| HOME | HELP | FEEDBACK | SUBSCRIPTIONS | ARCHIVE | SEARCH | TABLE OF CONTENTS |
|
|
|
|||||||
|
|||||||||
Reproductive Biology |
2Institut für Umweltwissenschaften, Universität Zürich, Winterthurerstrasse 190, 8057 Zurich, Switzerland; 3Fachgebiet Geobotanik, Technische Universität München, Am Hochanger 13, D-85350 Freising-Weihenstephan, Germany
Received for publication August 17, 2001. Accepted for publication March 5, 2002.
 |
ABSTRACT |
|---|
 TOP ABSTRACT INTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Key Words: Brassicaceae • Cochlearia bavarica • endemic plant species • inbreeding depression • Munich, Germany • pollen competition • pollen diversity • pollination distance • population size • sampling effect
|
INTRODUCTION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
). Small populations face higher risks of extinction because of environmental, demographic, and genetic stochasticity (Shaffer, 1987
; Bond, 1996
). Within a small population genetic variation decreases as a result of genetic drift (Ellstrand and Elam, 1993
; Montgomery et al., 2000
) and the average relatedness between individuals will increase (Falconer, 1989
). This increases the probability of inbreeding and its negative effects on reproductive success and offspring fitness (Lacey, 1987
; Ouborg and van Treuren, 1994
; Fischer and Matthies, 1998a
; Groom, 1998
).
In endemic species, a long history of genetic drift, isolation, and frequently occurring bottlenecks may have reduced genetic variation (Karron, 1987
) and allowed high loads of recessive deleterious mutations to accumulate (Lynch, Conery, and Bürger, 1995
). Thus, breeding between relatives enforced by a further decline in population size in such endemic species may be particularly problematic because the high genetic load will lead to inbreeding depression (Kirkpatrick and Jarne, 2000
). Although this situation is the precondition for purging the genetic load (Charlesworth, Morgan, and Charlesworth, 1992
; Husband and Schemske, 1996
), it also presents an extinction risk, thereby raising considerable concern about conservation.
If mating within a population is accompanied by inbreeding and inbreeding depression, crossing with pollen from outside the population may increase heterozygosity and thus fitness of descendants (Hauser and Loeschke, 1994
). However, if co-adapted gene complexes within the parental genomes break down (Templeton, 1986
; Dudash, 1990
), local adaptations are disrupted (Fenster and Dudash, 1994
), and outbreeding depression may result in reduced fitness of descendants (Fischer and Matthies, 1997
). If both inbreeding and outbreeding depression occur together and populations or species have a structure with spatial autocorrelation of genetic similarity, an optimal outcrossing distance should exist, in which the positive effects of unrelatedness of the pollen donor are greater than the negative effects of dissimilarity (Waser and Price, 1989
; Schierup and Christiansen, 1996
).
There is a further possibility to reduce effects of inbreeding depression in small populations, which has recently been suggested in animals (Tregenza and Wedell, 2002
). If individuals in small populations engage in multiple matings, they may sample a greater range of genetically different parents, thereby increasing the potential to select "good" gametes during the fertilization process. In plants, this selection could occur by some sort of female choice or pollen competition on the stigma or in the style (Aizen, Searcy, and Mulcahy, 1990
; Marshall, 1991
). If selection of pollen is possible, crossings by many compared with few or single pollen donors could have a beneficial effect on reproductive success and offspring fitness (Niesenbaum, 1999
), particularly if it occurs in small populations. Self-incompatible species represent a simple example of this effect. If the diversity of pollen that a plant within a small population can receive declines, the probability that pollen and ovules are compatible will decrease (Byers and Meagher, 1992
; Gigord, Lavigne, and Shykoff, 1998
). In other plant species, selfing or single-donor pollination can lead to reduced offspring fitness (Montalvo, 1992
).
Population sizes of the endemic Cochlearia bavarica Vogt have been declining since the late 1980s and small populations of the species show a pattern of reduced genetic variation, viability, and individual fitness when compared with larger populations (Paschke, Abs, and Schmid, 2002
). In this study we used an experimental approach to analyze if lower pollen diversity in small populations may be a cause of the observed pattern in C. bavarica. We artificially crossed maternal plants from small and large populations with different kinds and numbers of pollen donors. To minimize potential confounding effects of pollen load, we used the same number of pollen grains for all pollinations. We asked the following questions: Do offspring of plants from small populations show lower fitness than offspring of plants from large populations? Is decreasing pollen diversity accompanied by reduced reproductive success and fitness depression in offspring? Do pollinations between populations yield fitter offspring than pollinations within populations? Are there interactive effects between population size and pollination treatments such that pollen diversity and pollination between populations are relatively more beneficial to the fitness of offspring in small than in large populations? Is there an optimal outcrossing distance?
|
MATERIALS AND METHODS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
, is an allohexaploid (2n = 36) plant that presumably originated from hybridization between C. pyrenaica DC. (2n = 12) and C. officinalis L. (2n = 24) (Koch, Hurka, and Huthmann, 1996
). Cochlearia bavarica has a narrow distribution and grows in only two regions, west and southeast of Munich, Germany (Abs, 1999
). It occurs in 21 sites in approximately 30 populations. The species is monocarpic and mostly self-incompatible. However, individual plants differ in self-incompatibility. While some plants are strictly self-incompatible, about 40% within a population are able to self-fertilize (M. Fischer, M. Hock, and M. Paschke, unpublished data). Plants flower from May to June and develop about 300 flowers on a ramified primary inflorescence and several secondary inflorescences. Fruit set is, on average, 40%. Each fruit develops a maximum of six seeds. Insect pollinators are generalists, such as flies, bumble bees, other bees, or small moths (M. Paschke, personal observation).
Experiment 1: hand pollination with different pollen diversities within a population and with pollen from a nearby population
To test for inbreeding and outbreeding depression in large and small populations, we selected five small and five large populations for hand-pollination experiments in May 1998. Small populations had less than 100 flowering plants, while large ones had more than 1000. In each population we marked five flowering plants at random and estimated their size by counting the number of inflorescences. On the primary inflorescence of each marked plant, we randomly selected six branches and bagged five of them with nylon fabric (mesh size <0.25 mm). The unbagged branch served as control for open pollination (treatment 1). We hand-pollinated four of the bagged branches with pollen from one (treatment 2), three (treatment 3), and nine donor plants (treatment 4) of the same population or with pollen from nine donor plants of a neighboring population 200–1000 m away from the experimental population (treatment 5). The last bagged inflorescence branch was not pollinated to control for seed set after autonomous selfing (treatment 6). We marked pollen-donor plants at the beginning of the experiment. Within each population, we selected at random one neighboring pollen-donor plant about 0.5 m from each of the receiving plants (treatment 2) or a set of three (treatment 3) and nine pollen-donor plants (treatment 4), respectively. The pollen donors for treatments 2–4 were always different plants. In nearby populations, we also chose nine pollen-donor plants at random (treatment 5). We used these pollen-donor sets for all maternal plants within each population. To guarantee that we used the same quantity of pollen for each treatment, we collected pollen from 60–90 (treatment 2), 30 (treatment 3), or ten flowers (treatments 4 and 5), respectively, from each of the marked pollen-donor plants in each population. We dried the anthers for about 4 h so that they had time to open and release the pollen grains. One at a time, we hand-pollinated all open flowers on each of the marked inflorescence branches with the corresponding pollination treatment, moving a soft brush covered with pollen over the stigma. All plants were hand-pollinated four times at weekly intervals (it was unlikely that flowers could open and wilt between pollination events and thus remain undetected).
Thirty days after the first pollination, we determined the fruit set (ratio of developed to developed + undeveloped fruits) of the flowers that were open during the pollination treatments. We harvested ten randomly chosen developed fruits per plant and pollination treatment and specified seed set as the proportion of the maximum possible number of seeds set (i.e., 60 = 6 seeds per fruit x 10 fruits). We weighed ten randomly chosen seeds per plant and treatment. For germination, we put all developed seeds of each plant and treatment on wet filter paper in petri dishes and exposed them to a day-night regime of 14 h light at 16°C and 10 h dark at 10°C.
Seeds started to germinate after 3 d. After 15 d, there was hardly any new germination. Thus, we measured the germination rate after 15 d, as well as the size (root and leaf length) of three randomly chosen seedlings per petri dish. Immediately following the measurements, we planted a single randomly chosen seedling per mother plant and treatment in a 6 x 6 cm pot containing a mixture of one part sand and two parts soil (M. De Baat BV, Coevorden, The Netherlands). We put the pots in a completely randomized arrangement in a snail- and slug-protected plot in our experimental garden at the University of Zurich.
We measured survival and plant performance 210 and 300 d after the start of the experiment (i.e., after the first pollination). We counted the leaves and measured (to the nearest millimeter) the height of the longest leaf tip. As an overall estimate of plant performance, we used total plant size, defined as the product of the number of leaves and plant height. After 420 d, in spring 1999, we counted the plants that had become reproductive adults. In addition to the vegetative characters mentioned above, we also measured the height of the uppermost inflorescence and counted the number of inflorescences and the number of flowers of the primary inflorescence on these plants. The total number of flowers was defined as the product of the number of flowers and the number of inflorescences.
Experiment 2: hand pollination with pollen from different distances
To test for optimal outbreeding distance, in May 1997 we marked nine flowering individuals at random in one population of about 100 flowering plants and hand-pollinated them with pollen from different distances. On the primary inflorescence of these plants, we randomly selected six branches and bagged five of them with nylon fabric (mesh size <0.25 mm). The unbagged branch was used as control for open pollination (treatment 1). We hand-pollinated four of the bagged side branches with pollen from neighboring plants located 1 m (treatment 2) and 10 m (treatment 3) away, and with pollen from other populations located 100 m (treatment 4) and about 1000 m (treatment 5) away. The fifth bagged inflorescence branch was not pollinated to control for seed set after autonomous selfing (treatment 6). We repeated the hand pollinations every 3 d over 21 d in May 1997. For each pollination treatment, we collected pollen from ten plants selected at random. We hand-pollinated all open flowers, one at a time, on each of the marked inflorescence branches with the corresponding pollination treatment, moving a soft brush laden with pollen over the stigma. In June, at fruit maturity, we determined the fruit set (ratio of developed to developed + undeveloped fruits) for each treatment and plant. For ten randomly chosen developed fruits per plant and treatment, we counted the number of seeds per fruit and measured the seed mass of ten randomly chosen seeds.
Statistical analysis of experiment 1
The measured variables of reproductive success and offspring fitness were transformed when they deviated significantly from a normal distribution. In a sequential analysis of variance (ANOVA), we tested the effects of population size group, population identity, maternal plant, pollination treatments, and interactions of these factors on the measured variables. A skeleton ANOVA with the respective variance ratios is presented in Table 1. Mean maternal plant size was considered as a covariate but not included in the final ANOVA models because it only explained a small and nonsignificant proportion of the variance of the other measured variables.
|
). Pollination treatment 6 was omitted from the analyses because we found no spontaneous self-pollination in this experiment. In addition to ANOVAs for individual characters, we also calculated overall multivariate ANOVAs (MANOVAs) to check for the consistency of effects across the different characters. For these MANOVAs, we grouped the response variables into two sets: early characters (seed characters and offspring characters, including germination and seedling performance) and late characters (offspring performance after 210–420 d). The flowering characters of offspring after 420 d were not included in the MANOVA because only a few plants reached the flowering stage within this time.
We calculated the magnitude of fitness depression, 
in each character w for the two low levels of pollen diversity within populations (treatments 2 and 3), wi, and for the pollinations between populations (treatment 5), wo, in comparison with the high level of pollen diversity within populations (treatment 4, population averages), wc, using the coefficient of Johnston and Schoen (1996)
:
We tested whether the magnitude of fitness depression was stage-specific by using the coefficient defined above as dependent variable. Time, expressed as the number of days that had passed since pollination, and all interactions with time were integrated in the model as a source of variation after population size group, population identity, plant identity, and pollination treatment. We included the linear and quadratic term of time to avoid the problem of serial correlations in repeated-measures analysis (see, e.g., Elashoff, 1986
).
Statistical analysis of experiment 2
To study the influence of the pollination treatment on offspring performance in experiment 2, we again used an ANOVA with contrasts for the pollination treatments. The first contrast distinguished between open pollination and hand pollination. The second and third contrasts were linear and quadratic contrasts for the effect of the logarithm of pollination distance. Cubic deviations, given the four pollen distances, were the residual term. The contrast mean squares were tested against their respective interactions with maternal plant identity for fruit set, seeds per fruit, and seed mass.
|
RESULTS |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Effects of population size, population identity, and maternal plant identity
In large populations fruit set, germination rate of juveniles, survival of offspring after 420 d, and total number of flowers of flowering offspring were higher than in small populations, although some of the effects were only marginally statistically significant (Table 2), possibly because of substantial variation among populations and pollen recipients (Table 3). This latter variation, indicating specific maternal effects due to genetic or environmental variation, was particularly high for the early characters—i.e., fruit set, seed mass, and germination rate—but also significant for total plant size and inflorescence height at some stages later in offspring life (Table 3).
|
|
|
Interactions
Interactions between population size or identity and pollination treatments were rarely significant and therefore omitted from Table 3. In particular, only in one case did a pollination treatment affect plants from small vs. large populations differently: hand pollination had a positive effect on the total number of flowers in large but not in small populations (interaction "population size x hand vs. open pollination" significant at P < 0.05).
When the interactions between maternal plants and the three pollination contrasts C1–C3 were included in the statistical analysis and tested against the interaction "pollen recipient x pollination contrast C4" as error term, they were highly significant for seed mass (P < 0.005) but significant for only a few other characters, despite the large degrees of freedom and, therefore, considerable statistical power. Thus, specific maternal effects (e.g., Schmid and Dolt, 1994
), due to genetic or environmental variation did not alter the effects of pollination treatment on offspring fitness. Therefore, these interactions were pooled into a combined error term for the ANOVAs presented in Tables 1 and 3.
Timing of fitness depression
Population identity, pollination treatment, and time had significant effects on the fitness coefficient (Fig. 2, Table 4). On average, the coefficient was positive, indicating strong fitness depression, for the single-pollen-donor treatment, around zero for the between-population pollination treatment, and even slightly negative for the three-pollen-donor treatment. This indicates again that the nine-pollen-donor treatment resulted in somewhat lower offspring fitness than the three-pollen-donor treatment. Furthermore, the coefficient declined over time, again in agreement with the observation that increased reproductive success after pollination with nine donors from within a population may be at the expense of decreased offspring fitness. Population size group and its interactions had no effect on the fitness coefficient, but population identity effects and their interactions with time and with pollination treatments were substantial.
|
|
|
|
|
|
DISCUSSION |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
; Heschel and Paige, 1995
; Fischer and Matthies, 1998a
, b
; Fischer, van Kleunen, and Schmid, 2000
; Kéry, Matthies, and Spillmann, 2000
; Luijten et al., 2000
). Our pollination experiments with the rare, endemic plant Cochlearia bavarica also showed a tendency for reduced reproductive success and offspring fitness in small as compared with large populations. However, this effect was difficult to detect because of the large residual variation between populations (effect of population identity) and among maternal plants within populations (effect of pollen recipient). The negative effect of small population size might have been due to reduced availability of genetically different pollen donors, especially because C. bavarica is a self-incompatible species. As we will discuss below, increasing the chances of pollen recipients to obtain genetically different pollen did have a positive effect especially on reproductive success, albeit both in small and large populations.
The large variation among maternal plants with regard to seed and offspring characters declined with offspring age as may be expected for maternal carryover effects (Schmid and Dolt, 1994
). However, since we found no significant relationship between maternal plant size, used as a covariate, and seed and offspring characters, the maternal effects probably also reflected genetic differences between individual pollen recipients. Maternal plant size is usually seen as a good indicator for maternal resource availability and thus maternal carryover effects (Gorchov, 1988
).
Differences between hand pollination and open pollination
Although open pollination and hand pollination were equally successful for most of the scored seed and offspring characters of C. bavarica, fruit set was significantly higher after open pollination than after hand pollination (see Fig. 1A). This may have been due to a negative effect of bagging the inflorescences for the hand-pollination treatments.
Effects of pollen diversity
We found that increasing the number of pollen donors from one to three to nine had a positive effect on reproductive success (fruit set and seed set), whereas offspring characters peaked at the intermediate level of pollen diversity (root length and leaf length of seedlings, offspring survival after 420 d) (see Fig. 1). Because the total amount of pollen applied was the same for each level of pollination diversity (see MATERIALS AND METHODS section), these effects could not be explained as effects of pollen-load size. Rather, it seems likely that both effects (increase in female reproductive output with the number of pollen donors and optimum of offspring fitness for an intermediate level of multiple matings) resulted from variation in genetic diversity among pollen donors. Several, mutually nonexclusive mechanisms are possible. The increase in fruit and seed set could reflect an increased investment by the recipient plant for multiply-sired fruits, as has been found in wild radish (Marshall and Ellstrand, 1986
). Preferential investment for multiply-sired fruits may be adaptive for the recipient plant because, analogous to the sampling effect of diversity (Loreau, 2000
), an increasing number of pollen donors increases the chances for compatible pollen grains or among compatible ones for pollen grains with high fertilizing abilities (Bernasconi and Keller, 2001
) or less closely related to the recipient plant (Tregenza and Wedell, 2002
). Increased offspring fitness among multiply-sired progeny for intermediate levels of multiple pollination may arise through better resource partitioning among half than full sibs (Karron and Marshall, 1990
), a mechanism analogous to niche complementarity (Loreau, 2000
). Such an effect may follow an optimality curve if competition becomes predominant over complementarity for high levels of pollen diversity. Alternatively, the smaller seedling size and survival of offspring from the highest than the intermediate diversity treatment may indicate a trade-off between fertilizing ability and "father quality" or that optimal levels of polyandry differ for the male and female function in plants, as they do for instance in insects (Arnqvist and Nilsson, 2000
). However, such trade-offs to our knowledge have not been described so far in plants. Future studies will have to assess to which degree multiple pollination also results in multiple paternity among the seeds.
The low average fruit set resulting from the one-donor treatment was expected because the probability that a single pollen donor is not compatible with the recipient plant is relatively high in the endemic C. bavarica with sporophytic self-incompatibility (M. Fischer, M. Hock, and M. Paschke, unpublished data). Further, if a single pollen donor was compatible (there are degrees of compatibility in C. bavarica; for a further example see Gigord, Lavigne, and Shykoff, 1998
), it may still have been closely related to the recipient plant and thus inbreeding depression may have resulted. Indeed, we found that the stages of seed development until seed dispersal (30–60 d) expressed large fitness depressions after hand pollination with only one pollen donor (see Fig. 2). After 60–300 d, fitness depression was not apparent, but it did show up again at the last investigated stage (420 d after pollination).
Surprisingly, interactions between pollination treatments and population size group, population identity, or maternal plant identity (= effect of pollen recipient) were small and statistically almost never significant. Thus, the mentioned positive effects of increasing pollen diversity on reproductive success and of the intermediate pollen diversity on offspring characters were consistent across populations and maternal plants. Hence, we conclude that C. bavarica in both small and large populations may benefit from pollinator services that lead to multiple mating.
Effects of pollination distance and of pollen from outside the population
We found evidence for an optimal outcrossing distance between 10 and 100 m. Pollen collected within this distance, and representing a mix from ten donor plants each time, showed higher siring success after hand pollination than did pollen from 1 m away or from more than 100 m away. This optimal outcrossing distance could be explained by the appearance of inbreeding and outbreeding depression within the same species. Plants in the neighborhood of a maternal plant are probably more closely related than plants farther away, and thus the likelihood of inbreeding increases in low-distance pollinations (see, e.g., Fenster, 1991
). On the other hand, plants from much farther away may be too different, such that co-adapted gene complexes could break down or local adaptations disrupt. Optimal outcrossing distances have for instance also been observed in Ipomopsis aggregata (Pursh) V. Grant (1–10 m; Waser and Price, 1989
) and in a few other plant species (Waser, 1993
; Fischer and Matthies, 1997
).
Besides the negative effects of the largest pollination distances, we found significantly positive effects of pollen from nearby plants in a different population rather than the same population for small and large populations alike on seed mass and on offspring size after 420 d (see Fig. 1C, F). The positive effects of pollen from outside a population (and for pollen from 100 m away, which also came from a neighboring population in the pollination-distance experiment) showed that all populations might suffer some inbreeding depression. Sheridan and Karove (2000)
reported similar positive effects of intersite crosses in another rare plant.
Implications for conservation
Our pollination experiments suggest that pollination by multiple pollen donors or by pollen donors at some distance from a maternal plant has a beneficial effect on reproductive success and offspring fitness in the narrow endemic species C. bavarica. Pollination by single donors may result in inbreeding depression. Therefore, it is essential that pollinator services can be maintained within and among neighboring populations of C. bavarica. Because pollinator availability may be threatened particularly in small populations (Paschke, Abs, and Schmid, 2002
), and because small populations independent of pollination treatment had reduced reproductive success and offspring fitness in the present study, conservation efforts should focus on these small populations. If possible, one should try to increase the size of these populations or connect them to neighboring populations.
|
FOOTNOTES |
|---|
4 Author for reprint requests (paschke{at}uwinst.unizh.ch
)
|
LITERATURE CITED |
|---|
|
TOPABSTRACTINTRODUCTIONMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
|---|
Aizen M. A. K. B. Searcy D. L. Mulcahy 1990 Among- and within-flower comparisons of pollen-tube growth following self- and cross-pollinations in Dianthus chinensis (Caryophyllaceae). American Journal of Botany 77: 671-676[CrossRef][ISI]
Arnqvist G. T. Nilsson 2000 The evolution of polyandry: multiple mating and female fitness in insects. Animal Behaviour 60: 145-164[CrossRef][ISI][Medline]
Bernasconi G. L. Keller 2001 Multiple mating by females affects their sons' reproductive success in the red flour beetle Tribolium castaneum. Journal of Evolutionary Biology 14: 186-193
Bond W. J. 1996 Assessing the risk of plant extinction due to pollinator and disperser failure. In J. H. Lawton and R. M. May [eds.], Extinction rates, 129–146. Oxford University Press, Oxford, UK
Byers D. L. T. R. Meagher 1992 Mate availability in small populations of plant species with homomorphic sporophytic self-incompatibility. Heredity 68: 353-359[ISI]
Charlesworth D. M. T. Morgan B. Charlesworth 1992 The effect of linkage and population size on inbreeding depression due to mutational load. Genetical Research 59: 49-61[ISI][Medline]
Czech B. P. R. Krausman P. K. Devers 2000 Economic associations among causes of species endangerment in the United States. BioScience 50: 593-601[CrossRef][ISI]
Dudash M. R. 1990 Relative fitness of selfed and outcrossed progeny in a self-compatible, proteandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44: 1129-1139[CrossRef][ISI]
Elashoff J. D. 1986 Analysis of repeated measures designs. BMDP technical report 83. BMDP Statistical Software, Los Angeles, California, USA
Ellstrand N. C. D. R. Elam 1993 Population genetic consequences of small population size: implication for plant conservation. Annual Review of Ecology and Systematics 24: 217-241[CrossRef][ISI]
Falconer D. S. 1989 Introduction to quantitative genetics, 2nd ed. Longman, London, UK
Fenster C. B. 1991 Gene flow in Chamaecrista fasciculata (Leguminosae). II. Gene establishment. Evolution 45: 410-422[CrossRef][ISI]
Fenster C. B. M. R. Dudash 1994 Genetic considerations for plant population restoration and conservation. In M. L. Bowles and C. J. Whelan [eds.], Restoration of endangered species, 34–62. Cambridge University Press, Cambridge, UK
Fischer M. D. Matthies 1997 Mating structure and inbreeding and outbreeding depression in the rare plant Gentianella germanica (Gentianaceae). American Journal of Botany 84: 1685-1692[Abstract]
Fischer M. D. Matthies 1998a RAPD variation in relation to population size and plant fitness in the rare Gentianella germanica. American Journal of Botany 85: 811-819[Abstract]
Fischer M. D. Matthies 1998b Effects of population size on performance in the rare plant Gentianella germanica. Journal of Ecology 86: 195-204[CrossRef][ISI]
Fischer M. M. Van Kleunen B. Schmid 2000 Genetic allee effects on performance, plasticity, and developmental stability in a clonal plant. Ecology Letters 3: 530-539[CrossRef][ISI]
Gigord L. C. Lavigne J. A. Shykoff 1998 Partial self-incompatibility and inbreeding depression in a native tree species of La Réunion (Indian Ocean). Oecologia 117: 342-352[CrossRef][ISI]
Gorchov D. L. 1988 Effects of pollen and resources on seed set and other fitness components in Amelanchier aborea (Rosaceae: Maloideae). American Journal of Botany 75: 1275-1285[CrossRef][ISI]
Groom M. J. 1998 Allee effects limit population viability of an annual plant. American Naturalist 151: 487-495[CrossRef][ISI]
Hauser T. P. V. Loeschke 1994 Inbreeding depression and mating-distance dependent offspring fitness in large and small populations of Lychnis flos-cuculi (Caryophyllaceae). Journal of Evolutionary Biology 7: 609-622[CrossRef][ISI]
Heschel M. S. K. N. Paige 1995 Inbreeding depression, environmental stress, and population size variation in scarlet gilia (Ipomopsis aggregata). Conservation Biology 9: 126-133
Husband B. C. D. W. Schemske 1996 Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 54-70
Johnston M. O. D. J. Schoen 1996 Correlated evolution of self-fertilization and inbreeding depression: an experimental study of nine populations of Amsinckia (Boraginaceae). Evolution 50: 1478-1491[CrossRef][ISI]
Karron J. D. 1987 A comparison of levels of genetic polymorphism and self-compatibility in geographically restricted and widespread plant congeners. Evolutionary Ecology 1: 47-58
Karron J. D. D. L. Marshall 1990 Fitness consequences of multiple paternity in wild radish, Raphanus sativus. Evolution 44: 260-268[CrossRef][ISI]
Kery M. D. Matthies H.-H. Spillmann 2000 Reduced fecundity and offspring performance in small populations of the declining grassland plants Primula veris and Gentiana lutea. Journal of Ecology 88: 17-30[CrossRef]
Kirkpatrick M. P. Jarne 2000 The effect of a bottleneck on inbreeding depression and the genetic load. American Naturalist 155: 154-167[CrossRef][Medline]
Koch M. H. Hurka M. Huthmann 1996 Chloroplast DNA restriction site variation and RAPD-analyses in Cochlearia (Brassicaceae): biosystematics and speciation. Nordic Journal of Botany 16: 585-603[ISI]
Lacy R. C. 1987 Loss of genetic diversity from managed populations: interacting effects of drift, mutation, immigration, selection and population subdivision. Conservation Biology 1: 143-158
Loreau M. 2000 Biodiversity and ecosystem functioning: theoretical advances. Oikos 91: 3-17
Luijten S. H. A. Dierick J. G. B. Oostermeijer L. E. L. Raijman H. C. M. den Nijs 2000 Population size, genetic variation and reproductive success in a rapidly declining, self-incompatible perennial (Arnica montana) in the Netherlands. Conservation Biology 14: 1776-1787[CrossRef][ISI]
Lynch M. J. Conery R. Bürger 1995 Mutation accumulation and the extinction of small populations. American Naturalist 146: 489-518[CrossRef][ISI]
Marshall D. L. 1991 Nonrandom mating in wild radish: variation in pollen donor success and effects of multiple paternity among one- to six-donor pollinations. American Journal of Botany 78: 1404-1418[CrossRef][ISI]
Marshall D. L. N. C. Ellstrand 1986 Sexual selection in Raphanus sativus: experimental data on nonrandom fertilization, maternal choice, and consequences of multiple paternity. American Naturalist 127: 446-461[CrossRef][ISI]
Menges E. S. 1991 Seed germination percentage increases with population size in a fragmented prairie species. Conservation Biology 5: 158-164[CrossRef][ISI]
Montalvo A. M. 1992 Relative success of self and outcross pollen comparing mixed- and single-donor pollinations in Aquilegia caerula. Evolution 46: 1181-1198[CrossRef][ISI]
Montgomery M. E. L. M. Woodworth R. K. Nurthen D. M. Gilligan D. A. Briscoe R. Frankham 2000 Relationship between population size and loss of genetic diversity: comparisons of experimental results with theoretical predictions. Conservation Genetics 1: 33-43[CrossRef]
Neter J. M. H. Kutner C. J. Nachtsheim W. Wasserman 1996 Applied linear statistical models, 4th ed. Irwin, Chicago, Illinois, USA
Niesenbaum R. A. 1999 The effects of pollen load size and donor diversity on pollen performance, selective abortion, and progeny vigor in Mirabilis jalapa (Nyctaginaceae). American Journal of Botany 86: 261-268
Ouborg N. J. R. van Treuren 1994 The significance of genetic erosion in the process of extinction. IV. Inbreeding load and heterosis in relation to population size in the mint Salvia pratensis. Ecology 48: 996-1008
Paschke M. C. Abs B. Schmid 2002 Relations between population size, allozyme variation, and plant performance in the narrow endemic Cochlearia bavarica (Brassicaceae). Conservation Genetics, in press
SAS. 2000 JMP® statistics and graphics guide, version 4. SAS Institute, Cary, North Carolina, USA
Schierup M. H. F. B. Christiansen 1996 Inbreeding depression and outbreeding depression in plants. Heredity 77: 461-468
Schmid B. C. Dolt 1994 Effects of maternal and paternal environment and genotype on offspring phenotype in Solidago altissima L. Evolution 48: 1525-1549[CrossRef][ISI]
Shaffer M. 1987 Minimum viable populations: coping with uncertainty. In M. E. Soulé [ed.], Viable populations for conservation, 69–86. Cambridge University Press, Cambridge, UK
Sheridan P. M. D. N. Karove 2000 Inbreeding, outbreeding, and heterosis in the yellow pitcher plant, Sarracenia flava (Sarraceniaceae), in Virginia. American Journal of Botany 87: 1628-1633
Templeton A. R. 1986 Coadaptation and outbreeding depression. In M. E. Soulé [ed.], Conservation biology: the science of scarcity and diversity, 105–160. Sinauer, Sunderland, Massachusetts, USA
Tregenza T. N. Wedell 2002 Polyandrous females avoid costs of inbreeding. Nature 415: 71-73[CrossRef][Medline]
Vogt R. 1985 Die Cochlearia pyrenaica Gruppe in Zentraleuropa. Berichte der Bayerischen Botanischen Gesellschaft 59: 133-135
Waser N. M. 1993 Population structure, optimal outbreeding, and assortative mating in angiosperms. In N. Thornhill [ed.], The natural history of inbreeding and outbreeding: theoretical and empirical perspectives, 173–199. University of Chicago Press, Chicago, Illinois, USA
Waser N. M. M.V. Price 1989 Optimal outcrossing in Ipomopsis aggregata: seed set and offspring fitness. Evolution 43: 1097-1109[CrossRef][ISI]
This article has been cited by other articles:
|
|
 |
|
  A. Lankinen, W. S. Armbruster, and L. Antonsen Delayed stigma receptivity in Collinsia heterophylla (Plantaginaceae): genetic variation and adaptive significance in relation to pollen competition, delayed self-pollination, and mating-system evolution Am. J. Botany, July 1, 2007; 94(7): 1183 - 1192. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
D. L. Marshall, J. Reynolds, N. J. Abrahamson, H. L. Simpson, M. G. Barnes, J. S. Medeiros, S. Walsh, D. M. Oliveras, and J. J. Avritt Do differences in plant and flower age change mating patterns and alter offspring fitness in Raphanus sativus (Brassicaceae)? Am. J. Botany, March 1, 2007; 94(3): 409 - 418. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
J. D. Karron, R. J. Mitchell, and J. M. Bell Multiple pollinator visits to Mimulus ringens (Phrymaceae) flowers increase mate number and seed set within fruits Am. J. Botany, September 1, 2006; 93(9): 1306 - 1312. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
R. J. Mitchell, J. D. Karron, K. G. Holmquist, and J. M. Bell Patterns of multiple paternity in fruits of Mimulus ringens (Phrymaceae) Am. J. Botany, May 1, 2005; 92(5): 885 - 890. [Abstract] [Full Text] [PDF]
|
|
|
|
|
|
W. S. Armbruster and D. Gobeille Rogers Does pollen competition reduce the cost of inbreeding? Am. J. Botany, November 1, 2004; 91(11): 1939 - 1943. [Abstract] [Full Text] [PDF]
|
|
| ||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||||
