Inbreeding depression and mating-distance dependent offspring fitness in large and small populations...

J. evol. Biol. 7: 609-622 (1994) 1010-061X/94/050609-14 $ 1.50+0.20/O

0 1994 Birkhauser Verlag, Base1

Inbreeding depression and mating-distance dependent offspring fitness in large and small populations of Lychnis flos -cuculi ( Caryophyllaceae)

Thure P. Hauser and Volker Loeschcke

Department of Ecology and Genetics, Ny Munkegade Bygn. 540, University of Arhus, DK-8000 C irhus, Denmark

Key words: Inbreeding depression; mating distance; population size.

Abstract

The spatial structure of four LychnisJlos-cuculi populations, varying in size and degree of isolation, was studied by comparing the fitness of offspring resulting from self-pollination and pollinations by neighbouring plants, plants within the same population, and plants from other populations. Selfed offspring had the lowest fitness of the four offspring groups. No significant difference was found between the performance of offspring from pollinations by neighbouring plants and offspring pollinated by plants further apart but within the same population. A lower fitness of offspring from pollinations between neighbours would be expected if these matings, on average, yielded inbred offspring which suffered from inbreeding depression. These results imply that either a tight neighbourhood structuring is not present, or that the inbreeding depression for offspring by neighbours is too low to detect, although these are inbred. Crossings between populations produced offspring with a significantly higher fitness than offspring sired within populations. There were no significant differences in response to inbreeding among the populations, and differences in mean fitness among populations had no clear relation to the population size or degree of isolation. A reduced fitness of small populations due to inbreeding depression or a less severe response to experimental inbreeding due to purging of deleterious alleles is therefore not supported by our results.

Introduction

Many species of flowering plants are characterised by limited pollen and seed dispersal. This, combined with the sessile habit of plants, may result in a spatial structuring of populations (Wright, 1946). Under such conditions, the relatedness

609

610 Hauser and Loeschcke

between plants decreases, on average, with increasing distance, and the fitness of offspring may therefore increase with the mating distance, if inbreeding depression affects the inbred offspring (Levin, 1981, 1984).

On the other hand gene flow may be more widespread than expected from average between-plant flight distances of pollinators and seed dispersal distances. Pollinators may deposit pollen over several flower visits, and pollen may also be transferred secondarily among flowers. This, together with rare long distance movements of pollinators, may cause a larger neighbourhood size than suggested by the mean flight distances between single plants (Wright, 1946; Campbell, 1991).

The sub-structuring of natural plant populations, and the fitness effects associated with this, may influence evolutionary processes in the populations. The evolution of plant selfing rates has been explained as a balance between the reduced fitness of selfed offspring due to inbreeding depression, and the selective advantage of transmitting more gene copies by selfing, assuming no pollen discounting (Fisher, 1941; Holsinger et al., 1984; Lande and Schemske, 1985; Charlesworth and Charlesworth, 1987). If the relative offspring fitness increases with mating distance because of isolation by distance, then the inbreeding depression measured as the relative fitness of selfing to outcrossing would also depend on the mating distance. In such cases variations in the pollinator fauna and behaviour could be responsible for fluctuations in the strength and direction of the evolution of selfing rate (Uyenoyama, 1986).

Highly complicated dynamics are expected to exist between the inbreeding level and the magnitude of inbreeding depression (Lande and Schemske, 1985; Charlesworth and Charlesworth, 1987; Charlesworth et al., 1990, 1991, 1992). Recessive deleterious alleles are more frequently expressed under inbreeding, thereby allowing selection to reduce their frequency. Over time, this may reduce the inbreeding depression in more inbred populations, such as population with tight neighbourhood structuring. Likewise, population size may affect fitness and inbreeding depression, as the extent of inbreeding is greater in small populations (Falconer, 1989). Mean fitness may thus be lower in the smaller populations due to inbreeding depression and fixation of deleterious alleles. Over time purging of the genetic load may restore or maintain the mean individual fitness to the level found in large populations, and may also lead to a reduction in inbreeding depression (Barrett and Charlesworth, 1991).

Inbreeding effects associated with small population size are of major interest for the conservation of species with fragmented and reduced populations. Inbreeding depression occurring in small populations has been invoked as a possible threat to the survival of such populations, but it is at present not clear whether fitness depression will occur as a result of increased inbreeding (Hauser et al., 1994).

In the present study we examine whether offspring fitness in populations of LychnisJIos-cuculi depend on mating distance, thereby indicating a neighbourhood structuring. We compare offspring fitness between pollination of self, neighbouring plants, plants within the same population, and plants from different populations. In addition, we determine whether populations of L. jlos-cuculi have different levels of

Mating distance, population size and inbreeding depression 611

inbreeding depression according to their size and degree of isolation by comparing the mean fitness and response to inbreeding among four different populations.

Materials and methods

Lychnis jIos-cuculi (L.) is a diploid perennial rosette plant growing in moist, grazed meadows. The flowers are hermaphroditic and the inflorescence is a bracteate dichasium, in which a flower can be assigned a position in the branching hierarchy ranging from 1 for the first terminal flower to 5 for flowers of the fourth order of branching. The capsules split open at the top upon ripening, and the seeds are dispersed by vibrations of the stiffened stalk. L.Jos-cuculi is mainly outcrossed (Biere, 199la), and is pollinated by many insect species (Hsvsgaard and Vejsnres, 1990).

Four populations of L. JEos-cuculi from central Jutland, Denmark, were chosen for this experiment to provide a range of population sizes and degrees of isolation. PIL: A small stretch of meadow along a creek that runs into woodland; small and isolated, with ca. 300 ramets. DOL: Approx. 3000 ramets in a large meadow area surrounded by land of higher elevation; judging from the surrounding vegetation, this population may have been about three times larger until recently. HOR: A small river-bend meadow isolated by forest and higher elevation; estimated population size: 5000-10 000 ramets. BRO: A very large, open population (size not estimated) in a large valley system; the size was even larger in the past. The histories of the populations are unknown, but as the species is restricted to low lying meadows, the topography and the fact that forests surrounding the first three populations have been permanent at least since late 1700s suggest that these populations have been rather isolated for a long time.

Forty five plants from each population were transplanted to the greenhouse just before flowering in May 1990. In each population, the plants were sampled from 9 patches evenly spaced on the circumference of a circle with a diameter of 15 m. From each patch one central plant was chosen as the pollen recipient, and 4 other plants, ca. 1 m away, were assigned as pollen donors. Four different pollen treatments could thereby be performed: sefJing (within the pollen recipients), neighbour (pollen from donors to recipients within the same patch), within populu- tion (pollen from 2 of the other patches lo- 15 m away in the population), and between population (pollen from random plants from two of the other populations). Each pollen recipient was treated with the four different pollen treatments in random sequence during flowering. For each pollen treatment except selfing at least two pollen donors from different neighbouring plants/patches/populations were used. These were randomly chosen among the donors available, and the final number of donors depended on the number of flowers on the recipients. The flowers on pollen recipients were emasculated before flowering.

Plants were grown in 5 litre pots filled with sphagnum, with pollen recipients and donors randomly placed on separate tables covered by mesh-tents. After pollination, the fruits were harvested just prior to capsule opening, and seeds were sorted


into the following categories and counted: undeveloped: small, yellow-brown, and partly translucent; aborted: seeds that had started developing, but shrunk before reaching full size; fully developed. Proportions of undeveloped and aborted seeds were calculated. Developed seeds were weighed in bulk for each capsule, and weight per seed calculated. The developed seeds were then used for either a germination trial or further growth.

To estimate the germination proportion (number of germinated/the total number of developed seeds) and the standardized germination proportion (number of seeds germinated by a given day/total number that germinated for that treatment), all developed seeds from 2 capsules per pollen treatment per pollen recipient (sired by different pollen donors) were germinated on filter paper covered by distilled water in petri-dishes, kept in a climate chamber at 18” C and 16 h light. Germination was scored as positive if the radicle had begun to stretch. Observations were made on day 6, 11, 18, and 34.

Seeds from each of 2 capsules per pollen treatment per pollen recipient (sired by different donors) were sown in pots filled with sphagnum in the greenhouse. After a month (August 1990) a maximum of 4 plants per pot were transplanted group- wise to an outdoor garden in a randomised design, with a total of 881 plants and 72 groups per pollen treatment. After natural flowering in July the following year, the numbers of surviving and flowering plants were scored, and developed capsules and withered flowers were counted. The mean cross area of developed capsules was estimated for each plant by placing them on a lightbox and measuring their area in pixels using video recordings and computer image processing (Pippin by K. Johansen, version 1991). The cross area of a capsule is expected to be highly correlated with the number of seed contained, and is thus used as a fitness component for relative comparisons. As the capsule is almost globular, detected differences in area among groups will be a conservative estimate of the correlated differences in seed number.

Overall offspring fitness was estimated for each pollen treatment within maternal plants as the product of [l-abortion rate], germination proportion, total seedling survival, proportion of plants flowering, number of capsules per plant, and area of capsules. Two estimates were calculated, with and without the area of capsules included. The proportion of undeveloped seeds was not included in the fitness estimate because these may represent unfertilised ovules, and therefore have no bearing on the fitness of zygotes.

The data were analysed in a two-way ANOVA with population and pollen treatment as main effects. These were tested against the within cell variance, as they were both considered fixed effects (the populations were chosen according to size and degree of isolation). A more detailed ANOVA design with the effect of “recipient within population” included was also analysed, but as this caused calculation problems due to the small number of flowers for some plants in population BRO, it was given up. The available results from this analysis were very similar to the ones from the present analysis.

Flower position and seed weight were used as covariates in order to control for differences in resource availability among flowers and seeds, as indicated in Table 2, which also specifies the data transformations used. Homogeneity of variances was


evaluated by plotting normalised residuals against estimated values, and normally was assessed graphically in a probit plot. Tukey’s and Scheffe’s tests were used for pairwise comparisons among factor levels.

For the between-population treatment, differences among paternal populations in the fitness of their offspring were tested in an ANOVA with the paternal population nested within the maternal. Differences in the fitness of offspring sired by individual pollen donors were analysed for each maternal population in an ANOVA with pollen donors nested within paternal population. The statistical analyses were performed using Systat for Macintosh (version 6.1 and 6.2).

Results

The pollen treatment did not significantly affect the number of developed seeds per capsule (Tabs. 1, 2) whereas a higher abortion rate was found for the selfed seeds than for other treatments. The proportion of undeveloped seeds did not show any effect of pollen treatment (results not shown). The average seed weight varied significantly among pollen treatments but not consistently with distance. The germination proportion was significantly lowest for the selfed seeds, and the germination speed (indicated by the standardized germination proportion by day 11) was significantly higher for the between-population treatment than for other treatments (Tabs. 1, 2; Fig. 1).

Fig. 1. Standardized germination proportion, i.e. the number of seeds germinated by a given day relative to the total number that germinated by the end of the experiment (day 34) for each pollen treatment.

Tabl

e 1.

M

eans

of

th

e sc

ored

ch

arac

ters

fo

r po

llen

treat

men

ts

and

popu

latio

ns.

Sam

ple

sizes

an

d st

anda

rd

erro

rs

are

given

in

pa

rent

hese

s,

Sign

ifica

nt

pairw

ise

diffe

renc

es

betw

een

polle

n tre

atm

ents

or

po

pula

tions

ar

e in

dica

ted

by

diffe

rent

le

tters

. Su

pers

crip

ts

on

the

mul

tiplic

ative

fit

ness

es

indi

cate

1)

caps

ule

area

no

t in

clude

d an

d 2)

ar

ea

inclu

ded.

Self

Polle

n tre

atm

ent

Neigh

bour

W

ithin

POP

Betw

een

POP

PIL

Popu

latio

n

DOL

HOR

BRO

Num

ber

of

deve

loped

seed

s pe

r

caps

ule

Seed

abor

tion

rate

Seed

we

ight

low5

g

Stan

dard

ized

germ

inat

ion

day

II

Ger

mina

tion

prop

ortio

n

111

(85,

4)

115

(117

,3)

108

(142

, 3)

108

(140

, 3)

121’

(147

33)

102”

(97,

4)

100”

(586

)

0.02

1b

( 11

8,0.

003)

0.04

0”

(85,

0.00

5)

0.01

9b

(144

,0.0

02)

0.01

5b

(144

,0.0

02)

0.01

0’

(151

,O.O

Ol)

0.02

6b

(98,

0.

004)

0.03

0”

( 18

I)

0.00

2)

0.02

0b

(61,

0.00

3)

19.5

”

(82,

0.3)

0.75

”

(51,

0.04

)

19.9

”h

20.4

b

( 116

,0.3

) (1

40,0

.3)

0.84

”

(61,

0.03

)

0.86

”

(60,

0.03

)

19.9

ab

(141

,0.2

)

0.91

b

(63,

0.02

)

20.3

b

(148

0.3)

0.78

a

(67,

0.04

)

18.0

"

(96,

0.

3)

0.84

b

(61,

0.

03)

20.3

b

(180

, 0.

2)

0.88

b

(64,

0.

03)

21.7

b 3:

(5

5,0.

4)

i

0.88

b ;

(43,

0.03

) %

F b

0.81

8 a

(42,

0.04

) 6

0.88

b

(61,

0.02

)

0.75

”

(51,

0.04

)

0.91

b

(59,

0.02

)

0.93

b

(61,

O.O

l)

0.89

(65,

0.03

)

0.88

(61,

0.

02)

0.89

(64,

0.02

)


Table 2. ANNOVA analysis of pollen treatments and recipient populations. Degrees of freedom (dF), mean squares (MS). F-values, and significances (*: p < 0.05; **: p < 0.01; ***: p < 0.001). Transforma-

tions are as follows: a) O.S(arcsinJm + arcsinJ(X + l)/(n + I)), where X/n is the actual proportion (Zar, 1984); b) log transformed; c) arcsine transformed; d) quadratically transformed. Covariates are: I) flower position; II) seed weight, Superscripts on the multiplicative fitness indicate I) capsule area not included and 2) area included.

dF MS F

Number of developed seeds

Seed abortion ratea)

Seed weight”)

Relative

germination day 11’)

Germination

proportion’)

Seedling survival*)

Proportion plants flowering

Proportion flowers developing capsules

Population 3 26412

pollen treatm. 3 1078

pop x pollen 9 991

covariate’ I 211204

error 467 768

Population 3 0.132

pollen treatm. 3 0.067

pop x pollen 9 0.004

covariate’ I 0.068

error 414 0.005

Population 3 0.595

pollen treatm. 3 0.063 pop x pollen 9 0.011 covariate’ I 1.161

error 462 0.019

Population 3 0.547

pollen treatm. 3 0.869 pop x pollen 9 0.047 covariate” I 1.929

error 218 0.144

Population

pollen treatm. pop x pollen covariate”

error

Population pollen treatm.

pop x pollen covariate” error


pop x pollen covariate” error


pop x pollen covariate”

error

3 0.166

3 0.694

9 0.033

1 0.885

215 0.073

3 0.974

3 0.387

9 0.042

1 0.666

213 0.082

3 0.003 3 0.006

9 0.007

1 0.020 209 0.005

3 0.222

3 0.015

9 0.023

I 0.048

211 0.014

34.38***

1.4

1.3

282.1+**

25.26***

12.87***

0.77

13.04***

30.56***

3.25*

0.57

59.68***

3.19*

6.03**

0.33

13.38***

2.27

9.51***

0.46

12.13***

11.82*** 4.70**

0.51

8.09**

0.65

1.21

1.39

3.97*

15.9***

1.1 1.6

3.4

Mating distance, population size and inbreeding depression

Table 2. (continued)

617

dF MS fi

Number of

capsules per planthI

Area of

capsules

Population

pollen treatm. pop x pollen covariate”

error

3

3 9

206

0.44

2.16 0.15 0.16

0.18

Population 3 1003

pollen treatm. 3 159 pop x pollen 9 80

covariate” I 116 error 208 89

2.40 11.92***

0.84 0.90

11.23***

8.49*** 0.90 1.29

Fitness”

Fitness”

Population pollen treatm. pop x pollen

error


pop x pollen error

3 3

9 112

3 3 9

III

99 1.86 1049 19.70***

28 0.53

53

1842315 2.20 17394200 20.78***

427579 0.51

837069

Selfed seedlings had a significantly lower survival than seedlings from other pollen treatments. Neither the proportion of the surviving plants that flowered, nor the proportion of flowers that developed into a capsule was affected by pollen treatment. Significantly fewer and smaller capsules were developed by the selfed plants.

Altogether, a highly significant effect of pollen treatment was found for the fitness estimates, with selfed offspring having the lowest fitness, and a generally increasing fitness with mating distance (Tabs. 1, 2; Fig. 2). If data from the neighbour and within-population crossings are pooled, offspring from these treatments were found to have a significantly lower fitness than offspring from the between-population crossings (p < 0.05).

Significant differences among maternal populations were found for the number of developed seeds, abortion rate, seed weight, standardized germination proportion, survival, proportion flowers developing capsules, and area of capsules. These differences had no clear relation to the size or degree of isolation of the populations, which did not differ in their estimated fitness (Tab. 1). No significant interactions were found among pollen treatments and populations, either for fitness components or for multiplicative fitness (Tab. 2).

No significant differences were found between paternal populations in the fitness of their offspring from between-population crossings. Differences among individual pollen donors in their offspring fitness were also found to be non-significant.


Fig. 2. Multiplicative fitness curves for pollen treatments in each of the four populations, shown in order of increasing population size. Estimates are calculated relative to the fitness for within-population outcrossings, and shown cumulatively for the life stages included in the multiplicative fitness, with

indices: 1) 1-(seed abortion rate); 2) germination proportion; 3) seedling survival; 4) proportion survived plants flowering; 5) number of capsules per plant; 6) mean area of capsules. Pollen treatments are indicated by: a) self; b) neighbour; c) within-population; d) between-population. Error bars show + or - standard error.

Discussion

Inbreeding clearly has a negative effect on fitness in all the populations studied, with the selfed offspring having significantly lower fitness than all others. Offspring from matings between neighbours had a slightly lower mean fitness than offspring from matings among plants further apart in the population, but this difference was not significant. A lower fitness would be expected if gene flow distances within populations were short, thereby creating population sub-structure such that matings among neighbours frequently yielded inbred offspring that suffer from inbreeding depression.


Average pollinator flight distances between plants suggest that gene flow could be restricted in L.Jlos-cuculi populations. The main pollinators, Bomhus and Syrphidae species, have flight distances between inflorescences averaging 0.5 m, and the more rare Lepidopterans 2.5 m (Hovsgaard and Vejsmes, 1990). Seeds are dispersed a few meters from the plants, at most.

The non-significant difference in fitness between offspring by neighbours and plants further apart could be due to the fitness differentials being too low to yield significant results, even if a genetic structuring is present within the populations. Results from another crossing experiment on L. ,flos-cuculi with several known inbreding levels indicate that inbreeding depression for sib-matings and lower levels of inbreeding may be impossible to detect under the present experimental conditions (Hauser and Loeschcke, in prep.). The relatively beneficial growing conditions in the greenhouse could also make it less likely to detect small fitness differences between different inbreeding levels, as environmental conditions may influence the magnitude of the inbreeding depression (Dudash, 1990; Biere, 1991b).

Realised gene flow distances may alternatively be larger than expected from the average inter-plant flight distances of pollinators, with no or only a weak sub-structuring of the populations as a result. The leptocurtic relationship between the inter-plant flight distances and their frequencies is characterised by occasional long-distance pollinator flights (Hsvsgaard and Vejsmes, 1990). Pollen may also be transferred over several subsequent flower visits (pollen carry-over), increasing the effective dispersal distances over what is expected from between-plant flight distances (Campbell, 1991; Fenster, 1991a). The distances travelled in an hour by L. JEos-cuculi pollinators are in the order of 55-450 m with the potential for large pollen carry-over distances (Hovsgaard and Vejsnzs. 1990).

Overall, it is not possible from this experiment to ascertain whether the studied populations of L. jlos-cuculi are neighbourhood structured, with offspring by neighbours being inbred but not suffering from a detectable inbreeding depression, or whether the populations are not structured as a consequence of larger realised gene flow than expected. A detailed study of the spatial genetic structure in the populations would be needed to decide between these alternatives.

Increased offspring vigour with increased parental distance has been found for some species (e.g. Levin, 1984; Waser and Price, 1989; Fenster, 1991 b; McCall et al., 1991) whereas no effect has been found in others (Newport, 1989). Results from studies on the spatial genetic structure, inferred by using isozymes, suggest that although a structure is present in some populations, it is often weak or absent even under conditions that could be expected to yield a neighbourhood structuring of the populations (Campbell and Dooley, 1992; Waser, 1993). Gene flow within plant populations may thus be more widespread than previously thought, which seems to be corroborated by recent results from paternity analysis (Ellstrand, 1992).

Offspring from matings between the populations of L. Jos-cuculi were found to have a higher fitness than offspring from matings within populations (pooled neighbour and within-population crossings). Whereas heterosis is expected to be at its maximum in the F, generation, an eventual “outbreeding depression”, caused by reduced environmental or inter-genomic adaptations, increases in the F2 and F3


generations. A relatively high fitness thus may be found for the F,, even if the fitness of the F2 and F3 generations is below the parental fitness (Falconer, 1989; Lynch, 1991). This could be the case for our populations, but as we did not obtain results from all these generations, we can only conclude that there is at least no indication of outbreeding depression in the F, .

In this study four L. j?os-cuculi populations differing in size and degree of isolation were chosen in order to compare their mean population fitness and their response to inbreeding. No clear trend was found among the populations studied with respect to the mean fitness of individuals relative to the population size. Population PIL, which is the smallest and most isolated, had the highest estimated offspring fitness, but this was non-significant. This does not support the idea that individual fitness in small populations is reduced due to a higher overall level of inbreeding. A similar result was found for Salvia pratensis (Ouborg, 1992) and for Scabiosa columbaria (van Treuren et al., 1993).

The lack of a correlation between population size and mean fitness could be because the smaller populations have been isolated and small for too few generations for the inbreeding level to rise and have effects on the mean fitness. However, judging by the topology and landscape elements around the smallest population PIL, this population seems likely to have maintained its present state for a long time. Another explanation could be that selection has purged parts of the genetic load in the smaller populations, and thus maintained a relatively high mean fitness of the individuals. Hauser et al. (1994) simulated the fitness consequences of a drop in population size, based on a deleterious alleles model. In general, the mean fitness did not decrease as a consequence of the increased inbreeding due to size, whereas fixation of slightly deleterious alleles caused a gradual drop in fitness over many generations. The four populations of L. jlos-cuculi studied here may thus have experienced different levels of inbreeding during their existence, but the average fitness has not diverged in response to population size suggesting that selection has reduced the genetic load as the inbreeding level increased. With respect to fixation of deleterious alleles, the small population may still be too large, or the population size small for too few generations for the effect to be seen.

No significant differences in inbreeding depression were found among the four populations, as indicated by the finding of no significant interactions between the population and pollen treatments. The largest population, BRO, seemed to have a relatively large difference in offspring fitness between self and within-population pollinations, and relatively large inbreeding effects in the early life stages, as would be expected if larger populations have higher frequencies of lethal and deleterious alleles, that are expressed in the early life stages of the plants. Whether this is an effect of inbreeding and population size that is not large enough to reach significance is unclear, and a larger experiment would be needed to resolve this. Ouborg ( 1994) and van Treuren et al. ( 1993) found no reduction of inbreeding depression in smaller populations, either.

If purging of deleterious alleles is invoked as a possible explanation for the lack of correlation between population size and mean individual fitness, this suggests that the smaller populations should experience a lower inbreeding depression due to


a reduced frequency of deleterious alleles. Simulations (Hauser et al., 1994) suggest that, even if the inbreeding depression is lower in smaller populations, the difference may be too small to be detected unless the mutation rate is very high. These conclusions were derived from populations with very few individuals (N = 20), and the smallest population of this study may thus be too large for a lower inbreeding depression to be detected. If natural populations experience a constant low level of inbreeding due to selfing or neighbourhood structuring, the influence on fitness of a reduction in size may be lower than suggested by the population sizes, and a difference in inbreeding depression would thus be harder to detect.

Acknowledgements

The design and procedures of this experiment were improved by discussions with Denis Couvet and

information on pollination procedures of L. Jios-cuculi from Dorte Hsvsgaard and Flemming Vejsnres. Annie Solling and the technical staff at the Experimental Station of the Botanical Institute assisted during the experiment. We are grateful to Bob Krebs, Christian Damgaard, Joop Ouborg, Francis Ratnieks and an anonymous reviewer for comments on earlier drafts of the manuscript, and to The Natural Science Research Council (Grant 1 l-9025-1 and 11-9639-l) and the Natural Science Faculty of

the University of Aarhus for financial support.

References

Barrett, S. C H. and D. Charlesworth. 1991. Effects of a change in the level of inbreeding on the genetic load. Nature 352: 5222524.

Biere, A. 1991a. Parental effects in Lychnisjos-cud’. I: Seed size, germination and seedling performance in a controlled environment. J. Evol. Biol. 4: 4477465.

Biere, A. 1991b. Parental effects in Lychnis Jlos-cuculi. II: Selection on time of emergence and seedling

performance in the field. J. Evol. Biol. 4: 467-486. Campbell, D. R. 1991. Comparing pollen dispersal and gene flow in a natural population. Evolution 45:

196551968. Campbell, D. R. and J. L. Dooley. 1992. The spatial scale of genetic differentiation in a hummingbird-

pollinated plant: Comparison with models of isolation by distance. Am. Nat. 139: 7355748. Charlesworth, D. and B. Charlesworth. 1987. Inbreeding depression and its evolutionary consequences.

Ann. Rev. Ecol. Syst. 18: 237-268. Charlesworth, D., M. T. Morgan and B. Charlesworth. 1990. Inbreeding depression, genetic load, and

the evolution of outcrossing rates in a multilocus system with no linkage. Evolution 44: 1469-

1489. Charlesworth, B., M. T. Morgan and D. Charlesworth. 1991. Multilocus models of inbreeding

depression with synergistic selection and partial self-fertilization. Genet. Res., Camb. 57: 177- 194. Charlesworth, D., M. T. Morgan and B. Charlesworth. 1992. The effect of linkage and population size

on inbreeding depression due to mutational load. Genet. Res., Camb. 59: 49961.

Dudash, M. R. 1990. Relative fitness of selfed and outcrossed progeny in a self-compatible, protandrous species, Sub&a angukzris L. (Gentianaceae): A comparison in three environments. Evolution 44: 112991139.

Ellstrand, N. C. 1992. Gene flow by pollen: Implications for plant conservation genetics. Oikos 63: 77786.

Falconer, D. S. 1989. Introduction to Quantitative Genetics. 3rd edition. Longman, New York.

Fisher, R. A. 1941. Average excess and average effects of a gene substitution. Ann. Eugen. 11: 53363.


Fenster, C. B. I99Ia. Gene flow in Chamaecrista,fa.scicu/ata (Leguminosae). I. Gene dispersal. Evolution 45: 398-409.

Fenster, C. B. 1991b. Gene flow in Chamaecrista fusciculuta (Leguminosae). 2. Gene establishment. Evolution 45: 410-422.

Hauser, T. P., C. Damgaard and V. Loeschcke. Effects of inbreeding in small plant populations: Expectations, and implications for conservation. In V. Loeschcke, J. Tomiuk and S. K. Jain (eds.), Conservation biology. Birkhluser, 1994.

Holsinger, K. E., M. W. Feldman and F. B. Christiansen. 1984. The evolution of self-fertilization in plants: A population genetic model. Amer. Natur. 124: 446-453.

Hsvsgaard, D. and F. Vejsmes. 1990. The pollination biology of Lychnis jlos-cuculi. M.Sc. Thesis, University of Aarhus.

Lande, R. and D. W. Schemske. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39: 24-40.

Levin, D. A. 1981. Dispersal versus gene flow in plants. Ann. Missouri Bot. Gard. 68: 233-253.

Levin, D. A. 1984. Inbreeding depression and proximity-dependent crossing success in Phlox drum- mondii. Evolution 38: 116-127.

Lynch, M. 1991. The genetic interpretation of inbreeding depression and outbreeding depression.

Evolution 45: 622-629. McCall, C., T. Mitchell-Olds and D. M. Wailer. 1991. Distance between mates affects seedling characters

in a population of lmpatiens cupensis (Balsaminaceae). Amer. J. Bot. 78: 964-970. Newport, M. E. A. 1989. A test for proximity-dependent outcrossing in the alpine skypilot, Polemonium

uiscosum. Evolution 43: II IO- I1 13.

Ouborg, J. and R. van Treuren. 1992. Variation in fitness related characters among small and large populations of Sulviu prutensis. In J. Ouborg, On the relative contribution of genetic erosion to the chance of population extinction. Ph.D. Thesis, University of Utrecht.

Ouborg, J. and 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 Suiviu prutensis. Evolution

(in press). Uyenoyama, M. K. 1986. Inbreeding and the cost of meiosis: The evolution of selfing in populations

practising biparental inbreeding. Evolution 40: 3888404. Van Treuren, R., R. Bijlsma, N. J. Ouborg and W. Van Delden. 1993. Inbreeding depression and

heterosis effects due to se&g and outcrossing in Scubiosu columbariu. Evolution (in press). Waser, N. M. 1993. Population structure, optimal outbreeding, and assortative mating in Angiosperms.

In N. W. Thornhill (ed.), The Natural History of Inbreeding and Outbreeding: Theoretical and Empirical Perspectives. Chicago University Press, Chicago.

Waser, N. M. and M. V. Price. 1989. Optimal outcrossing in Ipomopsis uggreguta: Seed set and offspring fitness. Evolution 43: 109771109.

Wright, S. 1946. Isolation by distance under diverse systems of mating. Genetics 31: 39-59. Zar, J. H. 1984. Biostatistical Analysis. 2nd edition. Prentice-Hall, Englewood Cliffs, New Jersey.

Received 20 October 1993;

accepted I7 February 1994. Corresponding Editor: J. van Damme

Inbreeding depression and mating-distance dependent offspring fitness in large and small populations...

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