Journal of
Ecology 2006
94, 942–952
ESSAY REVIEW
Blackwell Publishing Ltd
How general are positive relationships between plant
population size, fitness and genetic variation?
ROOSA LEIMU*†¶, PIA MUTIKAINEN‡, JULIA KORICHEVA§ and
MARKUS FISCHER¶
†Section of Ecology, Department of Biology, FI-20014 University of Turku, Finland, ‡Department of Biology,
University of Oulu, PO Box 3000, FI-90014 Oulu, Finland, §School of Biological Sciences, Royal Holloway,
University of London, Egham, Surrey TW 20 0EX, United Kingdom, and ¶Institute for Biochemistry and Biology,
University of Potsdam, Maulbeerallee 1, D-14469 Potsdam, Germany
Summary
1 Relationships between plant population size, fitness and within-population genetic
diversity are fundamental for plant ecology, evolution and conservation. We conducted
meta-analyses of studies published between 1987 and 2005 to test whether these relationships are generally positive, whether they are sensitive to methodological differences
among studies, whether they differ between species of different life span, mating system
or rarity and whether they depend on the size ranges of the studied populations.
2 Mean correlations between population size, fitness and genetic variation were all
significantly positive. The positive correlation between population size and female
fitness tended to be stronger in field studies than in common garden studies, and the
positive correlation between genetic variation and fitness was significantly stronger in
DNA than in isoenzyme studies.
3 The strength and direction of correlations between population size, fitness and genetic
variation were independent of plant life span and the size range of the studied populations.
The mean correlations tended to be stronger for the rare species than for common species.
4 Expected heterozygosity, the number of alleles and the number or proportion of
polymorphic loci significantly increased with population size, but the level of inbreeding
FIS was independent of population size. The positive relationship between population
size and the number of alleles and the number or proportion of polymorphic loci was
stronger in self-incompatible than in self-compatible species. Furthermore, fitness and
genetic variation were positively correlated in self-incompatible species, but independent
of each other in self-compatible species.
5 The close relationships between population size, genetic variation and fitness suggest
that population size should always be taken into account in multipopulation studies of
plant fitness or genetic variation.
6 The observed generality of the positive relationships between population size, plant
fitness and genetic diversity implies that the negative effects of habitat fragmentation on
plant fitness and genetic variation are common. Moreover, the stronger positive associations observed in self-incompatible species and to some degree in rare species, suggest
that these species are most prone to the negative effects of habitat fragmentation.
Key-words: genetic diversity, habitat fragmentation, meta-analysis, plant fitness,
population size
Journal of Ecology (2006) 94, 942–952
doi: 10.1111/j.1365-2745.2006.01150.x
Introduction
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society
Present address and correspondence: Roosa Leimu, Institute for
Biochemistry and Biology, University of Potsdam, Maulbeerallee 1, D-14469 Potsdam, Germany (tel. +49 331 977 4863;
fax +49 331 977 4865; e-mail [email protected]).
The relationships between plant population size, fitness
and genetic diversity are of fundamental importance in
plant ecology, evolution and conservation. Although
943
Plant population
size, fitness and
genetic variation
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 942–952
many plant populations are naturally isolated and small,
populations of numerous plant species have become
more isolated and further decreased in size due to the
recent anthropogenic fragmentation of habitats. Small
populations are predicted to face the negative genetic
consequences of increased inbreeding and reduced
genetic variation caused by genetic drift, founder effects
and accumulation of deleterious mutations (Lynch et al.
1995; Young et al. 1996). In the long run, reduced genetic
diversity, mutation accumulation and increased inbreeding, decrease the evolutionary potential of species to
adapt to changing environments, and in the short run
they may reduce fitness, especially in small populations
(Ellstrand & Elam 1993). In addition to the genetic
mechanisms, ecological mechanisms, such as pollinator
limitation, may further reduce fitness in small populations
(e.g. Ågren 1996).
Positive relationships between population size, genetic
variation and fitness may come about for two reasons.
On the one hand, such associations may indicate an
extinction vortex where reductions in population size
decrease genetic variation. If this reduction leads to
inbreeding depression or reduced mate availability, it will
consequently reduce plant fitness and lead to a further
decrease in population size (Ellstrand & Elam 1993).
On the other hand, such positive relationships may
arise if plant fitness differs between populations due to
differences in habitat quality. This will result in variation
in population sizes and may consequently also influence
the level and distribution of genetic variation. These two
different causal backgrounds can be distinguished by
comparing field studies with experimental common
garden studies that examine plant fitness. This reveals
whether the associations between population size or
genetic variation and plant fitness observed in the field
are due to underlying differences in habitat quality
(Fischer & Matthies 1998).
During the past two decades, a number of studies
examined relationships between plant population size,
measures of fitness and genetic variation (Oostermeijer
et al. 2003). Although positive relationships were reported
in some studies, non-significant or even negative relationships were reported in others (see Appendix S1 in
Supplementary Material). Hence, it is not clear whether
these relationships are overall positive, and how strong
they are. Because most studies have been conducted in
the field and only very few in common environments, it
is not clear whether the reported relationships are due
to the effects of population size per se or due to confounding habitat differences. Moreover, it is not known
whether the different methods used to measure genetic
variation affect the observed relationships. Most studies
used near-neutral isoenzyme or DNA-markers to determine the level of genetic variation, although variation
for such neutral markers may correlate poorly with
traits under selection and does not necessarily reflect
the evolutionary potential of a population (Reed &
Frankham 2001). Moreover, the relationship between
population size and genetic variation has been suggested
to be strongest for neutral genetic markers and weakest
for the most strongly selected markers (Frankham
1996). Unfortunately, studies on quantitative genetic
variation of fitness-related traits in natural populations
are still very scarce.
The strength and direction of the relationships between
plant population size, fitness and genetic variation may
depend on different plant characteristics, especially life
span, mating system and rarity. Short-lived plants may
be more prone to the negative genetic consequences of
reduced population size. The more generations passed
during a given time span, the stronger will be the effect
of genetic drift (Hartl & Clark 1989). Therefore, drift is
likely to have greater impact on short-lived species with
generally shorter generation times compared with longlived species (Hamrick et al. 1979). Moreover, short-lived
species are likely to be more vulnerable to the ecological
consequences of small population size, such as increased
pollinator limitation, or increased demographic stochasticity in recruitment, which is essential for short-lived
species because they are mainly semelparous.
Associations between population size, genetic variation
and plant fitness can be stronger in self-compatible species
because in these species inbreeding depression may be
expressed more readily. However, genetic load may have
been purged in populations of self-compatible plants.
Thus, especially in populations with a long history of
inbreeding, self-compatible plants could also be less
vulnerable to inbreeding depression and therefore less
susceptible to the negative effects of small population
size (Busch 2005). In self-compatible species, genetic
variation resides largely between populations, whereas in
self-incompatible species it resides rather within populations (Hamrick & Godt 1989). Therefore, variation in
population size may have a greater impact on withinpopulation genetic variation in self-incompatible species.
Self-incompatibility may also break down in small and
isolated populations, especially after population bottlenecks (Porcher & Lande 2005), which can consequently
erase the differences in the strength of associations of
population size, genetic variation and fitness between
self-incompatible and self-compatible species.
Species rarity may also affect the relationships between
population size, genetic variation and fitness. Rare species
are typically considered to be genetically less variable than
common and widespread species (Karron 1987; Hamrick
& Godt 1989; Ellstrand & Elam 1993; Spielman, Brook
& Frankham 2004). This indicates that the level of
genetic variation might be less strongly associated with
population size in rare plants compared with common
plants. This is because genetic variation is likely to be
low in all populations of rare plants and higher in all
populations of common plants regardless of the size of the
populations. However, hybridization, recent speciation,
multiple origins or recent population bottlenecks may
result in high levels of genetic variation also in rare species
(Lewis & Crawford 1995; Purdy & Bayer 1995; Friar et al.
1996; Smith & Pham 1996). Moreover, when differences
between rare and common species are considered the
944
R. Leimu et al.
exact definition of rarity has to be taken into account
(Rabinowitz 1981). For example, in contrast to a widespread assumption, rare species do not always have small
population sizes (Rabinowitz 1981; Gitzendanner &
Soltis 2000).
Finally, whether positive associations of population
size, genetic variation and fitness become apparent may
depend on the size of the populations in a study. Although
these associations may be strong at low population sizes,
they may be less strong or absent for larger populations.
In this review, we use meta-analysis to examine the
relationships between plant population size, genetic
variation and fitness reported in studies published
between 1987 and 2005. Meta-analysis allows us to
combine the results of independent studies addressing
the same research question, to estimate the mean effect
size, and to identify the factors that influence the strength
and sign of the effect (Gurevitch & Hedges 2001). One of
the advantages of meta-analysis is that effects may be
detected across studies even for cases where individual
studies report non-significant effects because of lack of
statistical power. In particular, we examined: (i) whether
the relationships between plant population size, fitness
and genetic variation are generally positive; (ii) whether
they differ between field and common environment
studies of plant fitness, or between genetic studies using
isoenzymes or DNA-based analyses; (iii) whether they
differ between annual/biennial and perennial species,
self-compatible and self-incompatible species, or between
rare and common species; and (iv) whether they depend
on the actual size range of the studied populations.
Methods
 
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 942–952
We conducted key word searches in the Web of Science
(ISI) electronic bibliographic data base to find plant
studies on the relationships between population size and
fitness, between population size and genetic variation,
and between genetic variation and fitness. Using combinations of the key-words ‘population size’, ‘fitness’,
‘reproductive success’, ‘genetic variation’ and ‘genetic
diversity’ we obtained three data sets. The first set included
45 studies of the relationship between population size
and fitness measures in 34 plant species, the second set
consisted of 46 studies of relationships between plant
population size and genetic variation in 41 plant species,
and the third set included 14 studies of the relationship
between fitness and genetic variation in 12 plant species
(see Appendix S1 and S2). These studies were published
in 20 journals between 1987 and 2005.
Based on the information given in the articles, we
classified the species according to their longevity (annual/
biennial or perennial), mating system (self-incompatible
(SI) or self-compatible (SC)), and rarity (rare or common,
Table 1), and then tested for differences between these
classes of species in the strength and direction of the
correlations.
Because relationships between population size, fitness
and genetic variation were reported as r in most studies,
we used Pearson product-moment correlation coefficients
r as a measure of effect size. For studies not reporting rvalues we calculated them from the population mean
values of measures of fitness and genetic variation and
estimates of population size given in tables or figures.
To obtain data from figures, we enlarged graphs and
digitized data manually. From studies using regression
analysis we obtained r as square root of the coefficient
of the determination (r2).
Most studies reported several fitness measures, and
overall 19 different fitness measures were reported. For
the meta-analysis of the relationship between population
size and plant fitness, we used the number of flowers, fruit
set, seed set, the number of seeds or the number of fruits
(female fitness), and pollinator visitation rates and
pollen removal (male fitness), because these were most
frequently reported and because at least one of them
was used in each of the selected studies.
For the meta-analysis of the relationship between
population size and genetic variation, we considered
expected heterozygosity (HEXP), observed heterozygosity
(HOBS), the number or percentage of polymorphic loci
(P), the number of alleles (A), and for PCR studies
molecular variance.
For the meta-analysis of the relationship between
genetic variation and fitness, we considered the number
of flowers, fruit set, seed set, the number of seeds or the
number of fruits, and, for studies not providing a measure
of reproductive output, biomass, as fitness measures, and
expected heterozygosity (HEXP), observed heterozygosity
(HOBS), the number or percentage of polymorphic loci (P),
the number of alleles (A), or molecular variance (PCR),
as measures of genetic variation. In addition, we tested
the relationship between population size and the level
of inbreeding (FIS).
-
We performed all meta-analyses with Meta Win 2.0
(Rosenberg et al. 2000). We z-transformed individual
correlation coefficients and weighted them by their sample
size, i.e. by the number of studied populations. Across
studies we combined the transformed coefficients with
the mixed effects model, i.e. we assumed that differences
among studies are due to both sampling error and
random variation, which is the rule for ecological data
(Gurevitch & Hedges 2001).
To test whether effect sizes differed statistically
significantly from zero, we used bias-corrected 95%
bootstrap confidence intervals (Adams et al. 1997) of
the mean z-transformed correlation coefficients from
4999 iterations. We considered overall relationships as
significant if the confidence interval did not include zero.
To analyse the relationship between population size
and fitness, we first calculated mean effect sizes for each
species and study over the different measures of fitness
(female and male), and then used these data to calculate
945
Plant population
size, fitness and
genetic variation
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 942–952
Table 1 Characteristics of the plant species and populations included in the analyses. SC = self-compatible, SI = self-incompatible. For references see Appendix S2 in Supplementary Material
Species
Family
Longevity
Allium stellatum
Anacamptis palustris
Anacamptis pyramidalis
Antirrhinum charidemi
Arnica montana
Asclepias meadii
Asclepias verticillata
Austromyrtus bidwillii
Austromyrtus hillii
Banksia goodii
Brassica kaber
Calypso bulbosa
Centaurea scabiosa
Cestrum parqui
Cochlearia bavarica
Cochlearia bavarica
Dactylorhiza majalis
Eryngium alpinum
Eucalyptus albens
Festuca ovina
Gentiana lutea
Gentiana pneumonanthe
Gentiana pneumonanthe
Gentiana pneumonanthe
Gentianella austriaca
Gentianella germanica
Grevillea caleyi
Halocarpus bidwillii
Iris atrofusca
Leucochrysum albicans
Lupinus sulphureus ssp. kincaidii
Lychnis viscaria
Lychnis viscaria
Lythrum salicaria
Lythrum salicaria
Microseris lanceolata
Narcissus longispathus
Liliaceae
Orchidaceae
Orchidaceae
Scrophulariaceae
Asteraceae
Asclepiadaceae
Asclepiadaceae
Myrtaceae
Myrtaceae
Proteaceae
Brassicaceae
Orchidaceae
Asteraceae
Solanaceae
Brassicaceae
Brassicaceae
Orchidaceae
Apiaceae
Eucalyptaceae
Poaceae
Gentianaceae
Gentianaceae
Gentianaceae
Gentianaceae
Gentianaceae
Gentianaceae
Proteaceae
Podocarpaceae
Iridaceae
Asteraceae
Fabaceae
Caryophyllaceae
Caryophyllaceae
Lythraceae
Lythraceae
Asteraceae
Amaryllidaceae
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Annual
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Biennial
Biennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Rarity
Mating
system
SC
Rare
Rare
Rare
Rare
Rare
Rare
Common
Common
Rare
Common
Rare
Common
Common
Rare
Rare
Common
Rare
Rare
Common
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Common
Rare
Common
Common
Rare
Rare
SC
SI
SI
SI
SI
SI
SI
SI
SI
SC
SI
SI
SI
SI
SI
SC
SI
SI
SC
SC
SC
SC
SC
SC
SI
SI
SI
SC
SC
SC
SI
SI
SI
SC
Geometric mean
of population size
Size of smallest
population
Size of largest
population
39.1
821.9
72.6
50.4
21.1
42.4
47.3
15.1
16.0
34.3
15.2
134.7
141.9
3
100
11
23
2
5
11
8
7
8
3
101
27
1125
5000
400
150
690
400
80
20
41
150
78
178
650
67.4
87.8
286.0
797.1
199.1
149.3
10
8
24
35
14
15
4850
3215
1700
100000
10000
980
121.7
165.6
238.0
172.3
428.6
175.7
948.6
244.9
1554.7
3245.7
52.4
143.7
93.0
42.3
2267.3
208.0
5
5
8
15
40
9
20
15
74
805
10
7
1
1
87
40
50000
50000
100000
1000
5000
2000
400000
10000
50000
7928
680
1000
8680
19100
140000
600
Reference
Molano-Flores et al. (1999)
Cozzolino et al. (2003)
Fritz & Nilsson (1994)
Mateu-Andres & Segarra-Moragues (2000)
Luijten et al. (2000)
Tecic et al. (1998)
Fore & Guttman (1996)
Shapcott & Playford (1996)
Shapcott & Playford (1996)
Lamont et al. (1993)
Kunin (1997)
Alexandersson & Ågren (1996)
Ehlers (1999)
Aguilar et al. (2004)
Fischer et al. (2003)
Paschke et al. (2002)
Hansen & Olesen (1999)
Gaudeul et al. (2000)
Prober & Brown (1994)
Berge et al. (1998)
Kéry et al. (2000)
Oostermeijer et al. (1994)
Oostermeijer et al. (1998)
Raijmann et al. (1994)
Greimler & Dobes (2000)
Fischer & Matthies (1998)
Llorens et al. (2004)
Billington (1991)
Arafeh et al. (2002)
Costin et al. (2001)
Severns (2003)
Berge et al. (1998)
Lammi et al. (1999)
Waites & Ågren (2004)
Ågren (1996)
Prober, S. M. et al.
Barrett et al. (2004)
946
R. Leimu et al.
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 942–952
Table 1 continued
Species
Family
Longevity
Rarity
Nepeta cataria
Orchis palustris
Orchis spitzelii
Parnassia palustris
Pedicularis palustris
Phaseolus lunatus
Primula elatior
Primula elatior
Primula veris
Primula veris
Primula veris
Primula vulgaris
Rutidosis leptorrhynchoides
Rutidosis leptorrhynchoides
Salvia pratensis
Salvia pratensis
Salvia pratensis
Sarracenia rubra ssp. alabamensis
Scabiosa columbaria
Scabiosa columbaria
Scabiosa columbaria
Scorzonera humilis
Scutellaria montana
Sesleria albicans
Silene latifolia
Spiranthes sinensis
Succisa pratensis
Swainsona recta
Swertia perennis
Taxus baccata
Tetratheca juncea
Trillium camschatcense
Trollius europaeus
Vincetoxicum hirundinaria
Viscaria vulgaris
Scrophulariaceae
Orchidaceae
Orchidaceae
Saxifragaceae
Scrophulariaceae
Fabaceae
Primulaceae
Primulaceae
Primulaceae
Primulaceae
Primulaceae
Primulaceae
Asteraceae
Asteraceae
Lamiaceae
Lamiaceae
Lamiaceae
Sarraceniaceae
Dipsacaceae
Dipsacaceae
Dipsacaceae
Asteraceae
Scrophulariaceae
Poaceae
Caryophyllaceae
Orchidaceae
Dipsacaceae
Fabaceae
Gentianaceae
Taxaceae
Tremandraceae
Trilliaceae
Ranunculaceae
Asclepiadaceae
Caryophyllaceae
Perennial
Perennial
Perennial
Perennial
Biennial
Biennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Perennial
Common
Rare
Rare
Rare
Rare
Rare
Common
Common
Rare
Rare
Common
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Rare
Common
Common
Rare
Common
Rare
Rare
Common
Rare
Rare
Common
Common
Mating
system
SI
SC
SC
SC
SC
SC
SI
SI
SI
SI
SI
SI
SI
SI
SI
SI
SC
SC
SI
SI
SI
SI
SC
SI
SI
SC
SC
SI
SC
SI
SI
SI
SI
SC
SC
Geometric mean
of population size
Size of smallest
population
Size of largest
population
153.9
36.0
1251.3
149.2
8.1
81.7
170.2
26
3
140
3
3
13
20
2325
1000
10000
28500
60
2273
1000
45.8
284.0
789.6
97.6
96.5
174.3
176.0
360.2
789.4
990.6
1
13
5
23
5
22
30
9
14
35
700
5419
95240
350
1500
1500
1600
2000
100000
100000
91.2
370.1
11.3
14.3
10
5
6
3
500
50000
19
98
59.9
2394.3
191.9
1
7
21
430
118500
2500
2588.4
536.4
541.0
387.1
46
50
32
227
153600
1500
5200
660
Reference
Sih & Baltus (1987)
Fritz & Nilsson (1994)
Fritz & Nilsson (1994)
Bonnin et al. (2002)
Schmidt & Jensen (2000)
Bi et al. (2003)
Jacquemyn et al. (2004)
Van Rossum et al. (2002)
Brys et al. (2003)
Kéry et al.
Van Rossum et al. (2004)
Brys et al. (2004)
Morgan (1998)
Young et al. (1999)
Ouborg & Van Treuren (1995)
Van Treuren et al. (1991)
Van Treuren et al. (1993)
Godt & Hamrick (1998)
Pluess & Stöcklin (2004)
Van Treuren et al.
Van Treuren et al. (1993)
Colling & Matthies (2004)
Cruzan (2001)
Reisch et al. (2002)
Richards et al. (2003)
Sun (1996)
P. Vergeer et al.
Buza et al. (2000)
Lienert et al. (2002)
Hilfiker et al. (2004)
Gross et al. (2003)
Tomimatsu & Ohara (2003)
Despres et al. (2002)
Leimu & Mutikainen (2005)
Jennersten & Nilsson (1993)
947
Plant population
size, fitness and
genetic variation
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 942–952
the overall effect size and confidence intervals. To analyse
the relationship between population size and genetic
variation, we first calculated mean effect size for each
species and study over expected heterozygosity (HEXP),
observed heterozygosity (HOBS), the number or percentage of polymorphic loci (P), and the number of alleles
(A), and then used these data to calculate the overall
effect size and confidence interval. If several species were
examined in one study we calculated mean effect size for
each of the species separately. To analyse the relationship
between genetic variation and fitness, we calculated
mean effect size by study and by species and used these
pooled data to calculate overall mean effect size and
confidence intervals.
The number and proportion of alleles and polymorphic
loci depend on the number of individuals sampled and
different sample sizes, i.e. number of plants in different
studies might influence the results. Moreover, a small
sample size may bias the estimates of average heterozygosity (Nei 1978). Therefore, we tested whether the
number of plants sampled influences the strengths of
the associations between population size and genetic
variation, and between genetic variation and fitness. The
strength of the effects turned out to be independent of the
number of plants sampled. Furthermore, the strength
of the associations between genetic variation and
population size or fitness, did not differ between studies
correcting measures of genetic variation for sample size
and studies that did not (data not shown).
To examine the effects of potential sources of variation, including differences in methods or plant species
characteristics, on the strength of the relationships
between population size, genetic variation and plant
fitness, we examined between-group heterogeneity with
the chi-square test statistic Qb (Rosenberg et al. 2000).
In all analyses, we pooled the data by study and in cases
where several species were examined in the same study,
also by species. Because some studies examined same
species, we also ran the analyses using a data pooled by
species. The results did not differ depending on whether
the data were pooled by study or by species, indicating
that the results are not influenced by double counting
of some species, and thus we only present the results
obtained using the data pooled by study.
We tested whether the strength of the relationship
between population size and fitness differed between
female and male fitness, and between field studies and
those conducted in a common environment. Moreover, we
examined whether the strength and direction of relationships between population size, fitness and genetic
variation differed between species of different life span,
mating system or rarity. We also studied the associations
between the geometric mean of the population sizes
and the mean effect size in each study to examine the
effects of the size range of the populations. Moreover,
to test whether the sizes of the studied populations were
confounded with plant characteristics, we tested whether
the geometric mean of population size, or the size of the
smallest or largest population included in a study,
Fig. 1 Mean correlations (r+) between population size, female
fitness and genetic variation. In all figures, bars denote 95%
confidence intervals obtained by bootstrapping, and sample
size N denotes the number of independent studies included in
meta-analysis. The relationships are considered significant if
the confidence intervals do not include zero.
differs between rare and common species, between selfcompatible and self-incompatible species, or between
annual, biennial or perennial species. Population sizes
or size ranges were not statistically significantly affected
by any of these plant characteristics (Table 1; results
not shown). For the relationships that involved genetic
diversity, we examined whether the strength of the relationships between genetic variation and population size
or plant fitness differed between isoenzyme and DNAPCR studies. To compare relationships for the different
measures HEXP, P and A, and for the inbreeding coefficient
(FIS), for which the expected relationship with population
size is negative, we also carried out separate analyses
for each of these measures.
Using the funnel plot technique (Light & Pillemer
1984; Palmer 1999), we found no evidence for publication
bias among the selected studies. Furthermore, effect sizes
were independent of sample size, i.e. of the number of
populations in a study, for the associations between population size and fitness (r = 0.299, P = 0.064), population
size and genetic variation (r = 0.082, P = 0. 578), and
genetic variation and fitness (r = 0.306, P = 0.287), which
also indicates lack of publication bias (Palmer 2000).
Results
     
 
Overall, population size and fitness were significantly
positively correlated (Fig. 1). The strength and direction
of this correlation did not differ between rare and
common species (Qb = 0.7770, d.f. = 1, P = 0.391), or
between perennials and annuals/biennials (Qb = 0.2226,
d.f. = 1, P = 0.642), self-incompatible and selfcompatible species (Qb = 0.0019, d.f. = 1, P = 0.964), or
between field studies and common environment studies
(Qb = 2.118, d.f. = 1, P = 0.158) (Fig. 2). Furthermore, the
948
R. Leimu et al.
Fig. 3 Mean correlations (r+) between genetic variation and
population size according to plant life span, mating system,
rarity and method used to assess genetic variation.
Fig. 2 Mean correlations (r+) between (a) female and (b) male
fitness and population size according to plant life span, mating
system, rarity and type of study.
strength and direction of the effect were independent
of the geometric mean of the population sizes in the
different studies (Qb = 0.426, d.f. = 1, P = 0.514).
A significant positive correlation was found between
population size and female fitness (Fig. 2a), whereas the
correlation was non-significant for male fitness (Fig. 2b).
The strength and direction of the correlation between
population size and female fitness did not, however, differ
from that between population size and male fitness
(Qb = 0.1004, d.f. = 1, P = 0.752). The positive association between population size and male fitness did not
differ significantly between rare and common species
(Qb = 0.4072, d.f. = 1, P = 0.561), although the association was significant only for rare species (Fig. 2).
     
  
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 942–952
Overall, the mean correlation between population size
and genetic variation was significantly positive (Fig. 3),
and independent of the genetic method used (isoenzymes
vs. DNA-PCR) (Qb = 0.3450, d.f. = 1, P = 0.567; Fig. 3).
The strength and direction of this correlation did not
differ between rare and common species (Qb = 0.7454,
d.f. = 1, P = 0.404; Fig. 3), between perennial and annual/
biennial plants (Qb = 0.0529, d.f. = 1, P = 0.817; Fig. 3),
or between self-compatible and self-incompatible species
(Qb = 1.5240, d.f. = 1, P = 0.226; Fig. 3). Moreover,
the strength and direction of the correlation were independent of the geometric mean of the sizes of the study
populations (Qb = 0.976, d.f. = 1, P = 0.323).
When the different measures of genetic variation were
analysed separately, the correlation between genetic
variation and population size was significantly positive
for expected heterozygosity (HEXP), the number or proportion of polymorphic loci (P), and the mean number of
alleles (A) (r+ = 0.317, r+ = 0.465, r+ = 0.481, respectively), but not for the inbreeding coefficient FIS (r+ =
0.054). For all measures of genetic variation (HEXP, P, A
or FIS), the correlation between population size and
genetic variation was independent of plant longevity,
rarity, and the method used to assess genetic variation
(data not shown). The correlation between population
size and genetic variation was significantly greater in
self-incompatible species than in self-compatible species
when genetic variation was measured as the mean number
of alleles (Qb = 6.528, d.f. = 1, P = 0.016) or as the
number or proportion of polymorphic loci (Qb = 4.906,
d.f. = 1, P = 0.036), but not as expected heterozygosity
(Qb = 1.549, d.f. = 1, P = 0.234), although the mean
correlation between population size and heterozygosity
was significant only in self-incompatible plants (Fig. 4).
While the level of inbreeding (FIS) increased significantly
with population size in self-incompatible species, it
tended to decrease in self-compatible species (Fig. 4).
   
  
Overall, the mean correlation between genetic variation and fitness was significantly positive (Fig. 5). The
949
Plant population
size, fitness and
genetic variation
Fig. 4 Mean correlations (r+) between genetic variation and
population size in self-incompatible (black symbols) and selfcompatible (grey symbols) species for different measures of
genetic variation. Heterozygosity denotes expected heterozygosity.
magnitude and direction of the correlation was not
significantly influenced by plant rarity (Qb = 0.1585,
d.f. = 1, P = 0.713), or longevity (Qb = 0.3275, d.f. = 1,
P = 0.561) (Fig. 5). The association between genetic
variation and fitness was, however, significantly influenced by plant mating system (Qb = 5.9872, d.f. = 1,
P = 0.038). Fitness increased with genetic variation in
self-incompatible species, but not in self-compatible
species (Fig. 5). The association between genetic variation and fitness also differed between isoenzyme and
DNA studies (Qb = 7. 1842, d.f. = 1, P = 0.023). While
fitness increased with genetic variation in studies using
PCR (AFLP or RAPD), no significant association was
found in studies using isoenzyme electrophoresis (Fig. 5).
Discussion
   
 
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 942–952
Our meta-analyses clearly demonstrated that the relationships between population size, plant fitness and genetic
diversity are generally significantly positive (Figs 1 and 2).
The positive relationship between fitness and population size did not differ significantly between field and
common garden studies. This suggests that this association arises due to the negative effects of small population
size on genetic variation and plant fitness, rather than
due to the effects of habitat quality on plant fitness,
which would subsequently reduce population size and
genetic variation. Thus, our findings support the idea of
an extinction vortex of interdependently ever decreasing
population size, genetic variation and fitness. However,
the statistically non-significant, but large, difference
between field and common garden studies in the strength
of the mean correlation between population size and
fitness, suggests that reduced fitness in small populations results not only from reduced genetic variation or
Fig. 5 Mean correlations (r+) between genetic variation and
fitness according to plant life span, mating system, rarity and
method of assessing genetic variation.
increased inbreeding, but potentially also from environmental factors, demographic stochasticity and biotic
interactions. Undoubtedly, more studies conducted in
common environments are needed to resolve this question.
Associations between population size, genetic variation and fitness may be mediated by differences in the
demographic structure of plant populations, e.g. if small
plant populations only consist of old plants that no
longer contribute to offspring recruitment (Oostermeijer
et al. 1994). Because data on the demographic structure
of population was rarely provided, we were not able to
consider the role of demographic population structure
in our meta-analysis. However, even if the observed
relationships between population size, genetic variation
and fitness would have been mediated by the demographic structure of the populations, this would not
reduce their high biological importance.
Population size has been suggested to be the most
important variable explaining differences in allozyme
variation between populations (Frankham 1996).
Although population size and genetic variation were
positively associated and no significant differences were
found in the strength of the association irrespective of
whether DNA-markers or isoenzymes were used to assess
genetic variation, a significantly positive correlation
between the level of genetic variation and fitness was
found only for DNA studies. The latter suggests that
DNA methods should be favoured in this context, most
likely due to the higher resolution of DNA methods
compared with isoenzyme analysis.
According to theory, loss of rare alleles is a primary
consequence of small population size, whereas heterozygosity is reduced significantly only after the population
has been small for several generations (Barrett & Kohn
1991). Although expected heterozygosity and the number
of alleles and polymorphic loci all decreased with population size in our meta-analyses, this decrease tended to
be greater for the number of alleles and polymorphic
950
R. Leimu et al.
loci than for expected heterozygosity. This suggests that
in general genetic drift, rather than direct or biparental
inbreeding, causes the observed reduction in genetic
variation in small populations (e.g. Oostermeijer et al.
2003). This is further supported by the finding that the
inbreeding coefficient FIS, which measures withinpopulation inbreeding, was not related to population
size. At the same time, the independence of FIS from
population size suggests that in general there are no
differences in population substructure between small
and large populations.
In accordance with our results, a recent meta-analysis
by Reed & Frankham (2003) on 10 animal and 12 plant
species reported a positive mean association between
genetic diversity and fitness. Reduced genetic variation
in small populations may lead to reduced fitness for
several reasons. First, increased homozygosity may lead
to increased expression of inbreeding load. Secondly,
higher fixed mutation load may further decrease plant
fitness in small populations. Because only a few studies
have examined the association between heterozygosity and
fitness or experimentally separated the two possibilities
(Willi et al. 2005), we cannot distinguish between these
two possibilities in our meta-analyses. Furthermore,
because the number of marker loci is far smaller than the
total number of loci in a genome, finding a relationship
between fitness and marker heterozygosity is highly
unlikely (Mitton & Pierce 1980).
    
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 942–952
Contrary to our prediction, our meta-analysis indicates
that short-lived species are in general as prone to the
negative effects of small population size as long-lived
species. Possibly, differences between short-lived and
perennial plants will turn out to be more pronounced
than reported here once more data become available
on shrubs or trees that were hardly represented in the
reviewed literature.
The positive relationships between plant population
size, genetic variation and fitness tended to be stronger
for rare than for common species (Figs 2, 3 and 5), but
these differences were not significant. Possibly, differences
between rare and common species will only become
apparent when more studies are available, which would
also increase the statistical power for meta-analysis.
Nevertheless, male fitness, measured as pollinator
visitation and pollen removal, was significantly reduced
in smaller populations of rare, but not of common,
species. This suggests that reduced pollinator activity
generally contributes to reduced fitness of plants in
small populations of rare species. However, in general
the variation in the positive associations between
population size, genetic variation and fitness among the
study species was low. Therefore, a more fine-grained
classification of species according to the different
categories of rarity is not very likely to reveal further
differences in these associations between rare and
common species. Because populations of rare plants
are not necessarily smaller (Rabinowitz et al. 1986) or
have lower levels of genetic variation within or between
populations (Gitzendanner & Soltis 2000) than common
plants, these populations do not necessarily have to be
expected to be more prone to the negative effects of small
population size. Accordingly, the sizes or size ranges of
populations of the studies included in our analyses did
not differ between rare and common species (Table 1).
The negative effects of habitat fragmentation may be
especially pronounced for formerly more common and
recently declining species and populations, than for
naturally rare species and populations (Huenneke 1991).
Unfortunately, such historical information is hardly
available for species and populations in the published
studies and could therefore not be considered in our
analyses. If published studies focused on formerly
common species, which have declined because of anthropogenic habitat fragmentation, our meta-analyses might
possibly have overestimated the mean strength of relationships between population size, genetic variation
and fitness. However, this would make our data even
more relevant from a conservation point of view, where
species declining due to anthropogenic fragmentation
are of greatest interest and priority.
We found that male fitness tends to decrease more
strongly in small populations of self-incompatible
species than in self-compatible species, which suggests
higher pollinator limitation in small populations of selfincompatible species. Unfortunately, the interesting comparison between insect-pollinated and wind-pollinated
species was not possible because the examined plant
species included in our data were primarily insectpollinated and data from wind-pollinated species were
lacking almost completely.
The strength of the association between population
size and heterozygosity did not differ between selfcompatible and self-incompatible species, but the numbers
of alleles and polymorphic loci decreased more strongly
in small populations of self-incompatible species. Inbreeding within populations, estimated as the inbreeding
coefficient FIS, increased, however, with population size
in self-incompatible species, but not in self-compatible
species. These findings may possibly be explained by lower
ratios of effective genetic population sizes to census
population sizes in self-incompatible species than in
self-compatible species. Such differences in the ratios
between effective and census population size could be
caused by larger annual fluctuations in the sizes of selfincompatible species due to unreliable pollination in
some years, or by higher genetic substructuring of large
populations of self-incompatible species (Frankham
1995). However, published information is not sufficient
to test these hypotheses.
A positive association between fitness and the mean
level of genetic variation was found in self-incompatible
but not in self-compatible species. This may reflect
decreased availability of suitable mating partners in
small populations of self-incompatible plants due to
reduced genetic variation at the self-incompatibility
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Plant population
size, fitness and
genetic variation
loci (Fischer et al. 2003; Willi et al. 2005). Moreover,
because in self-compatible species inbreeding could be
high in all populations irrespective of their size, the level
of direct and biparental inbreeding may not increase as
much in small populations of self-compatible species
compared with self-incompatible species. Consequently,
if fitness is associated with genetic variation, this association should be stronger for self-incompatible than for
self-compatible species. Self-compatible species may
also be less susceptible to the negative effects of small
population size if a long history of inbreeding has
enabled purging of the genetic load (Busch 2005). Our
results suggest that in general the negative effects of
small population size are indeed less detrimental in
self-compatible species. Furthermore, our results are
in contrast to the idea that the breakdown of selfincompatibility in small populations would erase the
differences in the strength of the associations of population size, genetic variation and plant fitness between
self-compatible and self-incompatible species.
Conclusions
The close relationships between population size, genetic
variation and fitness imply that population size should
be taken into account in any multipopulation study of
plant fitness or genetic variation.
The observed generality of positive relationships between
population size, plant fitness and genetic diversity clearly
implies that the negative effects of habitat fragmentation on plant fitness and genetic variation are common.
Moreover, the stronger positive associations observed
in self-incompatible species and, to some degree, also in
rare species suggest that these species are most prone to
the negative effects of habitat fragmentation.
The small and sometimes unequal sample sizes in
some of our analyses suggest that the according results
and conclusions, especially on the relationship between
plant fitness and genetic variation within populations,
should be considered preliminary. At the same time this
indicates a need for future research. Our study revealed
a number of further gaps in our knowledge of relationships between population size, genetic variation and
fitness. In addition to observational studies, experiments
should address the relative importance of the potential
causal genetic and ecological mechanisms underlying the
relationships between population size, genetic variation
and fitness. Therefore, field studies should increasingly be
complemented by common environments. Moreover,
studies that also consider population history will be
highly valuable. Furthermore, quantitative genetic
variation in addition to neutral molecular markers
should be measured.
© 2006 The Authors
Journal compilation
© 2006 British
Ecological Society,
Journal of Ecology,
94, 942–952
Acknowledgements
We thank H. Prentice, L. Haddon and three anonymous
reviewers for constructive comments. This study was
supported financially by the Academy of Finland.
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Handling Editor: Honor Prentice
Supplementary material
The following supplementary material is available
online from http://www.Blackwell-Synergy.com
Appendix S1 Data used for the meta-analyses of relationships between population size, fitness and genetic
variation.
Appendix S2 Studies included in the meta-analyses of
the relationships between plant population size, fitness
and genetic variation.