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Management strategies for coral reefs are dependant on information about the spatial …
Biology Articles » Biogeography » Meta-population structure in a coral reef fish demonstrated by genetic data on patterns of migration, extinction and re-colonisation » Background
Coral reefs are important ecosystems in ecological, evolutionary and
socio-economic contexts but are under increasing threat from
anthropogenic impacts [1,2].
The most effective conservation tool available to coral reef managers
so far has been the use of individual or networks of Marine Protected
Areas (MPAs) [2,3].
To maximise the effectiveness of MPAs information about the spatial
population structure, patterns of connectivity and the stability of
local populations within and among protected areas is required [3,4]. Genetic tools can provide valuable information about the scale, structure and stability of populations  when direct census estimates required to empirically demonstrating these processes are impractical to obtain [6,7].
The development and application of molecular markers to examine
patterns of connectivity in coral reef organisms have increased greatly
in recent years , but comparatively little attention has been placed on examining predictions from meta-population theory 
despite the intuitive appeal of this approach in describing such
systems. Here we present only the second examination of genetic
meta-population dynamics in a coral reef fish in more than a decade and
the first to use a highly variable and drift-sensitive molecular marker.
Genetic models of spatial structure have developed from Wright's original island model  into the stepping-stone, or isolation-by-distance models [10-13], and later into meta-population models [e.g. [14-19]].
The island model has played a central role in the development of
population ecological and evolutionary theory because of its
mathematical simplicity and tractability, but it makes many assumptions
including equal population sizes, equal migration rates, discrete
generation times, amongst others .
When these assumptions are met, populations should display similar
genetic diversities, levels of sub-division and demographic histories .
The isolation-by-distance model relaxes these assumptions somewhat by
allowing migration rates to be higher among populations in close
proximity compared to more distant ones .
Both the island and isolation-by-distance models assume drift-migration
equilibrium, which may not be met when migration rates are low and/or
genetic bottlenecks are frequent .
In contrast to these island-based models, meta-population theory
attempts to understand systems of evolutionarily ephemeral, genetically
subdivided populations that persist through time via colonisation and
migration from source populations [21-23].
Such populations are connected by migration rates that are high enough
to rescue local populations from extinction, but low enough for genetic
drift to generate measurable genetic differences among populations .
Meta-population dynamics can therefore be distinguished from island
dynamics by low, variable levels of migration among populations. While
earlier models assumed that migration was infrequent, and only
re-colonised patches in which populations had gone extinct [14,15], it is becoming evident that migration rates may be asymmetrical  and can vary temporally [e.g. [25,26]], spatially [e.g. [27-29]] and behaviourally among individuals [e.g. [30-32]].
In turn, such variation in migration rates may generate a diversity of
genetic signatures depending on the relative importance of each process
A comparison of traditional (based on the island model) and
coalescence-based analytical approaches that can separate overall
genetic differentiation into reciprocal migration rates [33,34]
should be able to illuminate the roles of migration and drift in
establishing patterns of genetic differentiation among populations .
Theory suggests that the sources and rates of colonisation relative
to subsequent migration are critical determinants of the evolution of
the genetic structure of meta-populations [18,19,23].
In a meta-population with low levels of migration, the meta-population
propagule-pool model predicts high genetic differentiation among
populations if empty patches are colonised by individuals from a single
This high genetic differentiation results from genetic bottlenecks
arising from founder effects of a few, genetically similar individuals.
In contrast, under the meta-population migrant-pool model, low genetic
differentiation among populations should result if extinct patches are
colonised by many migrants from a larger number of source populations [18,19].
Because the colonisers are numerous and harbour greater genetic
diversity, the re-colonised population will not experience a
bottleneck, and because the genetic diversity is sampled from a range
of sources, differentiation among populations will be decreased under
this model. Under the propagule-pool model, populations will always
display greater genetic differentiation than under an island model
because of genetic bottlenecks associated with low and asymmetric
colonisation rates. In contrast, greater genetic differentiation among
populations will only occur under the migrant-pool meta-population
compared to an island model if rates of colonisation and migration
rates are low [18,19].
Consequently, meta-population dynamics can be distinguished from island
dynamics by a strong but variable level of genetic structure among
populations. Separating the effects of colonisation pattern and
subsequent migration in meta-populations, however, is often difficult
because the relative effects of colonisation and migration cannot be
estimated from a single estimate of genetic differentiation .
If the propagule-pool model is operating, and if migration rates are
low, then populations with younger coalescent histories should display
greater genetic structure among each other compared to that found among
older ones [35,23].
Therefore, it should be possible to distinguish different types of
meta-population dynamics among genetically structured populations by
patterns of genetic differentiation observed among populations that
have experienced more recent population bottlenecks compared to those
with older ones [36-40].
The effects of these meta-population dynamics on spatial genetic
structure have typically been estimated in terms of genetic
differentiation among populations, but may also be evident in patterns
of genetic diversity and demographic history of local populations [23,40,41].
As such, important information about the role of local extinctions in a
meta-population, and its importance in determining the geographic range
of species, may be gained by examining patterns of genetic diversity
and demographic history in sets of local populations [8,42,43].
In general, meta-population dynamics should reduce genetic diversity at
the level of the meta-population and genetic diversity within the
sub-populations compared to a panmictic population of equal size to the
The relative magnitude of this difference, however, may vary greatly
depending on the frequency and intensity of effective population size
reductions among the sub-populations, and the mode of subsequent
re-colonization and migration [
and references therein]. For example, reductions in genetic diversities
may be large where reductions in the effective size of sub-populations
are frequent and large, and if re-colonisation obeys a propagule-pool
model. Coalescence times within sub-populations are also reduced under
this scenario because of genetic bottlenecks associated with
propagule-pool colonisation .
If sub-populations experience minor fluctuations in population size, or
if colonisation obeys a migrant-pool model, where colonisers originate
from a range of populations, sub-populations may not experience genetic
bottlenecks and genetic diversities may not be affected to a measurable
Fishes on coral reefs occupy a naturally fragmented environment
where patches of suitable reef habitat are surrounded by unsuitable
habitat such as open sand and deep water making them amenable to
analysis under a meta-population framework. At present, however, we
know little about the presence, spatial extent and genetic consequences
of meta-populations dynamics in marine systems [, but see ].
Species with short, or non-existent larval durations generally display
considerable genetic structure across small spatial scales [45-48]
and have, therefore, the potential for genetic meta-population
dynamics. Coral reef fishes generally display large effective
population sizes 
and many marine fishes are characterised by relatively shallow
population genetic structures reflecting genetic bottlenecks associated
with Pleistocene climate variation [reviewed by [50,51]].
Genetic bottlenecks following post-Pleistocene extinctions of local
populations have previously been regarded as unimportant in the
population dynamics of coral reef fishes [44,52]. Recent studies, however, have uncovered a diversity of coalescent signatures operating at a range of temporal scales [e.g. [53-58]]
suggesting an important role of demographic bottlenecks and local
extinctions in the evolutionary ecology of coral reef fishes.
Acanthochromis polyacanthus is a common fish on Australia's
Great Barrier Reef (GBR) and lacks a dispersive larval phase. This
life-history trait, coupled with the physical history of the GBR, and
the sensitivity of mitochondrial molecular markers to drift, provides
an opportunity to evaluate the potential importance of meta-population
dynamics to the evolution of genetic structure on small spatial scales
in a natural marine system. Previous investigations of A. polyacanthus,
as well as the presence of several colour morphs on the GBR, suggest
that sufficient time has elapsed since colonisation of the GBR began by
this species for it to have evolved genetic differences among
populations separated by small geographic distances [46,57,59,60].
Here we examine if and how the genetic structure of this species varies
at two spatial scales (i.e. within and among regions). Using
conventional genetic estimates of fixation, we test whether the genetic
structure of this species is best described by equilibrium-island, or
isolation-by-distance models. Next, we examine the evidence for
meta-population dynamics in A. polyacanthus by evaluating
spatial differences in migration rates and conformation to predictions
from the propagule and migrant-pool re-colonisation models. Finally, we
evaluate the role of extinction by comparing patterns of genetic
diversity and demographic history among reefs and regions.
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