- Meta-population structure in a coral reef fish demonstrated by genetic data on patterns of migration, extinction and re-colonisation

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 [5] 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 [5], but comparatively little attention has been placed on examining predictions from meta-population theory [8] 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 [9] 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 [20]. When these assumptions are met, populations should display similar genetic diversities, levels of sub-division and demographic histories [20]. 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 [20]. 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 [8].

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 [22]. 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 [24] 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 [24]. 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 [8].

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 source [18,19]. 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 [35]. 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 meta-population [40]. 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 [[40] 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 [40]. 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 extent [23,40,41].

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 [[8], but see [44]]. 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 [49] 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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