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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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Pairwise genetic distances and asymmetric migration rates among reefs within regions. The thickness of arrows indicates the strength of genetic structure (ΦST: a – c) or rate of migration (4Nem: d – f) and the colour indicates statistical difference. For pairwise genetic distances black arrows indicate estimates significantly different from 0. For migration rates black arrows indicate that reciprocal estimates were different (95% confidence intervals of did not overlap) and grey arrows indicate that reciprocal estimates were not different (95% confidence intervals of estimates overlapped).
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Figure 3: Pairwise genetic distances and asymmetric migration rates among reefs within regions. The thickness of arrows indicates the strength of genetic structure (ΦST: a – c) or rate of migration (4Nem: d – f) and the colour indicates statistical difference. For pairwise genetic distances black arrows indicate estimates significantly different from 0. For migration rates black arrows indicate that reciprocal estimates were different (95% confidence intervals of did not overlap) and grey arrows indicate that reciprocal estimates were not different (95% confidence intervals of estimates overlapped).

Mentions: Pairwise ΦST estimates were significantly greater than 0 in more than 97% of all pairwise comparisons. Levels of genetic differentiation differed among reefs but the range of differentiation among reefs was similar within each of the three regions (Kruskal – Wallis Test = 1.21 df = 2, p = 0.55, Figure 3a – c, see Additional file 1). There was substantial variation in migration rates among reef samples and regions (Figure 3d – f). Migration rates were generally low (4Nem mostly < 1) and the frequency of significantly different reciprocal rates was higher in the southern region (i.e. 4Nem (x to y) vs. 4Nem (y to x): north = 23%, central = 20% and southern = 42%) (Figure 3d – f). All regions were characterised by one or two migration rates being significantly higher (4Nem ~ 4) than all other estimates. The level of fixation was greater between reef samples with more recent population expansions compared to the level of fixation among reef samples with older population expansions providing tentative support for the meta-population propagule-pool model of re-colonisation (Table 3).


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)

Pairwise genetic distances and asymmetric migration rates among reefs within regions. The thickness of arrows indicates the strength of genetic structure (ΦST: a – c) or rate of migration (4Nem: d – f) and the colour indicates statistical difference. For pairwise genetic distances black arrows indicate estimates significantly different from 0. For migration rates black arrows indicate that reciprocal estimates were different (95% confidence intervals of did not overlap) and grey arrows indicate that reciprocal estimates were not different (95% confidence intervals of estimates overlapped).
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 3: Pairwise genetic distances and asymmetric migration rates among reefs within regions. The thickness of arrows indicates the strength of genetic structure (ΦST: a – c) or rate of migration (4Nem: d – f) and the colour indicates statistical difference. For pairwise genetic distances black arrows indicate estimates significantly different from 0. For migration rates black arrows indicate that reciprocal estimates were different (95% confidence intervals of did not overlap) and grey arrows indicate that reciprocal estimates were not different (95% confidence intervals of estimates overlapped).
Mentions: Pairwise ΦST estimates were significantly greater than 0 in more than 97% of all pairwise comparisons. Levels of genetic differentiation differed among reefs but the range of differentiation among reefs was similar within each of the three regions (Kruskal – Wallis Test = 1.21 df = 2, p = 0.55, Figure 3a – c, see Additional file 1). There was substantial variation in migration rates among reef samples and regions (Figure 3d – f). Migration rates were generally low (4Nem mostly < 1) and the frequency of significantly different reciprocal rates was higher in the southern region (i.e. 4Nem (x to y) vs. 4Nem (y to x): north = 23%, central = 20% and southern = 42%) (Figure 3d – f). All regions were characterised by one or two migration rates being significantly higher (4Nem ~ 4) than all other estimates. The level of fixation was greater between reef samples with more recent population expansions compared to the level of fixation among reef samples with older population expansions providing tentative support for the meta-population propagule-pool model of re-colonisation (Table 3).

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