13 to 20 million years ago) for inquiry (reviewed in Critchfield 1986; Price et al., 1998; the species studied. Because spruces share many life his- Wang et al., 1999; Gernandt et al., 2005; Syring et al., tory traits with other temperate zone gymnosperm and 2005). To date, however, relationships among the ter- angiosperm trees (e.g., highly outcrossing, long-lived minal taxa remain nearly unresolved (reviewed in Sy- perennials with large effective population sizes), Bouill6 ring et al., 2005). In pines, low-copy nuclear genes are and Bousquet (2005) suggest that the incomplete lineage an untapped resource for clarifying these terminal re- sorting phenomenon detected in Picea could hinder the lationships, especially when genetic variation is inter- utility of the nuclear markers in phylogenetic analyses preted within a framework where species monophyly Downloaded from https://academic.oup.com/sysbio/article/56/2/163/1685319 by guest on 28 September 2021 of conifers and other trees. can be assessed, and where the impact of incomplete lin- The similarities in life history traits between Picea and eage sorting can be determined. Data from multiple low- Pinus (both genera of Pinaceae) suggest that incomplete copy nuclear loci in pines (Syring et al., 2005) provide lineage sorting could be a common feature of the 100+ initial evidence that intraspecific diversity is confined species in this genus, thus creating a potential obsta- within Pinus subsections, although the frequency of non- cle to phylogenetic analyses based on low-copy nuclear coalescence at the species level has not been previously genes. Pinus is a diverse and relatively ancient genus addressed. with origins that date to the early Cretaceous (145 to In this paper, we present a phylogenetic analysis of 125 million years ago; Alvin, 1960). Paleontological and subg. Strobus using the most informative nuclear locus molecular data suggest that the first major divergence identified in a recent survey (Syring et al., 2005), a ca. event separating extant lineages occurred perhaps 85 to 900-bp intron localized witliin a Late Embryogenesis 45 million years ago (Miller, 1973; Meijer, 2000; Magallon Abundant (LEA)-like gene. The goal of this study is to in- and Sanderson, 2002; Willyard et al., 2007), giving rise tensively sample the remaining species of subg. Strobus, to two distinct lineages recognized today as subg. Pinus particularly the species-rich subsects. Strobus and Cem- and subg. Strobus, the "hard" and "soft" pines, respec- broides,
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