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Population Biology |
Center for Population Biology, University of California, One Shields Avenue, Davis, California 95616 USA
Received for publication January 7, 2004. Accepted for publication July 9, 2004.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: biogeography • distribution • polyploidy • Ranunculus • speciation • sympatry • tetraploid • triploid
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). As many as 70% of flowering plant species may have duplicated genomes (Stebbins, 1970
; Grant, 1971
; Masterson, 1994
). Polyploidy can lead to significant reproductive isolation (Ramsey and Schemske, 1998
), changes in gene expression (Adams et al., 2003
), and alteration of ecological relations (Bretagnolle and Thompson, 1996
; Segraves and Thompson, 1999
).
Despite its importance to plant evolution, several aspects of polyploid speciation remain poorly understood. Polyploidy may arise multiple times within a species complex (Soltis et al., 1995
), but whether multiple origins are typical remains unclear. Triploid plants may play a critical role in both the origin of tetraploid individuals and the establishment of tetraploid populations (Felber and Bever, 1997
; Ramsey and Schemske, 1998
). However, relatively few studies have addressed the prevalence of triploids or their role in tetraploid demographics (but see Burton and Husband, 2000
). More broadly, little is known about how novel tetraploid plants overcome the likely negative interactions with their diploid progenitors (Levin, 1975
).
Distributional data have an important role to play in answering many of the unresolved questions surrounding polyploid speciation, complementing phylogenetic and experimental approaches. For instance, the presence of both diploid and tetraploid populations of Heuchera grossulariifolia (Saxifragaceae) in different river drainages is compatible with multiple tetraploid origins, a hypothesis supported by molecular phylogenetic work (Segraves et al., 1999
). Similarly, distribution studies can illuminate questions of niche differentiation and barriers to coexistence. In Chamerion angustifolium (Onagraceae) and Galax urceolata (Diapensiaceae), populations often have multiple cytotypes, which might be due to relatively minor negative interactions between cytotypes (Husband and Schemske, 1998
; Burton and Husband, 1999
; Husband, 2000
), while in other species, the lack of mixed-cytotype populations despite geographic proximity may be due to exclusion (Novak et al., 1991
; van Dijk and Bakx-Schotman, 1997
). Over the range of the species complex, a random distribution of diploid and tetraploid populations on the landscape would be compatible with the two cytotypes having similar habitat requirements, while distinct ranges for the two might result from differences in habitat requirements.
Ranunculus adoneus Gray (Ranunculaceae) is a perennial, herbaceous plant of the Rocky Mountains of Utah, Wyoming, and Colorado, USA, with morphologically similar diploid (2n = 2x = 16) and tetraploid (2n = 4x = 32) populations (Stanton et al., 1997
). Many Rocky Mountain buttercups exhibit polyploidy (Kapoor and Love, 1970
), as do a high proportion of plants in areas glaciated during the last ice age (Stebbins, 1984
). Diploid and tetraploid snow buttercups share finely dissected leaves that are distinct from parapatric buttercup species (Whittemore, 1993
). Likewise, observations of multivalents during meiosis and tetrasomic allozyme inheritance are consistent with autopolyploid origins of tetraploid snow buttercups (Stanton et al., 1997
).
As part of a broader investigation into polyploid speciation in snow buttercups, I examined the distribution of cytotypes across the range of the complex. I addressed the following questions: (1) Do diploid and tetraploid populations show segregation in relation to each other on the regional scale or local scale? (2) Is the triploid bridge a viable hypothesis for Ranunculus adoneus?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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; Harrington, 1964
; Welsh, 1993
; Whittemore, 1993
; Weber and Wittmann, 1996
). However, some treatments place R. adoneus as a variety within R. escholtzii (Hitchcock and Cronquist, 1973
). Within R. adoneus, some authors have proposed two varieties or subspecies based upon differences in the width of leaflet blades (Benson, 1948
), while others have found little consistency to support this division (Whittemore, 1993
). Snow buttercups differ from all other North American alpine buttercups in their fine, doubly divided leaves (Fisher et al., 1973
; Whittemore, 1993
). Diploid and tetraploid snow buttercups are probably distinct biological species due to barriers to reproduction between the two. However, diploid and tetraploid snow buttercups do not differ in floral morphology and show considerable overlap in leaf morphology (E. J. Baack, unpublished data). In the absence of diagnostic morphological characters, I use the same taxonomic name for both cytotypes.
Snow buttercups occur in late-melting snow beds in the central and southern Rocky Mountains. Plants emerge within a week of snow melt and flower immediately with 1–5 bright yellow flowers. They lack stolons but may have multiple ramets. Clonal growth is limited to clumps 3–5 cm in diameter. Most seeds disperse locally by gravity (<1 m) (Scherff et al., 1994
). Long-distance seed dispersal may occur passively via fur (Galen et al., 1997
) or through granivory by elk (Cervus elaphus) or brown-capped rosy finches (Leucosticte australis; Fringillidae). Plants mature in 3–5 yr and may live for decades.
Snow buttercups are limited to late-melting snow beds by competition, herbivory, and winter frost heave (Scherff et al., 1994
). Since suitable snow beds occur on leeward slopes and bowls, snow buttercup populations have discrete boundaries. Most of the subalpine and alpine habitat is apparently unsuitable.
Population sampling
I located populations using records from six herbaria in Colorado, New Mexico, Wyoming, and Utah. Thirty-five accessible snow buttercup populations were sampled, spanning the recorded range of the species (Whittemore, 1993
) with the exception of eastern Idaho (see Appendix 1 in Supplemental Data accompanying the online version of this article). Sampling of populations at the regional scale was most intense near the apparent boundary between diploid and tetraploid ranges near Hoosier Pass, Colorado (CO). Eight localities with other species of alpine buttercups were sampled as well to provide a broader context for understanding the biogeography and origins of the snow buttercup complex (see Appendix 2 in Supplemental Data accompanying the online version of this article).
Leaf samples from 15 plants were collected at each locality. Sampled individuals were separated by at least 1 m from each other. Subalpine plants were included when present at a site. Leaf samples were maintained in moist paper towels on ice up to 4 d until processing or freezing at –80°C. At some sites, 2–6 live plants were collected to provide root tissue for chromosome counts. Plants were maintained in a high-light environmental chamber at UC Davis.
Sampling at a contact zone
Along the east flank of Tundra Ridge at Hoosier Pass (Summit County, CO), I discovered a contact zone between diploid and tetraploid snow buttercup populations. To examine the spatial segregation of cytotypes at the microgeographic scale, I mapped every adult within a 10 x 25 m2 section spanning the contact zone and sampled a leaf from all plants with more than three leaves.
Root-tip squashes and flow cytometry
I made chromosome counts on root tips from 30 living snow buttercups using acetocarmine stain (Darlington and La Cour, 1975
). I performed flow cytometry on 15 of these plants to establish the relationship between ploidy and nuclear DNA content in snow buttercups. One fresh leaf (
1–2 cm2) was chopped with a double-sided razor in 200 µL of chopping buffer (50 mmol/L Tris, 0.1% Triton X-100, 1 mmol/L MgCl2, 2 µg/mL DAPI [Sigma-Aldrich, St. Louis, Missouri, USA], pH 7.5), then filtered through two layers of Miracloth (California Biochem, Pasadena, California, USA). Quantifications of nuclear DNA content (2C-value) for snow buttercups and other alpine buttercup species were made using barley (Hordeum vulgare cv. Sultan) as an internal standard (Bennett et al., 2000
).
Distribution of cytotypes at regional and microgeographic scales
Four hundred and six plants from 34 populations were scored using flow cytometry to determine the regional distribution of the two cytotypes. To characterize the distribution at the microgeographic scale, I used flow cytometry to cytotype five randomly selected plants from each 1 m2 section of the mapped contact zone on Tundra Ridge at Hoosier Pass, CO, unless fewer than five plants were found in that quadrat. In quadrats containing both diploid and tetraploid plants, I scored all individuals for ploidy, for a total of 1212 cytotyped plants from the contact zone.
Test for random distribution of cytotypes among populations
To determine whether the number of mixed populations was lower than expected, I used the binomial distribution to calculate the probability of finding only two mixed-cytotype populations and 24 single-cytotype populations. I excluded populations with fewer than five cytotyped individuals (see Appendix 1 in Supplemental Data accompanying the online version of this article) and scored the Guardsman Pass, Utah, population with one diploid individual as mixed.
Test for spatial segregation of populations
Clustered populations of diploids and tetraploids could either indicate that one or few independent tetraploid origins have succeeded or that diploid and tetraploid plants have different habitat requirements. I tested for segregation of diploid and tetraploid populations at the regional scale by determining the ploidy of the nearest neighboring population. If populations of each cytotype were randomly distributed, then the proportion of diploid populations with diploid nearest neighbors should equal the proportion of diploid snow buttercup populations sampled. Deviations from the random distribution were tested using Fisher's exact test (Pielou, 1969
). Populations within 5 km of another population of the same cytotype were excluded, unless their inclusion made finding a significant effect less likely. The mixed population at Tundra Ridge, CO, was scored as a diploid population with a tetraploid neighbor and as a tetraploid population with a diploid neighbor (see Appendix 1 in Supplemental Data accompanying the online version of this article).
Test for spatial segregation within a site
A similar method was used to test for microgeographic segregation of cytotypes within the contact zone at Tundra Ridge, on Hoosier Pass, CO. I scored each 1-m2 quadrat as having diploid buttercups present or absent, then did the same with respect to tetraploid buttercups. I tested for independence of the two distributions using a Fisher's exact test with one degree of freedom.
Comparisons of habitat
I investigated the effect of elevation and the origin of soil parent material on the distribution of Colorado snow buttercup populations. Elevations of diploid and tetraploid populations were compared using one-way ANOVA. Only Colorado sites were used, as alpine habitat occurs at lower elevations in Wyoming and Utah. I scored site parent material as sedimentary or igneous in origin using geological maps (Tweto, 1974a
, b
, 1979
; Tweto et al., 1978
). Differences in cytotype use of the two substrates were compared using Fisher's exact test.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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), with parapatric diploid taxa found in Colorado, Oregon, and California (see Appendix 2 in Supplemental Data accompanying the online version of this article).
Distribution of cytotypes among populations
Aside from the contact zone on Tundra Ridge at Hoosier Pass, CO (and one diploid scored from an otherwise tetraploid population at Guardsman Pass, Utah), diploid and tetraploid snow buttercups show complete segregation at the population level (Fig. 1). If each population has independent probabilities for containing individuals of each cytotype, 24.8% of populations should have both cytotypes. The probability of finding fewer than three mixed populations out of 26 is low (P = 0.027).
Segregation of populations
Diploid and tetraploid populations were not distributed at random with respect to each other; they tended to cluster with others of the same cytotype (P = 0.002).
Segregation of cytotypes within populations
Spatial segregation of cytotypes is also seen at the microgeographic scale. At the diploid–tetraploid contact zone on Tundra Ridge at Hoosier Pass, CO, the transition from 90% diploid plants to 90% tetraploid plants occurs over 3 m (Fig. 2A, B). Plants at the southern end of the east face of Tundra Ridge are diploid; those at the northern end of that face are tetraploid. At the 1-m2 scale, the segregation occurring at the contact zone is highly significant (
2 = 59, 1 df, P << 0.0001): quadrats tend to contain only one cytotype.
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Comparison of habitats
Tetraploid plants occupied both the southernmost and northernmost sites sampled (Fig. 1). Diploid snow buttercup populations occurred 50 m higher on average than tetraploid populations, but this was not significant (F = 0.43, 1 df, P = 0.52). Diploid buttercup populations were found on soils derived from igneous rock 57% of the time in Colorado, while tetraploid populations were found on igneous derived soils 46% of the time (P = 0.71).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The diploid population at Lake Stella, Nevada, lies far from the nearest diploid snow buttercup population (>1000 km) and from the nearest diploid plant at Guardsman Pass, Utah (289 km). This diploid population is unlikely to be due to a long-distance dispersal event. Two scenarios may account for this disjunct population. The Nevada diploid population lies nearer to diploid Ranunculus escholtzii var. trisectus in eastern Oregon (540 km) than to diploid snow buttercups in Colorado and may be more closely related to these (Fisher et al., 1973
). Alternatively, diploid snow buttercups may have occupied a larger distribution prior to the origin of tetraploid populations, and the Lake Stella population may be a remnant from this wider distribution.
Mixed populations
This survey found only two mixed populations, at Tundra Ridge, CO, and Guardsman Pass, Utah (UT). Scoring of the diploid individual from Guardsman Pass was done by chromosome counts of a root-tip squash, and the scored plant died prior confirmation by flow cytometry. Sampling at Guardsman Pass (N = 21 of 500 plants) failed to reveal a second diploid plant, so it is possible that the one diploid individual represents an error in chromosome counting. Mixed populations of snow buttercups could arise through two routes: novel tetraploids could arise repeatedly in diploid populations or dispersal could occur between diploid and tetraploid populations. Based on the absence of triploid and tetraploid plants in otherwise diploid populations, recurrent origins do not occur with high frequency in snow buttercups. Since diploid and tetraploid populations have distinct ranges, mixed populations due to dispersal might be limited to areas where the two cytotypes are in proximity. Near Hoosier Pass, diploid and tetraploid populations occur within 5 km of each other, well within the range of potential dispersers such as elk or rosy finches. Despite extensive sampling here, no mixed populations were found.
Explanations of segregation
Three nonexclusive hypotheses could explain the strong spatial segregation of the two cytotypes. First, diploid and tetraploid plants could occupy different ecological niches (Ehrendorfer, 1979
; Lewis, 1980
). If this hypothesis were correct, plants invading a population of the other cytotype would do poorly in the unsuitable habitat. Studies have found correlations between ploidy and elevation (Husband and Schemske, 1998), latitude, or edaphic factors (Ehrendorfer, 1979
). However, evidence from Ranunculus adoneus does not support the hypothesis of strong ecological differentiation. Diploid and tetraploid plants occur at similar latitudes and elevations (see Appendix 1 in Supplemental Data accompanying the online version of this article). Likewise, the two cytotypes do not appear to be segregated based on the soil parent material: the sedimentary soils of Tundra Ridge at Hoosier Pass in Colorado (Tweto, 1979
) are home to both diploid and tetraploid plants. The heart of the diploid distribution in the Front Range of Colorado likely differs in climate from the heart of the tetraploid distribution in central Colorado. However, these differences are unlikely to explain the location of the cytotype range boundaries near Hoosier Pass.
Second, segregation of diploid and tetraploid plants could be due to reproductive exclusion (Levin, 1975
; van Dijk and Bakx-Schotman, 1997
). Tetraploids invading a diploid population would face reduced reproductive success in many cases. Diploid and tetraploid snow buttercups flower at the same time when grown together and share the same pollinators (personal observation). Estimates of self-pollination in R. adoneus range from 30 to 70% (Stanton et al., 1997
). Therefore, a tetraploid invader would have a third or more of its ovules fertilized by gametes from diploid plants, resulting in triploid offspring that would likely have reduced fitness (Ramsey and Schemske, 1998
). While some reproduction would be possible for a minority tetraploid, neighboring diploid plants would have far higher reproductive success. Even in the absence of direct competition between plants, increased seed production by diploid neighbors would lead to higher probabilities of a seed finding a suitable site for establishment. Under this hypothesis, diploid and tetraploid snow buttercups would share a common fundamental niche, but would be unable to coexist over the long term due to reproductive interference.
Third, historical factors and dispersal limitation could contribute to the segregation of tetraploid and diploid snow buttercups. The two cytotypes could have colonized the Rockies from different source populations, leading each to occupy a distinct range. The Colorado Rockies have experienced periods of glaciation and subsequent warming to levels above the current average (Elias, 2001
). If these climatic fluctuations led to the extinction of most populations, then many suitable sites would have been available for colonization, with secondary contact between the two cytotypes occurring at Hoosier Pass. Rare long-distance dispersal would lead to few opportunities for mixed-ploidy populations to arise.
The macro-scale population data are compatible with both the reproductive exclusion and dispersal limitation hypotheses (Fig. 1). However, the pattern of micro-scale segregation observed at Hoosier Pass (Fig. 2A) suggests that dispersal limitation is less likely as an explanation for the current distribution. There, diploid and tetraploid plants intermingle over only a few meters without apparent differences in habitat.
Microgeographic segregation
Diploid and tetraploid snow buttercups may be two distinct biological species, with separate ranges and rare, low-fertility triploid hybrids. Thus, the contact zone between the two cytotypes at Tundra Ridge can be thought of as a hybrid zone between two species. The width of the hybrid zone is operationally defined as the distance over which species-specific markers change in frequency from 90 to 10% (Barton and Gale, 1993
; Harrison and Rand, 1993
). Using ploidy as a marker, this transition occurs over 3 m at Hoosier Pass (Fig. 2B). If stable, this sharp transition could be explained by an environmental discontinuity or by strong selection against hybrids, including strong genetic barriers to triploid formation. Analysis of soil nutrients (E. J. Baack, unpublished data) and local topography suggests that the 3-m zone of contact between the two cytotypes may have been disturbed by mining, but that the diploid and tetraploid areas are not fundamentally different. The disturbed area does not seem to be functioning as a barrier, as densities in the contact zone are relatively high (Fig. 2A). Therefore, if the transition zone is stable, reproductive exclusion seems the likely explanation for its steepness, making it a tension zone (Barton and Gale, 1993
; Harrison and Rand, 1993
).
Alternatively, the transition zone may be unstable. If one cytotype were invading at Tundra Ridge, the current boundary would be the invasion front. With more time, more mixing might occur or one cytotype might displace the other. Extensive diploid and tetraploid populations on other parts of Tundra Ridge suggest that this is not a recent invasion. Long-term monitoring is underway to test these hypotheses.
Role of triploids
In diploid populations, triploid plants arise through the production of unreduced gametes. The absence of triploids in the diploid populations suggests that unreduced gametes are either rarely produced or rarely lead to mature plants, so that tetraploid speciation via a triploid bridge is likewise relatively rare in snow buttercups. Hexaploid plants were 0.7% of the plants sampled in otherwise tetraploid populations (see Appendix 1 in Supplemental Data accompanying the online version of this article), most likely due to unreduced gametes. If a similar proportion of triploid plants occurred in otherwise diploid populations, this survey might well have missed their presence.
Triploids could also arise from pollinations between diploid and tetraploid plants where the two are found together. Even at the contact zone at Hoosier Pass, triploids were only 1.6% of the cytotyped plants, despite the presence of diploid and tetraploid plants in close proximity. Snow buttercup triploid frequency is lower than the 10% frequency observed in Galax urceolata (Burton and Husband, 1999
) or Chamerion angustifolium (Husband and Schemske, 1998
; Burton and Husband, 1999
), but similar to levels observed in Heuchera grossulariifolia (Thompson et al., 1997
).
Ancestry and origins of tetraploid snow buttercups
Tetraploid snow buttercups probably resulted from chromosome doubling within diploid snow buttercup populations, without hybridization. One near neighbor, Ranunculus macauleyi, is diploid (see Appendix 2 in Supplemental Data accompanying the online version of this article) but has nearly entire leaves and pilose sepals, making it an unlikely parent for tetraploid snow buttercups. The other near neighbor examined, Ranunculus escholtzii, is tetraploid in Colorado and hexaploid in Utah (Table 2) and has more nearly entire leaves, making it an unlikely parent as well. The nearest diploid species with somewhat divided leaves occur at the far edge of the range of snow buttercups, in Oregon and California (Whittemore, 1993
).
The current distribution of diploid and tetraploid snow buttercups could be explained by one or two tetraploid origins followed by range expansion rather than multiple origin events (although these data do not preclude multiple origins). This would be consistent with the relative rarity of triploid plants and unreduced gamete production. The scarcity of mixed-ploidy populations and the segregation found on Tundra Ridge at Hoosier Pass, CO, may result from the inability of tetraploid plants to persist with diploid plants, despite their perennial habit and ability to self-pollinate. If diploid and tetraploid plants do share a fundamental niche, in keeping with the evidence at Tundra Ridge, theoretical results suggest that tetraploid establishment should be very difficult (Fowler and Levin, 1984
; Rodriguez, 1996
).
Regional-scale distributions of diploid and tetraploid snow buttercups show a lack of coexistence within populations and spatial segregation between the two cytotypes. These data are compatible with three hypotheses. However, micro-scale segregation at Hoosier Pass seems best explained by reproductive exclusion of minority cytotypes. This would prevent the invasion of established populations by an alternate cytotype. Ongoing experiments are examining the reproductive success of minority diploid and tetraploid plants to test the reproductive exclusion hypothesis. At the same time, field seed and seedling transplant experiments are testing whether diploid and tetraploid snow buttercups do indeed share the same fundamental niche or whether the differences in distribution are due to differences in their habitat needs.
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FOOTNOTES |
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2 Present address: Department of Biology, Indiana University, 1001 East Third Street, Bloomington, Indiana 47405 USA (e-mail: ebaack{at}indiana.edu
)
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LITERATURE CITED |
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