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

Bay LK, Caley MJ, Crozier RH - BMC Evol. Biol. (2008)

Bottom Line: Variation in genetic diversities, demographic expansion and population growth estimates indicated more frequent genetic bottlenecks/founder effects and subsequent population expansion in the central and southern regions compared to the northern one.Instead, strong non-equilibrium genetic structure appears to be generated by genetic bottlenecks/founder effects associated with population reductions/extinctions and asymmetric migration/(re)-colonisation of such populations.Therefore, coral reef species may experience local population reductions/extinctions that promote overall meta-population genetic differentiation.

View Article: PubMed Central - HTML - PubMed

Affiliation: School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia. line.bay@jcu.edu.au

ABSTRACT

Background: Management strategies for coral reefs are dependant on information about the spatial population structure and connectivity of reef organisms. Genetic tools can reveal important information about population structure, however, this information is lacking for many reef species. We used a mitochondrial molecular marker to examine the population genetic structure and the potential for meta-population dynamics in a direct developing coral reef fish using 283 individuals from 15 reefs on the Great Barrier Reef, Australia. We employed a hierarchical sampling design to test genetic models of population structure at multiple geographical scales including among regions, among shelf position and reefs within regions. Predictions from island, isolation-by-distance and meta-population models, including the potential for asymmetric migration, local extinction and patterns of re-colonisation were examined.

Results: Acanthochromis polyacanthus displayed strong genetic structure among regions (PhiST = 0.81, P < 0.0001) that supported an equilibrium isolation-by-distance model (r = 0.77, P = 0.001). Significant structuring across the continental shelf was only evident in the northern region (PhiST = 0.31, P < 0.001) and no evidence of isolation-by-distance was found within any region. Pairwise PhiST values indicated overall strong but variable genetic structure (mean PhiST among reefs within regions = 0.28, 0.38, 0.41), and asymmetric migration rates among reefs with low genetic structure. Genetic differentiation among younger reefs was greater than among older reefs supporting a meta-population propagule-pool colonisation model. Variation in genetic diversities, demographic expansion and population growth estimates indicated more frequent genetic bottlenecks/founder effects and subsequent population expansion in the central and southern regions compared to the northern one.

Conclusion: Our findings provide genetic evidence for meta-population dynamics in a direct developing coral reef fish and we reject the equilibrium island and isolation-by distance models at local spatial scales. Instead, strong non-equilibrium genetic structure appears to be generated by genetic bottlenecks/founder effects associated with population reductions/extinctions and asymmetric migration/(re)-colonisation of such populations. These meta-population dynamics varied across the geographical range examined with edge populations exhibiting lower genetic diversities and higher rates of population expansion than more central populations. Therefore, coral reef species may experience local population reductions/extinctions that promote overall meta-population genetic differentiation.

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Mismatch distributions of pairwise sequence differences in Acanthochromis polyacanthus among regions and reefs. Panels represent the mismatch frequency distribution of individual reefs (n = 15) or regions (n = 3). Location abbreviations follow Table 1.
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Figure 4: Mismatch distributions of pairwise sequence differences in Acanthochromis polyacanthus among regions and reefs. Panels represent the mismatch frequency distribution of individual reefs (n = 15) or regions (n = 3). Location abbreviations follow Table 1.

Mentions: Three types of mismatch distributions could be distinguished (Figure 4). Five reef samples in the northern region (DAY, NDR, LIZ, LIN, MAR) were characterised by bimodal mismatch distributions (Figure 4) indicating the presence of two genetically divergent lineages (see Additional data file 2). As a consequence these populations displayed greater mismatch means and support for the constant population model was found in LIN (Table 4). Three reef samples (TRU, OTI, SYK) were characterised by narrow left skewed uni-modal mismatch distributions and low mismatch means and support for population expansion was obtained for two of these reefs (Figure 4, Table 4). The remaining populations (n = 7) displayed broader uni-modal mismatch distributions with larger mismatch means (Figure 4). Support for the expansion model was found in three central reefs (PIT, BRI, ORP); the constant population model was supported in three reefs (MYR, POL, BRO and near significant in YON) (Table 4). The age of population expansion (τ) followed a similar pattern to that of the mismatch means and error estimates from most reefs in all three regions overlapped to a great extent (Figure 5a). Greater values with large variances were observed in two northern reefs (NDR and LIN), lower and less variable estimates were found in one central location (TRU) and in two southern locations (OTI and SYK) (Figure 5a). The age of population expansion (τ) could not be distinguished from 0 in four locations: TRU and ORP in the central region and OTI and SYK in the southern region and the neutrality indices indicated population expansion in one of these (TRU) (Table 4 and 5). Population expansion rates varied significantly among reef samples (Figure 5b). All northern locations displayed negative growth rates close to 0. Reefs in the central region showed both positive and negative growth rates that were all close to 0 except TRU that displayed a highly positive value. The high mean regional growth rate in the southern region was contributed to by the high growth rates of three of the four southern reefs. The growth rates of these three reefs were greater than all other reefs analysed except one (TRU in the central region) (Figure 5b).


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

Bay LK, Caley MJ, Crozier RH - BMC Evol. Biol. (2008)

Mismatch distributions of pairwise sequence differences in Acanthochromis polyacanthus among regions and reefs. Panels represent the mismatch frequency distribution of individual reefs (n = 15) or regions (n = 3). Location abbreviations follow Table 1.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC2553088&req=5

Figure 4: Mismatch distributions of pairwise sequence differences in Acanthochromis polyacanthus among regions and reefs. Panels represent the mismatch frequency distribution of individual reefs (n = 15) or regions (n = 3). Location abbreviations follow Table 1.
Mentions: Three types of mismatch distributions could be distinguished (Figure 4). Five reef samples in the northern region (DAY, NDR, LIZ, LIN, MAR) were characterised by bimodal mismatch distributions (Figure 4) indicating the presence of two genetically divergent lineages (see Additional data file 2). As a consequence these populations displayed greater mismatch means and support for the constant population model was found in LIN (Table 4). Three reef samples (TRU, OTI, SYK) were characterised by narrow left skewed uni-modal mismatch distributions and low mismatch means and support for population expansion was obtained for two of these reefs (Figure 4, Table 4). The remaining populations (n = 7) displayed broader uni-modal mismatch distributions with larger mismatch means (Figure 4). Support for the expansion model was found in three central reefs (PIT, BRI, ORP); the constant population model was supported in three reefs (MYR, POL, BRO and near significant in YON) (Table 4). The age of population expansion (τ) followed a similar pattern to that of the mismatch means and error estimates from most reefs in all three regions overlapped to a great extent (Figure 5a). Greater values with large variances were observed in two northern reefs (NDR and LIN), lower and less variable estimates were found in one central location (TRU) and in two southern locations (OTI and SYK) (Figure 5a). The age of population expansion (τ) could not be distinguished from 0 in four locations: TRU and ORP in the central region and OTI and SYK in the southern region and the neutrality indices indicated population expansion in one of these (TRU) (Table 4 and 5). Population expansion rates varied significantly among reef samples (Figure 5b). All northern locations displayed negative growth rates close to 0. Reefs in the central region showed both positive and negative growth rates that were all close to 0 except TRU that displayed a highly positive value. The high mean regional growth rate in the southern region was contributed to by the high growth rates of three of the four southern reefs. The growth rates of these three reefs were greater than all other reefs analysed except one (TRU in the central region) (Figure 5b).

Bottom Line: Variation in genetic diversities, demographic expansion and population growth estimates indicated more frequent genetic bottlenecks/founder effects and subsequent population expansion in the central and southern regions compared to the northern one.Instead, strong non-equilibrium genetic structure appears to be generated by genetic bottlenecks/founder effects associated with population reductions/extinctions and asymmetric migration/(re)-colonisation of such populations.Therefore, coral reef species may experience local population reductions/extinctions that promote overall meta-population genetic differentiation.

View Article: PubMed Central - HTML - PubMed

Affiliation: School of Marine and Tropical Biology, James Cook University, Townsville, Qld 4811, Australia. line.bay@jcu.edu.au

ABSTRACT

Background: Management strategies for coral reefs are dependant on information about the spatial population structure and connectivity of reef organisms. Genetic tools can reveal important information about population structure, however, this information is lacking for many reef species. We used a mitochondrial molecular marker to examine the population genetic structure and the potential for meta-population dynamics in a direct developing coral reef fish using 283 individuals from 15 reefs on the Great Barrier Reef, Australia. We employed a hierarchical sampling design to test genetic models of population structure at multiple geographical scales including among regions, among shelf position and reefs within regions. Predictions from island, isolation-by-distance and meta-population models, including the potential for asymmetric migration, local extinction and patterns of re-colonisation were examined.

Results: Acanthochromis polyacanthus displayed strong genetic structure among regions (PhiST = 0.81, P < 0.0001) that supported an equilibrium isolation-by-distance model (r = 0.77, P = 0.001). Significant structuring across the continental shelf was only evident in the northern region (PhiST = 0.31, P < 0.001) and no evidence of isolation-by-distance was found within any region. Pairwise PhiST values indicated overall strong but variable genetic structure (mean PhiST among reefs within regions = 0.28, 0.38, 0.41), and asymmetric migration rates among reefs with low genetic structure. Genetic differentiation among younger reefs was greater than among older reefs supporting a meta-population propagule-pool colonisation model. Variation in genetic diversities, demographic expansion and population growth estimates indicated more frequent genetic bottlenecks/founder effects and subsequent population expansion in the central and southern regions compared to the northern one.

Conclusion: Our findings provide genetic evidence for meta-population dynamics in a direct developing coral reef fish and we reject the equilibrium island and isolation-by distance models at local spatial scales. Instead, strong non-equilibrium genetic structure appears to be generated by genetic bottlenecks/founder effects associated with population reductions/extinctions and asymmetric migration/(re)-colonisation of such populations. These meta-population dynamics varied across the geographical range examined with edge populations exhibiting lower genetic diversities and higher rates of population expansion than more central populations. Therefore, coral reef species may experience local population reductions/extinctions that promote overall meta-population genetic differentiation.

Show MeSH
Related in: MedlinePlus