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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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Sampling locations of Acanthochromis polyacanthus on the Great Barrier Reef. Fish illustrations indicate the distribution and sampling of colour morphs.
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Figure 1: Sampling locations of Acanthochromis polyacanthus on the Great Barrier Reef. Fish illustrations indicate the distribution and sampling of colour morphs.

Mentions: A region of 356 bases of the mtDNA control region I was obtained from a total of 283 individuals collected from 15 reefs in three regions (Figure 1). The average base frequencies were AT biased (A = 0.41, T = 0.40, C = 0.07, G = 0.12) as commonly observed in fish mtDNA [61,62]. The ts/tv ratio was 1.53:1 for all samples combined. Haplotype diversities were very high when summed over all populations (total ± SD = 0.97 ± 0.0003) and did not differ significantly among regions (Kruskal – Wallis = 0.187, df = 2, p = 0.91). Each region contained one or two reefs with significantly lower haplotype diversities than the rest (i.e., North = YON, Central = TRU, south = OTI and SYK, Table 1). Nucleotide diversities were high overall (total ± SD = 0.066 ± 0.37), and varied significantly among regions (Kruskal – Wallis Test = 10.64, df = 2, p = 0.005). Reefs in the northern region displayed the highest and most variable nucleotide diversities, whereas, nucleotide diversities were lower among locations within the central and southern locations (Table 1).


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)

Sampling locations of Acanthochromis polyacanthus on the Great Barrier Reef. Fish illustrations indicate the distribution and sampling of colour morphs.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Sampling locations of Acanthochromis polyacanthus on the Great Barrier Reef. Fish illustrations indicate the distribution and sampling of colour morphs.
Mentions: A region of 356 bases of the mtDNA control region I was obtained from a total of 283 individuals collected from 15 reefs in three regions (Figure 1). The average base frequencies were AT biased (A = 0.41, T = 0.40, C = 0.07, G = 0.12) as commonly observed in fish mtDNA [61,62]. The ts/tv ratio was 1.53:1 for all samples combined. Haplotype diversities were very high when summed over all populations (total ± SD = 0.97 ± 0.0003) and did not differ significantly among regions (Kruskal – Wallis = 0.187, df = 2, p = 0.91). Each region contained one or two reefs with significantly lower haplotype diversities than the rest (i.e., North = YON, Central = TRU, south = OTI and SYK, Table 1). Nucleotide diversities were high overall (total ± SD = 0.066 ± 0.37), and varied significantly among regions (Kruskal – Wallis Test = 10.64, df = 2, p = 0.005). Reefs in the northern region displayed the highest and most variable nucleotide diversities, whereas, nucleotide diversities were lower among locations within the central and southern locations (Table 1).

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