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Population Biology |
School of Biological Sciences, Washington State University, Pullman, Washington 99164 USA; Department of Biology, Boise State University, Boise, Idaho 83725 USA
Received for publication July 14, 2006. Accepted for publication May 11, 2007.
ABSTRACT
The invasive annual Bromus tectorum (cheatgrass) is distributed in Canada primarily south of 52° N latitude in two diffuse ranges separated by the extensive coniferous forest in western Ontario. The grass was likely introduced independently to eastern and western Canada post-1880. We detected regional variation in the grass's genetic diversity using starch gel electrophoresis to analyze genetic diversity at 25 allozyme loci in 60 populations collected across Canada. The Pgm-1a & Pgm-2a multilocus genotype, which occurs in the grass's native range in Eastern Europe, is prevalent in eastern Canada but occurs at low frequency in western Canada. In contrast, the Got-4c multilocus genotype, found in the native range in Central Europe, is widespread in populations from western Canada. Overall genetic diversity of B. tectorum is much higher in eastern Canada than in the eastern U.S., while the genetic diversity in populations in western North America is similar between Canada and the U.S. The distribution of genetic diversity across Canada strongly suggests multiple introduction events. Heterozygous individuals, which are exceedingly rare in B. tectorum, were detected in three Canadian populations. Formation of novel genotypes through occasional outcrossing events could spark adaptive evolution and further range expansion across Canada of this exceedingly damaging grass.
Key Words: allozyme • Bromus tectorum • cheatgrass • genetic diversity • heterozygosity • invader
Entry of a species into a new geographical area sets into motion a concatenation of factors and events that determine the immigrants' fate. The immigration of most plant populations consists of few plants (Mack, 2000a
and references therein), thereby providing the opportunity for founder events, population bottlenecks, and genetic drift (Lande, 1988
, but see Novak and Mack, 2005
). Where new ranges and nations are synonyms, the opportunity arises for entry at multiple points, which have historically been seaports (Ridley, 1930
) but can include international borders (Mack, 2003
and references therein) and more recently airports (Cavey, 2003
). Alien species often arrive not in a single immigration but through repeated immigrations (Mack and Erneberg, 2002
), giving researchers the opportunity to follow the fate of populations of different sizes and quite different genetic composition in a new range. Furthermore, all immigrations and subsequent events, whether eventual extirpation, persistence, or even invasion, constitute a history of the species in its new range (Mack et al., 2000
; Garnatje et al., 2002
; Roche et al., 2003
).
By documenting the size of the founder population(s), their points of entry, their date(s) of entry (or at least first detection), and their genetic diversity and structure, we can form a detailed picture of the genetic consequences of immigration, as well as the extent to which an invasion is the product of preadaptation or post-emigration adaptive evolution (Barrett and Richardson, 1986
; Lee, 2002
; Allendorf and Lundquist, 2003
). The entry and spread of a species in its new range can be reconstructed using genetic markers, herbarium specimens, and historical records (Novak and Mack, 2001
). Such reconstruction efforts not only provide information on introduction and range expansion for a single species, but they also provide insights into the invasion process in general. Aside from the fundamental value of this information in revealing how and why biological invasions occur (Barrett and Husband, 1990
), the efficacy of most control strategies, particularly biological control, depends on knowing the origin, character, and geographical extent of genetic diversity within and among introduced populations (Burdon and Marshall, 1981
; Van Driesche and Bellows, 1996
; McFadyen, 1998
).
The annual, cleistogamous grass Bromus tectorum L. (cheatgrass, downy brome) is native in temperate regions through much of Eurasia and northern Africa and also occurs in many new ranges, including Canada and the United States (Upadhyaya et al., 1986
; Novak and Mack, 2001
). Phenotypic expression in B. tectorum varies substantially, depending on environmental variation among sites and fluctuation in weather (Hulbert, 1955
; Mack and Pyke, 1983
). Persistence of B. tectorum is partially attributable to its production of multiple cohorts that emerge soon after precipitation events from early autumn to early spring; later emerging cohorts usually survive, even if older, potentially more fecund cohorts are destroyed (Mack and Pyke, 1983
, 1984
). Its persistence across a broad environmental gradient is attributed to phenotypic plasticity (Hulbert, 1955
; Rice and Mack, 1991a
–
c
). Genetic diversity in B. tectorum is low (Novak et al., 1991
, 1993
; Novak and Mack, 1993
; Bartlett et al., 2002
). Its range expansion has been facilitated by manmade disturbances, such as livestock grazing and trampling, agriculture, and road and railroad construction (Mack, 1981
and references therein), coupled with its common dispersal in hay and in contaminated seed lots (Longman and Smith, 1936
; Mack, 1981
; Yensen, 1981
).
Bromus tectorum was first detected in North America ca. 1790 in Lancaster Co., Pennsylvania, USA, but was rarely collected before 1860 (Bartlett et al., 2002
and references therein). The earliest known collection of B. tectorum in eastern Canada was made in 1886 in Kingston, Ontario, Canada (Macoun, 1888
). By 1889 the grass had also been discovered in western North America at Spences Bridge, British Columbia (Macoun 29988, CAN).
The genetic diversity and structure of plant populations in an introduced range can reflect patterns of human migration and international trade (Husband and Barrett, 1991
; Novak and Mack, 1993
, 2001
). In addition to extensive international commerce along both nations' coasts, Canada and the U.S. have been agricultural trading partners for more than 200 years (Jones, 1946
). Nevertheless, the character and history of domestic and international trade by Canada has been somewhat different from that of its southern neighbor (Glazebrook, 1938
), and these differences may have affected the course of B. tectorum entry and spread in Canada. Genetic diversity and structure of B. tectorum in the U.S. indicate unique introduction events on the east and west coasts (Novak et al., 1991
, 1993
; Novak and Mack, 1993
, 2001
; Bartlett et al., 2002
; Schachner, 2005
), the occurrence of multiple, preadapted genotypes (Rice et al., 1992
; Meyer and Allen, 1999
; Meyer et al., 2001
; Ramakrishnan et al., 2004
), and rare outcrossing events (Schachner, 2005
). Until now, comparing this U.S. history of B. tectorum with the history of B. tectorum in Canada has not been possible, aside from limited analyses of populations from British Columbia (Novak et al., 1991
, 1993
). By comparing the genetic composition of populations in Canada to those reported for the U.S., we can assess how introduction events have shaped the current genetic diversity of B. tectorum across its North American range.
We used starch-gel electrophoresis and historical records to examine the entry and spread of Bromus tectorum in its Canadian range. Specifically, these data were used to determine (1) the amount of genetic diversity in these populations; (2) the distribution of this diversity within and among populations; (3) differences in the amount and distribution of genetic diversity among regions in Canada; (4) similarities in genetic diversity between Canadian and U.S. populations; (5) the patterns of entry and spread portrayed by historical records in relation to the genetic analysis; and finally (6) the extent to which genotypes in Canada match potential donor populations in the native range.
MATERIALS AND METHODS
Collection history of Bromus tectorum in Canada
The distribution of B. tectorum in Canada was determined before sampling populations in 2004. In addition, we chronicled the spread of B. tectorum in Canada, using records in Dore and McNeill (1980)
, Raymond and Kucyniak (1948)
, and specimen records from the following herbaria: ACAD, ACK, ALTA, CAFB, CAN, DAO, DAS, GH, LKHD, MT, MTMG, OAC, QFA, QUE, SASK, UBC, US, UWO, and WIN. The sites of early collections, some of which no longer appear to support population of B. tectorum (e.g., the Yukon and apparently Quebec), were targeted as possible locales of early introduction. The dates of subsequent collections were used to estimate the spread of B. tectorum in Canada after its introduction. Our collecting was influenced but not dictated by the locales among these herbarium records.
Plant collection
Sixty populations from across the Canadian range of B. tectorum were included in this study (Fig. 1). Nine of these populations were previously analyzed by Novak et al. (1991)
, and 51 additional Canadian populations were sampled from mid-June to mid-August 2004. Mature panicles from about 50 individuals of all sizes were collected in each population and stored in individually numbered paper envelopes. Sampling was conducted throughout the entire population or within a 500-m2 area, whichever was smaller. Intervals at which individuals were collected largely depended on the size of the population, but plants were collected far enough apart to minimize collecting full sibs. In populations covering 100 to 500 m2, plants were collected about 3 m apart; in smaller populations plants were collected 1 m apart. Samples were collected from all individuals in populations with fewer than 30 plants.
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, 1993
; Novak and Mack, 1993
; Bartlett et al., 2002
) recognized three regions in the U.S. and one in Canada: Intermountain West, Nevada–California, eastern U.S., and BC. Previous genetic analysis of B. tectorum in Canada was restricted to 10 populations collected from south-central BC (Novak et al., 1991
, 1993
). Novak and Mack (1993)
assigned Eurasian populations of B. tectorum to two geographic regions, Europe and southwest Asia, a pattern we followed here.
Electrophoresis
Caryopses of B. tectorum were germinated on moistened filter paper and harvested for starch-gel electrophoresis when 3–10 cm tall. Initially, 30 individuals from each population were germinated and analyzed for genetic variability. If polymorphisms were discovered, additional individuals were analyzed. All individuals were analyzed in populations containing fewer than 30 individuals. Electrophoretic procedures followed those used by Novak et al. (1991)
. Fifteen enzymes were assayed: alcohol dehydrogenase (ADH), aldolase (ALD), glucose-6-phosphate dehydrogenase (G6PDH), glutamate dehydrogenase (GDH), glutamate oxalacetate transaminase (GOT), isocitrate dehydrogenase (IDH), leucine aminopeptidase (LAP), malate dehydrogenase (MDH), malic enzyme (ME), phosphoglucoisomerase (PGI), phosphoglucomutase (PGM), 6-phosphogluconate dehydrogenase (6PGD), shikimate dehydrogenase (SKDH), superoxide dismutase (SOD), and triosephosphate isomerase (TPI). The 15 enzymes were encoded by 25 putative loci (see Novak et al., 1991
). Nomenclature for loci and alleles follows Novak and Mack (1993)
.
Data analysis
Analysis of electrophoretic data followed Novak et al. (1991)
, Novak and Mack (1993)
, and Bartlett et al. (2002)
. Genotype frequencies from the 51 populations of B. tectorum sampled during the 2004 field season and nine British Columbian (BC) populations previously reported by Novak et al. (1991)
were analyzed using the program BIOSYS-1 (Swofford and Selander, 1981
). Populations were assembled in a geographical hierarchy consisting of eastern and western Canadian populations. Genetic diversity was expressed as mean number of alleles per locus (A), the percentage polymorphic loci (Pp), the mean observed heterozygosity (Hobs), and the expected mean heterozygosity (Hexp). Observed heterozygosity was generated using the direct count method. Expected heterozygosity is equivalent to expected genetic diversity and was calculated using Nei's (1978)
unbiased estimate method, which accounts for small population size.
Wright's fixation index (F) (Wright, 1965
) was calculated for each polymorphic locus, and the significance of any deviation of Hobs from Hexp was determined using a chi-square test. Partitioning of total allelic diversity (HT) within and among all polymorphic populations was calculated using Nei's (1973
, 1977
) gene diversity statistics. Total allelic diversity (HT) was partitioned into the within- (HS) and among-population (DST) components, such that HT = HS + DST. The ratio of the among-population component to the total allelic diversity equals the total allelic diversity partitioned among populations (GST = DST/HT).
RESULTS
Collection history of Bromus tectorum in Canada
The earliest collections of B. tectorum were made at opposite ends of the continent. The oldest record is 4 July 1886, in Kingston, ON (Millman 29990, CAN). This specimen and all other early records along the Great Lakes are from ports, and most of these records are from southern ON (Fig. 2a). Three years later Macoun (#29988, CAN) collected B. tectorum from an irrigated field at Spences Bridge, BC, more than 3000 km west of southern ON. This specimen is the earliest known collection of B. tectorum in western North America (Mack, 1981
; Upadhyaya et al., 1986
). In western Canada most (92.4%) herbarium specimens were collected below 52° N latitude and west of 106° W longitude. Further records were made in southern ON and Vancouver Island within 5 yr of these earliest dates, suggesting that B. tectorum was introduced repeatedly in the late 19th century along both coasts.
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Genetic variability
Estimates of allelic and genetic diversity for all 60 Canadian populations, including the nine BC populations previously reported by Novak et al. (1991)
, were based on an analysis of 1892 individuals. Across all 60 Canadian populations, at the 25 scored loci, a total of 30 alleles were detected (1.20 alleles/locus). Across all populations, four loci (16%) are polymorphic: Got-4, Pgm-1, Pgm-2, and Tpi-1 (Table 1); all other loci are monomorphic.
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When polymorphic, both Pgm-1 and Pgm-2 display the same allele frequencies (Table 1), suggesting that alleles at these two loci are linked, most probably due to gametic disequilibrium (S. J. Novak and R. N. Mack, unpublished data). Nine of the 13 populations (77%) from ON express the Pgm-1a & Pgm-2a multilocus genotype (Fig. 3a). Frequency of the Pgm-1 & Pgm-2 multilocus genotype is much lower in Alberta (AB), Saskatchewan (SK), and Manitoba (MB), with only three populations having this genotype (Waterton, AB; Maple Creek, SK; and Selkirk, MB). The seven BC populations with this multilocus genotype all occur in the central part of the province (Fig. 3b). Occurrence of the Got-4 multilocus genotype is highest in BC, where 16 of 25 populations (64%) contain individuals with this genotype. Four of 12 populations (33%) in southwestern AB have this multilocus genotype. The Got-4 multilocus genotype occurs in four populations in southern ON but at low frequency. Six individuals in Hamilton, three from Niagara, one from Guelph, and one from Port Colborne have this genotype. The population from Waterton, AB is the only Canadian population with individuals having the Got-4d multilocus genotype, and the only Canadian populations with the Tpi-1b multilocus genotype are Osoyoos, BC and Golden, BC. Only two individuals from Osoyoos and one from Golden possessed this genotype.
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Genetic diversity parameters within populations of the two regions in Canada were generally similar. For instance, nine of 16 (56%) populations from eastern Canada and 26 of 44 (59%) populations from western Canadian were polymorphic (Table 2). For all eastern Canadian populations, A = 1.05, Pp = 5.0, and Hexp = 0.013; for western Canadian populations, A = 1.04, Pp = 3.9, and Hexp = 0.012 (Table 3). Additionally, the level of genetic diversity in the two Canadian regions was similar to that of the populations in the mid-continent and western U.S., but higher than that reported for the eastern U.S. Genetic diversity within introduced populations of B. tectorum in Canada and the U.S. was similar and larger than the level of diversity in native populations from Eurasia (Table 3).
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for native populations (0.087) (Table 6). Unlike Canadian populations, most of the gene diversity of Eurasian populations was partitioned among populations (GST = 0.754). Mean values of GST and HT for Canadian populations were higher than those reported by Schachner (2005)
for populations of B. tectorum in the mid-continent region of the United States (Table 6). The mean GST for Canadian populations (0.405) was lower than the value reported for populations in the eastern U.S. and the western U.S. (GST = 0.560 and 0.617, respectively). The total gene diversity of B. tectorum in Canada (HT = 0.158) was most similar to that found in populations in the western U.S. (HT = 0.132) and was nearly two-fold larger than the gene diversity found in eastern U.S. populations (HT = 0.075) (Bartlett et al., 2002
). Populations of B. tectorum in western Canada and the western U.S. had almost identical levels of HT (0.131 and 0.132, respectively); however, this variation was partitioned mainly within populations in western Canada and among populations in the western U.S. (Table 6).
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in populations from the native range of B. tectorum (Table 7). The Got-4c multilocus genotype, found in eastern and western Canadian populations, has been found in only two populations from the native range (Bayreuth, Germany, and Libochovice, Czech Republic) (Novak and Mack, 1993
). We detected the Got-4d multilocus genotype in the population at Waterton, AB; this genotype has previously been detected in only one population in the native range (Vienna-Landstrasse, Austria). The Pgm-1a & Pgm-2a multilocus genotype was detected in eastern and western Canadian populations and was reported by Novak et al. (1993)
in two populations in the native range (Vac, Hungary, and Bratislava, Slovakia). The Tpi-1a multilocus genotype is the only one detected in Canada for which a direct link to a native population is not yet possible (Table 7).
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Collection records and the distribution of specific multilocus genotypes strongly suggest that B. tectorum entered Canada almost simultaneously on the eastern and western coasts in the last quarter of the 19th century. Despite contemporaneous introductions at the geographic extremes of the country, there are differences in the occurrence and frequency of different genotypes in southern Ontario, the site of the first detection in the East, and in BC, the likely entry point in the West. These differences suggest the movement of this alien grass along quite different transoceanic routes to Canada, as opposed to exclusively an eastern introduction and subsequent dispersal westward.
Collection history of Bromus tectorum in Canada
Documenting the proliferation of an invasive species in a new range is often an exercise in historical discovery (Stuckey, 1980
; Mack, 1981
, 2000a
). Herbarium records can be reliable resources for documenting a species distribution over time, provided their limitations are recognized. Variation in collection intensity between locales and years and the qualitative character of label information limit the completeness of chronologies assembled solely with these records (Mack, 2000b
). But when herbarium records are combined with additional contemporaneous information (e.g., local surveys, import records, and export records) and genetic analyses, much more can be gleaned about the entry and spread of a plant invader (Novak and Mack, 2001
; Bartlett et al., 2002
; Roche et al., 2003
).
Bromus tectorum was introduced into Ontario no later than 1886. The first specimen of this grass was collected from "waste places" (Millman #29990, CAN) in Kingston, Ontario, a major grain port along the Great Lakes in the 19th century (Baker, 1854
). Considering the frequent role of B. tectorum as a grain contaminant (Mack, 1981
; Updadhyaya et al., 1986), it is not surprising that the grass was first collected in the Kingston area. All the specimens from eastern Canada between 1886 to 1925 were collected in Ontario (Fig. 2a), and of these all but one were collected either in a port or along railroad right-of-ways within 50 km of a port. Great Lakes ports likely facilitated the introduction of B. tectorum to eastern Canada.
From 1926–2004, the range of B. tectorum increased substantially in eastern Canada (Fig. 2b). Most specimens (63%) collected between 1926 and 2004 in Quebec, Nova Scotia and New Brunswick were collected along railroads (Erskine s.n., ACAD; Webster s.n., ACAD; Raymond 824, MT; Germain 122, MT; Dore s.n., MT; Dore and Jenkins s.n., DAO; Groh s.n., DAO; Raymond and Kucyniak, 1948
). Frequent transport of agricultural commodities via railroads would have increased the introduction of new seeds. Furthermore, the persistent disturbance, well-drained regolith, and high insolation common in railway beds would have provided suitable conditions for the spread of B. tectorum across an otherwise heterogeneous landscape. Since 1960, regional railroad traffic has declined and in some areas rail lines have been removed. These events may have contributed to range contraction for B. tectorum in eastern Canada. One of us (M.T.V.) was unable to locate populations of B. tectorum collected between 1940 and 1960 along now-abandoned railroad right-of-ways north of Ottawa and in Nova Scotia. Subsequent intensive field searches in Quebec in 2005, plus queries to local botanists (J. Cayouette, personal communication; G. Hall, personal communication), identified no current localities for the grass.
Three yr after B. tectorum was first collected in Kingston, ON, (1886), it was collected in Spences Bridge, BC (1889). Although these provinces were connected by the Trans-Canadian railroad by 1885, the more than 3000 km that separate Kingston from Spences Bridge and the lack of any collections of B. tectorum between these two locations until 1915 in Lethbridge, AB (Jackson, 1915
) support the contention that the grass was introduced independently to eastern and western Canada. By 1930, B. tectorum had spread throughout the Okanagan Valley in BC (Groh, 1937
), was routinely collected in southwestern AB and had become established in SK (Fig. 2b). The grass had even been collected in the Yukon Territory in 1919 (Malte 165, CAN). This rapid increase in the number of collection sites in western Canada between 1889 and 1930 is unlike the pattern seen in the East (Fig. 2a).
Trade with the U.S. as well as human migration likely contributed to the spread of B. tectorum into and throughout western Canada. Longman and Smith (1936)
attributed the first major introduction of B. tectorum into AB to contaminated alfalfa seed and soil brought by settlers from Utah from 1886–1905 (Palmer, 1992
). The earliest herbarium record for AB was collected in 1915 at Lethbridge (Jackson, 1915
), the site of two major influxes of settlers from Utah ca. 1900. Bromus tectorum may have indeed arrived with these immigrants from Utah, a region which was extensively infested with the grass by 1900 (Mack, 1981
). Subsequent introductions likely occurred during winter, 1919–1920, with the importation of hay from eastern Canada, Washington, Oregon, and Nebraska. During that winter, some hay shipments were reported to consist almost entirely of B. tectorum (Longman and Smith, 1936
). The necessity of keeping livestock alive through winter trumped any concerns about seed contaminants in imported forage.
Bromus tectorum is today most extensive in southern BC and southwestern AB (Tisdale, 1947
; Upadhyaya et al., 1986
). Populations in eastern Canada, SK and MB are largely restricted to arid sites with light-textured soils and continual disturbance, e.g., near granaries, railroad beds, ports, roadsides, landfills, and agricultural fields (Douglas et al., 1990
). Bromus tectorum is surprisingly rare in southeast SK and southern MB. Only three herbarium specimens have been collected in these two provinces east of 106° W longitude (Fig. 2). Evidence for its apparent scarcity is also supported by a 1944 county-level survey of Canadian weeds (Groh, 1944
), which reported no evidence of B. tectorum in southeastern SK and southwestern MB (between 107° and 100° W longitude). A more recent survey of B. tectorum in southern SK (Douglas et al., 1990
), based on mail-in questionnaires, local inquires, and extensive ground surveys, documented only two infestations east of 106° W longitude.
Wheat has been farmed in southern MB and southeastern SK for more than 100 yr (Hurd and Grindley, 1931
). Given the long-term close association of B. tectorum with wheat agriculture, the grass has had ample opportunities for introduction to this region. Furthermore, many habitats (e.g., cultivated land, railroad beds, and construction sites) that have facilitated its establishment and spread elsewhere in North America (Mack, 1981
) are found in these prairie provinces. Its infrequency in this region must therefore stem from other factors that likely include the region's climate, including prolonged periods of freezing air/soil temperatures in winter with little or no snow cover (Hurd and Grindley, 1931
; National Atlas of Canada, 1957
) and extensive clayey or high organic matter soils (Clayton et al., 1977
; Mermut and Arnaud, 1983
; National Atlas of Canada, 1993
). These environmental features limit or even preclude establishment of B. tectorum (Fleming, 1942
; Evans and Young, 1972
; Mack and Pyke, 1983
).
Genetic variability
An immigrant population usually possesses only a subset of the genetic diversity found collectively among populations in the species' native range (Barrett and Shore, 1989
; Barrett and Husband, 1990
; Tsutsui et al., 2000
), a reduction that is exacerbated if the species displays uniparental reproduction (Glover and Barrett, 1987
; Novak et al., 1993
). Genetic bottlenecks do not always occur (cf. Holland, 2001
; Squirrel et al., 2001
), but if they do, the resultant reduction in genetic diversity of introduced populations can often be mitigated by continual migration of genetically diverse individuals from donor ranges (Kolbe et al., 2004
; Novak and Mack, 2005
).
Genetic diversity of B. tectorum in Canada was quite different from that reported by Novak and Mack (1993)
for the grass in its native range. Four loci (Table 1) were variable across all Canadian populations, compared to the 13 polymorphic loci across populations in the native range (Novak et al., 1991
). In addition, 30 alleles were detected (at the 25 scored loci) across all Canadian populations, whereas 43 alleles were detected across all native populations. Conversely, the average number of alleles per locus within populations was slightly higher in Canada than populations of the native range (A = 1.04 vs. A = 1.01), but both Pp and Hexp were more than two-fold larger within Canadian populations of B. tectorum. Founder events were most likely responsible for the reduction in the number of alleles and polymorphic loci detected across Canadian populations. Higher genetic diversity on average within Canadian populations indicates that these populations may be genetic admixtures resulting from the introduction of different genotypes from divergent native range populations (Novak and Mack, 2005
).
Genetic diversity within all 60 Canadian populations analyzed in this study was low (A = 1.04, Pp = 4.20, and Hexp = 0.012, Tables 2 and 3) compared with values reported by Hamrick and Godt (1990)
for other selfing species (A = 1.31, Pp = 20.0, and Hexp = 0.074), but is similar to levels of genetic diversity for other introduced selfing plants (Marshall and Weiss, 1982
; Garcia et al., 1989
). The amount of genetic diversity within populations in Canada and the U.S. were generally similar (Table 3). The Pp for eastern Canadian populations, however, was nearly five-fold greater than values reported by Bartlett et al. (2002)
for 38 populations of B. tectorum in the eastern U.S. (Table 3). These differences in genetic variation likely reflect independent introduction(s) into each region.
Deviation from Hardy–Weinberg equilibrium
Outcrossing events leading to the formation of heterozygous individuals are rare in Canadian populations of B. tectorum. Values for Wright's fixation index (F) for Canadian populations are significant at all loci (Table 4), indicating a violation of Hardy–Weinberg equilibrium. For example, heterozygous individuals were detected in only three Canadian populations (Table 2), and the mean observed heterozygosity (Hobs = 0.0001) in the Canadian range is less than 1% of the expected mean heterozygosity (Hexp = 0.012). The mean observed heterozygosity (Hobs) is slightly higher for Canadian populations than for populations from the U.S. but equal to values reported for by Novak and Mack (1993)
for 51 Eurasian populations (Table 3). Outcrossing is likely occurring at levels greater than we measured. PCR-based markers, which are more polymorphic than allozymes, could potentially provide better estimates of outcrossing and heterozygosity in these populations (O'Hanlon et al., 2000
), although Ramakrishnan et al. (2002)
detected no heterozygotes in B. tectorum, using microsatellite markers. These results collectively reinforce the observation that B. tectorum is a highly selfing plant species (McKone, 1985
; Bartlett et al., 2002
).
Novel allele combinations produced through outcrossing can increase the rate of local adaptation (Garcia et al., 1989
; Allard et al.,
1993) and thereby potentially increase the species' invasive ability (Ellstrand and Schierenbeck, 2000
; Gaskin and Schaal, 2002
). Outcrossing in B. tectorum has implications for its northward range extension in Canada. Few legal safeguards currently block the grass's spread in Canada (White et al., 1993
), and dispersal apparently occurs intermittently to regions outside its largely southern Canadian range (Macoun 39060, CAN; Malte 39055, CAN; Friesen 50623, SASK; King, s.n., UBC; Krajina, s.n., UBC). The introduction of more genetically diverse individuals of B. tectorum to northern regions may lead to persistence in areas where heretofore only ephemeral populations have appeared.
Population differentiation
Most (59.5%) allelic diversity in Canadian populations of B. tectorum is distributed within rather than among populations (GST = 0.405) (Table 5), but the distribution of allelic diversity varies between eastern and western ranges. The majority of the allelic diversity is partitioned within populations in both regions (Table 6), but the GST value among populations in western Canada is lower than among populations in the East (GST = 0.316 vs. 0.447), which may be a function of the larger numbers of populations we sampled in the West (Fig. 1, Table 2). Alternatively, repeated introductions of B. tectorum to western Canada from the native range, the U.S., and eastern Canada could explain our finding that most of the total gene diversity in western Canada is partitioned within populations.
Gene diversity statistics between regions in Canada and the U.S. follow patterns similar to those portrayed by our measures of genetic diversity. Total gene diversity (HT) is much higher in eastern Canadian populations than in eastern U.S. populations (HT = 0.265 and 0.075, respectively) (Table 6). While 55.3% of the genetic diversity is partitioned within populations in eastern Canada, nearly the same amount of genetic diversity (56%) is partitioned among populations in the eastern U.S. (Bartlett et al., 2002
). Conversely, gene diversity statistics for western Canadian populations are intermediate between those for populations in the mid-continent U.S. and the western U.S. (Table 6). Genetic structure of the populations in these three regions is quite similar, which may reflect analogous patterns of entry and spread of the grass across western North America.
Mean total gene diversity (HT) for B. tectorum is nearly two-fold higher for populations in Canada than reported for populations in the native range by Novak and Mack (1993)
(Table 6). A much smaller proportion of the total gene diversity is partitioned among populations in Canada (GST = 0.405) than in Eurasia (GST = 0.754). If introduced populations are genetic admixtures, they would become more genetically similar, and the proportion of variation among populations would decrease (GST < 0.50) (Brown and Marshall, 1981
; Barrett and Husband, 1990
). Gene flow in predominantly selfing plants largely depends on seed dispersal (Loveless and Hamrick, 1984
; Hamrick, 1989
). Thus, higher level of genetic diversity within Canadian population of B. tectorum, relative to native populations (Tables 3 and 6), likely reflect multiple introductions and gene flow as seeds dispersed among populations. Differences between gene diversity statistics for Canadian and Eurasian populations indicate rapid range expansion of introduced genotypes in Canada.
Donor populations and shared multilocus genotypes
Nearly obligate cleistogamy minimizes the opportunity for outcrossing in B. tectorum. Consequentially, the new populations in an area retain the allelic variation of their donor populations, and the entry and spread of these genotypes in the new range can be traced (Novak et al., 1991
, 1993
; Novak and Mack, 2001
). Our analysis reveals a minimum of three independent introductions of B. tectorum to eastern Canada and at least five to western Canada. However, all these genotypes are found elsewhere in North America (Novak et al., 1991
; Bartlett et al., 2002
; Schachner, 2005
) and in other naturalized populations around the world (James et al., 1996
). As a result, we cannot establish direct links between populations in Canada and those in the native range; any genotype in Canadian populations may be the product of random genetic sampling in native and/or naturalized ranges. Plausible scenarios for the entry and spread of each genotype in the Canadian range, however, can be formed based on allozyme data and historical evidence.
Three multilocus genotypes are widespread across Canada: MCG (the most common genotype), Got-4c, and Pgm-1a & Pgm-2a (Table 7). The MCG was detected in all but one Canadian population (Chatham, ON) (Fig. 3a). The Got-4c multilocus genotype is widespread throughout BC (Fig. 3a) and elsewhere in western North America (Novak and Mack, 1993
), but until its detection in southern ON, this allele had not been reported east of Laramie, Wyoming (Schachner, 2005
). Only 11 of the 420 plants (2.6%) analyzed in southern ON were homozygous for Got-4c; these individuals were detected in four populations (Fig. 3a, Table 7). In eastern Canada, the Pgm-1a & Pgm-2a multilocus genotype is present in 56% of the populations sampled. This genotype is less frequent in western Canada (only 23% of populations), and most (70%) of these populations occur in the Okanagan Valley of BC (Fig. 3b). In the U.S., the Pgm-1a & 2a multilocus genotype is most common in mid-continent populations (Schachner, 2005
) but has also been found at low frequencies among populations in the eastern and western U.S. (Novak et al., 1991
; Bartlett et al., 2002
). The Mississippi and Ohio Rivers have long been shipping routes between the midwestern U.S. and southern Ontario (Haites et al., 1975
), and it is plausible that seeds of B. tectorum have dispersed repeatedly along these routes.
Central BC has the longest collection history of B. tectorum in western North America. Six of the 10 BC populations sampled in 1990 by Novak et al. (1991)
contained the Pgm-1a & 2a multilocus genotype. Fifteen years later, we sampled an additional 16 populations from southern BC; the only population that contained this genotype (Kamloops, BC) occurs amongst the six populations that Novak et al. (1991)
analyzed (Fig. 3b). Populations with this genotype do not appear to have increased their range in central BC in the last 15 yr.
In contrast, the Tpi-1b and Got-4d multilocus genotypes are exceedingly rare among populations in Canada and were found only in the West (Fig. 3a) and at low frequencies (Table 1). The Tpi-1b multilocus genotype has been reported in Osoyoos, BC (Novak et al., 1991
), but its discovery in Golden, BC repesents a new report in the province for this genotype, which remains intriguingly undetected in Western Europe. The Got-4d multilocus genotype has a restricted range in Central Europe (Novak and Mack, 1993
) and had previously been found in two nearby populations (Provo, Utah and Dubois, Idaho) (Novak et al., 1993
). In Canada this genotype was detected only in the population from Waterton, AB. The occurrence of a population with this genotype in a part of AB heavily settled by people from Utah at the end of the 19th century, as well as along the route taken by these settlers migrating from Utah to southern AB (at Dubois, Idaho), and in a major settlement at Provo, Utah (Jensen, 1992
), supports Longman and Smith's (1936) contention that settlers from Utah inadvertently introduced B. tectorum to southern AB. If accurate, this scenario would represent one of the best-documented cases of B. tectorum dispersal along paths of human migration.
Implications for future quarantine and control
Beyond assessing the genetic diversity of B. tectorum in Canada, our results identify consequences for the grass's future importation and dispersal. Bromus tectorum is deemed a noxious weed in SK and MB and a nuisance plant in AB, but its control is not regulated elsewhere in Canada (White et al., 1993
). Comparisons of different genotypes of B. tectorum in common gardens (Kinter, 2003
), however, illustrate that the role of this grass—whether a minor community member or an aggressive invader—turns on which genotype arrives in a region. There is no assurance that all genotypes, including some that may be preadapted to Canadian environments, have already reached Canada. Moreover, the detection of outcrossing in some populations suggests the de novo creation of genotypes in Canada that could emerge as further weedy threats. As a result, blocking the spread of B. tectorum both internationally and domestically is clearly in any nation's environmental/economic interests.
FOOTNOTES
1 The authors thank S. J. Darbyshire for invaluable assistance in locating herbarium records, historic collection documents, and populations in the field. B. Bennett, K. Burdon, N. Cappuccino, T. A. Cope, S. Denison, S. Hay, N. Khan, L. Kinter, S. Marner, L. McDade, K. McGuinness, A. V. Novak, S. N. Novak, M. I. Novak, G. Russell, L. Schachner, C. Stern, A. Stillman, G. Turner, and D. H. Webster provided logistical or research assistance during the study. R. A. Black, M. Brooke, S. Mortenson, and M. Webster provided further assistance and encouragement. They thank the herbaria ACAD, ACK, ALTA, CAFB, CAN, DAO, DAS, GH, LKHD, MT, MTMG, OAC, OXF, QFA, QUE, SASK, UBC, US, UWO, and WIN for access to their early specimens of Bromus tectorum. This research was funded substantially through support from the Betty W. Higginbotham trust at Washington State University. Additional funding was provided by the Faculty Research Grant Program at Boise State University. 
4 Author for correspondence (snovak{at}boisestate.edu
; present address: CSIRO European Laboratory, Campus International de Baillarguet, 34980 Montferrier-sur-Lez, France.
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  L. J. Schachner, R. N. Mack, and S. J. Novak Bromus tectorum (Poaceae) in midcontinental United States: Population genetic analysis of an ongoing invasion Am. J. Botany, December 1, 2008; 95(12): 1584 - 1595. [Abstract] [Full Text] [PDF]
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