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Achillea, an Autopolyploid Complex of Ecological Races

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Achillea, an Autopolyploid Complex of Ecological Races ORIGINAL ARTICLE doi:10.1111/j.1558-5646.2007.00264.x RAPID ADAPTIVE DIVERGENCE IN NEW WORLD ACHILLEA, AN AUTOPOLYPLOID COMPLEX OF ECOLOGICAL RACES Justin Ramsey,1,2,3 Alexander Robertson,1 and Brian Husband1 1Department of Integrated Biology, University of Guelph, 488 Gordon St, Guelph, ON N1G 2W1, Canada 2E-mail: justin [email protected] Received February 9, 2006 Accepted September 4, 2007 Adaptive evolution is often associated with speciation. In plants, however, ecotypic differentiation is common within widespread species, suggesting that climatic and edaphic specialization can outpace cladogenesis and the evolution of postzygotic reproductive isolation. We used cpDNA sequence (5 noncoding regions, 3.5 kb) and amplified fragment length polymorphisms (AFLPs: 4 primer pairs, 1013 loci) to evaluate the history of ecological differentiation in the North American Achillea millefolium, an autopolyploid complex of “ecological races” exhibiting morphological, physiological, and life-history adaptations to diverse environments. Phy- logenetic analyses reveal North American A. millefolium to be a monophyletic group distinct from its European and Asian relatives. Based on patterns of sequence divergence, as well as fossil and paleoecological data, colonization of North America appears to have occurred via the Bering Land Bridge during the Pleistocene (1.8 MYA to 11,500 years ago). Population genetic analyses indi- cate negligible structure within North American A. millefolium associated with varietal identity, geographic distribution, or ploidy level. North American populations, moreover, exhibit the signature of demographic expansion. These results affirm the “ecotype” concept of the North American Achillea advocated by classical research and demonstrate the rapid rate of ecological differentiation that sometimes occurs in plants. KEYWORDS: Achillea, adaptation, ecotype, niche, phylogeography, polyploidy, speciation. Botanists have historically emphasized intraspecific ecologi- and Grant 1996). In contrast, discussions of ecological differen- cal races as primary examples of adaptive evolution (Turesson tiation in animals have tended to emphasize niche conservatism, 1925; Clausen et al. 1939, 1940, 1948; Stebbins 1950; Clausen developmental constraints, and the coincidence of adaptation and 1951; Kruckeberg 1951). Classical transplant studies by G¨ote speciation (Futuyma 1987; Gould and Eldridge 1993; Schluter Turesson and Jens Clausen demonstrated dramatic examples 2000; Wiens 2004). of adaptation—including fundamental changes in anatomical, Surprisingly, few molecular studies have tested the phyloge- life-history and physiological characteristics—occurring within netic hypotheses of early plant evolutionists, in particular, that so- widespread plant species. Such ecotypic differences exist at small called ecotypes do not in fact represent well-differentiated cryp- spatial scales and involve populations isolated by few intrinsic tic species with distinct evolutionary histories. Here we evaluate reproductive barriers. As a consequence, botanists often regard the phylogenetic and demographic history of the North Amer- ecological differentiation as a rapid process that can be decoupled ican Achillea millefolium, a complex of “ecological races” that from speciation (Antonovics et al. 1971; Schemske 1984; Linhart is a textbook example of plant ecotypic differentiation. In their studies, Clausen and his colleagues at the Carnegie Institute of 3Present address: Department of Biology, University of Rochester, Washington (Division of Plant Biology, Stanford University) 213 Hutchison Hall, River Campus, Rochester, NY 14627. investigated phenotypic characteristics of Achillea populations C C ! 2008 The Author(s). Journal compilation ! 2008 The Society for the Study of Evolution. 639 Evolution 62-3: 639–653 JUSTINRAMSEYETAL. Figure 1. Geographic distribution of the ecological races of North American A. millefolium. Pictograms show characteristics of the sampled varieties, including stem size, root structure, pubescence, and vegetative growth (see Table 1). along an altitudinal transect in California that ran from sea level current neopolyploid formation via unreduced gametes (Clausen to alpine regions (Clausen et al. 1940, 1948). Using experimental et al. 1940, 1948; Lawrence 1947; Kruckeberg 1951; Hiesey and transplant gardens, the Carnegie group documented local adap- Nobs 1970; Ehrendorfer 1973; Tyrl 1975; Purdy and Bayer 1996; tation of A. millefolium populations to their native environments. Ramsey 2007). The North American Achillea belongs to the cir- In total, nine ecological races were described from western North cumpolar “A. millefolium aggregate,” and ecological races are America, including forms adapted to coastal habitats, salt marshes, generally recognized as varieties of A. millefolium (Nobs 1960; oak woodlands, coniferous forests, sagebrush steppe, and alpine Hiesey and Nobs 1970; Hickman 1993; Table 1). Eurasian mem- meadows (Nobs 1960). The varieties are distinguished primarily bers of the A. millefolium aggregate are geographically widespread on the basis of stem features (height and diameter), leaf char- but phenotypically less diverse than North American populations acteristics (pubescence, color, fleshiness), phenology (dormancy, and are largely restricted to grasslands and forest margins (Tutin flowering times), and habitat associations (Fig. 1; Table 1). et al. 1976; Stace 1997; Ehrendorfer and Guo 2006; Table 1). The North American A. millefolium is an autopolyploid com- Here we use phylogenetic and population genetic analyses of plex of tetraploid (2n 4x 36) and hexaploid (2n 6x chloroplast sequence and amplified fragment length polymor- = = = = 54) populations that exhibit multisomic inheritance (random as- phisms (AFLPs) to evaluate historical relationships among the sociation of homologous chromosomes during meiosis) and re- North American A. millefolium and related Eurasian taxa. We 640 EVOLUTION MARCH 2008 Table 1. Distribution, ecology, and phenotypic characteristics of North American A. millefolium and related Eurasian taxa. Taxon Ploidy Geographic Habitat Stems Foliage Roots Vegetative Flowering level distribution reproduction phenology A. millefolium 4x w. North America alpine 10–30 cm; gray, villous fibrous, along extensive July–Sept. var. alpicola (mountains) meadows slender rhizomes A. millefolium 6x w. North America sand dunes, 20–80 cm; gray, densely fibrous plus extensive April–June var. arenicola (coasts of CA, OR, WA) grasslands stout villous, fleshy central taproot A. millefolium 6x w. North America sand dunes, 20–40 cm dark green, fibrous, along extensive June–Sept. var. borealis (coasts of AK, BC) forest margins lightly villous rhizomes A. millefolium 6x w. North America oak woodlands 30–120 cm gray green, fibrous plus extensive March–June var. californica (interior CA, OR) villous central taproot A. millefolium 6x w. North America freshwater 100–220 cm; gray, wooly deep taproot absent (all May–July var. gigantea (Central Valley, CA) “tule” ponds robust stems repro- ductive) A. millefolium 4x w. North America sagebrush steppe, 30–70 cm; gray, wooly fibrous plus extensive April–June var. lanulosa (Great Basin, Palouse) dry grasslands stout central taproot A. millefolium 4x w. North America (coasts mesic grasslands, 30–90 cm; dark green, fibrous plus extensive June–Sept. var. litoralis of CA, OR, WA, BC) forest margins robust sparsely villous, central taproot RAPIDECOLOGICALDIVERGENCEIN fleshy A. millefolium 4x w. North America open coniferous 30–90 cm; green, fibrous, along extensive June-Sept. var. pacifica (Pacific lowlands) forest slender sparsely villous rhizomes EVOLUTION A. millefolium 4x w. North America salt marshes 80–180 cm; dark green, fibrous, absent (all July–Sept. var. puberula (coast of central CA) robust hairless, very at stem base stems repro- ± fleshy ductive) A. millefolium 2x,4x China, Russia grasslands, riparian 20–60 cm; green, fibrous, along extensive June-Sept. MARCH 2008 var. mandshuricum areas sparsely villous rhizomes A. millefolium 2x Spain, France open coniferous 20–40 cm; green, fibrous, along extensive July–Sept. var. ceretanica (Pyrenees Mountains) forest slender sparsely villous rhizomes A. millefolium 6x Europe grasslands, riparian 20–60 cm green, fibrous, along extensive June–Sept. var. millefolium areas sparsely villous rhizomes 641 ACHILLEA JUSTINRAMSEYETAL. seek to identify the timeframe of adaptation and ask whether the on agarose gels to confirm amplification. Products were purified North American plants represent (1) a monophyletic grouping with Montage´ TM plates (Millipore, Billerica, MA). of recently diverged but ecologically distinct forms; (2) a mono- Cycle-sequencing reactions were performed in a 12.5-␮l phyletic grouping of highly divergent evolutionary lineages; or (3) volume that included 1 ␮l cleaned PCR product, 1 ␮l of each a polyphyletic assemblage of historically Eurasian lineages that primer (10 mM stock), 1␮l Big Dye (ver. 3.1; Applied Biosys- now co-occur in the western United States and Canada. tems, Foster City, CA) and 1 ␮l Big Dye buffer (5 Termina- × tor; Applied Biosystems). Samples were sequenced in forward and reverse directions. Sequence products were cleaned using Materials and Methods sephadex columns in combination with HV Plates (Millipore) and sequenced on an ABI 3730 capillary sequencer. Sequences were SAMPLING manually aligned using SequencherTM (ver. 4.1; Gene Codes, Ann We sampled the nine varieties of western North American
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