ArticlePDF Available

Hufford KM, Mazer SJ. Plant ecotypes: genetic differentiation in the age of ecological restoration. Trends Ecol Evol 18: 147-155

Authors:

Abstract and Figures

Recent studies illustrate the emerging field of restoration genetics, which is a synthesis of restoration ecology and population genetics. The translocation of organisms during the restoration of native ecosystems has provoked new questions concerning the consequences of sampling protocols and of intraspecific hybridization between locally adapted and transplanted genotypes. Studies are now underway to determine both the extent of local adaptation among focal populations and the potential risks of introducing foreign genotypes, including founder effects, genetic swamping and outbreeding depression. Data are needed to delineate ‘seed transfer zones’, or regions within which plants can be moved with little or no consequences for population fitness. Here, we address the revival of transplant and common garden studies, the use of novel molecular markers to predict population genetic consequences of translocation, and their combined power for determining appropriate seed transfer zones in restoration planning for native plant populations.
Content may be subject to copyright.
Plant ecotypes: genetic differentiation
in the age of ecological restoration
Kristina M. Hufford and Susan J. Mazer
Department of Ecology, Evolution, and Marine Biology, University of California, Santa Barbara, CA 93106, USA.
Recent studies illustrate the emerging field of restor-
ation genetics, which is a synthesis of restoration ecol-
ogy and population genetics. The translocation of
organisms during the restoration of native ecosystems
has provoked new questions concerning the conse-
quences of sampling protocols and of intraspecific
hybridization between locally adapted and transplanted
genotypes. Studies are now underway to determine
both the extent of local adaptation among focal popu-
lations and the potential risks of introducing foreign
genotypes, including founder effects, genetic swamping
and outbreeding depression. Data are needed to deline-
ate ‘seed transfer zones’, or regions within which plants
can be moved with little or no consequences for popu-
lation fitness. Here, we address the revival of transplant
and common garden studies, the use of novel molecular
markers to predict population genetic consequences of
translocation, and their combined power for determin-
ing appropriate seed transfer zones in restoration plan-
ning for native plant populations.
The preservation of native plant communities must
include their restoration if land managers and conserva-
tion biologists are to counter the pressures of urban
development and the threat of invasive exotic species.
However, restoration ecology is a relatively young science
and few criteria exist for the creation of self-sustaining
populations that retain adaptive genetic variation. Specifi-
cally, ecological restoration of native plant species often
requires seed stock to replace or augment threatened plant
communities. Seeds derived from different sources might
represent genetically novel or depauperate material
because of the combination of restricted gene flow among
populations, adaptation to LOCAL (see Glossary) environ-
mental conditions and limited seed collections.
The geographical distribution of many plant species
included in restoration efforts spans a wide range of
climatic and edaphic conditions. Habitat heterogeneity,
combined with natural selection, often results in multiple,
genetically distinct ECOTYPES within a single species
[13]. Given the potential for introducing genotypes that
are poorly adapted to the site of restoration, studies of
LOCAL ADAPTATION assume new importance if we aim to
restore population fitness as well as increase the abun-
dance of native plant species. This awareness, combined
with recent studies of the negative consequences of
outbreeding, has fueled new efforts to understand the
effects of large-scale introductions on population mean
fitness [410].
Here, we review field and greenhouse studies that have
direct implications for the effects of TRANSLOCATION on
plant community restoration, particularly those resulting
from INTRASPECIFIC HYBRIDIZATION. Moreover, we aim to
clarify the differences among alternative genetic phenom-
ena that might result in the reduced performance of first-
(F1) and/or second-generation (F2) hybrids. Distinguish-
ing among the alternative causes of such OUTBREEDING
DEPRESSION could, in turn, assist in the identification of
populations between which seeds might be transferred
Glossary
Co-adapted gene complexes: particular combinations of genes at multiple loci
that interact to confer higher fitness relative to other genotypes.
Cryptic invasion: an undetected increase in frequency of foreign genotypes
following introduction of genetic variants of the same species or of a closely
related congener. Results in genetic swamping of native genotypes.
Dilution: reduction in fitness of hybrids relative to parents caused by
expression of only one half of locally adapted alleles. The heterozygous
hybrids are underdominant relative to the performance of each parental
population in its home environment. Also known as the ‘ecological’ or
‘environmental’ mechanism of outbreeding depression.
Ecotypes: distinct genotypes (or populations) within a species, resulting from
adaptation to local environmental conditions; capable of interbreeding with
other ecotypes or epitypes of the same species.
Epitypes: distinct genotypes (or populations) within a species, resulting from
adaptation to a specific (local) genetic background; capable of interbreeding
with other epitypes or ecotypes of the same species.
Genetic swamping: rapid increase in frequency of an introduced genotype (or
introduced allele) that might lead to replacement of local genotypes; caused by
a numerical and/or fitness advantage.
Home-site advantage: fitness advantage of local genotypes (ecotypes) relative
to introduced genotypes (ecotypes).
Hybrid breakdown: reduction in fitness of hybrids relative to parents caused by
disruption of co-adapted gene complexes via recombination. Hybrid break-
down might not occur until the F2 and subsequent generations. Also known as
the ‘physiological’ or ‘genetic’ mechanism of outbreeding depression.
Intraspecific hybridization: mating between individuals from genetically
distinct populations of the same species.
Introduced: genotype moved into a new site. Common synonyms include
‘alien’, ‘foreign’ and ‘nonlocal’.
Local: previously existing genotype at a site. Common synonyms include
‘existing’, ‘extant’, ‘indigenous’ and ‘native’.
Local adaptation: process by which populations genetically diverge in
response to natural selection specific to their habitat.
Outbreeding depression: reduction in mean population fitness resulting from
hybridization between genetically distinct individuals or populations of the
same species; detected in F1 or subsequent generations.
Seed transfer zones: geographical regions within which individuals (seeds,
seedlings, or adults) of native species can be transferred with no detrimental
effects on population mean fitness.
Translocation: a deliberate or accidental movement of species by humans
that ‘includes reintroduction, introduction, relocation, re-enforcement, sup-
plementation, restocking and other synonymous terms’ [4].
Corresponding author: Kristina M. Hufford (hufford@lifesci.ucsb.edu).
Review TRENDS in Ecology and Evolution Vol.18 No.3 March 2003 147
http://tree.trends.com 0169-5347/03/$ - see front matter q2003 Elsevier Science Ltd. All rights reserved. doi:10.1016/S0169-5347(03)00002-8
with low risks of fitness reduction following hybridization.
Ideally, ‘restoration genetics’ combines familiar common
garden and reciprocal transplant studies with the use of
molecular markers to detect gene flow and hybridization.
Estimates of local adaptation, gene flow among conspecific
populations, gene flow following translocations and the
fitness consequences of intraspecific hybridization con-
tribute critically to the delineation of SEED TRANSFER
ZONES used for the collection of seed or vegetative stock
in restoration.
Population genetic effects of translocation
Founder effects
Founder effects are likely to occur if seeds used to
revegetate restoration sites are collected from a limited
number of sources. Similar to episodes of colonization, the
‘founding’ propagules can represent only a portion of the
allelic diversity present in the source populations, and
they might hybridize with local genotypes. Resulting
genetic bottlenecks can be severe if the local population
is no longer present at the restoration site and the
INTRODUCED population size is small [11]. Ultimately,
levels of genetic variation and inbreeding in the restored
population will be determined by the number and genetic
diversity of founders, the mating system and the popu-
lation growth rate [12].
Two recent examples illustrate the role of founder
effects in restoration efforts. Williams and Davis [13]
compared levels of genetic diversity of restored eelgrass
Zostera marina populations with levels observed in
undisturbed populations. Molecular analyses revealed
significantly lower genetic diversity in transplanted
eelgrass beds than in natural beds, and a subsequent
study [14] determined that the genetic bottleneck was
caused by collection protocols. Moreover, the loss of genetic
variation corresponded to lower rates of seed germination
and fewer reproductive shoots, suggesting that there
might be long-term detrimental effects for population
fitness [14].
In a second example, an investigation of population
genetic integrity following the re-introduction of the
endangered Mauna Kea silversword Argyroxiphium sand-
wicense ssp. sandwicense determined that the restored
population of ,1500 plants is descended from only two or
three founders [15,16]. As a result of limited seed
collections, the restored population suffered a severe
genetic bottleneck, the fitness consequences of which are
not yet documented (because of the long-lived, predomin-
antly monocarpic character of the species). Efforts to
increase the number of founders are reportedly underway
[15,17].
Genetic swamping
If remnants of the focal species are present at the
restoration site, translocation of native species during
restoration might result in the GENETIC SWAMPING of local
genotypes [1820]. Swamping can occur in the absence of
intraspecific hybridization because of either a numerical or
fitness advantage of introduced plants. Alternatively,
swamping might result from the introgression of genes
of introduced plants through hybridization with the local
population.
For example, a recent study of common reed Phragmites
australis determined that the current, rapid expansion of
this species in North America originated with the intro-
duction of a genetic variant from Eurasia in the early
1900s [20]. Although P. australis is native to North
America, the spread of the aggressive genotype represents
aCRYPTIC INVASION that was detected via molecular
analysis of chloroplast DNA haplotypes [20,21]. The
expansion coincides with a loss of genetic diversity as
historic North American genotypes are swamped by the
aggressive strain. Phragmites australis spreads primarily
through vegetative growth and its range expansion corre-
sponds to genetic swamping with no reported intraspecific
hybridization [22].
Swamping via intraspecific hybridization as a conse-
quence of plant species restoration has not been studied.
Instead, research has focused on interspecific hybridiz-
ation and its consequences for the conservation of native
populations [2325]. Genetic swamping of local genotypes
can occur by hybridization between two congeners, as has
occurred between the native California cordgrass Spartina
foliosa and the introduced S. alterniflora. Anttila et al. [26]
discovered that rare F1 hybrids of the two species are
highly vigorous and threaten the genetic integrity of the
native plant populations because of enhanced pollen
production and dispersal. This phenomenon can also be
expected when genetically distinct conspecific populations
hybridize, but it is relatively difficult to detect. To docu-
ment swamping within a single species, molecular
analyses of local and introduced plants must occur before
and after the translocation.
Heterosis and outbreeding depression
When there are remnant populations at a restoration site,
translocation of conspecifics with compatible and pheno-
logically synchronous mating systems can result in
intraspecific hybridization. The fitness of hybrids (grown
in the habitat of the local parent) relative to their parents
will depend on the underlying cause of genetic differen-
tiation among parental populations. Consequences of
intraspecific hybridization might include heterosis
and/or outbreeding depression.
If population divergence is caused by genetic drift,
hybridization often results in heterosis, or increased vigor
of F1 hybrid progeny [8,27 32]. Heterosis occurs when
hybrid fitness is enhanced relative to the local parental
population and is caused by either the masking of reces-
sive deleterious alleles or by an overall fitness advantage
of heterozygotes (overdominance) [30,33]. Multilocus
mechanisms that account for the higher performance of
hybrids include the combination of favorable dominant
alleles fixed at different loci in parental populations, and
the generation of novel and favorable multilocus genotypes
(epistasis) [33].
Alternatively, hybridization between individuals from
genetically distinct populations can result in the lower
fitness of hybrids through outbreeding depression. Two
proposed genetic mechanisms that underlie outbreeding
depression are DILUTION and HYBRID BREAKDOWN (Box 1).
Review TRENDS in Ecology and Evolution Vol.18 No.3 March 2003
148
http://tree.trends.com
Whereas dilution is a consequence of local adaptation,
hybrid breakdown can result from hybridization between
populations that have diverged in one of two ways [34].
First, hybrid breakdown can result from mating among
genotypes adapted to distinct environments. Second, hybrid
breakdown can result from mating among genotypes
with distinct combinations of epistatically interacting
loci (CO-ADAPTED GENE COMPLEXES). In the second case,
populations do not represent ecotypes adapted to either
the biotic or abiotic environment, but instead have become
differentiated by genetic drift followed by selection for
alleles favored within each population-specific genetic
background [35,36].
We distinguish between the two cases of hybrid break-
down by contrasting ecotypes with EPITYPES (a new term
introduced here and distinct from the same term used in
botanical nomenclature). In the simplest cases, where
restoration efforts combine different ecotypes, F1 hybrid
fitness should be intermediate between the two parents
observed at the local parents’ site. Where the parent
populations represent epitypes, F1 or subsequent hybrid
fitness might be lower than that of either parent observed
in the habitat of the local parents (Box 2).
Experimental studies of intraspecific hybridization
Recent studies of heterosis and outbreeding depression in
plant species are summarized in Table 1. To date, most
research examines the fitness consequences of intra-
specific hybridization by comparing parents to F1 hybrid
progeny [10,2729]. However, there is a growing effort to
contrast the performance of F2 (and later) hybrid progeny
as well as F1 hybrids with parental genotypes [7,8,30].
These studies reveal a pattern of F1 hybrid heterosis
followed by outbreeding depression expressed in later
generations. An intermediate crossing distance advantage
is also often observed in F1 hybrids [37,38]. This is
explained by the expression of inbreeding depression
following crosses between near neighbors and outbreeding
depression following crosses between distant parents.
However, patterns of hybrid fitness are not consistent
among all traits or taxa. Similar to scenarios presented in
Box 2, some results suggest heterosis alone regardless of
outcrossing distance [27,29] whereas others detect only
outbreeding depression [10].
Among these studies of intraspecific hybridization, an
increasing number are being conducted in the context of
ecological restoration [7,8,10]. This new emphasis follows
the realization that introgression of maladapted genotypes
after translocation can threaten the long-term sustain-
ability of restored populations. Keller et al. [8] examined
fitness effects of hybridization among introduced and local
populations of three species used in wildflower reseeding
of Swiss agricultural field margins. Results for two fitness
traits (shoot biomass and seed mass) in two species are
shown in Fig. 1. Other combinations of heterosis and
outbreeding depression have been found in Chamaecrista
fasiculata and Lotus scoparius (Table 1), indicating a
need for more research to determine the patterns of out-
breeding depression that are relevant to restoration [7,10].
Box 1. Mechanisms of outbreeding depression
Outbreeding depression is the reduction in tness of individuals
resulting from crosses between genetically distinct parents
(e.g. intraspecic hybridization), and is caused by one of two
mechanisms. The rst mechanism is the dilutionof locally adapted
genotypes following hybridization between populations that have
diverged because of natural selection, and which have become xed
for different alleles [7,9,62]. F1 hybrids are heterozygous at locally
adapted loci, resulting in the 50% dilutionof each differently adapted,
parental genome. The resulting underdominance (where the hybrid
performs worse than either parental genotype) is expressed in F1
hybrids raised in the native environments of both parents.
The second mechanism is hybrid breakdownthrough the loss
of co-adapted gene complexes or intrinsic co-adaptation
[7,34,62,63]. Hybrid breakdown results from the recombination or
shufingof adaptive, multi-locus gene combinations during
sexual reproduction, and might not be expressed until the F2
generation or later. This one-generation delay is explained by the
presence in F1 hybrids of two intact, adaptive multilocus gene
combinations (one from each parent) that later break downin the
second generation when recombination rst occurs [33,62 64].
Ultimately, hybrid breakdown is the reduction in tness associated
with the disruption of epistatic interactions among loci.
Fig. 1. Examples of heterosis and/or outbreeding depression following hybridiz-
ation between local and foreign genotypes raised under common eld conditions.
Gray bars represent deviations (of the corresponding green bar) from the expected
values assuming no heterosis or epistasis (*P,0.05; ** P,0.01). (a) Mean phe-
notypes for shoot biomass of parental genotypes and F1 and F2 hybrids of Agros-
temma githago raised in Switzerland. Localand Foreignparental genotypes
were sampled from Switzerland and central Germany, respectively. The F2 hybrids
were produced by backcrossing maternal Swiss genotypes to paternal F1 hybrids.
The mean biomass of the F1 hybrids did not differ signicantly from that expected
in the absence of heterosis. The mean biomass of the F2 hybrids was signicantly
lower than that expected, revealing hybrid breakdown. (b) Mean phenotypes for
seed weight of parental genotypes and F1 and F2 hybrids of Silene alba raised in
Switzerland. Localand Foreignparental genotypes were sampled from Switzer-
land and Hungary, respectively, and crossed to produce F1 and F2 progeny as in
(a). The F1 hybrids exhibit heterotic effects on seed mass, whereas the F2 hybrids
exhibit outbreeding depression; F2 seed mass was lower than that expected when
assuming no epistasis. Adapted, with permission, from [8].
TRENDS in Ecology & Evolution
(a) (b)
Local Foreign
–0.2
0.2
0.4
0.6
0.8
1.0
0
F1 **
F2
Seed weight (mg)
Local Foreign
F2F1
–1.5
2.5
4.5
6.5
8.5
0.5
*
*
Biomass (g)
Review TRENDS in Ecology and Evolution Vol.18 No.3 March 2003 149
http://tree.trends.com
Table 1. Studies to detect outbreeding depression among geographically isolated populations of the same species
a
Species No. of populations used in
crosses/crossing dist.
Hybrid
gen.
Performance of F1 generations Performance of F2 and
later generations
Refs
Arnica
montana
5 pop.; inter- and intrapop.
crosses
F1 Heterosis for total seed number per
plant, and for probability of
owering by adults
N/A [32]
Delphinium
nelsonii
155 plants in 1 pop.; dist.
classes: 1 m, 3 m, 10 m and
30 m
F1 Inbreeding and outbreeding
depression observed for growth
and survival
N/A [37]
Progeny of intermediate distance
crosses performed
58 times better than did progeny
of 30-m cross
Eupatorium
resinosum
2 pop. (1-way crosses); dist.
classes: near neighbors,
distant neighbors within
pop., and between pop.
F1 Plant size and reproduction
increased with crossing distance
N/A [28]
Near-neighbor crosses produced
less t progeny than did distant-
neighbor and between-pop. crosses
Gentiana
pneumonanthe
58 plants in 1 pop.; dist.
classes: self, 150 cm,
50100 cm, 12m,25m,
510 m, 10 20 m,
&greater;20 m and 800 m
F1 No effect of pollen donor dist. if
selng and interpop. crosses
excluded
N/A [27]
Heterosis observed for seed set
Inbreeding depression observed for
seed mass and adult biomass
Ipomopsis
aggregata
Partial diallel breeding
design using 60 parents; dist.
classes: 1 m, 10 m and 100 m
F1 Signicantly greater seedling
emergence for 1-m and 10-m
progeny compared with 100-m
progeny
N/A [38]
Optimal outcrossing distance
observed; progeny from 10-m
crosses outperformed progeny
from 1-m and 100-m crosses for
estimates of lifetime tness, but
differences not signif.
Lotus
scoparius
6 pop.; 80400 km apart F1 Outbreeding depression following
pollinations
(seeds/ower £seedlings/seed);
magnitude positively correlated
with genetic distance among pop.
N/A [10]
Survival x fruit production
increased with mean environmental
dist. among pop.
Sarracenia
flava
6 pop.; 4 dist. classes or
pollination treatments:
control, self-pollination,
intrasite cross and intersite
cross
F1 Greater seed set, seed mass,
germination, survivorship and
growth observed in most years for
intra- and intersite crosses relative
to selfs
N/A [31]
Seed mass and seedling vigor
greater for inter- than for intrasite
crosses
Silene
nutans
2 pop. 30 km apart; dist.
classes: selng, outcrossing
within, and between pop.
F1 Performed as well or better than
parents, but effect of distant pollen
source depended on direction of
interpop. Cross
N/A [29]
Agrostemma
githa
78 pop. min.; 4 European
countries
F1,F2 Heterosis observed for seed mass
and, in some cases, for shoot
biomass
Strong hybrid breakdown
observed for shoot biomass
[8]
Chamaecrista
fasciculate
1015 maternal families per
pop.; 3 target pop.; dist.
classes: 0.1 km, 1 km, 10 km,
100 km and 1000s of km
F1,F2,F3 Heterosis observed for germination,
survivorship and vegetative
biomass
Hybrid breakdown in F2 fruit
production
[30]
Pattern of heterosis consistent with
drift being largely responsible for
genetic divergence among pop.
5/6 cases showed hybrid
breakdown in F3 (germination,
biomass and fruit production)
Greater hybrid breakdown in F3
suggests outbreeding
depression increases with
additional recombination
5 pop. in each of 3 regions;
dist. classes: 0.1 km, 1 km,
10 km, 100 km and 1000s km
F1,F3 Heterosis observed for germination,
nal biomass, survivorship and fruit
production
F3 tness often equal to parents
for same traits observed in F1
[7]
Review TRENDS in Ecology and Evolution Vol.18 No.3 March 2003
150
http://tree.trends.com
Alternate outcomes of intraspecific hybridization are likely
to reflect the number of hybrid generations studied, crossing
distances and underlying spatial environmental heterogen-
eity, the life-history traits examined, the degree of popu-
lation inbreeding, different mechanisms of outbreeding
depression and the degree of linkage (and subsequent time
for disruption) of co-adapted loci.
Detecting local adaptation and risks of translocation
If researchers are to predict the population genetic
consequences of translocation, estimates are needed of
ecotypic and epitypic differentiation and of the likelihood
of hybridization, all of which increase the potential for
outbreeding depression. Here, we discuss the resurgence
of classic approaches (common garden and reciprocal
transplant studies) and identify applications of molecular
marker assays that are relevant to restoration genetics.
Each method addresses factors that are important for our
understanding of the effects of interpopulation seed
transfer on population mean fitness.
Common garden studies
Variation in morphology and life history within species is
significant for restoration only in cases where population
divergence has a genetic basis. The classic method of
determining whether observed differences among popu-
lations are genetically based is the common garden study
[1,2,39]. In recent studies of perennial grass species
subject to restoration, common gardens were established
that represented seven or more populations and were then
used to detect intraspecific genetic variation [4042].In
each case, significant differences among populations for
quantitative traits were observed in the common environ-
ment. The discovery of such heritable variation suggests
that caution is needed in seed transfers between dissimilar
populations of these grasses. However, common garden
studies do not distinguish between divergence caused by
drift or natural selection.
Reciprocal transplants of parental genotypes
Reciprocal transplants among sites make it possible to
determine whether population divergence represents an
adaptive response to natural selection [39]. Adaptive
differences between populations are detected as a HOME-
SITE ADVANTAGE, whereby each genotype (i.e. ecotype)
performs best at its native site [9,43]. Given the potential
for the disruption of local adaptation by translocation,
investigators have tested the home-site advantage hypoth-
esis in several plant taxa used in restoration [9,41,44,45].
Strong evidence of local adaptation was discovered in 11
out of 13 species, suggesting that interpopulation trans-
plants would suffer significantly reduced fitness at
transplant sites [9,45,46]. However, there might be
translocation risks even in the absence of local adaptation,
when hybridizing populations represent epitypes rather
than ecotypes. If epitypic differentiation is present,
parental genotypes might do equally well in either
parental environment, and a decline in population mean
fitness would not occur until recombination disrupts co-
adapted gene complexes.
Relative performance of hybrids and parents
The approaches described above can also be used to
detect heterosis and outbreeding depression following
intraspecific hybridization. Heterosis is detected as a
fitness advantage of F1 hybrids, whereas outbreeding
depression is detected as a fitness reduction of F1 (or
later) hybrids, when compared with either parental
population. Distinguishing between the mechanisms of
outbreeding depression requires the comparison of F1
and F2 (or later) hybrid progeny raised in the same
environment to determine the timing of reduced fitness
(Box 2). Using these methods, researchers have
discovered evidence for dilution in intraspecific F1
hybrids of Delphinium nelsonii and Lotus scoparius,
and hybrid breakdown in later generations of Chamae-
crista fasiculata [10,30,37].
Table 1 (continued)
Species No. of populations used in
crosses/crossing dist.
Hybrid
gen.
Performance of F1 generations Performance of F2 and
later generations
Refs
Strong effects of crossing distance,
year and environment on hybrid
breakdowm
Reduced tness in F3 vs. F1
because of loss of
heterozygosity and co-adapted
gene complexes
Strong effects of crossing
distance, year and environment
on expression of hybrid
breakdown
Papaver
rhoeas
78 pop. min.; 4 European
countries
F1,F2 Slight outbreeding depression
observed for survival
Hybrid breakdown observed for
survival
[8]
Trend of reduced tness observed
for hybrid progeny
Some evidence of hybrid
breakdown observed for shoot
biomass
Silene
alba
78 pop. min.; 4 European
countries and 1 USA location
F1,F2 Heterosis observed for seed mass
and shoot biomass
Hybrid breakdown observed for
seed mass and shoot biomass,
but depended on cross and trait
observed
[8]
Reduced tness observed in most
distant cross (Swiss £USA)
No hybrid breakdown in
Swiss £Hungarian cross
a
Studies not consistent with respect to traits examined, but all kinds of traits can show evidence of heterosis and/or outbreeding depression. More studiesare needed of F2 and
subsequent generations to determine whether F1 heterosis accurately reects long-term effects on population mean tness of intraspecic hybridization.
Review TRENDS in Ecology and Evolution Vol.18 No.3 March 2003 151
http://tree.trends.com
Molecular marker assays
There is no strong consensus regarding how best to use
molecular markers in studies of local adaptation or
restoration. If molecular markers could easily detect
locally adaptive traits, then labor-intensive reciprocal
transplant experiments would not be necessary to detect
ecotypic differentiation. There is inconsistent evidence,
however, that this is the case [46– 49]. Molecular markers
(e.g. allozymes, amplified fragment length polymorphisms
and microsatellites) often represent neutral genetic
variation within and among populations, which does not
necessarily correspond to adaptive variation [46,47].
Nevertheless, molecular markers are very useful for
detecting three phenomena that either predict or reflect
population genetic risks of restoration: (1) strong founder
effects; (2) genetic swamping; and (3) population genetic
divergence that might indicate ecotypic or epitypic
variation [16,20,50,51]. Several recent studies serve as
models for these applications of molecular markers in
restoration genetics. For example, co-dominant nuclear
marker analyses of A. sandwicense and clover Trifolium
amoenum populations estimated small numbers of found-
ing individuals and/or detected a loss of genetic vari-
ation as a consequence of restoration protocols [16,52].
Box 2. Fitness effects of intraspecic hybridization
Heterosis and outbreeding depression can have separate or combined
effects on the tness of intraspecic hybrids. Figure I depicts four
potential qualitative outcomes of intraspecic hybridization on popu-
lation mean tness that have been observed in natural or experimental
populations. Each graph illustrates the population mean tness for the
original, local population (dark-green bars) relative to two generations
of hybrids (light-green bars) and the total population (hybrids and
parental genotypes combined; red bars) following a single translocation
event. Other combinations and intensities of heterosis, underdomin-
ance and hybrid breakdown would affect the short- and long-term
effects of hybridization on population mean tness. A thorough review
of the underlying genetic interactions (e.g. additivity, dominance and
epistasis) that might cause either enhanced or reduced hybrid tness is
beyond the scope of this article, but detailed discussions can be found
elsewhere [30,33,36].
(a) Heterosis alone
Hybrid vigor might result when hybridization occurs between indi-
viduals from populations that are genetically depauperate because of
drift and inbreeding (Fig. Ia). In this case, increased heterozygosity after
one generation of hybridization would result in higher tness of F1
hybrid progeny [8,27,29,31]. The relative mean tness of the total
population will also increase, but to a lesser extent, because heterosis is
only apparent in hybrid individuals. Heterozygosity will decline in
subsequent generations as mating (or self-fertilization) reconstitutes
homozygotes among F1 progeny.
(b) Dilution (underdominance)
If introduced and local genotypes are adapted to different environ-
ments, the tness of hybrid progeny could decrease because of a
50% dilution of the genome of the local population following
hybridization [10,37] (Fig. Ib). In this case, outbreeding depression
would be expressed in F1 hybrid progeny because of under-
dominance at loci formerly xed for adapted alleles. Mating
among the F1 progeny (or backcrossing) in the absence of further
introductions would result in increased tness of both hybrids and
the total population in the F2 generation as high-tness homo-
zygotes are reconstituted. Recovery of population tness would
depend on the strength of local adaptation, the intensity of selection
against hybrids, and the time required to restore homozygosity at
loci adapted to the local environment.
(c) Hybrid breakdown alone
Hybrid breakdown might be the sole outcome of intraspecic
hybridization between genotypes (Fig. Ic). Assuming that no other
genetic interactions are operating (e.g. dominance or heterosis), we
expect no change in population mean tness among the F1 progeny
because these hybrids contain both intact multilocus gene combin-
ations. In the F2 generation, however, total population mean tness and
the mean tness of hybrids will decline as co-adapted gene complexes
are disrupted by recombination (there is some evidence for this in
Papaver and Silene [8]). Reduced tness caused by hybrid breakdown
might occur regardless of whether the parent populations represent
ecotypes or epitypes.
(d) Heterosis and hybrid breakdown present
Both heterosis and hybrid breakdown might occur after intraspecic
hybridization (Fig. Id). In this case, the initial outcome of hybridization
between local and introduced genotypes is hybrid vigor caused by
increased heterozygosity. As a result, the total population mean tness
would also increase. However, recombination in the subsequent F2
generation would disrupt co-adapted gene complexes and counteract
the increase in tness caused by heterosis. Both F2 hybrids and the total
population would suffer a corresponding loss of tness. The severity of
tness effects in the F2 generation would depend on the joint effects of
heterosis and hybrid breakdown. In addition, strong linkage between
co-adapted loci might delay tness costs until the F3 generation or later
[30]. The combination of heterosis followed by hybrid breakdown in the
F2 generation was found in Agrostemma githa and Silena alba [8],
whereas hybrid breakdown was delayed until the F3 generation in
Chamaecrista fasciculata [7].
Fig. I.
TRENDS in Ecology & Evolution
Generation
PF1F2 Generation
PF1F2
Generation
PF1F2
Generation
PF1F2
Population mean fitness
Population mean fitness
Population mean fitness
Population mean fitness
(a) (b)
(c) (d)
Review TRENDS in Ecology and Evolution Vol.18 No.3 March 2003
152
http://tree.trends.com
Uniparentally inherited markers revealed cryptic inva-
sion via swamping by an aggressive genotype in P.
australis [20]. Finally, molecular analyses have detected
strong population differentiation in North American
grasses, suggesting low levels of gene flow and potential
ecotypic (or epitypic) divergence among populations [42,
50]. These results imply that translocation among these
populations can result in outbreeding depression, but such
marker-based predictions are best combined with field
studies to confirm that genetic differentiation reflects
adaptive or epistatic variation.
In theory, another application of molecular markers is
to use them as a tool to monitor hybridization when a
population is augmented with seeds from other sites.
However, current research to detect hybrid individuals is
reported primarily for interspecific hybrid zones and
rarely addresses issues in restoration [53,54]. In the
future, highly polymorphic genetic markers could be used
to distinguish among introduced and local conspecific
populations. This will enable the detection of genetic
swamping and the identification of F1 (and possibly later)
hybrids that might pose risks for the long-term sustain-
ability of the restored population [55].
Delineation of seed zones
Seed transfer zones were first defined in recognition of
strong regional differences in life-history traits of commer-
cially important species of conifers [56,57]. These studies
have compelled restoration ecologists to adopt the concept
of seed zones (with new emphasis on the potential con-
sequences of hybridization) in efforts to maximize the
viability of genotypes introduced in restoration. Several
investigators have reviewed the practical considerations of
seed and vegetative collections that will affect restoration
success [5760]. Their recommendations, along with the
methods of predicting fitness consequences of transloca-
tion discussed here, are powerful steps towards determin-
ing appropriate seed transfer zones.
First, there is growing recognition that seed collections
should be made near the restoration site to ensure the
genetic similarity of introduced and local populations,
minimizing the probability of outbreeding depression.
Recent population structure and transplant studies sug-
gest, however, that the distance between populations is not
always the best indicator of population genetic similarity
[9,10,48,50]. Instead, genetic divergence among popu-
lations is likely to reflect spatial environmental hetero-
geneity [40]. As a result, careful efforts should be made to
match germplasm for both abiotic and biotic factors, such
as elevation, soil characteristics, climatic regime, patho-
gens and predators.
Second, it is important that seed transfer zones
incorporate life-history characteristics of the focal species.
In particular, the mating system of plant taxa will
determine patterns of gene flow and levels of within and
among population differentiation. [61]. Highly outcrossing
taxa are less likely to represent ecotypic or epitypic
differentiation because of the homogenizing effect of gene
flow. By contrast, highly inbreeding taxa are likely to form
ecotypes and/or epitypes because of their greater isolation
and independent evolution. Seed transfer zones will there-
fore be larger for outcrossing species given that popu-
lations linked by long-distance pollen dispersal are less
likely to exhibit outbreeding depression if they hybridize.
As a final consideration, once a seed zone is delineated,
collections must be made from a large enough number of
individuals to represent population variation adequately
and to avoid severe genetic bottlenecks. Combining these
principles with empirical studies of ecotypic and epitypic
differentiation, gene flow and fitness in both F1 and F2
(and later) hybrids is the most promising approach to
identifying the populations among which plants may be
safely transferred.
Conclusions
Translocations of native species in restoration represent
‘experiments in progress’ and will open new avenues of
research in the study of ecotypic and epitypic variation,
Box 3. Future directions
There is an immediate need for additional research to describe the
genetic consequences of translocation of plant species in the context of
ecological restoration. In addition, these studies will improve basic
understanding of the occurrence and frequency of different mechan-
isms of outbreeding depression. Specically, future directions should
include the following.
Effects of outbreeding depression on long-term population
persistence
Future studies should evaluate the degree to which natural
selection effectively eliminates poorly adapted genotypes resulting
from intraspecic hybridization. This will help determine the best
restoration practices (such as the use of composite mixtures of
genotypes versus the use of local genotypes) when augmenting
populations [59,65 67]. In addition, the presence of hybrids that
fail to reproduce may reduce effective population size, threatening
sustainability [68].
Timing of outbreeding depression
Given the potential for outbreeding depression in F2 or later hybrid
progeny, more studies of multiple generations of hybrids are needed to
document the occurrence and frequency of outbreeding depression
among plant species. We also encourage accurate records of restoration
practices so that plant ecologists or managers of mixed populations can
return to restored sites and monitor long-term population tness
(e.g. survival and fecundity).
Predictability of intraspecic hybridization and outbreeding
depression
More research that describes the expression of outbreeding depression
in multiple species might help us to anticipate the attributes of species
most likely to exhibit this problem. For example, highly inbred taxa are
more likely than highly outcrossing taxa to evolve epitypic or ecotypic
differentiation, and therefore are probably at higher risk for outbreeding
depression [11]. By contrast, intraspecic hybridization is less likely to
occur in inbreeding taxa.
Local adaptation in species targeted for restoration
Studies should evaluate potential source populations to determine
whether they represent ecotypes or epitypes, with the goal of
delineating appropriate seed transfer zones for single species or groups
of species.
Review TRENDS in Ecology and Evolution Vol.18 No.3 March 2003 153
http://tree.trends.com
and intraspecific hybridization (Box 3). It is clear that
founder events and inbreeding depression should be
avoided. However, there are gaps in our knowledge
about the magnitude of outbreeding depression in aug-
mented populations and its consequences for population
persistence. Indeed, it is unknown whether natural selec-
tion will eliminate poorly adapted genotypes generated by
translocation, reducing the need to consider outbreeding
depression in restoration. Ultimately, strong research
programs must be combined with monitoring by land
managers to develop restoration protocols not only for the
reconstruction of threatened populations, but also for the
maintenance of their evolutionary potential in the face of
future environmental change.
Acknowledgements
We have benefited greatly from discussions with Arlee Montalvo, Michael
Wade and Kevin Rice. This work was funded, in part, by the Doctor Pearl
Chase Fund for Local Community Development, Conservation or Historic
Preservation Research Projects.
References
1 Turesson, G. (1922) The species and the variety as ecological units.
Hereditas 3, 100–113
2 Clausen, J. et al. (1940) Experimental Studies on the Nature of Species.
I. The Effect of Varied Environments on Western North American
Plants, Carnegie Institute of Washington
3 Linhart, Y.B. and Grant, M.C. (1996) Evolutionary significance of
local genetic differentiation in plants. Annu. Rev. Ecol. Syst. 27,
237–277
4 Hodder, K.H. and Bullock, J.M. (1997) Translocations of native
species in the UK: implications for biodiversity. J. Appl. Ecol. 34,
547–565
5 Montalvo, A.M. et al. (1997) Restoration biology: a population biology
perspective. Restor. Ecol. 5, 277 290
6 van Andel, J. (1998) Intraspecific variability in the context of
ecological restoration projects. Perspect. Plant Ecol. Evol. Syst. 1,
221–237
7 Fenster, C.B. and Galloway, L.F. (2000) Inbreeding and outbreeding
depression in natural populations of Chamaecrista fasciculata
(Fabaceae). Conserv. Biol. 14, 1406– 1412
8Keller, M. et al. (2000) Genetic introgression from distant
provenances reduces fitness in local weed populations. J. Appl.
Ecol. 37, 647–659
9 Montalvo, A.M. and Ellstrand, N.C. (2000) Transplantation of the
subshrub Lotus scoparius: testing the home-site advantage hypoth-
esis. Conserv. Biol. 14, 1034– 1045
10 Montalvo, A.M. and Ellstrand, N.C. (2001) Nonlocal transplantation
and outbreeding depression in the subshrub Lotus scoparius
(Fabaceae). Am. J. Bot. 88, 258–269
11 Barrett, S.C.H. and Kohn, J.R. (1991) Genetic and evolutionary
consequences of small population size in plants: implications for
conservation. In Genetics and Conservation of Rare Plants (Falk, D.A.
and Holsinger, K.E., eds) pp. 3– 30, Oxford University Press
12 Hedrick, P.W. (2000) Genetics of Populations, (2nd edn), Jones and
Bartlett Publishers
13 Williams, S.L. and Davis, C.A. (1996) Population genetic analyses of
transplanted eelgrass (Zostera marina) beds reveal reduced genetic
diversity in Southern California. Restor. Ecol. 4, 163 180
14 Williams, S.L. (2001) Reduced genetic diversity in eelgrass transplan-
tations affects both population growth and individual fitness. Ecol.
Appl. 11, 1472– 1488
15 Robichaux, R.H. et al. (1997) Molecular genetic consequences of a
population bottleneck associated with the reintroduction of the Mauna
Kea silversword (Argyroxiphium sandwicense spp. sandwicense
[Asteraceae]). Conserv. Biol. 11, 1140 1146
16 Friar, E.A. et al. (2000) Microsatellite analysis of a population crash
and bottleneck in the Mauna Kea silversword, Argyroxiphium
sandwicense spp. sandwicense (Asteraceae), and its implications for
restoration. Mol. Ecol. 9, 2027–2034
17 Robichaux, R. et al. (2000) Reintroudcing Hawaii’s silverwoods.
Endangered Species Bull. 25, 22–23
18 Lenormand, T. (2002) Gene flow and the limits to natural selection.
Trends Ecol. Evol. 17, 183– 189
19 Morrison, S.L. and Molofsky, J. (1999) Environmental and genetic
effects on the early survival and growth of the invasive grass Phalaris
arundinacea.Can. J. Bot. 77, 1447 –1453
20 Saltonstall, K. (2002) Cryptic invasion by a non-native genotype of the
common reed, Phragmites australis, into North America. Proc. Natl.
Acad. Sci. U. S. A. 99, 2445 –2449
21 Grosholz, E. (2002) Ecological and evolutionary consequences of
coastal invasions. Trends Ecol. Evol. 17, 22– 27
22 Chambers, R.M. et al. (1999) Expansion of Phragmites australis into
tidal wetlands of North America. Aquat. Bot. 64, 261 273
23 Levin, D.A. et al. (1996) Hybridization and the extinction of rare plant
species. Conserv. Biol. 10, 10– 16
24 Ellstrand, N.C. et al. (1999) Gene flow and introgression from
domesticated plants into their wild relatives. Annu. Rev. Ecol. Syst.
30, 539–563
25 Soltis, P.S. and Gitzendanner, M.A. (1999) Molecular systematics and
the conservation of rare species. Conserv. Biol. 13, 471 –483
26 Anttila, C.K. et al. (2000) Reciprocal hybrid formation of Spartina in
San Francisco Bay. Mol. Ecol. 9, 765 770
27 Oostermeijer, J.G.B. et al. (1995) Effects of outcrossing distance and
selfing on fitness components in the rare Gentiana pneumonanthe.
Acta Bot. Neerl 44, 257–268
28 Byers, D.L. (1998) Effect of cross proximity on progeny fitness in a rare
and a common species of Eupatorium (Asteraceae). Am. J. Bot. 85,
644– 653
29 Hauser, T.P. and Siegismund, T.P. (2000) Inbreeding and outbreeding
effects on pollen fitness and zygote survival in Silene nutans
(Caryophyllaceae). J. Evol. Biol. 13, 446 –454
30 Fenster, C.B. and Galloway, L.F. (2000) Population differentiation
in an annual legume: genetic architecture. Evolution 54,
1157– 1172
31 Sheridan, P.M. and Karowe, D.N. (2000) Inbreeding, outbreeding and
heterosis in the pitcher plant, Sarracenia flava (Sarraceniaceae), in
Virginia. Am. J. Bot. 87, 1628– 1633
32 Luijten, S.H. et al. (2002) Demographic consequences of inbreeding
and outbreeding in Arnica montana: a field experiment. J. Ecol. 90,
593– 603
33 Lynch, M. (1991) The genetic interpretation of inbreeding depression
and outbreeding depression. Evolution 45, 622 –629
34 Templeton, A.R. (1986) Coadaptation and outbreeding depression. In
Conservation Biology: The Science of Scarcity and Diversity (Soule
´,
M.E., ed.), pp. 105–116, Sinauer
35 Wade, M. (2001) Epistasis, complex traits, and mapping genes.
Genetica 112 – 11 3, 5 9 – 69
36 Wade, M. (2002) A gene’s eye view of epistasis, selection and speciation.
J. Evol. Biol. 15, 337 –346
37 Waser, N.M. and Price, M.V. (1994) Crossing-distance effects in
Delphinium nelsonii: outbreeding and inbreeding depression in
progeny fitness. Evolution 48, 842–852
38 Waser, N.M. et al. (2000) Outbreeding depression varies among
cohorts of Ipomopsis aggregata planted in nature. Evolution 54,
485– 491
39 Mazer, S.M. and LeBuhn, G. (1999) Genetic variation in life-
history traits: heritability estimates within and genetic differen-
tiation among populations. In Life History Evolution in Plants
(Vuorisalo, T.O. and Mutikainen, P.K., eds) pp. 86–171, Kluwer
Academic Publishers
40 Dyer, A.R. and Rice, K.J. (1997) Evidence of spatial genetic structure in
a California bunchgrass population. Oecologia 112, 333– 339
41 Gordon, D.R. and Rice, K.J. (1998) Patterns of differentiation in
wiregrass (Aristida beyrichiana): implications for restoration efforts.
Restor. Ecol. 6, 166 174
42 Knapp, E.E. and Rice, K.J. (1998) Comparison of isozymes and
quantitative traits for evaluating patterns of genetic variation in
purple needlegrass (Nassella pulchra). Conserv. Biol. 12,
1031– 1041
43 Galloway, L.F. and Fenster, C.B. (2000) Population differentiation in
an annual legume: local adaptation. Evolution 54, 1173– 1181
44 Keller, M. and Kollmann, J. (1998) Bedeutung der Herkunft von
Review TRENDS in Ecology and Evolution Vol.18 No.3 March 2003
154
http://tree.trends.com
Saatgut. Untersuchungen an Buntbrachen und anderen o
¨kologischen
Ausgleichsfla
¨chen. Naturschutz Landschaftsplanung. 30, 101 106
45 Joshi, J. et al. (2001) Local adaptation enhances performance of
common plant species. Ecol. Lett. 4, 536–544
46 Milligan, B.G. et al. (1994) Conservation genetics: beyond the
maintenance of marker diversity. Mol. Ecol. 3, 423– 435
47 Hedrick, P.W. (2001) Conservation genetics: where are we now? Trends
Ecol. Evol. 16, 629–636
48 Petit, C. et al. (2001) Gene flow and local adaptation in two endemic
plant species. Biol. Conserv. 100, 21– 34
49 Vitalis, R. et al. (2001) Interpretation of variation across marker loci as
evidence of selection. Genetics 158, 1811– 1825
50 Knapp, E.E. and Rice, K.J. (1996) Genetic structure and gene flow in
Elymus glaucus (blue wildrye): implications for native grassland
restoration. Restor. Ecol. 4, 1–10
51 Friar, E.A. et al. (2001) Population structure in the endangered Mauna
Loa silversword, Agryroxiphium kauense (Asteraceae), and its bearing
on reintroduction. Mol. Ecol. 10, 1657–1663
52 Knapp, E.E. and Connors, P.G. (1999) Genetic consequences of a
single-founder population bottleneck in Trifolium amoenum
(Fabaceae). Am.J.Bot.86, 124 –130
53 Daehler, C.C. and Strong, D.R. (1997) Hybridization between
introduced smooth cordgrass (Spartina alterniflora; Poaceae) and
native California cordgrass (S. foliosa) in San Francisco Bay,
California, USA. Am. J. Bot. 84, 607–611
54 De Greef, B. and Triest, L. (1999) The use of random amplified
polymorphic DNA (RAPD) for hybrid detection in Scirpus from the
river Schelde (Belgium). Mol. Ecol. 8, 379 386
55 Allendorf, F.W. et al. (2001) The problems with hybrids: setting
conservation guidelines. Trends Ecol. Evol. 16, 613– 622
56 Kitzmiller, J.H. (1990) Managing genetic diversity in a tree improve-
ment program. For. Ecol. Manage. 35, 131 149
57 Millar, C.I. and Libby, W.J. (1989) Disneyland or native ecosystem:
genetics and the restorationist. Restor. Manage. Notes 7, 18 24
58 Knapp, E.E. and Rice, K.J. (1994) Starting from seed: genetic
issues in using native grasses for restoration. Restor. Manage.
Notes 12, 40 –45
59 Lesica, P. and Allendorf, F.W. (1999) Ecological genetics and the
restoration of plant communities: mix or match? Restor. Ecol. 7, 42– 50
60 Rice, K.J. and Knapp, E.E. (2000) Evolutionary factors affecting the
probability of local adaptation or should we expect to see ecotypes
behind every rock? In 2nd Interface Between Ecology and Land
Development in California (Keeley, J.E. et al., eds), pp. 221– 226, US
Geological Survey Open-File Report 00-62
61 Hamrick, J.L. and Godt, M.J.W. (1996) Effects of life history traits on
genetic diversity in plant species. Philos. Trans. R. Soc. Lond. B Biol.
Sci. 351, 1291– 1298
62 Roff, D.A. (1998) Evolutionary Quantitative Genetics, Chapman & Hall
63 Fenster, C.B. and Galloway, L.F. (1997) Developmental homeostasis
and floral form: evolutionary consequences and genetic basis. Int.
J. Plant. Sci. 158, S121 –S130
64 Lynch, M. and Walsh, B. (1998) Genetics and Analysis of Quantitative
Traits, Sinauer
65 Templeton, A.R. (1991) Off-site breeding of animals and implications
for plant conservation strategies. In Genetics and Conservation of Rare
Plants (Falk, D.A. and Holsinger, K.E., eds) pp. 182– 194, Oxford
University Press
66 Reinartz, J.A. (1995) Planting state-listed endangered and threatened
plants. Conserv. Biol. 9, 771– 781
67 Burton, P.J. and Burton, C.M. (2002) Promoting genetic diversity in
the production of large quantities of native plant seed. Ecol. Restor. 20,
117 – 1 23
68 Ryman, N. et al. (1995) Supportive breeding and variance effective
population size. Conserv. Biol. 9, 1619– 1628
Keep your eye open for the March issue of Endeavour,
the history of science journal
Articles to be published in this issue include:
Carl Linnaeus: pictures and propaganda
Patricia Fara
The philosophy of chemistry
Joachim Schummer
Aeld of great promise: soil bacteriology in America, 1900 1925
Eric D. Kupferberg
Depictions of the Copernican system in the 17th century
Volker R. Remmert
Integrating mind and brain: Warren S. McCulloch, cerebral localization and experimental epistemology
Tara H. Abraham
Jeanne Baret: the rst woman to circumnavigate the globe
Londa Schiebinger
Review TRENDS in Ecology and Evolution Vol.18 No.3 March 2003 155
http://tree.trends.com
... However, there are concerns that the use of genetic rescue for augmenting populations or admixture to establish new populations can have adverse consequences. Genetic rescue may lower the fitness of the population being augmented by swamping the gene pool of the locally adapted plants with hybrids between the local and introduced plants, which are less adapted to the local conditions (Hufford and Mazer 2003;Whiteley et al. 2015). Admixture or genetic rescue can result in a population with reduced fitness because of outbreeding depression when the new genetic material is introduced from a genetically differentiated, ecologically dissimilar or geographically distant population (Hufford and Mazer 2003;Edmands 2007;Shi et al. 2018). ...
... Genetic rescue may lower the fitness of the population being augmented by swamping the gene pool of the locally adapted plants with hybrids between the local and introduced plants, which are less adapted to the local conditions (Hufford and Mazer 2003;Whiteley et al. 2015). Admixture or genetic rescue can result in a population with reduced fitness because of outbreeding depression when the new genetic material is introduced from a genetically differentiated, ecologically dissimilar or geographically distant population (Hufford and Mazer 2003;Edmands 2007;Shi et al. 2018). Additionally, there are doubts as to how long the fitness benefits of heterosis last, with maximum fitness benefits predicted for the F1 and F2 generations before a decline in benefits for subsequent generations (Bell et al. 2019). ...
... subulifolia showed that this is not the case and that genetic rescue of the small population (Lockier) or admixture to establish a new translocation is unlikely to result in substantially increased levels of genetic diversity or increased seed fitness. Our study highlighted that research into the levels of genetic diversity and genetic divergence among populations will be a valuable tool to support seed-sourcing decisions (Hufford and Mazer 2003), particularly before undertaking translocation actions such as admixture and genetic rescue. Where consideration is being given for sourcing new genetic material for translocations that maybe more distantly related (even between subspecies), these genetic studies will provide essential information, as will ex situ cross-pollination studies, to reduce the potential for outbreeding depression. ...
Article
Context To establish translocated populations of threatened plants with the genetic resources to adapt to changing environmental conditions, the source of propagation material is an important consideration. Aim We investigated the fitness consequences of genetic rescue and admixture for the threatened annual daisy Schoenia filifolia subsp. subulifolia, and the common S. filifolia subsp. filifolia, to inform seed-sourcing strategies for translocations of the threatened subspecies. Methods We evaluated genetic diversity of two populations of S. filifolia subsp. subulifolia and four populations of S. filifolia subsp. filifolia by using microsatellite markers. We grew seedlings from each study population and cross-pollinated inflorescences within and among populations of the same subspecies, and between subspecies. We evaluated the fitness consequences of each cross by using seed set, seed weight and seed viability. Key results There was a lower genetic diversity in the small (<50 plants, Nar = 3.28, He = 0.42) compared to the large (>10 000 plants, Nar = 4.42, He = 0.51) population of S. filifolia subsp. subulifolia, although none of the measures was significantly different, and seed fitness was slightly, although not significantly, reduced in interpopulation crosses compared with the small population. Genetic diversity was similar between the threatened and widespread subspecies; however, the subspecies were genetically divergent (Fst = 0.242–0.294) and cross-pollination between subspecies produced negligible amounts of seeds (<3% seed set). Conclusions Although genetic rescue or admixture of S. filifolia subsp. subulifolia would not necessarily result in greatly increased levels of genetic diversity or seed fitness, we still consider it a potential option. Negligible seed set in crosses between subspecies indicates that deliberate hybridisation is not a possibility. Implications Studies of fitness consequences of admixture or genetic rescue are rare yet critical to assessing the benefits of different translocation strategies.
... Genetic rescue introduces or restores gene flow between populations to alleviate fitness consequences of inbreeding through the introduction of genetic variation. However, while rare species may exhibit small effective population sizes and reduced adaptive potential, disruption of local adaptation may lead to outbreeding depression, or reduced fitness of progeny following admixture between genetically differentiated lineages (Edmans, 2007;Goto et al., 2011;Hufford & Mazer, 2003). Thus, considering the contribution of natural selection to the evolution of population genetic differences is important for genetic rescue, as it may ultimately lead to maladaptation of migrants or translocated individuals (Lowry et al., 2008;Nosil et al., 2005). ...
... An understanding of demographic and adaptive evolutionary history is invaluable for rare species of conservation concern, particularly when management decisions impact populations at risk of extinction. Teasing apart the contribution of both stochastic and deterministic evolutionary processes to population genomic differentiation over time and space can be used to inform species conservation decisions, including the potential consequences of genetic rescue (Frankham et al., 2011;Hufford & Mazer, 2003;Ralls et al., 2018). ...
... Torrey pine, critically endangered and endemic to just two native populations, suffers from extremely low effective population size (N I = 2305, N M = 1715) relative to other pines (Menon et al., 2018;Xia et al., 2018). (Goto et al., 2011;Hufford & Mazer, 2003;Montalvo & Ellstrand, 2001). ...
Article
Understanding the contribution of neutral and adaptive evolutionary processes to population differentiation is often necessary for better informed management and conservation of rare species. In this study, we focused on Pinus torreyana Parry (Torrey pine), one of the world’s rarest pines, endemic to one island and one mainland population in California. Small population size, low genetic diversity, and susceptibility to abiotic and biotic stresses suggest Torrey pine may benefit from inter‐population genetic rescue to preserve the species’ evolutionary potential. We leveraged reduced representation sequencing to tease apart the respective contributions of stochastic and deterministic evolutionary processes to population differentiation. We applied these data to model spatial and temporal demographic changes in effective population sizes and genetic connectivity, to identify loci possibly under selection, and evaluate genetic rescue as a potential conservation strategy. Overall, we observed exceedingly low standing variation within both Torrey pine populations, reflecting consistently low effective population sizes across time, and limited genetic differentiation, suggesting maintenance of gene flow between populations following divergence. However, genome scans identified more than 2000 candidate SNPs potentially under divergent selection. Combined with previous observations indicating population phenotypic differentiation, this indicates natural selection has likely contributed to the evolution of population genetic differences. Thus, while reduced genetic diversity, small effective population size, and genetic connectivity between populations suggest genetic rescue could mitigate the adverse effects of rarity, evidence for adaptive differentiation suggests genetic mixing could disrupt adaptation. Further work evaluating the fitness consequences of inter‐population admixture is necessary to empirically evaluate the trade‐offs associated with genetic rescue in Torrey pine.
... Following the recognition of cryptic taxa, conservation efforts must adapt accordinglypopulations previously thought to be of low conservation value may become an immediate priority if they represent a rare, newly defined taxon. The strategies employed to conserve populations with reciprocal gene flow will also differ to those required to conserve populations between which there is little or no gene flow (Hufford and Mazer, 2003;Brown et al., 2014). Further, the ecological requirements of the cryptic species may differ from each other (Schönrogge et al., 2002). ...
Article
Full-text available
Morphologically cryptic taxa must be accounted for when quantifying biodiversity and implementing effective conservation measures. Some orchids pollinated by sexual deception of male insects contain morphologically cryptic ecotypes, such as the warty hammer orchid Drakaea livida (Orchidaceae). This species is comprised of three cryptic pollination ecotypes, which can be distinguished based on differences in pollinator species and floral volatiles. The present study aims were: (a) to investigate the geographic range of the three D. livida ecotypes, enabling assessment of their conservation status; and (b) to test the efficacy of different methods of identifying the D. livida ecotypes. Three methods of ecotype identification were assessed: morphometric analysis, genome size comparison, and analysis of chemical volatile composition of labellum extracts from pollinated flowers. MaxEnt species distribution models revealed that each ecotype has a different predicted geographic range, with small areas of overlap at the range margins. One ecotype is known from just ten populations over a limited geographic area, the majority of which has been cleared for agriculture, and urban development. While there was broad overlap between the ecotypes in individual morphological traits, multivariate analysis of morphological traits provided correct assignment to ecotype in 87% of individuals. Using the labellum of pollinated flowers, screening for volatile chemical compounds associated with particular ecotypes returned an even higher correct assignment rate, of 96.5%. As such, we advocate that the use of volatiles from the labellum of recently pollinated flowers is an effective way to determine the ecotype of unknown individuals of D. livida, with minimal impact on the flowering plant.
... Following the recognition of cryptic taxa, conservation efforts must adapt accordinglypopulations previously thought to be of low conservation value may become an immediate priority if they represent a rare, newly defined taxon. The strategies employed to conserve populations with reciprocal gene flow will also differ to those required to conserve populations between which there is little or no gene flow (Hufford and Mazer, 2003;Brown et al., 2014). Further, the ecological requirements of the cryptic species may differ from each other (Schönrogge et al., 2002). ...
Preprint
Full-text available
Although many plant species are reliant on insect pollination, agricultural plant breeding programs have primarily focused on traits that appeal to growers and consumers, rather than on floral traits that enhance pollinator attraction. In some vegetable seed production systems, this has led to declining pollinator attraction and poor seed yields. We predicted that low-yielding crop varieties would be less attractive to pollinators due to deficiencies in nectar rewards or volatile floral attractants. To test our prediction, we used a chemical phenotyping approach to examine how floral chemical traits of five carrot lines affect honey bee visitation. In bioassays, honey bees avoided feeders containing nectar from all carrot lines indicating a general non-attractant effect. Certain compounds in carrot flowers and nectar not only failed to elicit attraction but functioned as repellents, including the sesquiterpenes α-selinene and β-selinene. Others enhanced attraction, e.g. β-ocimene. The repellent sesquiterpenes have previously been implicated in plant defense suggesting a fine balance between pollination and plant protection, which when disrupted in artificial selection in plant breeding programs can impact the crop yield. These new insights highlight the importance of bioactive compounds in attracting pollinators toward floral resources in both ecological and agricultural settings.
... Plant species that form conspecific ecotypes in response to contrasting environmental conditions offer excellent opportunities for studying the significance of specific traits for plant existence in a given habitat in closely related and geographically closely located study systems bearing sufficient phenotypic variation. Ecotypes are locally adapted (groups of) populations within a species that are characterized by a combination of heritable and non-heritable traits [18,19] and are frequently still interfertile [20]. With the recent advance in genetic methods, ecotypes are receiving increasing interest [21], especially ecotypes resulting from parallel evolution [22], which is the independent polytopic evolution of ecotypes in response to similar selection pressures [23]. ...
Article
Full-text available
Functional and structural adjustments of plants in response to environmental factors, including those occurring in alpine habitats, can result in transient acclimation, plastic phenotypic adjustments and/or heritable adaptation. To unravel repeatedly selected traits with potential adaptive advantage, we studied parallel (ecotypic) and non-parallel (regional) differentiation in leaf traits in alpine and foothill ecotypes of Arabidopsis arenosa. Leaves of plants from eight alpine and eight foothill populations, representing three independent alpine colonization events in different mountain ranges, were investigated by microscopy techniques after reciprocal transplantation. Most traits clearly differed between the foothill and the alpine ecotype, with plastic adjustments to the local environment. In alpine populations, leaves were thicker, with altered proportions of palisade and spongy parenchyma, and had fewer trichomes, and chloroplasts contained large starch grains with less stacked grana thylakoids compared to foothill populations. Geographical origin had no impact on most traits except for trichome and stomatal density on abaxial leaf surfaces. The strong parallel, heritable ecotypic differentiation in various leaf traits and the absence of regional effects suggests that most of the observed leaf traits are adaptive. These trait shifts may reflect general trends in the adaptation of leaf anatomy associated with the colonization of alpine habitats.
... Additionally, in a longterm study the number of seeds could be used as an additional indicator of fitness. Overall these results suggest that the different varieties were given shape by something different than evolutionary adaptation to their environment and consequently should perhaps not be defined as different ecotypes (Hufford and Mazer 2003) ...
... Adaptation to a saline habitat that is the intertidal zone is a likely explanation for our observation (Song et al., 2008). Locally adapted seeds are prone to withstand the harsh conditions of their provenance and preferably used for restoration purposes (Hufford and Mazer, 2003; Frontiers in Plant Science 06 frontiersin.org Broadhurst et al., 2008). ...
Article
Full-text available
Phragmites australis is highly adaptable with high competitive ability and is widely distributed in the coastal wetland of the Yellow River Delta. However, allelopathic effects of P. australis on the growth of neighboring plants, such as Suaeda salsa , are poorly understood. In this study, germination responses of S. salsa seeds collected from two different habitats (intertidal zone and inland brackish wetland) to the extracts from different part of P. australis were compared. Potential allelopathic effects on germination percentage, germination rate, radicle length, and seedling biomass were analyzed. The germination of S. salsa was effectively inhibited by P. australis extract. Extract organ, extract concentration, and salt concentration showed different effects, the inhibitory rates were highest with belowground extract of P. australis between the four different parts. Germination percentage and germination rate were significantly decreased by the interactive effect of salt stress and extract concentration in S. salsa from a brackish wetland but not in S. salsa from the intertidal zone. The impact of different extracts of P. australis on radicle length and seedling biomass of S. salsa showed significant but inconsistent variation. The response index results showed that the higher concentration of extract solution (50 g·L ⁻¹ ) of P. australis had stronger inhibitory effect on the seed germination and seedling growth of S. salsa while the belowground extract had the strongest negative effect. Our results indicated that allelopathy is an important ecological adaptation mechanism for P. australis to maintain a high interspecific competitive advantage in the species’ natural habitat.
... Widely distributed species are typically able to tolerate multiple environmental conditions, through a combination of extensive phenotypic plasticity and/or locally adapted genetic variation (Stamp & Hadfield, 2020). Populations that are genetically adapted to their local environmental conditions can be defined as ecotypes (Hufford & Mazer, 2003). A single species can be composed of multiple genetically distinct and locally adapted ecotypes (Linhart & Grant, 1996). ...
Article
Full-text available
Ecotypes are distinct populations within a species that are adapted to specific environmental conditions. Understanding how these ecotypes become established, and how they interact when reunited, is fundamental to elucidating how ecological adaptations are maintained. This study focuses on Themeda triandra, a dominant grassland species across Asia, Africa and Australia. It is the most widespread plant in Australia, where it has distinct ecotypes that are usually restricted to either wetter and cooler coastal regions or the drier and hotter interior. We generate a reference genome for T. triandra and use whole genome sequencing for over 80 Themeda accessions to reconstruct the evolutionary history of T. triandra and related taxa. Organelle phylogenies confirm that Australia was colonised by T. triandra twice, with the division between ecotypes predating their arrival in Australia. The nuclear genome provides evidence of differences in the dominant ploidal level and gene‐flow among the ecotypes. In northern Queensland there appears to be a hybrid zone between ecotypes with admixed nuclear genomes and shared chloroplast haplotypes. Conversely, in the cracking claypans of Western Australia, there is cytonuclear discordance with individuals possessing the coastal chloroplast and interior clade nuclear genome. This chloroplast capture is potentially a result of adaptive introgression, with selection detected in the rpoC2 gene which is associated with water use efficiency. The reason that T. triandra is the most widespread plant in Australia appears to be a result of distinct ecotypic genetic variation and genome duplication, with the importance of each depending on the geographic scale considered.
Article
Full-text available
Background: Allegheny woodrats (Neotoma magister) are found in metapopulations distributed throughout the Interior Highlands and Appalachia. Historically these metapopulations persisted as relatively fluid networks, enabling gene flow between subpopulations and recolonization of formerly extirpated regions. However, over the past 45 years, the abundance of Allegheny woodrats has declined throughout the species' range due to a combination of habitat destruction, declining hard mast availability, and roundworm parasitism. In an effort to initiate genetic rescue of a small, genetically depauperate subpopulation in New Jersey, woodrats were translocated from a genetically robust population in Pennsylvania (PA) in 2015, 2016 and 2017. Herein, we assess the efficacy of these translocations to restore genetic diversity within the recipient population. Results: We designed a novel 134 single nucleotide polymorphism panel, which was used to genotype the six woodrats translocated from PA and 82 individuals from the NJ population captured before and after the translocation events. These data indicated that a minimum of two translocated individuals successfully produced at least 13 offspring, who reproduced as well. Further, population-wide observed heterozygosity rose substantially following the first set of translocations, reached levels comparable to that of populations in Indiana and Ohio, and remained elevated over the subsequent years. Abundance also increased during the monitoring period, suggesting Pennsylvania translocations initiated genetic rescue of the New Jersey population. Conclusions: Our results indicate, encouragingly, that very small numbers of translocated individuals can successfully restore the genetic diversity of a threatened population. Our work also highlights the challenges of managing very small populations, such as when translocated individuals have greater reproductive success relative to residents. Finally, we note that ongoing work with Allegheny woodrats may broadly shape our understanding of genetic rescue within metapopulations and across heterogeneous landscapes.
Article
Forest trees species are often genetically adapted to local environmental conditions. Therefore, local seeds are recommended for ecological restoration. However, seedlings of broad‐leaved tree species, such as Japanese beech (Fagus crenata), are limited in their commercial seedling production in Japan. Thus, long‐distance transfer of seeds and/or seedlings is common. F. crenata's distinct geographical structure is well known; large‐scale seed transfer may increase the risk of genetic disturbance. Several provenance trials of the species revealed that phenotypic traits such as leaf area and bud flush date differed latitudinally and/or between the Pacific Ocean side and the Japan Sea side. We investigated leaf size and bud flush date and identified the chloroplast DNA haplotype of trees planted in two provenance trials established in Hokkaido, Japan. We then examined whether cpDNA haplotype information is useful as a proxy in ecological restoration when using seedlings with incomplete seed source information. This study indicated that suitable seedlings could be selected based on chloroplast DNA haplotype information in F. crenata in the case of incomplete seed source information. Fagus chloroplast utility.
Article
Full-text available
The study discusses possible implications of the introduction of foreign seed material on ecological compensation sites. Eight herbaceous species of compensation sites on farmland were used as an example. First experiments with up to eleven European provenances revealed differences in establishment, phenological patterns and life cycle. Some of them are probably adaptations to climatic differences. The results indicate that the introduction of foreign seed has potentially detrimental effects. However, legal consequences of translocating native species are still under debate. Future research should focus on the effects of non-native populations on the genetic diversity of local genotypes.
Article
Inbreeding with close relatives and outbreeding with members of distant populations can both result in deleterious shifts in the means of fitness-related characters, most likely for very different reasons. Such processes often occur simultaneously and have important implications for the evolution of mating systems, dispersal strategies, and speciation. They are also relevant to the design of breeding strategies for captive populations of endangered species. A general expression is presented for the expected phenotype of an individual under the joint influence of inbreeding and crossbreeding. This expression is a simple function of the inbreeding coefficient, of source and hybridity indices of crossbreeding, and of specific forms of gene action. Application of the model may be of use in identifying the mechanistic bases for a number of evolutionary phenomena such as the shift from outbreeding enhancement to outbreeding depression that occurs with population divergence.
Article
In plants, selfing and outcrossing may be affected by maternal mate choice and competition among pollen and zygotes. To evaluate this in Silene nutans, we pollinated plants with mixtures of (1) self- and outcross pollen and (2) pollen from within a population and from another population. Pollen fitness and zygote survival was estimated from the zygote survival and paternity of seeds. Self pollen had a lower fitness than outcross pollen, and selfed zygotes were less likely, or as likely, to develop into seeds. Hybrid zygotes survived as frequently or more than local zygotes, and pollen from one of the populations fertilized most ovules in both populations. Our results thus indicate strong maternal discrimination against selfing, whereas the success of outbreeding seems mostly affected by divergent pollen performance. The implications for the evolution of maternal mate choice are discussed.
Article
Population structure and history have similar effects on the genetic diversity at all neutral loci. However, some marker loci may also have been strongly influenced by natural selection. Selection shapes genetic diversity in a locus-specific manner. If we could identify those loci that have responded to selection during the divergence of populations, then we may obtain better estimates of the parameters of population history by excluding these loci. Previous attempts were made to identify outlier loci from the distribution of sample statistics under neutral models of population structure and history. Unfortunately these methods depend on assumptions about population structure and history that usually cannot be verified. In this article, we define new population-specific parameters of population divergence and construct sample statistics that are estimators of these parameters. We then use the joint distribution of these estimators to identify outlier loci that may be subject to selection. We found that outlier loci are easier to recognize when this joint distribution is conditioned on the total number of allelic states represented in the pooled sample at each locus. This is so because the conditional distribution is less sensitive to the values of nuisance parameters.
Article
Reviews the problems of the commitment to genetic purity, and suggests way of compromising and at the same time of minimising risk. Discusses the problems of restoration in forestry and offers guidelines for successful restoration. -S.J.Yates