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a Department of Biology, University of Utah, Salt Lake City, Utah 84112; b Garrett Herbarium, Utah Museum of Natural History, University of Utah, Salt Lake City, Utah 84112; and c Department of Botany and Range Science, Brigham Young University, Provo, Utah 84602
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Key Words: Arctomecon • bear poppy • heterozygosity • gene flow • genetic diversity • Papaveraceae
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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According to Wright's (1943, 1946) isolation by distance models, mating is dependent on the distance between individuals and their ability to disperse propagules. Based on these models, inbreeding may occur if isolation increases and prevents gene flow between small patch populations. Habitat fragmentation and loss of critical habitat are becoming increasingly more common for many species, especially those in and around urban centers. Rare and/or endangered plant species often occur in small, disjunct populations with reduced genetic diversity due to increased habitat fragmentation and inbreeding (Stebbins, 1980; Simberloff, 1988; Barrett and Kohn, 1991; Godt, Johnson, and Hamrick, 1996; Sun, 1996).
Arctomecon humilis Coville (Papaveraceae), the dwarf bear poppy, is a short-lived perennial herb (average life span ~5 yr) restricted to gypsiferous shale substrates in Washington County, Utah (Atwood, 1977). The species occupies isolated sites within a 10-km radius of the city of St. George, Utah. During the last decade, urban development in the St. George area has eliminated or fragmented much of the critical habitat for the species. From 1970 to 1995, Washington County, Utah, grew by an average annual rate of 6.6%, which was by far the fastest growth rate of any county in the state of Utah (Christiansen and Robson, 1997). Washington County increased its population by 45% from 1990 to 1994 making it the fifth fastest growing county in the United States (Wright, 1996). By the year 2000, the city of St. George, Utah, has been estimated to grow to a population level of over 82 000 people, in addition to the estimated 2 million tourists that visit annually (Governor's Office of Planning and Budget, 1997).
The distribution of A. humilis is typically restricted to the white-gray (Shinob Kibe) or sometimes red gypsiferous members of the Moenkopi Formation, substrates that support only sparse vegetation (Nelson and Harper, 1991). These Moenkopi shale substrates are attractive to off-road vehicle users that not only destroy living plants, but also accelerate soil compaction and erosion. Much of this gypsum substrate is covered by mining claims. The 1872 General Mining Law required annual labor ($100 per claim) for the maintenance of these gypsum mining claims (MacDonnell, 1993). This work was often very disruptive and destructive. Many claim holders, for example, simply used a bulldozer to move soil around at a claim site, thus fulfilling the annual labor requirement. Today these activities are much reduced by mandatory fees (MacDonnell, 1993). Nevertheless, these labor requirements, in the past, have marred significant bear poppy habitat.
In 1979, the U.S. Fish and Wildlife Service listed A. humilis as an endangered species (U.S. Fish and Wildlife Service, 1979). In response to increasing threats, several hundred acres of poppy habitat were closed to off-road vehicle use by the Bureau of Land Management and the state of Utah (U.S. Bureau of Land Management, 1987). These closures include three populations (Red Bluff, Beehive Dome, and Warner Ridge), which are the largest extant populations of the species. Although these areas are posted, the closures have not completely curtailed use by off-road vehicles. In addition, housing development continues in the St. George area. These forces threaten the existence of the 11 extant populations of the species, especially the eight unprotected populations. Because of the narrow endemism and decline due to many human related factors, bear poppy has become one of the most critically endangered species in Utah.
Land managers faced with the difficult task of developing recovery plans for A. humilis have had to rely on information from habitat studies and demographic surveys (Nelson, 1989; Nelson and Harper, 1991). Recent analysis of DNA markers in these known populations using randomly amplified DNA procedures showed little variation among populations but offered no insight into genetic variation within populations, since the analysis was based on bulked samples from the individual populations (Van Buren and Harper, 1996). Management decisions regarding the future of these populations would be much improved by more detailed information concerning the genetics of the species in its various subpopulations (Falk and Holsinger, 1991).
A recent reproductive study of A. humilis reveals that the species has a mixed mating system (V. J. Tepedino, Utah State University, personal communication). The species requires an insect vector for successful fertilization of its ovules. The species is partially self-compatible. However, only approximately half of geitonogamously crossed flowers set fruit, while all of xenogamously crossed flowers set fruit (V. J. Tepedino, personal communication). The species is primarily bee pollinated (Tepedino and Griswold, 1989). The flowers are visited by an array of native, ground-nesting bees (often, a different suite of bees for each population) and Apis mellifera, the domestic honey bee. The native bees are often more efficient than the honey bees at pollination in A. humilis (visiting when stigmas are more receptive) and several of these native bee species are quite rare (V. J. Tepedino, personal communication; Tepedino and Griswold, 1989). Seed dispersal in this species is short-distance, primarily by ants attracted to the seeds by arils (Nelson, 1989).
Conservation and management suggestions for several rare plant and animal species have been made based on recent genetic analyses (Odasz and Savolainen, 1996; Sheely and Meagher, 1996; Cummings et al., 1997; Godt, Walker, and Hamrick, 1997; Ramirez and Froehlig, 1997; Sipes and Wolf, 1997). It is important that land mangers understand how genetic diversity is distributed among the remaining natural populations of A. humilis, if they are to preserve its remaining genetic diversity. This is especially critical considering the high levels of habitat loss and fragmentation due to housing development, gypsum mining claims, and off-road vehicle use, and considering the short-distance dispersal of pollen and seeds of this species. Short-distance dispersal of propagules, in association with increased isolation of populations due to habitat fragmentation, may result in inbreeding (Wright, 1943, 1946). In order to facilitate preservation of genetic diversity within the species, genetic variability and gene flow within and among the populations of A. humilis were evaluated in this study.
The research addressed in this manuscript explored the following questions. Does gene flow exist among these populations? How much genetic diversity exists within populations? How is genetic diversity distributed among populations and age classes within a given population? How does genetic variability in A. humilis compare with that of a near relative A. californica Torr.&Frem.?
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Distribution of genetic variation among populations was estimated using Nei's (1973) genetic diversity statistics employing Lynsprog, a statistical genetics program written by M. D. Loveless (College of Wooster, Wooster, Ohio). These included: total genetic diversity (Ht), intrapopulation genetic diversity (Hs), diversity between populations (Dst), and the proportion of genetic variation distributed among populations (Gst). Gene flow (Nm, number of migrants per generation) among populations was calculated based upon Gst, using methods of Wright (1951).
The fixation index (F) was computed for each locus and each population using methods of Wright (1965). Chi-square analysis of Wright's fixation indices for study populations was used to test significance of deviations from Hardy-Weinberg expectations. Fixation indices and deviations from Hardy-Weinberg expectations were computed following Hamrick, Linhart, and Mitton (1979), Hedrick (1985), and Hamrick and Godt (1990) using Lynsprog, a statistical genetics program written by M. D. Loveless (College of Wooster, Wooster, Ohio).
Average linkage clustering using the unweighted pair-group method (UPGMA) was performed for study populations using Nei's genetic identities (Romesburg, 1984) in order to graphically portray genetic similarity among populations. Percentage similarity was computed among A. humilis populations for abiotic (soil) characteristics (Nelson and Harper, 1991) using Ruzicka's (1958) similarity index. A UPGMA phenogram was generated from these similarity indices (Romesburg, 1984). The UPGMA phenogram generated from abiotic characteristics of A. humilis populations (Nelson and Harper, 1991) was compared with the UPGMA phenogram constructed based on Nei's genetic identities, using only the populations considered in the abiotic UPGMA phenogram.
Percent similarity was computed among age-classes using genotype frequencies at the Pgi-2 locus and Ruzicka's (1958) similarity index. Mean Ho was calculated over all loci for each age class among all populations (Nei, 1973). Populations were bulked in this analysis because sample sizes by age class were small within populations (only 8–10 individuals). A one-way ANOVA and Tukey-Kramer multiple means comparisons were performed to test for significant differences among age-classes (SAS, 1994).
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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Most of the total gene diversity (Ht = 0.339) in A. humilis was distributed among populations (Dst = 0.209). Gst (the proportion of genetic variation distributed among populations) was estimated as 0.617, thus 61.7% of the genetic variability was distributed among populations. Total gene flow across all populations was low (Nm = 0.155).
Fixation index (F) was determined for all loci in each population of A. humilis. Chi-square analysis demonstrated significant deviation from Hardy-Weinberg expectations for some of the populations and loci (Table 4). SE Boomer Hills, the most genetically variable of the study populations, showed significant deviation from Hardy-Weinberg at two enzyme loci. Warner Ridge and WD also exhibited significant deviation (P 
0.05) from Hardy-Weinberg expectations at Tpi-3 (Table 4). Since six populations were sampled and ten loci, there were a total of 60 determinations of F deviations from Hardy-Weinberg equilibrium. For A. humilis, four of the 60 determinations (~7%) deviated significantly (P 0.05) from Hardy-Weinberg. This is only slightly more than you would randomly expect to be significant by chance alone (at the 5 % level). However, only two populations of A. californica were sampled for this study. Of the 20 possible determinations of F deviations from Hardy-Weinberg expectations, five showed significant deviation (Pgm-1 and Tpi-1 for both populations and Nadh-dp for the OVER population; Table 4). This is much greater than might be expected by chance alone. In addition, the He values for these populations are much higher than the Ho values (Table 3), thus suggesting that the two A. californica populations sampled are significantly deviating from Hardy-Weinberg expectations.
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The genetically diverse western populations of A. humilis (RB and SEBH) also exhibited patterns of temporal (age class) variability evident only at the Pgi-2 locus. Similar genotypes for this locus were observed in the seedling and old age classes, while intermediate age classes typically possessed an alternate set of genotypes at Pgi-2 (Table 6). However, while the temporal variability was evident at both populations, RB and SEBH had different distributions of genotype frequencies among the age classes. Percentage age similarity (Ruzicka, 1958) was calculated among age classes for both the RB and SEBH populations based on genotype frequencies at Pgi-2. Seedlings and old individuals are 56.2% similar at Pgi-2 for RB and SEBH. Seedlings and intermediate-aged individuals are only 23.2% similar and intermediates and old individuals are 24.6% similar. Statistical analyses were not performed due to the small sample sizes by age-class for each population and the inability to bulk the populations due to the different distribution of genotype frequencies within the two populations (Table 6).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONREFERENCES |
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The most genetically unique of the sampled populations is Shinob Kibe. This population lies on privately owned land, which is being heavily developed. The Nature Conservancy is now attempting to purchase ~28 ha of land adjacent to the Shinob Kibe Butte. If purchased, the land would be fenced to exclude off-road vehicles and casual foot traffic. We previously mentioned a recent study performed on the genus Arctomecon using RAPD (randomly amplified polymorphic DNA) markers (Van Buren and Harper, 1996). The RAPD study suggested that the Shinob Kibe (SK), the most northern population, had a genetic make-up somewhat different from other populations because it had the fewest number of RAPD markers shared with other populations. These data are consistent with our findings based on genetic identity values among populations. Shinob Kibe had the lowest mean genetic identity value with other sampled populations (Fig. 2).
Most of the total genetic diversity (Ht) of the species, using data from this study, is distributed between populations and gene flow between populations is low. Populations of A. humilis are becoming progressively more fragmented and isolated from one another due to housing developments and disturbance from off-road vehicles. However, Van Buren and Harper (1996) stated that A. humilis showed little RAPD variation among populations. In this manuscript, we find that 61.7% of all the variability in A. humilis is distributed among populations. Van Buren and Harper (1996) bulked leaf material from all sampled individuals in a population into a single sample for each population. This type of bulking prevents any interpretation on variability within populations. This type of sampling also prevents an accurate assessment of the distribution of genetic variability among populations. Markers are typically noted for a particular population without any consideration of their frequency within the population.
Distribution of genetic diversity may be affected by spatial and historical factors (Kimura and Maruyama, 1971; Slatkin, 1987; Sheely and Meagher, 1996) and/or ecological and life history traits (Hamrick et al., 1979; Karron, 1987; Karron et al., 1988; Hamrick and Godt, 1990). The historical range and past population sizes in A. humilis are relatively unknown. However, one of the authors of this manuscript (K. T. Harper) has observed a decline in the number of individuals in several of the populations over the past 20 yr.
Arctomecon humilis is confined to the Shinob Kibe member of the Moenkopi formation. This geologic formation is often discontinuous across the landscape surface. Some of the sampled populations, therefore, may have been isolated for a long period of time, because the substrate was laid down during the Holocene (Hintze, 1973). The SK population is located on the edge of the Shinob Kibe Butte that is more geologically separated from the other populations, which might explain its genetic uniqueness.
Some of the populations (RB, SEBH, and WD), on the other hand, are growing on different parts of a, at one time, continuous member (Shinob Kibe) of the Moenkopi formation. Little development has occurred between the RB and SEBH populations. It is, therefore, likely that gene flow events may occasionally occur between these two populations. However, much urban development has occurred between the RB and WD populations, including the construction of a major interstate (Interstate 15) and a suburban development (Bloomington). This urban development might explain the genetic differentiation between the WD and the RB and SEBH populations. Off-road vehicle users have also heavily hit the WD population. The authors have seen a significant reduction in the number of individuals in this population over the past 10 yr. The WD population was also the least genetically variable of the A. humilis populations.
Since genetic distance could not be correlated with geographic distance in this study, historic and geologic distribution of populations may be responsible for the observed distribution of genetic diversity among populations, rather than a disruption of gene flow due to habitat fragmentation. However, additional study is necessary. We feel that this manuscript provides baseline genetic information for future studies. In the future, allozyme variation should be reassessed in these populations to look at the long-term effects of human induced habitat fragmentation and habitat degradation on genetic diversity and genetic structure in this species.
Some populations of A. humilis, especially SEBH, appear to be inbreeding (F values varied significantly from zero). This population was the smallest of the study populations (<100 individuals, Table 1). Inbreeding may result in reduced fitness for some of these populations (Schemske and Lande, 1985; Simberloff, 1988; Levin, 1991). However, more compelling are the data on F deviations from zero in A. californica. Because only two populations of this more common species were sampled in this study, we will refrain from discussing possible reasons for the H-W deviations. We note that a graduate student (L. Hitchcock, Utah State University) is assessing allozyme diversity in A. californica. It will be interesting to compare the results of the two studies upon completion.
Mean observed heterozygosity is significantly lower in A. humilis (Ho = 0.100) than other outcrossing plant species (Ho = 0.167) and dicots (Ho = 0.136), but only slightly lower than other short-lived herbaceous perennials (Hamrick and Godt, 1990; Table 7). Genetic diversity in A. humilis is consistent with the level of variation observed in other narrow endemic species (Ho = 0.096; Hamrick and Godt, 1990). Arctomecon humilis populations exhibit less genetic variability on average than the sampled populations of A. californica. Both species are endemic to gypsic soils of Mojave Desert regions. However, A. californica is geographically more widespread and occupies an ecologically broader range of habitats than A. humilis (Nelson and Welsh, 1993). These results are consistent with examples in the literature of geographically restricted species having less genetic variation than more widespread congeners (Karron, 1987; Karron et al., 1988; Hamrick et al., 1991; Hamrick and Godt, 1996; Godt, Walker, and Hamrick, 1997). Arctomecon californica exhibited significantly higher number of effective alleles per locus than other comparative species groups (Hamrick and Godt, 1990; Table 7). The species' mean observed heterozygosity (0.175) was higher than other dicots, short-lived, herbaceous perennials, and outcrossing (requiring an animal vector) and endemic species (Hamrick and Godt, 1990; Table 7).
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Allozyme markers have been considered as "neutral" genes reflecting evolutionary processes affecting the entire genome (Avise, 1994). Mitton (1994), however, postulates that environment may occasionally select for allozyme markers. The phenogram resulting from cluster analysis of the populations based upon Nei's genetic identities is similar to that based on soil analyses for the same populations (Nelson and Harper, 1991). These results suggest that abiotic conditions may have selected for the allozyme markers observed in A. humilis. Before this hypothesis can be accepted, however, genetic variability within and among populations must be assessed using a molecular technique with known neutrality of markers.
The patterns of genetic variability among age classes in the Red Bluff and SE Boomer Hill populations were only observed at the Pgi-2 locus, which is a rapidly evolving and highly variable enzyme locus (Gillespie and Kojima, 1968). The observed genetic differences among the three age classes indicate that age structure in existing populations is important and should be considered in preservation of genetic diversity within A. humilis populations.
Seeds of the Papaveraceae are dispersed before they mature and require a prolonged period of after-ripening followed by a specific weather regime (cool, wet springs) to germinate (Nelson, 1989). This may require years of residence in the seed bank before germination. The time necessary for completion of development and germination is unknown. Therefore, the seed bank undoubtedly has a major impact on a population's gene pool. Seed banks are believed to buffer populations against changes in genetic composition and increase the effective population size (Epling, Harlan, and Ball, 1959). They may also serve as a source of novel genetic variation because of mutations in seeds as they age (Levin, 1990). Soil erosion and compaction, however, could eliminate a viable seed bank.
Age classes of A. humilis plants differ with respect to mean heterozygosity. Heterozygosities and polymorphic indices have been demonstrated to increase with age in some trees and long-lived perennials (Schaal and Levin, 1976; Hamrick, 1979). It appears, however, that even in a short-lived perennial (average longevity <5 yr) such as A. humilis, heterozygosity may increase survivorship and thus longevity. Such a conclusion is supported by recent work with two herbaceous perennials (Cabin, 1996; Hossaert-McKey et al., 1996).
Recovery plans for endangered species, especially A. humilis, should not only consider the genetic variability among populations, but variability within populations. This research provides exceptions to common generalizations. First, it is risky to generalize that the largest populations of any species are the most variable genetically. Several of the large populations of A. humilis possessed very little genetic variability. Second, protection for an endangered species should include not only all ages within a given population, but the seed bank as well. In order to preserve genetic variability in species where populations are declining as with A. humilis, managers should attempt to preserve individuals representative of all age classes. In situations where areas are reseeded, seed should be collected from all age classes in a given population, as well as from the seed bank.
We recognize, however, the limitation of our small sample sizes per population (24–30 individuals). Interpretation of within-population and age-class variation is difficult when only 30 individuals out of several hundred are sampled. Therefore, future genetic studies in A. humilis should also include larger sample sizes for a better understanding of the distribution of variation among age classes within populations in A. humilis.
Because the historical range and past population sizes in A. humilis are relatively unknown, interpretation of the data presented in this manuscript is difficult. However, it is evident that populations are becoming fragmented and lost. Off-road vehicles and development still pose a serious threat to the existence of the dwarf bear poppy. If these current human activities continue, it is likely that gene flow among populations will continue to be interrupted and genetic differentiation and drift among populations will therefore increase. We also feel that the data in this manuscript illustrate the importance of maintaining the age structure within populations. Since the seed bank is vital to the species, it is critical that land managers enforce restrictions to off-road vehicle use. Additional dwarf bear poppy populations will likely go extinct. However, land managers and groups, like the Nature Conservancy, can use these genetic data to ensure that the genetic diversity within A. humilis is preserved.
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FOOTNOTES |
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5 Author for correspondence, current address: Department of Botany and Range Science, Brigham Young University, Provo, UT 84602 (email:LAWoolst{at}bioag.byu.edu). |
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