Range-Wide Chloroplast and Mitochondrial DNA Imprints Reveal Multiple Lineages and Complex Biogeographic History for Douglas-Fir
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Tree Genetics & Genomes (2011) 7:1025–1040 DOI 10.1007/s11295-011-0392-4 ORIGINAL PAPER Range-wide chloroplast and mitochondrial DNA imprints reveal multiple lineages and complex biogeographic history for Douglas-fir Xiao-Xin Wei & Jean Beaulieu & Damase P. Khasa & Jesús Vargas-Hernández & Javier López-Upton & Barry Jaquish & Jean Bousquet Received: 6 December 2010 /Revised: 15 March 2011 /Accepted: 29 March 2011 /Published online: 21 April 2011 # Springer-Verlag 2011 Abstract The contemporary genetic structure of species cpDNA lineages corresponding to the Pacific Coast, the offers key imprints of how organisms responded to past Rocky Mountains, and Mexico were observed. The split geological and climatic events, which have played a crucial time of the two lineages from the Rockies lineage was role in shaping the current geographical distribution of dated back to 8.5 million years (Ma). The most recent north-temperate organisms.Inthisstudy,range-wide common ancestors of Mexican and coastal populations patterns of genetic variation were examined in Douglas-fir were estimated at 3.2 and 4.8 Ma, respectively. The (Pseudotsuga menziesii), a dominant forest tree species northern populations of once glaciated regions were distributed from Mexico to British Columbia in western characterized by a high level of genetic diversity, indicating North America. Two organelle DNA markers with con- a large zone of contact between ancestral lineages. A trasting modes of inheritance were genotyped for 613 possible northern refugium was also inferred. The Mexican individuals from 44 populations. Two mitotypes and 42 lineage, which appeared established by southward migration chlorotypes were recovered in this survey. Both genomes from the Rockies lineage, was characterized by the lowest showed significant population subdivision, indicative of genetic diversity but highest population differentiation. These limited gene flow through seeds and pollen. Three distinct results suggest that the effects of Quaternary climatic Communicated by S. Aitken Electronic supplementary material The online version of this article (doi:10.1007/s11295-011-0392-4) contains supplementary material, which is available to authorized users. : X.-X. Wei (*) J. Vargas-Hernández J. López-Upton State Key Laboratory of Systematic and Evolutionary of Botany, Programa Forestal–Campus Montecillo, Colegio de Institute of Botany, Chinese Academy of Sciences, Postgraduados, km 36.5 Carretera México-Texcoco, 20 Nanxincun, Xiangshan, Texcoco, México C.P. 56230, Mexico Beijing 100093, China e-mail: [email protected] X.-X. Wei : J. Beaulieu : D. P. Khasa : J. Bousquet Canada Research Chair in Forest and Environmental Genomics, Forest Research Centre and Institute for Systems and Integrative Biology, 1030 avenue de la Médecine, Université Laval, Québec, Québec G1V 0A6, Canada J. Beaulieu B. Jaquish Natural Resources Canada, Canadian Forest Service, Canadian British Columbia Ministry of Forests and Range, Research and Wood Fibre Centre, 1055 du P.E.P.S., Knowledge Management Branch, Kalamalka Forestry Centre, P.O. Box 10380, Stn. Sainte-Foy, 3410 Reservoir Road, Québec, QC G1V 47C, Canada Vernon, BC V1B 2C7, Canada 1026 Tree Genetics & Genomes (2011) 7:1025–1040 oscillations on the population dynamics and genetic diversity America, a more limited number of studies have focused of Douglas-fir varied substantially across the latitudinal on the southern part of North America including Mexico, section. The results emphasize the pressing need for the (reviewed in Jaramillo-Correa et al. 2009), a region conservation of Mexican Douglas-fir. characterized by unusually high species diversity as well as geographical and geological complexity. This complexity Keywords Genetic diversity. Population structure . has been shown to promote vicariance, isolation, and Biogeographic history . Molecular clock . Cytoplasmic genetic drift, given that many tree species have retreated DNA . Douglas-fir to high altitudes with the Holocene warming (Jaramillo- Correa et al. 2006). These processes and their genetic consequences are quite different than those seen in the Introduction north, leading to drastic differences in the patterns of genetic diversity and population genetic structure in Global climate changes, in particular the climatic oscillations various parts of the continent (Jaramillo-Correa et al. of the Quaternary period, have been proposed as critical 2009). Hence, it would be of interest to investigate more factors in inducing speciation and shaping the contemporary species, in particular those with wide distributions encom- distribution of biological diversity in the northern hemisphere passing several regions and potential vicariance factors, to get (Comes and Kadereit 1998;Hewitt1996, 2000;Klickaand a broader picture of how the genetic architecture of wide- Zink 1997; Lemmon et al. 2007;Opgenoorthetal.2010; range species has been affected by past climate changes. Such Perron et al. 2000). In response to Quaternary expansions knowledge will contribute to our understanding of the and contractions of the glacial ice sheets, most surviving contemporary distribution of genetic diversity and assist in organisms either shifted their ranges to southern refugia designing more efficient conservation and sustainable during glacial cycles and recolonized northward following management plans at national and international levels. the receding ice sheets during interglacial cycles or they Douglas-fir (Pseudotsuga menziesii) is an ecologically experienced altitudinal shifts and range fragmentation and economically important coniferous tree species with a (Hewitt 2000; Jaramillo-Correa et al. 2009; Petit et al. broad latitudinal distribution in western North America. It 2003, 2008;Roweetal.2004). As a consequence of occupies a wide variety of climatic conditions from the successive founder events during postglacial colonization, maritime climate of the Pacific Northwest to the mild low genetic diversity in previously northern glaciated areas continental climates of the Rocky Mountains and the warm, and high diversity in the southern refugia are expected. dry climate of central Mexico. Two varieties are well Indeed, numerous genetic surveys in Europe and North recognized: coastal (P. menziesii var. menziesii (Mirb.) America revealed this pattern (e.g., Comes and Kadereit Franco) and interior, or Rocky Mountains, Douglas-fir (P. 1998;Hewitt1996, 1999, 2000; Ibrahim et al. 1996;Soltiset menziesii var. glauca (Beissn.) Franco). The native range of al. 1997; Taberlet et al. 1998). the coastal variety extends from central British Columbia However, this general pattern predicted under simple (55° N) south along the Pacific Coast Range into central models of colonization, i.e., a gradual decrease in diversity California to a latitude of 34°55′ N, whereas the interior away from the source populations (Hewitt 1996, 2000), is variety extends from central British Columbia (55° N) now increasingly challenged by genetic evidences in both south along the Rocky Mountains to a latitude of 17° N in Europe and North America, especially from tree species. In the mountains of Oaxaca in Southern Mexico where it has a Europe, it was found that the genetically most diverse patchier distribution (Debreczy and Racz 1995; Hermann populations of tree and shrub species were located in the and Lavender 1999; Wright et al. 1971). north rather than in the south of the main mountain ranges Li and Adams (1989) contributed the first range-wide (Petit et al. 2003). Such contrasting patterns of diversity molecular investigation of population structure in Douglas-fir were also observed in North America, where zones of based on allozymes using an intensive sampling of distinct or higher diversity in the north were inferred as populations from Canada and the USA and from two footprints of cryptic refugia at high latitudes (Anderson et populations from Mexico. Their study revealed a large al. 2006; Gérardi et al. 2010; Godbout et al. 2008, 2010; genetic differentiation between the coastal and interior Jaramillo-Correa et al. 2004; Provan and Bennett 2008), or varieties but provided less information on the evolution secondary contact on once glaciated regions between of Mexican Douglas-fir. Recently, based on chloroplast genetically distinct glacial lineages (Godbout et al. 2005, and mitochondrial DNA markers, Gugger et al. (2010a) 2008; Jaramillo-Correa et al. 2004, 2009; Naydenov et al. investigated the geographic structure of Douglas-fir 2007; Walter and Epperson 2005). distributed in the USA and Canada. Following this study, In addition, contrary to the intensive studies of the they investigated the phylogeographic history of Mexican postglacial history of plant species in northern North Douglas-fir separately (Gugger et al. 2010b). The divergence Tree Genetics & Genomes (2011) 7:1025–1040 1027 times between major groups were estimated and a number of two species in Asia (Farjon 1990)) were used as outgroups in refugia were inferred in their studies. Given the genetic the cpDNA haplotype network and Bayesian phylogenetic complexity of the species, the present study aimed at analyses (see below), respectively, because of their sister investigating the genetic diversity of Douglas-fir and its relationships with P. menziesii and with North American geographical structure throughout its entire natural range species, respectively (Wei et al. 2010). Eight individuals of from a mixed population genetics and phylogenetic perspec- P. macrocarpa from California