Download Colonisation as a common denominator in plant

Landscape Ecology (2006) 21:837–848
DOI: 10.1007/s10980-005-5389-7
Springer 2006
-1
Research Article
Colonisation as a common denominator in plant metapopulations and range
expansions: effects on genetic diversity and sexual systems
John R. Pannell* and Marcel E. Dorken
Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK; *Author for
correspondence (e-mail: john.pannell:@plants.ox.ac.uk)
Received 1 December 2004; accepted in revised form 12 April 2005
Key words: Androdioecy, Baker’s Law, Colonisation, Dioecy, FST , Genetic diversity, Metapopulation
dynamics, Monoecy, Population subdivision, Range expansion, Self-compatibility, Tristyly
Abstract
Colonisation plays a central role in both the initial occupancy of a region through range expansions as well
as in metapopulations, where local extinctions are balanced by re-colonisations. In this paper, we review the
effects that colonisation is expected to have on patterns of genetic variation within a species, and we draw
attention to the possibility of interpreting these patterns as signatures of colonisation in the past. We briefly
review theoretical predictions for the effect of colonisation on both neutral genetic diversity and on variation at genetic loci that regulate the sexual system of plant populations. The sexual system represents a
particularly important trait in this context because it is affected by both selection during colonisation, and
because it influences gene flow amongst populations. Finally, we introduce four case studies of plant species
that show variation in their sexual systems that is consistent with theoretical predictions.
Colonisation is a fundamental process for all
organisms that occupy habitat in a fragmented
landscape. This applies both to the non-equilibrium
occupation by a species of new habitat during the
expansion of its range into a new region (Hewitt
2000), as well as to its persistence in a metapopulation, in which local population extinctions are
balanced by the colonisation of available habitat
elsewhere in the region (Pannell and Charlesworth
2000; Wakeley 2004). Thus, although range
expansions and metapopulation dynamics influence species distributions and abundance on different spatial scales, they share the process of
colonisation as a common denominator.
The ecological and demographic factors affecting colonisation are complex. They include the
availability of suitable sites, the rate at which
available habitat patches are occupied, and the
number and origin of individuals that found each
new population. Given the complexities of colonisation and dispersal, it would be sensible to omit
them from models or hypotheses, whenever they
are unlikely to contribute to our understanding of
biological patterns observed in a landscape. The
important question is, of course: when will colonisation matter, and when will it not?
The answer to this question depends on the type
of biological phenomenon we are interested in
explaining. For example, colonisation might be
important in regulating the proportion of habitat
occupied by a species at a given point in time, but
gene flow subsequent to colonisation might be
sufficiently strong to erase the genetic signature left
by colonisation. Here, colonisation matters, but it
will be hard to detect without long-term studies. In
contrast, if dispersal between populations is low, a
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genetic signature of colonisation might persist beyond the time that populations reach demographic
equilibrium following a colonisation event. In this
situation, a population ecologist might find the
metapopulation concept unhelpful, whereas an
investigator interested in the level of genetic
divergence between populations would be unable
to explain observed data without it. In light of
these potentially differing perspectives, it is
instructive to consider ‘ecological metapopulations’ and ‘genetic metapopulations’ separately
(Ives and Whitlock 2002); they might or might not
coincide for any given species.
It will be evident to any ecologist that plant
populations are typically separated from one another in space in much the same way as animal
populations are. However, although the utility of
the metapopulation concept is fully accepted by
zoologists, there is still some controversy about its
applicability for plants (Bullock et al. 2002;
Freckleton and Watkinson 2002). Two of the main
points at issue here are the extent to which plant
habitat patches can be easily recognised and
studied as discrete local units (Pannell and Obbard
2003), and the difficulty of incorporating seed
bank dynamics into metapopulation concepts
(Freckleton and Watkinson 2002; Ouborg and
Eriksson 2004). The question of how to define a
local unit of study is particularly relevant, because
patch dynamics can be driven by colonisation at
small spatial scales within sites that remain permanently occupied at a larger scale. There is a
great need for more empirical data bearing on this
question from a demographic point of view.
However, increasing evidence suggests that colonisation has left its mark in the way genetic
diversity is distributed within and amongst plant
populations, and these data can be understood
within a well developed theoretical framework.
Metapopulation theory makes predictions about
the distribution of genetic diversity in recently
colonised populations in a fragmented landscape,
both for neutral genes (Pannell and Charlesworth
2000; Wakeley 2004) and for genes that affect
important aspects of a species’ biology, such as its
sexual system (Barrett and Pannell 1999; Ronce
and Olivieri 2004). These predictions are important
for two reasons. First, from the perspective of
neutral genetic variation, failure to recognise the
signature of colonisation can lead to erroneous
estimates of historical patterns of dispersal based
on molecular markers (Whitlock and McCauley
1999). Second, from the perspective of adaptive
variation amongst populations, it is important to
recognise that natural selection can operate not
only within populations but also at the regional
level, especially on traits that affect dispersal
(Olivieri et al. 1997; Barrett and Pannell 1999).
Species that vary in their sexual system, which includes both the mating system of a population and
the allocation of resources to male and female
reproductive functions amongst its individuals,
provide examples for the outcome of selection
operating at local and regional scales. Importantly,
such variation can be difficult to interpret on the
basis of within-population processes only and can
serve as a useful signature of colonisation and the
rate and scale of dispersal amongst populations.
In this paper, our primary aim is to review
briefly the way in which colonisation is expected to
leave its mark in the genetic diversity of plant
populations (Holderegger et al. 2005). We begin
by providing an overview of some of the useful
predictions made by metapopulation genetic theory for neutral genetic diversity in fragmented
populations with colonisation and extinction
dynamics. We then note that some of the same
predictions can be made for the effects of colonisation during the range expansion of a species, and
that the way ongoing colonisation shapes genetic
diversity of a species at a regional level must be
interpreted against the background of the signature left of earlier range expansion at a potentially
much larger spatial scale. We conclude this conceptual overview by drawing attention to the
interactions we expect to occur between colonisation and the sexual system, as well as to the signature that these interactions leave in neutral
genetic diversity. In the second section of this review, we illustrate some of the ideas presented with
reference to four species that show interesting
large-scale variation in their sexual systems.
Conceptual considerations
The effect of colonisation on neutral genetic
diversity
Analysis of the effects of colonisation on patterns
of genetic diversity has focused on aspects of genetic structure and measures of variation within
species. These can usefully be subdivided into two
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broad categories: (1) absolute measures of diversity and the frequency of genetic variants maintained within local populations, or in a
metapopulation as a whole; and (2) the way that
the total or metapopulation-wide diversity is partitioned amongst local populations.
The total genetic diversity maintained across a
metapopulation or species is often written as HT
(when calculated on the basis of allele frequencies)
or pT (for sequence data) (Nei 1987). Generally,
population turnover is expected to cause a dramatic reduction in species-wide diversity, because
genetic drift is enhanced by the fluctuations of
population size and by the repeated genetic bottlenecks that accompany colonisations (Whitlock
and Barton 1997; Pannell and Charlesworth 1999;
Wakeley and Aliacar 2001). Similarly, genetic
bottlenecks or founder events associated with
colonisation are expected to reduce the average
amount of diversity that we expect to find within
local populations, usually written as HS or pS for
allele frequency data or sequence data, respectively
(Slatkin 1977; Pannell and Charlesworth 1999)
(Figure 1). In addition to reducing the average
genetic diversity of local populations, colonisation
should also alter the frequency distribution of alleles in favour of more common variants (Luikart
et al. 1998a, b).
Figure 1. A graphical depiction of the signature of colonisation
and its erosion by subsequent migration. Populations are colonised by one or a small number of founder individuals. Population growth increases the number of individuals but not the
genetic diversity of the population, so that initially withinpopulation diversity is low. Because different populations are
founded by different genotypes, recently colonised populations
are expected to be genetically well differentiated. With time,
migration between extant populations (represented by the vertical arrows) both increases the within-population diversity and
reduces the genetic differentiation amongst different populations.
Colonisation also affects the genetic differentiation amongst populations, because different populations will by chance be colonised by individuals
with different combinations of neutral genes
(Wade and McCauley 1988; Whitlock and
McCauley 1990). With time, migration amongst
established populations will tend to reduce the
differentiation caused by colonisation, so that the
genetic signature of colonisation is gradually
erased (Figure 1). Genetic differentiation is often
calculated as FST, or the fraction of the specieswide diversity that can be accounted for by differences amongst populations (Hartl and Clark
1997). FST is calculated on the basis of loci with
two segregating alleles, but similar ratios can be
calculated for loci with more than two alleles (e.g.,
GST) or for microsatellite loci where alleles differ in
sequence length (RST). These measures have often
been used to infer the amount of historical gene
flow amongst subpopulations of geographically
separated populations, using the expression
FST ¼
1
;
1 þ 4Nm
where Nm is the average number of immigrants
that move into each subpopulation per generation.
However, this expression is not valid when populations are not at a demographic equilibrium, e.g.,
when populations fluctuate in size or exist in a
metapopulation with extinctions and colonisations
(Whitlock and McCauley 1999). For a dynamic
metapopulation, more complex formulas have
been derived that take into account not only the
amount of gene flow amongst established populations, but also the rate at which new populations
are established and the number and origin of
individuals that colonise them (Wade and
McCauley 1988; Whitlock and McCauley 1990).
In the simple metapopulation model introduced
by Slatkin (1977) and further developed by Wade
and McCauley (1988); Whitlock and McCauley
(1990) and others (Pannell and Charlesworth
2000), genetic differentiation is always increased
by colonisation above that predicted by the above
equation if populations are founded by individuals
from a single source population. If the founding
individuals represent a random sample of the
whole metapopulation, genetic differentiation is
increased if the colonists are fewer than approximately twice the number of migrants that move
between established populations (Wade and
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McCauley 1988; Whitlock and McCauley 1990).
Only if there are more than approximately twice as
many colonists than the number of subsequent
migrants between extant sites per generation will
genetic differentiation in a metapopulation be
lower than that predicted by models that do not
account for population turnover (Wade and
McCauley 1988; Whitlock and McCauley 1990).
Importantly, these predictions apply to a simple
demographically stable metapopulation in which
extinctions are balanced by colonisation events,
and also to the peripheral populations of a species
expanding its range (Austerlitz et al. 1997; Le
Corre and Kremer 1998). In this latter case, colonisations are not balanced by extinctions, but the
genetic differentiation amongst peripheral populations is still governed by the relative numbers
and origins of migrants into new extant populations.
It is important to stress that the metapopulation
models reviewed here are not spatially explicit.
These models are useful for comparisons between
species in different contexts that may be subjected
to different rates of population turnover or different migration rates between established populations. However, they do not account for the
strong spatial structure that populations are likely
to have in a fragmented landscape and that might
contribute to the detailed way in which genetic
diversity is patterned amongst neighbouring and
more widely separated populations. Analysis that
incorporates this sort of spatial structure can be
more revealing, particularly when we are interested
in the patterns of movement of individuals across a
landscape rather than in just the average effect of
processes occurring at a regional scale (Gaggiotti
et al. 2004).
Finally, we note that the demographic complexity of metapopulation scenarios will be difficult to characterise precisely when based only on
variation at a single locus. This is because each
locus represents a single genealogical history,
drawn from a statistical distribution of histories
with very high variance (Nordborg 2001). Power
to discriminate between different scenarios is thus
weak (Pannell 2003). To increase statistical power
of discrimination between contrasting models, or
to increase the precision for statistical inference of
model parameters, we are therefore compelled to
sample from several genetic loci. For populations
that have been recently colonised, it is possible to
assign source populations to the colonising individuals by analysing the genetic associations between different loci in the genome before these are
broken down by subsequent mating and recombination (Gaggiotti et al. 2004). However, these
powerful analytic tools only allow inference for
populations that are a single generation old. In
plants, the longer-term signature of colonisation
will be left largely in maternally inherited genes
(chloroplast or mitochondrial DNA), because
pollen dispersal is expected to rapidly erase signals
at biparentally inherited loci (nuclear DNA).
Unfortunately, this places a severe limit on the
precision of inference or model discrimination,
because maternally inherited genes together only
represent a single locus, because they are inherited
as a single genetic unit and do not recombine. This
constraint may become an advantage when our
aim is to infer the specific historical context of
colonisation.
Phylogeography and the historical context
of colonisation
Metapopulation theory predicts that geographic
groups within a species will display contrasting
levels of genetic diversity if they differ in their rates
of population turnover. The fact that such differences have typically not been found (Charlesworth
and Pannell 2001) is most likely due to the fact
that metapopulation-wide absolute diversity levels
equilibrate slowly, at a rate governed by the
mutation process (Pannell and Charlesworth
1999), and may thus be more strongly influenced
by the historical patterns of colonisation that first
established the metapopulation. In other words,
for long periods following the occupation of a new
region, e.g., after post-glacial range expansion, the
effect of recurrent colonisation in a metapopulation will simply be the re-distribution of a
sub-sample of the standing genetic variation
maintained in the species’ glacial refugium. It is
thus important to consider the historical context of
inter-regional colonisation as well as the effect of
on-going colonisation within regions, e.g., in
metapopulations (Figure 2).
Phylogeography is the study of the evolutionary
relationships among populations in a geographical
region and provides the historical context for
understanding how gene flow, colonisation, range
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Figure 2. The expected qualitative effects of regional colonisation during range expansion and local colonisation in a metapopulation on three measures of diversity: regional absolute
diversity, denoted as HT; diversity within local populations or
populations, denoted as HS; and genetic differentiation amongst
populations within a region, denoted as FST. Range expansion
can occur from either an established metapopulation (left) or
from a single large refugium population (right).
expansion and adaptation affect the present-day
distribution of genetic variation in a species’ range
(Avise 2000). Phylogeographic studies offer insights into a wide variety of research topics in
ecology and evolution, including species invasions
(Saltonstall 2003; Schaal et al. 2003), the demographic history of species (Tobler et al. 2004), and
the evolution of different character states (Dorken
and Barrett 2004). In general, however, the primary focus of phylogeographic studies has been to
examine patterns of post-glacial colonisation by
plants and animals. These studies have revealed
the location of glacial refugia and the historical
routes of migration, providing insights that are not
apparent from the fossil record (Stehlik 2002; Petit
et al. 2003). Phylogeography can thus be seen as a
particular field of landscape genetics (Manel et al.
2003).
Phylogeographic inferences are made from the
distribution of genetic variation among populations, typically in organelle genomes (i.e., mitochondria in animals and plants, and chloroplasts
in plants). Recombination in these genomes is
rare, and inheritance is usually uniparental, so
that the various genotypes in a sample (i.e., unique combinations such as gene sequences or socalled restriction site combinations) may be placed
in an ordered hierarchy of genealogical descent
(Olmstead and Palmer 1994). The result is a
phylogenetic network of genotypes from the
populations sampled, revealing the evolutionary
relationships of populations across a landscape
(Avise 2000).
The most informative markers for phylogeographic inference are those that have evolved on a
timescale similar to that of the migration or colonisation process. Using such markers, dispersal
routes can be traced with reference to a genetic
signature left in populations that formed its stepping stones (Cruzan and Templeton 2000). For
relatively quickly evolving genes or regions of the
genome, DNA sequences provide the most information, largely because a simple model of mutation can be assumed (i.e., each new mutation is
unique, back mutation does not occur, and the
accumulation of new mutations along a sequence
reflects shared ancestry). For studies of animals,
the rapidly evolving mitochondrial genome has
been useful to this end (Avise 2000). However,
mitochondria and chloroplast sequences evolve
much more slowly in plants, and this places a limit
on the resolution of phylogeographic inference
(Schaal et al. 1998). Studies of plant populations
have therefore tended to use more variable loci,
such as allozymes, AFLPs, or microsatellites. The
use of these variable markers allows the examination of the geographic distribution of neutral genetic variation, at the cost of making historical
inferences based on phylogenetic reconstructions.
However, this drawback can be overcome if there
is clear geographic structure in the genetic variation (Charlesworth et al. 2003).
Microsatellites are sequences of repetitive DNA
in which mutations theoretically cause changes in
the number of di-, tri-, or tetra-nucleotide repeats
(Goldstein and Schlötterer 1999). They may be
particularly useful for inferring patterns of
migration and gene flow for two reasons. First,
their high mutation rate means that spatial patterns of genetic diversity can be informative over
short time scales (although they may be less
informative over longer time scales; Provan et al.
2001). And second, because microsatellites are
thought to increase or decrease incrementally in
length with each new mutation, correlations in
length between different sequences can help to reveal patterns of descent in a way that is not possible for loci at which alleles are simply either the
same or different. In particular, they can be used to
reveal the extent to which genetic differentiation
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contains a signature of historical colonisation in
range expansion (Pons and Petit 1996).
Although they are less useful, measures of
genetic diversity such as HT and HS can also
provide evidence of patterns of historical colonisation. For example, gradients of reduced genetic
variation in previously glaciated areas relative to
putative historical refugia can point to range
expansion along specific colonisation routes
(Hewitt 2000). Nevertheless, the geographic
structure of genetic diversity can reflect ongoing
as well as historical processes, and phylogeographic interpretations must be made with caution. Another caveat is that areas of high
diversity may not correspond to the location of
glacial refugia, but rather to the recently colonised areas in which variation is the outcome of
colonisation from more than one refugium. For
example, Petit et al. (2003) used a comparative
approach for their investigation of the history of
colonisation of 22 widespread and co-distributed
European trees and shrubs. They found that
hotspots of genetic diversity in the colonised
ranges were the result of mixed colonisation from
genetically isolated eastern and western European
refugia (Petit et al. 2003).
The effect of colonisation and of the sexual
system on genetic diversity
It has long been recognised that patterns of genetic
diversity in plants vary with aspects of life history
and sexual systems (Stebbins 1950; Baker 1953;
Brown 1979; Hamrick and Godt 1996; Charlesworth and Pannell 2001). For instance, geographical patterns of genetic diversity differ
between long-lived perennials and annuals (Hamrick and Godt 1996; Austerlitz et al. 2000), and
between self-fertilising and outcrossing plants
(Charlesworth and Pannell 2001). Simple population genetic theory predicts that, all else being
equal, fully selfing species should maintain half the
total genetic diversity as outcrossing species (Pollak 1987). All else is seldom equal, however, and
there is little empirical support for this prediction
from comparisons between related taxa that differ
in their mating system: species-wide genetic
diversity in selfers and outcrossers does not differ
in a predictable way (Charlesworth and Pannell
2001). This is perhaps not surprising, given the
differing evolutionary histories and different population sizes possessed by different species.
Although selfing and outcrossing species do not
differ in their genetic diversity at a regional level in
a consistent way, many studies have shown that
selfers tend to have much lower diversity within
local populations, and that geographically separated selfing populations are typically more highly
differentiated than outcrossers (Charlesworth and
Pannell 2001; Charlesworth 2003). These differences may be partly due to the smaller local
effective population size of selfers (Pollak 1987),
but it is usually much too high to be explained in
this way alone. Reasons for the discrepancy are
not totally clear, but two causes seem plausible,
one demographic and the other genetic (Figure 2).
The first possible cause of the reduced withinpopulation diversity and the higher differentiation
amongst populations of selfing lineages is the effect
of colonisation itself. Because selfers are more
likely to be colonising species than outcrossers
(Baker 1955; Pannell and Barrett 1998), there will
be automatic associations between mating system
and patterns of genetic diversity caused by genetic
bottlenecks during colonisation, and by the reduced levels of gene flow that occur among
established populations of self-fertilising plants.
Reasons for this reduction in gene flow are discussed briefly in the next section.
The dramatically low diversity found within
selfing populations might also be due to so-called
genetic hitchhiking associated with local adaptation (Charlesworth et al. 1997). It is well known
that environmental conditions vary amongst
localities and that natural selection may cause
adaptations to differ amongst sites as a result of
the spread of alleles that confer a selective
advantage locally. In outcrossing species, the increase in frequency of an allele at a selected locus
can occur largely independently of neutral loci
elsewhere in the genome, because each generation
genetic recombination allows the independent
segregation of alleles at unlinked loci (e.g., loci on
different chromosomes). In contrast, genetic
recombination is much less effective in selfing
populations (because it occurs in largely homozygous genomes), so that associations between
physically unlinked loci in the genome are broken
down more slowly. When an allele is swept to high
frequency in the population by natural selection,
neutral alleles at other loci are also likely to be
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Figure 3. An illustration of the reduction of within-population diversity as a result of a selective sweep caused by local adaptation.
Horizontal lines represent chromosomes; vertical strokes represent neutral genetic loci that differ amongst individuals within the
population before local adaptation and the selective sweep have occurred. Before the selective sweep (a), the population is genetically
diverse. One individual (indicated by the asterisk) acquires an advantageous mutation (indicated by the open circle on its chromosome). This mutation is positively selected and sweeps to fixation in the population. Thus, after the sweep (b), all individuals possess
the advantageous mutation (the population has become more locally adapted). If the sweep takes place more quickly than migration
occurs from other populations, within-population diversity is also depleted at genetically linked neutral loci.
dragged to high frequency by association (Figure 3). The result is a decline in diversity at all
hitchhiking loci, because only those neutral alleles
associated with the selected allele will be left in the
population after the sweep has ended (Maynard
Smith and Haigh 1974; Charlesworth and Pannell
2001). If different alleles are swept to high frequency in different populations, the process will
also lead to increased levels of population differentiation at neutral loci, which is in fact observed
(Charlesworth et al. 1997).
Colonisation and selection on the sexual system
Plants are outstanding in the variation they display
amongst species in their mating system and sex
allocation (Barrett 2002). Much of this variation
can be interpreted in terms of sexual specialisation,
the abundance of mates and/or pollinators, competition between individuals and/or gametes for
mating opportunities and fertilisation success, or
reduced progeny fitness upon inbreeding. However, in colonising species, or in species with a
history of long-distance dispersal during range
expansions, the bottlenecks associated with the
occupation of new habitat can themselves become
a selective agent that acts on the sexual system.
One effect of colonisation on the sexual system
was first noted by Baker (1955), who drew attention to the fact that a capacity for uniparental
reproduction, i.e., selfing tends to be more frequent on islands and on the edge of a species
range. This association, known as Baker’s Law
(Stebbins 1957), is illustrated by examples from
both plants and animals and points to the selective
advantage that colonising individuals enjoy when
they are able to reproduce on their own. Baker’s
Law originally referred to long-distance colonisation of remote habitat patches, but the same
selective process will occur in a metapopulation in
which colonisations take place repeatedly (Pannell
and Barrett 1998).
The action of Baker’s Law in a metapopulation
has been modelled from the perspective of both
selection for selfing vs. outcrossing (Pannell and
Barrett 1998) and for combined vs. separate sexes
(Pannell 1997). A key result is that the selective
advantage of individuals capable of self-fertilisation is expected to increase dramatically as the
proportion of habitat within a landscape occupied
by a given species approaches zero, because colonisation by single individuals becomes increasingly
prevalent (Pannell and Barrett 1998). This, of
course, corresponds to the situation that we expect
to find at the edge of species distribution during
range expansion. From the point of view of combined vs. separate sexes, modelling has confirmed
the intuitive idea that hermaphroditism becomes
increasingly common with increases in the rate of
population turnover and/or reductions in the
numbers of individuals immigrating into new
habitat as colony founders (Pannell 1997; Figure 4).
At the same time, the repeated events of colonisation select for increased allocation of resources
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Figure 4. The proportion of males or females (unisexuals)
maintained in a metapopulation with hermaphrodites, as a
function of the mean number of individuals immigrating into
local populations per generation (i.e., the mean number of
colonists that establish new populations, or the mean number of
individuals moving into established populations). The model
assumes an extinction and colonisation rate of 0.05, unisexuality determined by a dominant allele, and colonisations by as
Poisson-distributed number of colonists. Modified after Pannell
(1997).
to female function at the expense of the male
function, as a result of enforced inbreeding when
populations are small (Hamilton 1967; Pannell
2001). This latter effect is likely to affect the genetic
diversity found in colonising species: selection that
reduces resource allocation to pollen production
and dispersal in self-fertilising species will tend to
reduce gene flow through pollen migration
amongst populations (Charlesworth and Pannell
2001). The increased genetic differentiation
amongst populations that also results from restricted gene flow will accentuate the bottleneck
effect of colonisation by single individuals.
Inferences from case studies
The interactive effects of colonisation and breeding-system evolution on regional patterns of genetic diversity are brought into focus by plants
that display variation in their sexual systems between geographical regions. In this section, we
briefly discuss the cases of four species that have
been the subject of intensive study: Eichhornia
paniculata and Sagittaria latifolia, which are both
aquatic herbs in South and North America,
respectively, and Mercurialis annua and Silene
vulgaris, which are annual colonisers of disturbed
habitat in Europe; S. vulgaris has also been
introduced into North America. These species all
display sexual polymorphisms in which the frequencies of easily identifiable phenotypes vary
across space in ways that point to the importance
of colonisation during range expansion and/or in a
balance with extinction in a metapopulation. Indeed, it is difficult to account for the phenotypic
variation observed in these species without
invoking the effects of colonisation.
Eichhornia paniculata is a self-compatible and
tristylous herb: populations comprise three classes
of individuals that differ in the position of their
anthers and stigmas (Barrett 1985). The reciprocal
placement of anthers and stigmas between phenotypes promotes mating between phenotypes and
hinders mating amongst individuals with the same
phenotype. In a large part of its range in northeastern Brazil, the three phenotypes are equally
frequent within populations. However, one or two
of the phenotypes are absent from many populations in extensive areas, where populations are
smaller and geographically more separated (Barrett 1985; Barrett et al. 1989). It is likely that these
populations were colonised by smaller numbers of
individuals, and that reproductive assurance during population establishment has selected for
phenotypes with increased selfing rates. Indeed,
there is a high proportion of individuals with
modified stamens that promote self-pollination in
these regions (Husband and Barrett 1995). These
populations are also more highly differentiated
genetically, as we might expect if inter-population
gene flow is reduced or populations have been recently colonised as part of a metapopulation.
Similar observations have been made on the island
of Jamaica, where only two of the three phenotypes successfully established following colonisation and where genetic variation is greatly reduced
in comparison with mainland populations (Husband and Barrett 1991). Selfing variants are also
more common on the island than in mainland
South America, and levels of genetic differentiation among populations in Jamaica are higher
than corresponding estimates from mainland
populations (Glover and Barrett 1987).
Sagittaria latifolia is an aquatic herb whose
populations are either monoecious (or functionally
hermaphroditic) or dioecious (with males and females co-occurring), with the two systems often
845
occurring in close geographic proximity (Wooten
1971). Self-compatibility and the occupation of
more disturbed habitats by monoecious populations suggest that colonisation could be differentially involved in structuring genetic variation
among populations. The higher rate of population
turnover (Dorken and Barrett 2003) and the greater
genetic differentiation among monoecious compared with dioecious populations support this idea
(Dorken et al. 2002). Nevertheless, the lack of gene
flow between monoecious and dioecious populations in areas of geographic overlap (Dorken and
Barrett 2003) also suggests the importance of an
historical perspective for explaining the regional
coexistence of sexual systems in S. latifolia. Indeed,
dioecious populations are genetically divergent
from monoecious populations, and phylogeographic evidence indicates that both breeding systems recolonised the north of their current range
independently of one another (Dorken and Barrett
2004).
Mercurialis annua varies in its sexual system
across Europe, with dioecy, monoecy and androdioecy (the co-occurrence of males and hermaphrodites) all common over large parts of its range
(Durand 1963; Pannell et al. 2004). This variation
points to the differential importance of metapopulation dynamics (Pannell 1997, 2001; Figure 5).
Under the metapopulation model, selection for
reproductive assurance during the repeated bouts
of colonisation favours self-fertile hermaphroditism, because only hermaphrodites are able to
found new populations on their own (Pannell
1997). The recurrent inbreeding that accompanies
colonisation selects for female-biased sex allocation in the hermaphrodites, and this sets the stage
for the invasion and local spread of males (Pannell
2001; Figure 5). This provides a possible explanation for the mix of monoecious and androdioecious populations in the regions of M. annua
in which males occur (Durand 1963). If the rate of
population turnover is sufficiently high, however,
males are excluded from the metapopulation
altogether, and it is thought that monoecious regions of M. annua that lack males correspond to
areas of elevated rates of colonisation and extinction. In the absence of population turnover, or
with low rates of extinction and high levels of inter-population gene flow, males are maintained at
high frequencies and the potentially hermaphroditic phenotype is functionally female (J.R. Pan-
nell, unpubl. data). This situation may characterise
the large areas in which dioecy prevails. Preliminary estimates of genetic diversity in monoecious vs. androdioecious populations, as well as
measures of population size and separation are
consistent with the metapopulation hypothesis
(D.J. Obbard, S.A. Harris, S.M. Eppley and J.R.
Pannell, unpubl. data).
Finally, Silene vulgaris is a weedy annual that
displays gynodioecy, a dimorphism in which females and hermaphrodites co-occur at varying
frequencies. As in the case of M. annua, hermaphrodites should have an advantage of reproductive
assurance during colonisation, and they have been
found to produce more seeds than females when
spatially isolated from potential mates (Taylor
et al. 1999). Within local populations, however,
females produce more seeds than hermaphrodites,
especially when females are rare (McCauley et al.
2003). Selection thus occurs in opposite directions
at the population and metapopulation levels in S.
vulgaris, as it does in M. annua. In S. vulgaris, genetic variation is similar between northern and
southern regions in the sample, indicating that
Figure 5. A graphical depiction of a model for the maintenance
of androdioecy (the co-existence of males and hermaphrodites)
in a metapopulation. Males and hermaphrodites are symbolised
by open and closed circles, respectively; block arrows represent
population growth; simple arrows represent dispersal. According to the model, established androdioecious populations (1)
disperse propagules across the metapopulation (2 and 5). Only
hermaphrodites can establish populations as sole colonisers due
to reproductive assurance (2). New populations (3) grow initially
through self-fertilisation (4). With population growth, levels of
inbreeding fall, allowing the invasion of males (5). The age
structure of the metapopulation is maintained through a balance
of extinction and recolonisation. Inbreeding during repeated
colonisation events selects for female-biased sex allocation in the
hermaphrodites From Pannell et al. (2004), with permission.
846
ongoing, long-distance seed dispersal is involved in
the establishment of populations (Olson and
McCauley 2002). Within regions, however, most
genetic variation is distributed among local populations, an observation consistent with recurrent
genetic bottlenecks that occur during colonisation
(Olson and McCauley 2002).
Conclusions
It is sometimes useful to contrast equilibrium with
non-equilibrium processes when interpreting patterns of genetic diversity. However, the non-equilibrium process assumed in models of range
expansion and the equilibrium process assumed in
metapopulation models share the process of colonisation as a common factor. Colonisation shapes
the differences in diversity levels between the genetic source, often a glacial refugium, of a species
and the more recently occupied parts of its range,
as well as the details of within-population diversity
and differentiation between populations at the
leading edge of an expanding range. Similarly, it is
colonisation, and its importance compared with
migration amongst extant populations, that governs the patterns of diversity in a metapopulation
at equilibrium. This is why predictions made for
diversity patterns at the leading edge of a range
expansion and amongst local populations in a
metapopulation are largely the same (Le Corre
and Kremer 1998). It is also why the effects of
colonisation by long-distance dispersal and of repeated bouts of colonisation in a metapopulation
might be expected to select similar sexual strategies
(Barrett and Pannell 1999). Nevertheless, the
interpretation of the effects of colonisation on genetic diversity may benefit by being placed within
their phylogeographic context, because regional
processes largely re-pattern the genetic variation
inherited from a more distant past.
The majority of phylogeographic studies have
largely set out to describe the history of a species
range expansion (Avise 2000). However, by
revealing the geographic distribution of genetic
variation, phylogeographic studies also have the
potential to address specific hypotheses in ecology
and evolution. For example, a key gap in our
understanding of the factors regulating the size of
species distributions and the potential for range
expansion are the demographic and genetic prop-
erties of populations at the edge of species’ ranges.
Various measures of genetic diversity, such as the
numbers of alleles and gene diversity, as well as
differences in DNA sequences, are commonly observed to be lower towards the extremities of a
species’ range (Dorken and Eckert 2001). Peripheral populations are, in some cases, associated with
uniparental modes of reproduction such as selffertilisation or asexual propagation (Eckert et al.
1999), causing reduced genetic variation at the
edge of the species’ range. These differences in
genetic diversity among populations may be due to
reduced rates of population growth or to reductions in the size of local populations and of the
regional density of populations. However, they
may also be influenced by patterns of colonisation,
and these alternatives can be distinguished using
phylogeographic techniques.
Because of the sessile habit of plants and the
often strong geographical structure of their populations, plants offer broad scope for the study of
dispersal. This applies not only to effects on neutral genetic diversity, but also to non-neutral genetic variation affecting aspects of a species’
biology such as its sexual system. Indeed, plant
species that display polymorphism in their sexual
system have provided us with excellent natural
experiments for testing ecological and evolutionary theory. Thus, species such as Eichhornia
paniculata, Mercurialis annua, Sagittaria latifolia
and Silene vulgaris whilst they represent unusual
examples of within-species variation in their sexual
systems, have contributed a great deal to our
understanding of the effect of colonisation on
neutral and non-neutral genetic variation.
Acknowledgements
We thank R. Holderegger, V. L. Sork and an anonymous reviewer for comments on the manuscript,
and we acknowledge financial support to JRP
through a grant from the NERC, UK, and a postdoctoral fellowship to MED from NSERC, Canada.
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