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The significance of genetic erosion in the process of extinction. I. Genetic differentiation in Salvia pratensis and Scabiosa columbaria in relation to population size


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As part of a programme to determine the importance of the loss of genetic variation for the probability of population extinction, the amount of allozyme variation was determined in 14 populations of Salvia pratensis and in 12 populations of Scabiosa columbaria. Significant correlations were found between population size and the proportion of polymorphic loci (Salvia: r=0.619; Scabiosa: r=0.713) and between population size and mean observed number of alleles per locus (Salvia: r=0.540; Scabiosa: r=0.819). Genetic differentiation was substantially larger among small populations than among large populations: in Salvia GST was 0.181 and 0.115, respectively, and in Scabiosa 0.236 and 0.101, respectively. The results are discussed in relation to genetic drift, inbreeding and restricted gene flow.
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Heredity66 (1991) 181—189
Genetical Society of Great Britain Received 30Apr11 1990
The significance of genetic erosion in the
process of extinction.
I. Genetic differentiation in Salvia pratensis
and Scabiosa columbaria in relation to
population size
* Department of Genetics, University of Groningen, Kerklaan 30, 9751 NN Haren, and tDepartment of Plant Ecology,
Institute for Ecological Research, P.O. Box 40, 6666 ZG Heteren, The Netherlands
As part of a programme to determine the importance of the loss of genetic variation for the
probability of population extinction, the amount of allozyme variation was determined in 14
populations of Salvia pratensis and in 12 populations of Scabiosa columbaria. Significant correla-
tions were found between population size and the proportion of polymorphic loci (Salvia:
r= 0.619; Scabiosa: r= 0.713) and between population size and mean observed number of alleles
per locus (Salvia: r =0.540; Scabiosa: r = 0.819). Genetic differentiation was substantially larger
among small populations than among large populations: in Salvia GST was 0.181 and 0.115,
respectively, and in Scabiosa 0.236 and 0.101, respectively. The results are discussed in relation to
genetic drift, inbreeding and restricted gene flow.
Keywords: conservation biology, extinction, genetic erosion, population size, Salvia pratensis,
Scabiosa columbaria.
Dueto the activities of man, populations of many plant
and animal species have become small, fragmented and
isolated. Research is needed to develop effective
measures for conservation. Until the beginning of the
last decade conservation was mainly the domain of
ecologists, but recently much attention has been
focused on the importance of the population genetic
aspects (Soulé & Wilcox, 1980; Frankel & Soulé, 1981;
Schonewald-Cox et a!., 1983; Soulé, 1986, 1987).
Population genetic theory predicts that, as a con-
sequence of genetic drift and inbreeding, small popula-
tions will have decreased levels of genetic variation.
Even favourable alleles may be lost and the potential to
adapt to a changing environment may be seriously
diminished (Vrijenhoek, 1985). Moreover, inbreeding
results in increased levels of homozygosity which may
cause inbreeding depression (Frankel R., 1983). Both
processes may thus lead to 'genetic erosion', reduce the
fitness of individuals in a population and increase the
chance of the extinction of the population. Ultimately
this may lead to the extinction of the species. The
deleterious effects of genetic erosion in populations,
however, can be counteracted by gene flow renewing
the genetic variation.
Because experimental data about the significance of
genetic erosion in extinction are virtually absent, we
started a project to examine these processes in two
plant species in The Netherlands: Salvia pratensis and
Scabiosa columbaria. These species were selected
because: (i) the number of populations has significantly
declined in the last decades, (ii) they occur in both
small and large populations, (iii) both are thought to be
predominantly outbreeding. The research described in
this paper is part of a comprehensive research project
to determine the importance of genetic factors for
population extinction and to develop effective manage-
ment measures that could prevent species from becom-
ing extinct. In this paper we present data on the amount
of allozyme variation and the extent of genetic differen-
tiation in relation to population size.
Materials and methods
Both Salvia pratensis and Scabiosa columbaria are
gynodioecious, protandric perennials and are diploid
with 2n= 18 (Tutin eta!., 1972) and 2n= 16 (Tutin et
a!., 1976), respectively. Salvia occurs in dry, sunny,
calcareous grassland on river dunes and dikes,
Scabiosa in dry, grassy places on calcareous soils. The
number of (1 X 1 km) grid squares in which Salvia and
Scabiosa was observed, declined between 1950 and
1980 from 92 to 78 and from 82 to 52, respectively
(Mennema et a!., 1985). In 1988 only 39 populations
of Salvia and 24 populations of Scabiosa were
recorded (Ouborg eta!., 1989).
The location of the populations examined is given in
Fig. 1. The mean distance between the examined
populations and their nearest neighbouring population
was 4 km for Salvia and 7 km for Scabiosa. Because
both species are pollinated mainly by bees, which are
known to forage within considerably smaller distances
(Levin & Kerster, 1974), gene flow between popula-
tions by means of pollen was expected to be restricted.
Because seeds of both species have no special means of
transport, seed dispersal may even be less important
(Levin & Kerster, 1974).
In 1988, the size of small populations was deter-
mined by counting the total number of flowering indivi-
duals, whereas the size of large populations was
estimated by stratified sampling of square metres and
the subsequent extrapolation to total population area.
Populations were grouped in two distinct size classes
(small and large populations). This classification,
however, was partly arbitrary. Criteria were such that
the difference in population size between the largest
small population and the smallest large population had
to be substantial and that the difference in number of
populations in each size class had to be as small as
possible (Table 1).
Individual plants were sampled in all populations in
1988 by cutting pieces of leaf material. In small
populations as many plants as possible were sampled,
whereas in large populations about 50 individuals were
sampled with regular spacing, using the whole popula-
tion area. The samples were put in plastic bags with a
small amount of water and kept in a portable cooler. In
the laboratory the samples were stored in a refrigerator
(4°C) until the moment of electrophoretic analysis. The
activity of the enzymes remained sufficiently high for at
least 3 weeks. Of the 29 enzyme systems tested for
electrophoresis, 10 showed a sufficiently clear pattern
and were used for genetic analyses (Table 2).
Buffer systems. Tris-citrate pH 7.0, LiOH-borate pH
8.3 and Iris-borate EDTA pH 8.6. Apart from GPI,
lCD and PGD for Salvia, which were performed on
polyacrylamide, electrophoretic analyses were carried
out on starch gels. Electrophoretic methods and
recipes for buffers (except tris-borate EDTA pH 8.6)
and staining solutions (except SORDH) are described
Fig. 1 Location of the examined populations of Salvia pratensis (a) and Scabiosa columbaria (b) in The Netherlands. For
Salvia, the following three locations consisted of two (sub )populations (their interpopulational distances given between
brackets): 1(320 m), c (580 m) and b (160 m).
(a) (b)
030 60km 030 60km
Table 1 Examined populations of Salvia and Scabiosa with their abbreviated name
(A), number of flowering (N) and sampled (n) individuals. Populations are grouped
according to size (see text)
Small populations (A) NnLarge populations (A) Nn
SalviaForten 1 ft 5501st o300 49
Forten 2 f2 14 14 Ruitenberg r300 50
Neerijnen n 17 17 Cortenoever 2 c2 310 66
Lexmond 130 20 Wilpse klei w400 50
Hoenwaard h46 34 Bijiand 2 b2 1000 36
Bijiand 1 b1 60 14 Koekoekswaard k1500 60
Cortenoeverl c1 60 10
Piekenwaard p61 43
Scab iosa
Hoenwaard h14 6 Terwolde t200 50
Kwartierse dijk kw 35 25 Wilpse klei wi 200 50
Ruitenberg r90 42 Bemelerberg b300 50
Kannerhei k 100 21 Wolfskop wo 25000 48
Zalk z118 30 01stJulianagroeve
Table 2 Enzymes studied and buffer-systems used for Salvia and Scabiosa
Enzyme Abbreviation E.C. number
Buffer pH
Salvia Scabiosa
Sorbitoldehydrogenase SORDH 8.3
Malic enzyme ME 8.3
Isocitratedehydrogenase lCD 7.0
Phosphogluconate dehydrogenase PGD 7.0 7.0
Peroxidase PEROX 8.6
Glutamate—oxaloacetate transaminase GOT 8.3 8.3
Phosphoglucomutase PGM 8.6 8.6
Aconitase ACN 8.6
Triose phosphate isomerase TPI 8.6 8.3
Glucose phosphate isomerase GPI 7.0 7.0/8.6
in Hofman (1988). The recipe of the tris-borate EDTA
buffer-system pH 8.6 was: 12.11 g Tris/1 aquadest
(0.1 M), 1.86 g EDTA/1 aquadest (0.005 M), adjust to
pH 8.6 with boric acid. The staining solution of
SORDH was: 50 ml 0.06 M Tris-HC1 pH 8.1 (7.27 g
Tris/1 aquadest, adjust to pH 8.1 with 25 per cent HC1),
125 mg sorbitol, 20mg NAD, 5 mg MTT, 1 mg PMS,
50 mg pyrazol and 50 mg sodium pyruvate. Because of
the complexity of some enzyme-activity patterns, due
to the presence of a gene duplication (R. Van Treuren
& R. Bijlsma, in preparation), electrophoresis of
Scabiosa for GPI was performed on two buffer
systems. On tris-citrate pH 7.0 electrophoretic mobility
was higher (better separated bands), whereas tris-
borate EDTA pH 8.6 gave a higher resolution (sharper
Estimation of genetic variation
Toestimate the amount of genetic variation, the follow-
ing measures were calculated: (i) the proportion of
polymorphic loci (P), (ii) the mean observed number of
alleles per locus (A0) and (iii) gene diversity (He). A
locus was considered polymorphic if the frequency of
the most frequent allele was less than 0.99. Gene
diversity and standard genetic distance were computed
according to Nei (1987) in which corrections were
made for small sample sizes.
Enzyme variability is given in Table 3. Because the
allelic variation and number of subunits of Pgd-2 for
Scabiosa was only recently established, the results for
this locus were omitted from the genetic analyses. In
order to determine if the inheritance of the allozymes
was Mendelian, crosses were performed with plants
grown from seeds collected in 1987. Because not all
genotypes were represented in the seed samples, only
the relatively frequent variants could be tested (Table
4). No significant deviation from Mendelian inheri-
tance was found for any of the loci examined. Indepen-
dent segregation was observed for most loci, strong
linkage was only found between Pgd-1 and Gpi-2 of
Scabiosa. Recombination between these loci was
estimated to occur at a frequency of about 6 per cent
(R. Van Treuren & R. Bijisma, in preparation).
To establish the relationship between population
size and the amount of genetic variation, corrections
for differences in sample size were calculated in two
different ways. Firstly, Spearman's rank correlation
Table 3 Enzyme variability of Salvia and Scabiosa. Loci coding for similar enzymes
were numbered in ascendence according to the electrophoretic mobility of their
gene products. Alleles were named according to their relative position to the N
(normal) allele, which was present in every population and which was usually the
most frequent. I was intermediate between S (slow) and N, 12 between N and F
Salvia Scabiosa
Locus Isozyme
structure Alleles Locus Isozyme
structure Alleles
5, NS,11,N
N5, N, F
5, N, F
S, N, F
S, N, F
5, N, F
S,NS, N5, NS, N, F
S, N5, N, F
Table 4 Parental genotypes (P) and genotype numbers in the F1-generation with Chi-square values for the deviation from
Mendelian segregation
Salvia Scabiosa
Locus Pgd-2 Perox Got-i Got-2 Pgm-i Pgm-2 Tpi-1 Pgd-1 Got-i Tpi-i Gpi-i Gpi-2
F1 SN 7
SF 14
NN 9
NF 7
NF 11
FF 8
SS 6
SN 20
NN 16
SS 5
SN 15
NN 9
NN 9
NF 13
FF 7
NI2 15 11N19
NN 18 SS 22
SN 61
NN 24
SS 23
SN 58
NN 26
SS 16
SN 41
NN 12
SS 8
SN 16
NN 10
NF 40
FF 15
x2 3.541 1.966 4.857 1.138 0.586 1.324 0.027 2.178 0.925 2.913 0.353 1.000
1-00 10 00 000 lOOC
(b ••••
10 00 1000 i00C
I10 100 1000 10000 - 0
PpulQtion size
100 000 10000 100000
Popu'ation size
coefficients were calculated between population size,
sample size and the amount of genetic variation. Sub-
sequently, by keeping sample size constant, the partial
correlation coefficients (Sokal & Rohlf, 1981) between
population size and the amount of genetic variation
were computed. Significant correlations were found
between population size and the proportion of poly-
morphic loci (Salvia: r=0.807, t=4.534, P<0.0005;
Scabiosa: r'0.622, t=2.386, 0.01<P<0.025) and
between population size and the mean observed
number of alleles (Salvia: r=0.570, t=2.303,
0.01 <P< 0.025; Scabiosa: r= 0.653, t=2.584,
0.01 <P< 0.025), although it should be stressed that P
and A0 are not independent measures. However, no
significant correlation was found between population
size and gene diversity (Salvia: r=0.051, t=0.169,
0.4<P; Scabiosa: r0.135, t0.410, 0.3<P<0.4).
Secondly, repeated samples of equal size were taken
from the master file (Salvia: sample size =5; Scabiosa:
sample size =6), the number of repetitions in each
population were determined by the original sample
size. Subsequently, the mean values of P, A0 and He
were used in a weighted regression (Fig. 2). Again,
significant positive correlations were found between
the population size and proportion of polymorphic loci
(Salvia: r= 0.6 19, t=2.73, 0.005 <P< 0.01; Scabiosa:
r 0.713, t=3.21, 0.001 <P< 0.005) and between
population size and the mean observed number of
alleles (Salvia: r=0.540, t=2.22, 0.01<P<0.025;
Scabiosa: r= 0.819, t=4.51, 0.0005 <P< 0.001), but
not between the population size and gene diversity
(Salvia: r=0.309, t=1.12, 0.1<P<0.15; Scabiosa:
r=0.490, t=1.78, 0.05<P<0.075). The lack of
correlation between the population size and He in both
species was mainly due to the smallest population
showing a relatively high value and the largest popula-
tion showing a relatively low value.
To establish the extent of genetic differentiation
Scab ass
10 10 100 000 10000 100000
10 000 000 0000 00000
0-2C c)
0-15 II
0-05 r0 490
Fig. 2 Weighted regression of proportion of polymorphic loci (a), mean observed number of alleles (b) and gene diversity
(c) on population size (log scale) for both Salvia and Scabiosa. r is the correlation coefficient.
Table 5 Analysis of gene diversity (Nei, 1987) in populations of Salvia and Scabiosa, together with the Chi-square value of G1
for the deviation from zero. The coefficient of gene differentiation (GST ) is the proportion of the total gene diversity (HT) that
can be attributed to the average gene diversity between populations (HT —Ha). Deviation of GST from 0 (no differentiation) was
tested by using the Chi-square test of heterogeneity of gene frequencies (Workman & Niswander, 1970)
Salvia Scabiosa
Locus HT HGST x2 Locus HT H5 GST x2
Allpopulations Sordh
Populations (all loci)
All 0.136 0.115 0.156 0.129 0.107 0.175
Small 0.128 0.105 0.181 0.131 0.100 0.236
Large 0.144 0.127 0.115 0.124 0.112 0.101
*001 <P<0.025.
P< 0.0005.
among populations, an analysis of gene diversity was
performed (Table 5). Significant differentiation was
found for alllociof both species. For all loci combined,
GST was 0.156 and 0.175 for Salvia and Scabiosa,
respectively. A subsequent analysis of gene diversity hi
the group of small populations and in the group of
large populations showed that the coefficient of gene
differentiation was substantially higher in the group of
small populations (Salvia: G5T=O.lSl and 0.115,
respectively; Scabiosa: GST = 0.236 and 0.101, respec-
The basic assumption underlying our research project
was the hypothesis that, as a consequence of genetic
drift, inbreeding and restricted gene flow, small and
isolated populations show decreased levels of genetic
variation. The smaller number of variable loci and the
smaller number of alleles found in the small popula-
tions are in agreement with this prediction. Similar
results have been reported by Hamrick et at. (1979),
Levin etal. (1979), Schmidtke & Engel (1980), Moran
& Hopper (1983) and Karron (1987). No significant
correlation was found between population size and
gene diversity. However, 'rare' alleles reach high
frequencies (possibly due to genetic drift) only in small
populations. This effect will inflate He in small popula-
tions and consequently weaken the correlations
between He and the population size. Therefore, gene
diversity appears not to be a useful comparative
measure of genetic variation in small populations.
Moreover, many other population characteristics, such
as population structure (neighbourhood size, relative
plant density, etc.), effective population size and breed-
ing system might affect not only He but also the other
measures of genetic variation. Varvio-Aho (1981) for
example showed that gene diversity in the Finnish
watertrider was not correlated with population size
but clearly with effective population size. The impact of
these other population characteristics is currently
being investigated.
If genetic drift predominantly affects allelic fre-
quencies in populations, and levels of gene flow
between populations are low, population genetic
theory predicts genetic differentiation between popula-
tions. The results of the analysis of gene diversity agree
with this prediction. Loveless & Hamrick (1984)
analysed the available data that describes genetic
differentiation from a large number of studies and
computed the mean GST values for a number of
variables. They found that GST was 0.118, 0.109 and
0.077 for predominantly outcrossing species (n =76),
dioecious species (n =3) and long-lived perennials
(n =48), respectively. The mean GST of 43 predomi-
nantly outcrossing, long-lived perennials was 0.068.
Compared to these values, Salvia (GST= 0.156) and
Scabiosa (GST =0.175) show substantial genetic differ-
entiation, probably resulting from a significant amount
of genetic drift in the small populations. This explana-
tion is supported by the finding that small populations
are more differentiated from each other than are large
populations. Together with the observation that
average gene diversity did not differ substantially
between the group of small and large populations
(Table 5), our results are similar to those of Brakefield
(1989). Rich et a!. (1979) also found a significant
increase in the variance of allelic frequencies among
populations due to genetic drift and showed that this
increase was inversely proportional to population size.
This agrees with our observation that the rare alleles
are found in high frequency only in small populations,
resulting in larger variances of allelic frequencies and
subsequently larger GST values in the group of small
If allelic frequencies in populations are predomi-
nantly affected by genetic drift and gene flow between
populations is restricted, it is also to be expected that
genetic differentiation occurs even within relatively
short distances. No significant correlations are found
between geographic and genetic distances (Salvia:
r= —0.022, t= —0.206, P<0.4; Scabiosa: r=0.167,
t=1.357, 0.075<P<0.1), which suggests that gene
flow is indeed restricted. The genetic structure of both
species resembles an island model of population struc-
ture, as found for Desmodium nudi:florum (Schaal &
Smith, 1980) and Sarracenia purpurea (Schwaegerle &
Schaal, 1979), where populations are geographically
isolated from each other with the chance of gene flow
between populations being greatly reduced.
Estimates of the average level of gene flow between
natural populations can be derived from the GST values
(Slatkin & Barton, 1989). GST values of 0.156 (Salvia)
and 0.175 (Scabiosa) are equivalent to Nm= 1.166 and
Nm =0.990 respectively, which means about only one
migrant every generation. It has been suggested that the
exchange of a single individual per generation among
small endangered (sub)populations is sufficient to have
them behave almost as one panniictic population (e.g.
Franklin, 1980; Frankel & Soulé, 1981; Allendorf,
1983; and Frankel, 0.11., 1983). This general guideline
for the management of small populations has been
deduced from the equilibrium theory of Wright's
infinite island model (Wright, 1931). However, popula-
tions are generally not in equilibrium and the number
of subpopulations is often small. Therefore, Varvio et
a!. (1986) studied the dynamics of genetic differentia-
tion by using the finite island model and showed that
the values of H, HT and GST in transient populatioils
depend on the pattern of population subdivision and
that it may take time for them to approximate the equi-
librium values. Furthermore, the problem is compli-
cated, among others, by fluctuating population sizes,
subdivision and extinction of subpopulations. They
therefore concluded that a single guideline, e.g. the 'one
migrant per generation' rule, is not theoretically well
In practice it is difficult to separate the role of selec-
tive and non-selective forces in genetic differentiation
(Varvio-Aho, 1983). A way to examine the problem is
to investigate whether the gene frequency variation is
homogeneous over loci. If so, genetic differentiation
is most likely to be the result of random processes
because they affect all loci simultaneously and to the
same extent (Lewontin & Krakauer, 1973; Schaal,
1975; Varvio-Aho, 1983). FST values for individual
alleles range from 0.031 to 0.243 (Salvia) and from
0.018 to 0.450 (Scabiosa). The ratio observed/
expected variance in FST which is Chi-square/d.f.
distributed (Lewontin & Krakauer, 1973) is 2.264
(0.0005 <P< 0.00 1) and 3.332 (P< 0.0005) for Salvia
and Scabiosa respectively, indicating that the differen-
tiation of gene frequencies is clearly non-random. It
seems unlikely, therefore, that the genetic constitution
of both species can be entirely accounted for by
random processes.
The amount of allozyme variation is clearly corre-
lated with population size, the small populations being
less variable. The genetic structure of Salvia and
Scabiosa in The Netherlands can most satisfactorily be
explained by an island model of population structure,
with restricted gene flow between populations. This
may imply that: (i) small populations are also less
variable with respect to favourable alleles and/or fixed
for deleterious ones, as a result of genetic drift and
inbreeding, and/or (ii) small populations have reduced
evolutionary potential but are well adapted to their
current environment, as a result of selective forces.
Experiments are planned to reveal whether: (i) plants in
small populations show decreased fitness due to
inbreeding depression, and/or (ii) plants in small
populations experience different environmental condi-
tions to which they have become adapted. The out-
come of these experiments will be used to evaluate the
effectiveness of measures proposed to restore the level
of genetic variation. Hybridization of populations, for
example, will increase genetic variability and fitness
when populations are suffering from inbreeding
depression but will result in outbreeding depression
(Templeton, 1986) when populations have been
adapted to differential local conditions.
We would like to thank an anonymous reviewer for
constructive comments on the manuscript and A. C.
Boerema, J. Haeck and K. Reinink for support in
carrying out the experiments. This research project is
partly subsidized by the Ministry of Agriculture,
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... Small, fragmented plant populations often have reduced genetic diversity, which risks elevating inbreeding and genetic drift within populations (Templeton et al. 1990;van Treuren et al. 1991;Heywood 1993;Furlan et al. 2012;Neaves et al. 2015). Inbreeding and genetic drift are particularly concerning for small populations because they can increase the prevalence of disease (O'Brien and Evermann 1988;Hajjar et al. 2008). ...
... Inbreeding and genetic drift are particularly concerning for small populations because they can increase the prevalence of disease (O'Brien and Evermann 1988;Hajjar et al. 2008). Genetic erosion is the reduction in effective population size within a population over time; where infrequently occurring alleles are likely to be lost, further hindering population survival by reducing adaptive potential (van Treuren et al. 1991). In addition, populations an important representative of Australian botanical diversity (Jusaitis and Adams 2005;Clarke et al. 2013;Bickerton et al. 2018). ...
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Understanding population structure and genetic diversity is important for designing effective conservation strategies. As a critically endangered shrub, the six remaining extant populations of spiny daisy ( Acanthocladium dockeri ) are restricted to country roadsides in the mid-north of South Australia, where the species faces many ongoing abiotic and biotic threats to survival. Currently the spiny daisy is managed by selecting individuals from the extant populations and translocating them to establish insurance populations. However, there is little information available on the genetic differentiation between populations and diversity within source populations, which are essential components of planning translocations. To help fill this knowledge gap, we analysed population structure within and among all six of its known wild populations using 7,742 SNPs generated by a genotyping-by-sequencing approach. Results indicated that each population was strongly differentiated, had low levels of genetic diversity, and there was no evidence of inter-population gene flow. Individuals within each population were generally closely related, however, the Melrose population consisted entirely of clones. Our results suggest genetic rescue should be applied to wild spiny daisy populations to increase genetic diversity that will subsequently lead to greater intra-population fitness and adaptability. As a starting point, we suggest focussing on improving seed viability via inter-population crosses such as through hand pollination experiments to experimentally assess their sexual compatibility with the hope of increasing spiny daisy sexual reproduction and long-term reproductive fitness.
... Genetic theory predicts that such populations are highly susceptible to extinction due to stochastic events (Lynch et al., 1995) and lack of connectivity reducing habitat recolonization. Furthermore, fragmented populations are particularly prone to experience inbreeding and loss of genetic diversity, a process referred to as genetic erosion (Rogers, 2004;Van Treuren et al., 1991). Fueled by impaired dispersal and geneflow (Frankham, 2005;Goldingay et al., 2013), this can lead to a decrease in fitness and evolutionary adaptive potential (Bijlsma & Loeschcke, 2012;Leroy et al., 2018;Van Treuren et al., 1991). ...
... Furthermore, fragmented populations are particularly prone to experience inbreeding and loss of genetic diversity, a process referred to as genetic erosion (Rogers, 2004;Van Treuren et al., 1991). Fueled by impaired dispersal and geneflow (Frankham, 2005;Goldingay et al., 2013), this can lead to a decrease in fitness and evolutionary adaptive potential (Bijlsma & Loeschcke, 2012;Leroy et al., 2018;Van Treuren et al., 1991). Ultimately, without counteracting the genetic consequences of habitat loss and fragmentation, we risk witnessing extirpation and ultimately species extinction (Bijlsma & Loeschcke, 2012;Ceballos et al., 2017;Frankham, 2005;Goldingay et al., 2013;Spielman et al., 2004). ...
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Fragmentation of habitat is a major threat across a wide range of taxa. Subsequent effects include reduced population sizes and isolation of populations. Both can have detrimental consequences for populations as they increase the risk of genetic erosion. While it is critical to prevent and, if required, reverse genetic erosion, we often lack adequate data to assess whether and how much genetic erosion has occurred. Here, we present a genetic monitoring study where we investigated changes in genetic diversity and genetic patterns in a threatened, specialist mammal, the koala (Phascolarctos cinereus). Our study population inhabits an increasingly fragmented landscape and has experienced a sharp decline in population size within the past three decades. We used 1038 single nucleotide polymorphic loci (SNPs) to compare measures of genetic diversity between samples collected in 2018 and in 2006 (two generations prior) and investigated simultaneous changes in the environment. We found a decline in both heterozygosity and effective population size (Ne), and an increase in sub‐structuring, average relatedness, and inbreeding (FIS) alongside an increasingly threatening and more fragmented environment. Given the extent of genetic erosion in only two generations, we urge consideration for the implementation of mitigation measures for this population and for threatened populations in similar conditions. Our study further emphasizes the importance of effective management of at‐risk populations including monitoring of genetic erosion. Wildlife populations around the globe are impacted by anthropogenic actions. Many vulnerable species have experienced a loss of genetic diversity over the past decades. This study found evidence of loss of genetic diversity alongside other negative effects in a population of a specialist mammal, likely due to anthropogenic impacts.
... Each flower can produce up to four nutlets which drop from the calyces once they mature and dry (Scott, 1989). Barochory (seed dispersal by gravity alone) is considered the chief dispersal route for S. pratensis and most seeds fall close to the parent plant (Diacon-Bolli et al., 2013;Ouborg et al., 1991;van Treuren et al., 1991). ...
... Both British and Dutch S. pratensis populations are now generally only found in places protected by conservation efforts (Hegland et al., 2001;Ouborg & van Treuren, 1995;Rich et al., 1999). Since the 1950s, the number of British populations has remained almost constant, restricted to sites managed with more traditional, less intensive farming practices (Rich et al., 1999 (Ouborg & van Treuren, 1994;Ouborg et al., 1991;van Treuren et al., 1991). In the British Isles, Kay and John (1995) (Scott, 1989). ...
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This account presents information on all aspects of the biology of Salvia pratensis L. (Meadow Clary) that are relevant to understanding its ecological characteristics and behaviour. The main topics are presented within the standard framework of the Biological Flora of the British Isles: distribution, habitat, communities, responses to biotic factors, responses to environment, structure and physiology, phenology, floral and seed characters, herbivores and disease, history, and conservation. Salvia pratensis is an erect, rosette‐forming, perennial herb with a broad native distribution covering much of Europe – from the British Isles, Spain and Morocco in the west, across Europe into Asia, as far east as the Urals. In the British Isles, the species is nationally scarce, confined to a few south‐ to west‐facing sites with calcareous soils in Southern England and one site in Wales. It is predominately found in unimproved pasture, hay meadows and grassy verges, but can occur on the fringes of scrub or woodland. Although the species is abundant in central Europe, changes to land management since the mid‐twentieth century have resulted in fragmented and threatened populations in several European countries. It is cultivated as an ornamental, as is S. × sylvestris, the hybrid with S. nemorosa. Populations are typically gynodioecious, having both female (male‐sterile) and hermaphrodite individuals at variable proportions. The species has a mixed mating system and is self‐compatible via insect pollination, but predominantly outcrosses. Honeybees and bumblebees are abundant pollinators, but a diverse range of bee species and other insect species visit S. pratensis flowers. Inbreeding depression has been documented, presenting a conservation concern for small, fragmented populations. The species is the focus of conservation efforts and has been reintroduced to sites where it had become locally extinct in Britain. To sustain favourable habitat, site management should maintain low soil nutrient levels, and prevent scrub encroachment and the dominance of coarse grasses. The removal of sward by hay cutting or grazing after plants have flowered and set seed is advised, in addition to maintaining a degree of disturbance to provide bare patches of soil for seedling recruitment.
... Furthermore, habitat fragmentation can change the spatial distribution of plants, which in turn changes foraging patterns of pollinators (Cresswell, 1997). If the distance between plants to be pollinated is too large, pollination is limited (Schmitt, 1983;Klinkhamer et al., 1989) and plant fitness may be reduced due to inbreeding and/or outbreeding depression caused by increased genetic drift (Waser and Price, 1983;Van Teuren et al., 1991;Holsinger, 1993;Percy and Cronk, 1997;Gigord et al., 1999). Thus, a change in pollinator behaviour might strongly affect plant reproductive success and plant fitness. ...
... Comparatively few studies have interrogated the relationships between population genetics and population dynamics directly, in part because collection of complementary genetic and demographic data is uncommon (Bozzuto et al., 2019;Freitas et al., 2020;Heschel & Paige, 1995;Richards et al., 2003). Further, when such relationships are studied, proxy measurements for genetic variation (e.g., population size [Fischer & Matthies, 1998;Menges, 1991]) and/or demographic performance (e.g., individual fitness components [Heschel & Paige, 1995;Jiménez et al., 1994;Menges;1991;Oostermeijer et al., 1994], population size [van Treuren et al., 1991]) are often used instead of more directly relevant metrics such as quantitative estimates of standing genetic variation and long-term population growth rates. Finally, even those studies that do explicitly characterize both genetic and demographic patterns across populations rarely assess the relationships among these metrics, treating them instead as separate lines of evidence to consider when making management decisions (Schemske et al., 1994) or comparing the outcomes of experiments or demographic simulations manipulating genetic variation categorically, at coarse scales (e.g., increased vs. decreased ID [Johnson et al., 2011]; with or without translocations from genetically diverse populations [Madsen et al., 1999;Westemeier et al., 1998]). ...
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Quantifying relationships between genetic variation and population viability is important from both basic biological and applied conservation perspectives, yet few populations have been monitored with both long‐term demographic and population genetics approaches. To empirically test whether and how genetic variation and population dynamics are related, we present one such paired approach. First, we use eight years of historical demographic data from five populations of Boechera fecunda (Brassicaceae), a rare, self‐compatible perennial plant endemic to Montana, USA, and use integral projection models to estimate the stochastic population growth rate (λS) and extinction risk of each population. We then combine these demographic estimates with previously published metrics of genetic variation in the same populations to test whether genetic diversity within populations is linked to demographic performance. Our results show that in this predominantly inbred species, standing genetic variation and demography are weakly positively correlated. However, the inbreeding coefficient was not strongly correlated with demographic performance, suggesting that more inbred populations are not necessarily less viable or at higher extinction risk than less inbred populations. A contemporary re‐census of these populations revealed that neither genetic nor demographic parameters were consistently strong predictors of current population density, although populations showing lower probabilities of extinction in demographic models had larger population sizes at present. In the absence of evidence for inbreeding depression decreasing population viability in this species, we recommend conservation of distinct, potentially locally adapted populations of B. fecunda rather than alternatives such as translocations or reintroductions.
... This differentiation is likely due to strong genetic drift in the very small wild population, which at the time of sampling consisted of 20 individuals and may have been even smaller at some times during the 30 years since seeds were collected the first time. Small population size usually leads to reduced genetic diversity within populations and increased differentiation among populations (van Treuren et al., 1991;Wei and Jiang, 2020). Genetic erosion depends on the number of generations and may be much less pronounced in long-lived plants (e.g., Rosche et al., 2018). ...
Premise: Ex situ cultivation is important for plant conservation, but cultivation in small populations may result in genetic changes by drift, inbreeding or unconscious selection. Repeated inbreeding potentially influences not only plant fitness, but also floral traits and interactions with pollinators, which has not yet been studied in an ex situ context. Methods: We studied the molecular genetic variation of Digitalis lutea L. from a botanic garden population cultivated for 30 years, a frozen seed bank conserving the original genetic structure, and two current wild populations including the source population. In a common garden we studied the effects of experimental inbreeding and between-population crosses on performance, reproductive traits and flower visitation of plants from the garden and a wild population. Results: Significant genetic differentiation was found between the garden population and the wild population from which the seeds had originally been gathered. After experimental selfing, inbreeding depression was only found in germination and leaf size of plants from the wild population, indicating a history of inbreeding in the smaller garden population. Moreover, garden plants flowered earlier and showed floral traits related to selfing, whereas wild plants showed traits related to attracting pollinators. Bumblebees visited more flowers of outbred than inbred plants and of wild than garden plants. Conclusions: Our case study suggests that high levels of inbreeding during ex situ cultivation can influence reproductive traits and thus interactions with pollinators. Together with the effects of genetic erosion and unconscious selection this may affect the success of reintroductions into natural habitats. This article is protected by copyright. All rights reserved.
... These factors could also alter the abundance and behavior of pollinators and restrict seed dispersal [5,6]. The primary changes during habitat fragmentation include reduced population sizes and increased spatial isolation among populations [7]. Consequently, a deleterious erosion of genetic diversity and intensification of inter-population divergence would occur by random genetic drift, elevated inbreeding, and decreased inter-population gene flow [8,9]. ...
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Glaciation and mountain orogeny have generated new ecologic opportunities for plants, favoring an increase in the speciation rate. Moreover, they also act as corridors or barriers for plant lineages and populations. High genetic diversity ensures that species are able to survive and adapt. Gene flow is one of the most important determinants of the genetic diversity and structure of out-crossed species, and it is easily affected by biotic and abiotic factors. The aim of this study was to characterize the genetic diversity and structure of an alpine species, Festuca ovina L., in Xingjiang, China. A total of 100 individuals from 10 populations were analyzed using six amplified fragment length polymorphism (AFLP) primer pairs. A total of 583 clear bands were generated, of which 392 were polymorphic; thus, the percentage of polymorphic bands (PPB) was 67.24%. The total and average genetic diversities were 0.2722 and 0.2006 (0.1686-0.2225), respectively. The unweighted group method with arithmetic mean (UPGMA) tree, principal coordinates analysis (PCoA) and STRUCTURE analyses revealed that these populations or individuals could be clustered into two groups. The analysis of molecular variance analysis (AMOVA) suggested that most of the genetic variance existed within a population, and the genetic differentiation (Fst) among populations was 20.71%. The Shannon differentiation coefficient (G’st) among populations was 0.2350. Limited gene flow (Nm = 0.9571) was detected across all sampling sites. The Fst and Nm presented at different levels under the genetic barriers due to fragmentation. The population genetic diversity was significant relative to environmental factors such as temperature, altitude and precipitation.
Ongoing global warming, coupled with increased drought frequencies, together with other biotic drivers may have resulted in complex evolutionary adaptation. The resurrection approach, comparing ancestors raised from stored seeds with their contemporary descendants under common conditions, is a powerful method to test for recent evolution in plant populations. We used 21‐26‐year‐old seeds of four European plant species – Matthiola tricuspidata, Plantago crassifolia, Clinopodium vulgare and Leontodon hispidus – stored in seed banks together with re‐collected seeds from their wild populations. To test for evolutionary changes, we conducted a greenhouse experiment that quantified heritable changes in plant responses to drought and simulated insect herbivory. In three out of the four studied species, we found evidence that descendants evolved shorter life cycles through faster growth and flowering. Shifts in the osmotic potential and leaf dry matter content indicated that descendants also evolved increased drought tolerance. A comparison of QST vs. FST values, using ddRAD genotyping data, suggested that directional selection, and therefore adaptive evolution, was underlying some of the observed phenotypic changes. In summary, our study reveals evolutionary changes in plant populations over the last decades that are consistent with adaptation of drought escape and tolerance as well as herbivory avoidance.
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Crop diversity underpins the productivity, resilience, and adaptive capacity of agriculture. Loss of this diversity, termed crop genetic erosion, is therefore concerning. While alarms regarding evident declines in crop diversity have been raised for over a century, the magnitude, trajectory, drivers, and significance of these losses remain insufficiently understood. We outline the various definitions, measurements, scales, and sources of information on crop genetic erosion. We then provide a synthesis of evidence regarding changes in the diversity of traditional crop landraces on farms, modern crop cultivars in agriculture, crop wild relatives in their natural habitats, and crop genetic resources held in conservation repositories. This evidence indicates that marked losses, but also maintenance and increases in diversity, have occurred in all these contexts, the extent depending on species, taxonomic and geographic scale, and region, as well as analytical approach. We discuss steps needed to further advance knowledge around the agricultural and societal significance, as well as conservation implications, of crop genetic erosion. Finally, we propose actions to mitigate, stem, and reverse further losses of crop diversity.
ASSESSING GENETIC DIVERSITY AND POPULATION STRUCTURE OF THYME (Thymus schimperi RONNIGER) IN EASTERN, CENTRAL AND NORTHERN HIGHLANDS OF ETHIOPIA Tesfaye Woldesemayate1, Kassahun Tesfaye2, Eleni Shiferaw3 and Tesfaye Awas4 ABSTRACT Thymus schimperi Ronniger (Ethiopian thyme) is wild-growing endemic perennial herb which is rich in medicinally important metabolites. However, little is known about its genetic diversity and population genetic structure. Nine T. schimperi populations were collected from Bale, North Shewa and East Gojam zones of Ethiopia and analyzed using five ISSR markers. Seventy-seven amplicons showed an overall 100% polymorphism, corresponding to an average of 15.4 bands per primer. At the individual population level, the percentage of polymorphic loci (PPL) within population ranged from 63.64 % for Dargegne to 87.01 % for Rira population, with an average of 74%. Nei's genetic diversity (H) was 0.25 on average at the population level and 0.36 at the species level, while Shannon indices (I) were 0.39 and 0.54, respectively. Percentage of polymorphic bands (PPB) varied from 15.79% to 100% in different primers with an average of 75.2%. The Gst value for the overall loci was 0.31 indicating moderate differentiation among populations and lower gene flow (Nm = 1.133). AMOVA showed that total genetic variance, partitioned as 4%, 27% and 69% (P< 0.00) between populations from different regions, among populations within regions and within individual populations, respectively. Mantel’s test results with significance detected using ISSRs among all of the tested populations was; r =0.304 (P < 0.001,999 permutations). UPGMA cluster analysis indicated grouping of the populations regardless of their geographical locations. This is the first report to demonstrate the use of molecular markers for diversity analysis in Ethiopian thyme and the result obtained suggests an urgent need for conservation of the existing natural population and implement alternative measures to meet the market demand. Keywords: Ethiopian thyme, Endemic species, Genetic Diversity, Genetic Differentiation, ISSR marker,medicinal plant 1 Ethiopian Biodiversity Institute ,Addis Ababa Ethiopia E-mail:- 2 Addis Ababa University Addis Ababa , Ethiopia E-mail:- 3 Ethiopian Biodiversity Institute ,Addis Ababa Ethiopia 4 Ethiopian Biodiversity Institute ,Addis Ababa Ethiopia
Three methods for estimating the average level of gene flow in natural population are discussed and compared. The three methods are FST , rare alleles, and maximum likelihood. All three methods yield estimates of the combination of parameters (the number of migrants [Nm] in a demic model or the neighborhood size [4πDσ(2) ] in a continuum model) that determines the relative importance of gene flow and genetic drift. We review the theory underlying these methods and derive new analytic results for the expectation of FST in stepping-stone and continuum models when small sets of samples are taken. We also compare the effectiveness of the different methods using a variety of simulated data. We found that the FST and rare-alleles methods yield comparable estimates under a wide variety of conditions when the population being sampled is demographically stable. They are roughly equally sensitive to selection and to variation in population structure, and they approach their equilibrium values at approximately the same rate. We found that two different maximum-likelihood methods tend to yield biased estimates when relatively small numbers of locations are sampled but more accurate estimates when larger numbers are sampled. Our conclusion is that, although FST and rare-alleles methods are expected to be equally effective in analyzing ideal data, practical problems in estimating the frequencies of rare alleles in electrophoretic studies suggest that FST is likely to be more useful under realistic conditions.
The apportionment of genetic variation within and among populations of Desmodium nudiflorum (L) DC was determined. Allozyme frequencies within populations conform to Hardy-Weinberg expectations and no population substructure was detected. Within populations FST values average 0.015 and are not significant. Most of the genetic diversity within a population, 75%, is due to differences between individuals rather than differences between subpopulations. In contrast, there is significant genetic differentiation between populations. Standardized genetic variances average 0.165 Each population contains a unique set of polymorphic loci; loci which are polymorphic in more than one population have significant differences in gene frequencies. A large portion of the genetic diversity of the species, 47.4%, is not represented within individual populations. Genetic distances between populations average 0.014 and are independent of geographical distance. The genetic structure of D. nudiflorum is most similar to a random patchwork.