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Population Biology |
Department of Botany and Plant Sciences and Center for Conservation Biology, University of California, Riverside, California 92521 USA
Received for publication August 11, 2000. Accepted for publication December 22, 2000.
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ABSTRACT |
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 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Key Words: conservation • Eriogonum • inbreeding • mating systems • outcrossing rates • San Bernardino Mountains
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INTRODUCTION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Conserving many large populations over the ecological and geographic range of the taxon of interest is considered the best way to capture most of the adaptive variation present (e.g., Schemske et al., 1994
). Often, however, many large populations do not exist, and, even if they do, it is rarely possible to conserve all desired populations. Understanding how diversity is structured and predicting future changes in that diversity is essential to designing effective reserve networks and assessing consequences of particular trade-offs. Knowledge of mating systems can aid in this understanding because of their role in structuring genetic diversity, transmitting diversity across generations, and determining rates of loss of that diversity (Hamrick, Linhart, and Mitton, 1979
; Brown, 1989
; Ritland, 1989
).
The importance of mating systems in structuring genetic variation within and among populations is well documented (Hamrick, Linhart, and Mitton, 1979
; Loveless and Hamrick, 1989; Hamrick and Godt, 1989
). Predominantly outcrossing taxa typically have most of their diversity residing within populations with relatively little differentiation among populations; highly selfing species show just the opposite pattern. This information has bearing on conservation priorities for in situ conservation and on collection (Brown and Briggs, 1991
) and breeding strategies (Ritland and El-Kassaby, 1985
) for ex situ conservation and reintroductions. Genetic diversity (at least for neutral or nearly neutral loci) in highly outcrossed taxa is thought to be effectively conserved by maintaining a few populations of sufficient size to be protected from drift. Additional populations provide redundancy but are not likely to capture additional diversity (e.g., Brown, 1989
). In contrast, capturing the range of genetic diversity present in differentiated populations of a highly selfed taxon requires protection of a larger number of populations, even if these populations are somewhat smaller.
Effects of mating system characteristics on maintenance of diversity are also well documented. The degree of nonrandom matings in a population, particularly self-fertilization, directly affects rates of inbreeding (reviewed in Barrett and Kohn, 1991
). The most immediate effect of inbreeding is to decrease the frequency of heterozygotes in a population relative to a randomly mating population with the same allele frequencies. Inbreeding is of particular interest because it can result in inbreeding depression, lowered fitness of inbred individuals relative to individuals from random matings (e.g., Wright, 1965
; Charlesworth and Charlesworth, 1987
). Selfing can also indirectly increase loss of diversity due to genetic drift by decreasing effective population size. Consequences of such losses are debated and include possibly limiting the evolutionary potential of a taxon (Barrett and Kohn, 1991
).
Three aspects of mating system may make major contributions to nonrandom mating in populations and thus have direct application to conservation: selfing rate, amount of biparental inbreeding, and correlation of outcrossed paternity. If matings are some combination of selfing and random outcrossing, inbreeding will occur only in the portion of the progeny derived from self-fertilization (Fyfe and Bailey, 1951
; Clegg, 1980
). Thus, knowing the selfing rate in a population provides information about risks of loss of genetic diversity. However, if outcrossed matings occur more frequently among close relatives than expected under random mating, apparent selfing rates also include results of consanguineous matings (Ellstrand, Torres, and Levin, 1978
; Ellstrand and Foster, 1983
; Ritland, 1984
). Such matings among related individuals, or biparental inbreeding, can result from spatial substructuring of genotypes in a population (Ennos and Clegg, 1982
) due to limited dispersal of pollen and seed (Turner, Stephens, and Anderson, 1982
), or from temporal variation in synchrony of mating among individuals (Hall, Walker, and Bawa, 1996
). Biparental inbreeding is typically less severe than inbreeding from selfing, but may still cause substantial inbreeding depression (Nason and Ellstrand, 1995
). Because of different levels of severity, it is important to separate contributions of biparental inbreeding from selfing.
Further deviations from random matings can occur if outcrossed siblings tend to be sired by the same father (Ritland and El-Kassaby, 1985
). This type of correlated mating can be estimated as the correlation of outcrossed paternity (Ritland, 1989
), which is the proportion of randomly chosen outcrossed progeny pairs from a family that are full sibs. High correlation of outcrossed paternity can yield a more closely related population than indicated by outcrossing rates alone. This correlation can be accentuated in small populations due to low numbers of potential pollen donors, by reduced pollinator visitation (Young and Brown, 1998
), or if male fitness is not evenly distributed among plants (e.g., Devlin and Ellstrand, 1990
). A consequence of higher genetic relatedness is increased covariance among sibs and variance among sibships, which reduces the effectiveness of natural selection (Ritland, 1989
).
Clearly, understanding mating patterns can be helpful in managing rare plant taxa to maintain genetic diversity. The purpose of our research was to estimate mating system parameters in six populations of a federally listed endangered plant taxon, Eriogonum ovalifolium var. vineum (Small) Jepson (Polygonaceae), using isozyme electrophoresis of naturally pollinated progeny arrays. Specifically, we compared mating-system parameters among populations across the environmental range of the taxon and examined relationships between mating-system parameters and plant density, fruiting success, and number of inflorescences per plant. We then examined the role of these results in conservation of E. ovalifolium var. vineum.
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MATERIALS AND METHODS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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). Corolla length measures only 2–7 mm (Hickman, 1993
); however, hundreds of perfect flowers are clustered into showy, 2–3 cm diameter, head-like inflorescences. Nothing is known of the timing of maturity of male and female parts within flowers, however the large numbers of flowers on a plant open simultaneously, providing ample opportunities for geitenogamous pollination. Perianths are composed of six tepals, the colors of which range from creamy white through yellowish white, light pink, and burnt orange to magenta. As with many Eriogonum flowers, there is a dark stripe along the midrib of each tepal that contrasts with the typically lighter colored tepal margins. Fruits are 2–3 mm long achenes (Hickman, 1993
) that typically fall from the plant attached to the dried corolla when mature. Pollinators include members of the order Diptera in the families Bombyliidae, Chloropidae, Muscidae, Tachinidae, and Anthomyiidae as well as the family Halictidae in the order Hymenoptera (S. Morita, personal communication, University of California, Davis).
Eriogonum ovalifolium var. vineum is endemic to limestone and dolomite substrates that are found in an 
13 000-ha region in the San Bernardino Mountains of southern California (Hickman, 1993
; USFWS, 1994
). The taxon grows between 1400 and 2400 m elevation (Gonella and Neel, 1995
; Neel, 2000
) in limited and often isolated areas totaling 550 ha within this range (S. Redar, personal communication, San Bernardino National Forest). Some populations have been lost, and others have been reduced in size due to surface mining of limestone that threatens the taxon throughout its range (USFWS, 1994
).
Environments vary greatly over the elevational range of the taxon, extending from desert to montane conditions. At lower elevations annual precipitation averages 14 cm, and temperature extremes vary from –17° to 43°C. At higher elevations precipitation averages 58 cm/yr, and temperatures range from –28° to 32°C. (U.S. Department of Commerce, 1999
). Habitats in which this taxon occurs vary correspondingly over this environmental gradient (Gonella and Neel, 1995
; Neel, 2000
). Lower elevations are dominated by pinyon–Utah juniper/black bush scrub vegetation characterized by an open shrub canopy (primarily Coleogyne ramosissima (black bush)) with low densities of Pinus monophylla (single-needle pinyon pine) and Juniperus osteosperma (Utah juniper) in the overstory. Mid-elevations support various phases of single-needle pinyon–Utah Juniper woodland. High-elevation occurrences are in Jeffrey pine–mountain juniper woodlands codominated by Pinus jeffreyi, Juniperus occidentalis ssp. australis, and P. monophylla. Despite the substantial variation described above, habitats supporting E. ovalifolium var. vineum all tend to have open overstory and shrub canopies, as well as high soil pH and percentage calcium (Neel, 2000
).
Population sampling and tissue extraction
Mating system
Mating-system parameters were estimated using naturally pollinated progeny arrays from ten maternal individuals in each of six E. ovalifolium var. vineum populations (Fig. 1). These populations reflected the elevational range of the taxon including two low-, two mid-, and two high-elevation populations. Maternal individuals were selected randomly under the condition that the selected individual had at least five inflorescences with 20 or more flowers with mature fruits per inflorescence to ensure sufficient sample sizes. Fruits were deemed mature if they fell off an inflorescence when shaken or brushed. Leaf tissue was collected from each maternal plant in each population and was stored on ice until reaching the laboratory. From that time until extraction (within 48 h) leaf tissue was stored at 8°C. Approximately 50 mg of tissue were ground with laboratory-grade quartz sand in ten drops of the extraction buffer of Mitton et al. (1979)
. Crude extract was soaked onto filter paper wicks and stored at –80°C for up to 2 mo before running.
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Plant density and inflorescence and achene characteristics
Density of Eriogonum individuals was estimated by counting the number of individuals at a site and measuring the area occupied. All individuals located within the designated area were marked with pin flags as the area was traversed repeatedly by two observers. The areas in which densities estimated included all of the individuals sampled for mating system characteristics in each population. This method provided a single density estimate for each population; however, each estimate is based on a relatively large area. We chose this method over more numerous small plots due to the large number of empty plots and variation among plots found in preliminary sampling efforts. At sites LOW-2, MID-1, and HIGH-1, all individuals were counted, and the total area occupied was measured. The count from site LOW-1 is considered to be fairly complete, but it is not considered exhaustive because additional searching was limited by steep terrain. Populations at sites MID-2 and HIGH-2 were too large and extensive to obtain complete counts. At these sites we counted the number of individuals within an area measuring 5000 m2 (comparable to the area occupied by the first site sampled). Actual area varied due to constraints imposed by steep terrain.
Number of inflorescences was recorded on each plant sampled for mating system parameters. Where possible we counted the number of live achenes produced from 50 flowers on each of 5–6 randomly chosen inflorescences per plant (a total of 299 inflorescences were examined). It was not possible to find 50 flowers on each inflorescence as some flowers had already abscised at the time of sampling. For inflorescences with <50 flowers, all flowers were counted. The actual number counted ranged between 4 and 50 and averaged 37.2 flowers/inflorescence (SD = 12.4). Achenes were considered live if they were plump and colored green or beige to pale rust. These achenes were easily distinguished from dark brown to rust colored, shriveled, achenes that were considered aborted. This method likely overestimates the number of live achenes produced as no germination trials were conducted.
Electrophoresis
Achenes and maternal leaf samples were assayed for four polymorphic allozyme loci using electrophoresis: phosphogluco-isomerase (PGI; EC 5.3.1.9), phosphoglucomutase (PGM; EC 5.4.2.2), leucine amino peptidase (LAP; EC 3.4.11.1), and uridine-5'-diphosphatase (UDP EC 2.7.7.9). Systems were resolved on a discontinuous lithium hydroxide-borate gel system (Ashton and Braden, 1961
) on 9% starch gels. Gels were run at 75 mA and 200 V until the borate front reached the end of the gel (5 h). Internal controls were used to calibrate allele assignment across gels. Staining protocols followed Wendel and Weeden (1989)
. The Mendelian basis of the banding patterns was inferred from comparison of progeny and maternal zymograms. Banding patterns were explained by codominance of electromorphs.
Only progeny that could be resolved for at least two loci were included in analyses. It was not possible to score complete genotypes for some maternal individuals in four populations (LOW-2, MID-1, MID-2, and HIGH-2). Population LOW-2 proved most problematic, yielding no complete maternal genotypes.
Data analysis
Allozyme polymorphisms
Allozyme polymorphisms were described as the number of alleles per population and number of alleles per locus from all individuals in each population.
Population mating system parameters
Multilocus (tm) and single-locus (ts) outcrossing rates and correlation of outcrossed paternity (rp) were estimated for each population using maximum likelihood procedures. These parameters were estimated using the multilocus mating system program MLTR (Multilocus t, Revision) (Ritland, 1990, 1996
), based on the multilocus mixed-mating model of Ritland and Jain (1981)
and on the correlated matings model of Ritland (1989)
. When maternal genotypes were missing, the most likely genotype was inferred from progeny arrays following Brown and Allard (1970)
. Likelihood equations were maximized using the Newton-Raphson method as recommended by Ritland (1996)
. Neighborhood size, i.e., the number of pollen donors contributing to a family, was estimated as the reciprocal of rp (Ritland, 1989
). Standard errors were calculated from 500 bootstrap replicates with resampling among maternal plants within populations. We examined potential effects of missing maternal genotypes on outcrossing estimates by comparing estimates of tm and ts calculated based on inferred maternal genotypes with estimates calculated based on known maternal genotypes in each of the five populations with complete or nearly complete maternal data (i.e., all but LOW-2).
Family outcrossing rates
Multilocus, family outcrossing rates (tmf) for individuals within each population were estimated using Newton-Raphson iterations in MLTR. We estimated tmf in two ways: holding pollen allele frequencies (p) constant to the population values and jointly estimating tmf and p (i.e., allowing p to vary among families) (Ritland and El-Kassaby, 1985
). The former estimate was compared with population level outcrossing rates; the latter estimate was used in assessing contribution of biparental inbreeding to apparent selfing rates as described below. Standard errors of family estimates were based on 100 bootstraps with resampling of individuals within families. One family estimate in population MID-2 failed to converge and was removed from further family-level analyses.
Biparental inbreeding and apparent selfing rates
While outcrossing rates can be estimated directly, only indirect estimates of contributions of biparental inbreeding to apparent selfing rate are possible. We used three comparisons to assess levels of biparental inbreeding: tm with ts (tm – ts from MLTR), inbreeding coefficients of progeny (FP) with inbreeding coefficients expected at equilibrium (Feq), and the two estimates of tmf. In absence of biparental inbreeding, the estimates will be the same in each comparison; with biparental inbreeding the estimates will differ as follows. Single-locus outcrossing rate will be less than tm (Shaw, Kahler, and Allard, 1981
; Ritland, 1990
) because outcrossing events that are not detected at single locus due to alleles that are identical by descent have a higher probability of being detected as more loci are examined. Inbreeding coefficients expected at equilibrium will be less than FP due to higher than expected inbreeding levels (Brown, 1979
). Multilocus, family outcrossing rates estimated jointly with p values will be less than tmf estimated holding p constant and equal to the population frequency because when jointly estimated with p, tmf excludes apparent selfs due to consanguineous matings; these mating events are included in tmf when p is held constant to the population value as a result of covariation of pollen allele frequencies and maternal genotypes (Ritland and El-Kassaby, 1985
). Most studies have compared inbreeding coefficients of mothers (FM) to Feq to quantify biparental inbreeding (
F of Brown, 1979
). Because FM can include effects of selection between seed and adult life stages, we used FP as a more direct reflection of mating system effects.
Inbreeding estimates
Inbreeding coefficients for maternal individuals (FM) were estimated for each population using maximum likelihood procedures in MLTR (Ritland, 1996
). The equilibrium value of the inbreeding coefficient (Feq) was calculated as Feq = (1 – tm)/(1 + tm) (Fyfe and Bailey, 1951
); Feq represents the level of inbreeding expected from selfing alone under the mixed mating model. Progeny inbreeding coefficients (FP) were calculated from one randomly selected offspring per family using the program GDA (Genetic Data Analysis) (Lewis and Zaykin, 2000
). Standard error for each coefficient was calculated from 500 bootstrap replicates.
The three F values were compared within and among populations as described below to analyze patterns of inbreeding. Means differing by more than ±1.96 x SE were considered significantly different. Estimates of both FM and FP were compared with the like estimate among populations to determine whether levels of inbreeding varied along the environmental gradient. We compared FM with FP in each population to assess generational changes in inbreeding. If FP was greater than FM selection against homozygotes between seed and adult populations was indicated, assuming inbreeding levels of adults are at equilibrium (Ritland, 1990
). Additionally, we compared FM with Feq in each population to assess whether levels of inbreeding observed in adults could be explained by mating system alone.
Plant density and inflorescence and achene characteristics
Plant densities in each population were normalized to the number of individuals in a 100-m2 area. Differences among populations in number of inflorescences per plant were examined through analysis of variance using Statistica (StatSoft, 1997
). Variation in proportion of live achenes among inflorescences on plants, among plants in populations, and among populations was examined with nested analysis of variance using SAS (SAS, 1998
). Proportion of successful achenes was transformed using an arcsine square-root transformation. Actual proportions are presented in the RESULTS. We examined relationships of mating-system parameters tm and rp with plant density, mean number of inflorescences per plant, and the untransformed proportion of flowers producing achenes using Pearson product-moment correlation in Statistica (StatSoft, 1997
). Relationships between tmf and number of inflorescences per plant, and the untransformed proportion of successful achenes on all plants were also examined using Pearson product moment correlation. Inbreeding coefficients for maternal individuals and FP were compared with plant density, mean number of inflorescences per plant, and the untransformed proportion of flowers producing achenes using Pearson product-moment correlation to assess the relationship between inbreeding and ecological factors.
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RESULTS |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Estimates of correlation of outcrossed paternity averaged 0.42 and were significantly different from 0 in four populations (Table 1). As with other mating-system parameters, rp did not differ significantly among populations due to large amounts of error in the estimates. Observed values of rp indicate that few fathers contributed to individual progeny arrays in most populations. In five populations, neighborhood size was less than three individuals (Table 1). In contrast, the neighborhood size in population LOW-2 was 24.4.
Family outcrossing rates
In general, tmf estimated holding p constant to the population value was high and averaged 0.88 (SE = 0.03) across all families (N = 58) in all populations (Table 1). However, rates for individual families were highly variable. For example, estimates within populations ranged from 0.48 to 1.87 overall, and in one population alone they ranged from 0.65 to 1.87 (MID-2). Estimates of tmf were not significantly different from one in 60–100% of the families in each population. In four populations, outcrossing rates for more than 89% of the families were not significantly different than 1. The population average of tmf differed from 1 only in population LOW-2 (Table 1). Mean values of tmf in each population were generally higher than population estimates of tm, although the family estimates were each more variable and thus the two estimates did not differ significantly (Table 1). Estimates of tmf made allowing p to vary averaged 0.75 (SE = 0.04) and were smaller than estimates made holding p constant in 93% of the families and in five of six populations (Table 1).
Biparental inbreeding and apparent selfing rates
Two of the three comparisons indicated that biparental inbreeding contributed to the apparent selfing rate in some populations of this taxon. Population tm values were consistently larger than ts values and values of tm – ts were significantly different from zero in four populations (Table 1). Inbreeding coefficients of progeny were significantly greater than Feq in three populations (Fig. 2), indicating more inbreeding than expected based on the observed outcrossing rates. Comparisons of the two estimates of tmf provided no strong evidence for biparental inbreeding (Table 1). Estimates of tmf made while holding p constant to the population value were higher than estimates calculated jointly with estimates of p in 54 of 58 families examined and in five of the six populations. However, average differences between the two estimates within populations were not significantly different due to high levels of variation within populations (Table 1). Differences approached significance in populations LOW-1, MID-2, and HIGH-1.
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Plant densities and inflorescence and achene characteristics
Plant density varied by over 16-fold among populations (Table 1). In general, populations appeared to be larger at higher elevations (Table 1); however, there was no apparent relationship between density and the environmental gradient.
Number of inflorescences per plant differed significantly among populations (F5,58 = 4.10, P < 0.05), but differences were not associated with the elevational gradient (Table 2). Proportion of live achenes varied significantly among plants within populations and among populations, but not among inflorescences within plants (Table 3). There was no relationship between proportion of live achenes and the environmental gradient (Table 2). Additionally, achene set and number of inflorescences produced did not covary (r2 = –0.21, P = 0.10, N = 58).
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There was no significant correlation between plant density and FM (r2 = –0.46, P = 0.35, N = 6) or FP (r2 = –0.53, P = 0.20, N = 6). In contrast, FP significantly decreased as the number of inflorescences per plant increased (r2 = –0.87, P = 0.02, N = 6). There was no such relationship between FM and number of inflorescences per plant (r2 = –0.60, P = 0.21, N = 6).
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DISCUSSION |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Unfortunately, we cannot be certain whether E. ovalifolium var. vineum is self-compatible with some mechanism to promote outcrossing or whether it is self-incompatible and outcrossing events went undetected due to the small number of loci examined. Results from controlled pollinations in other Eriogonum taxa indicate a range from self-compatibility to incompatibility within the genus and thus are not helpful in providing an expected mating system (Moldenke, 1976
). Typically, outcrossing rates vary among populations in self-compatible taxa (e.g., Schoen, 1982
; Holtsford and Ellstrand, 1989
; Liengsiri, Boyle, and Yeh, 1998
). In contrast, outcrossing rates did not differ significantly among populations of E. ovalifolium var. vineum despite large differences in habitat characteristics (Table 1), plant density (Table 1), numbers of inflorescences (Table 2), and proportion of live achenes (Tables 2 and 3). Uniform outcrossing rates over populations support the possibility that E. ovalifolium var. vineum is self-incompatible. However outcrossing rates do not vary among populations in all self-compatible taxa. For example, Kennington and James (1997)
found consistently high outcrossing rates and high rates of seed abortion in the self-compatible rare taxon Eucalyptus argutifolia. Geitonogamy is common in Eucalyptus argutifolia, and there is no prezygotic self-incompatibility mechanism. Instead, high outcrossing rates are maintained by preferential abortion of seeds that result from self-fertilization. A similar mechanism may be working in E. ovalifolium var. vineum; however, confirmation of this possibility would require further investigation that is beyond the scope of the present research.
The possibility that E. ovalifolium var. vineum is self-incompatible is also supported by the low success rate for achene production (20% over all populations), which is typical for outcrossing taxa (Wiens et al., 1987
). It should be noted that self-incompatibility is often a quantitative trait. For example, phenotypic plasticity in self-incompatibility has been documented in Campanula rapunculoides, a taxon with gametophytic self-incompatibility (Vogler, Das, and Stephenson, 1998
). There is some evidence for variation in self-incompatibility in our taxon based on the variation in tmf estimates within populations. However, such variation can also result from neighborhood structuring within populations. Furthermore, tmf estimates were somewhat unreliable due to small sample sizes and must be interpreted cautiously. It is also possible that E. ovalifolium var. vineum exhibits cryptic self-incompatibility as defined by Bateman (1956)
(i.e., outcrossed pollen has a siring advantage over selfed pollen when both are present).
If the taxon is self-incompatible, the level of selfing observed could be the result of undetected outcrossing events due to the small number of loci examined or of biparental inbreeding. The former is unlikely because, given the allelic polymorphism observed in populations, four loci should have been sufficient to detect most outcross events. Biparental inbreeding has resulted in substantial amounts of apparent selfing. For example, Ellstrand, Torres, and Levin (1978)
documented selfing rates as high as 0.66 resulting from biparental inbreeding in the self-incompatible Helianthus annuus. Differences between tm and ts in E. ovalifolium var. vineum indicate levels of biparental inbreeding (a minimum of 3–10%) sufficient to account for the observed selfing rates in all but one population (LOW-2). Additionally, the highest level of biparental inbreeding was found in the population with the lowest outcrossing rate (LOW-2).
Thus, it is not clear whether E. ovalifolium var. vineum is self-incompatible and the observed selfing resulted from biparental inbreeding or if the taxon selfs but preferentially aborts self-fertilized ovules. Regardless of the specific mechanism responsible for the high outcrossing rates, mating patterns have contributed to maintenance of a great deal of genetic diversity in this taxon. For example, the number of alleles per locus was higher and level of inbreeding at the species level was lower than one would otherwise expect in a narrowly endemic plant taxon (Hamrick, Linhart, and Mitton, 1979
; Karron, 1987
; Hamrick and Godt, 1989
). This high diversity illustrates the importance of mating system in influencing levels and allocation of genetic diversity within and among plant populations. Of course, other factors such as founder effects and evolutionary history may also be important in determining levels of species-wide genetic diversity (e.g., O'Brien, Wildt, and Bush, 1983
; McCauley, Raveill, and Antonovics, 1995
).
As is typical for a predominantly outcrossed taxon (Brown, 1979
), progeny tended to be more inbred than expected based on the observed outcrossing rate and more inbred than adults (Fig. 2). Decreases in the magnitude of inbreeding coefficients between progeny and adults provide evidence for selection against selfed/homozygous offspring although error on FM estimates was large (Ritland, 1990
). Sufficient selection would result in low levels of effective inbreeding. Inbreeding in maternal plants was generally not different than expected at equilibrium given the observed levels of selfing (Fig. 2). Thus, selection may act against selfed individuals during pollination and against homozygotes derived from selfing and consanguineous matings both during and after seed maturation.
While E. ovalifolium var. vineum is mostly outcrossed, the observed rp values indicate that outcrossed matings did not occur randomly. In five of the six populations examined, 35–60% of the outcrossed progeny pairs within a family were full sibs, indicating neighborhood sizes of less than three individuals in the paternal mating pool (Table 1). This level of correlated mating is comparable to within-capsule levels observed in Mimulus guttatus (Ritland, 1989
) and is much higher than was found in Centaurea solstitialis individuals (Sun and Ritland, 1998
). This correlation indicates that progeny will be more closely related than predicted based on observed outcrossing rates. The correlation of outcrossed paternity could be the result of a combination of repeated independent matings to a limited pollen pool or of nonindependent mating events as a consequence of pollinator behavior (Ritland, 1989
). Observations indicate that pollinators spend a great deal of time crawling around within and among inflorescences on a single plant before moving to the next plant and repeating the process (S. Morita, personal communication, University of California Davis). Thus, pollen brought in from one plant by one insect is likely to be deposited on many flowers during a single visit to a plant with little carryover to subsequent plants. However, many individual insects repeat this behavior and could be independently bringing pollen from the same sources such as adjacent plants. Distinguishing between these two explanations would require knowledge of pollinator behavior, which plants were potential fathers (i.e., which plants were in bloom when the flowers were pollinated), as well as genotypes of those plants, all of which we do not have. The observed pollinator behavior also provides opportunities for extensive geitonogamous matings that are not reflected in the progeny arrays. Only one population (LOW-2) had a low rp and thus a large paternal pollen pool. Among-population variation in rp is often related to ecological factors such as pollen load competition, fertility variation, pollen carryover, and population substructure (e.g., Barrett, Kohn, and Cruzan, 1992
; Sun and Ritland, 1998
). The cause of this difference is not clear; however, LOW-2 was the smallest and lowest density population (Table 1). Further, while numbers of inflorescence per plant were not extreme they were higher than average (Table 2).
Implications of our results for conservation of E. ovalifolium var. vineum include assessment of potential for loss of genetic diversity, guidelines for conserving populations, and also the importance of maintaining pollinators. This taxon appears to have substantial levels of genetic diversity, and its mating system is functioning such that diversity will be maintained as long as populations are not drastically reduced in density or size. Empirical and experimental evidence indicates that density of conspecifics, particularly flowering individuals, has more of an impact on outcrossing rates than does population size. Outcrossing rates tend to be positively correlated with plant density in self-compatible taxa (e.g., Murawski and Hamrick, 1992
; Van Treuren et al., 1993, 1994
; Karron et al., 1995
; Liengsiri, Boyle, and Yeh, 1998
) and negatively correlated in obligately outcrossing taxa (Ellstrand, Torres, and Levin, 1978
; Young and Brown, 1998
). This negative relationship is thought to be due to substructuring of genotypes within higher density populations that result in more opportunities for consanguineous matings (Ellstrand, Torres, and Levin, 1978
; Ellstrand and Foster, 1983
). Such correlation yields unequal reproductive contributions and results in lower effective population size (Ne) and thus higher rates of drift than would be found in a randomly mating population of the same census size. However, our results indicated few significant mating-system differences over the range of densities and population sizes sampled. It is possible that stronger relationships would have been detected if we had measured densities in the immediate vicinity of maternal plants. Furthermore, although densities varied 16-fold, the highest density of 28 plants/100 m2 was still very low, potentially below the point at which effects of density differences affect mating-system parameters.
Altering population size or density or degrading and fragmenting associated habitats could also affect pollinator communities and decrease pollinator service (e.g., Rathcke and Jules, 1993
). Quantitative reduction in levels of pollinator service could be detrimental because the high observed outcrossing rates indicate that E. ovalifolium var. vineum is dependent on pollen vectors for successful reproduction and production of fit progeny. Changes in pollinator activities could also affect mating-system characteristics. For example, lower outcrossing rates in self-compatible species at lower plant densities are often attributed to pollinator behavior. At relatively low plant densities pollinators spend more time among flowers on an individual plant than travelling among plants (Van Treuren et al., 1993, 1994
; Karron et al., 1995
). When insects do travel among plants, they tend to visit nearest neighbors (Schaal, 1978
), which tend to be related. This is supported by the highest rate of biparental inbreeding in the lowest density population of E. ovalifolium var. vineum. Reduced seed set in low-density populations of Delphinium nuttallianum and Aconitum columbianum documented by Bosch and Waser (1999)
was attributed to a greater frequency of selfed and other inbred pollen rather than to differences in numbers of pollinators visiting plants.
Considering the consistently high outcrossing rates we observed, we would not expect to see large increases in rates of selfing if E. ovalifolium var. vineum populations were reduced in size or density; rather, we would expect elevated biparental inbreeding, as we see in population LOW-2. Such increases in nonrandom mating could cause substantial inbreeding depression, as typically outcrossed taxa tend to have large genetic loads (Charlesworth and Charlesworth, 1987
). Genetic load may already be causing abortion of achenes and the reduction in inbreeding observed between seeds and adults in E. ovalifolium var. vineum (Fig. 2). Interestingly, despite the low proportion of successful achenes, the actual number of fruits produced by a typical plant was high. If we multiply the number of inflorescences per plant by a conservative estimate of 100 flowers and by the proportion of live achenes observed on each plant, average plants would produce 589 fruits (SE = 77) with a range of 51–2868 fruits per plant. As a result, limited fruit production is not currently a concern for this taxon, at least in the populations examined. We have no information on fitness of these progeny or on mortality at later life history stages. In general, however, managing for ecological security of this taxon will most likely sufficiently address maintenance of genetic diversity within populations. Further, if restoration of currently disturbed sites is undertaken, efforts should include large numbers of genetically unrelated individuals to prevent increased inbreeding in this taxon.
Beyond this specific case, studies of mating patterns are important in conservation genetics. Changes in allele frequencies in populations and in levels of inbreeding or increased differentiation among populations due to degradation, loss, or fragmentation may not be detectable for many generations using population survey data. For long-lived taxa such as E. ovalifolium var. vineum, this delay may be on the order of centuries. Even when detrimental effects can be detected, it is not possible to separate historical from current processes using F statistics (Sork et al., 1999
). In contrast, increases in correlated matings and decreases in neighborhood sizes can be detected immediately and can provide an early warning of impending loss of diversity (Aldrich et al., 1998
).
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FOOTNOTES |
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2 Author for reprint requests, current address: The Marine Biological Laboratory, 7 MBL Street, Woods Hole, Massachusetts 02543 USA (phone: 508-548-3705 ext. 6634, mailen{at}mail.ucr.edu
).
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LITERATURE CITED |
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TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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