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Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp.

Fraser CI, Thiel M, Spencer HG, Waters JM - BMC Evol. Biol. (2010)

Bottom Line: Among populations from central Chile (32 degrees-44 degrees S), substantial phylogeographic structure was evident across small spatial scales, and a significant isolation-by-distance effect was observed.In contrast to the genetic structure found among central Chilean populations, samples from the southern Chilean Patagonian region (49 degrees-56 degrees S) were genetically homogeneous and identical to a haplotype recently found throughout the subantarctic region.We conclude that rafting facilitates colonisation of unoccupied shores, but has limited potential to enhance gene-flow among established populations.

View Article: PubMed Central - HTML - PubMed

Affiliation: Allan Wilson Centre for Molecular Ecology and Evolution, Department of Zoology, University of Otago, 340 Great King St, Dunedin 9016, New Zealand. ceridwen.fraser@gmail.com

ABSTRACT

Background: South America's western coastline, extending in a near-straight line across some 35 latitudinal degrees, presents an elegant setting for assessing both contemporary and historic influences on cladogenesis in the marine environment. Southern bull-kelp (Durvillaea antarctica) has a broad distribution along much of the Chilean coast. This species represents an ideal model taxon for studies of coastal marine connectivity and of palaeoclimatic effects, as it grows only on exposed rocky coasts and is absent from beaches and ice-affected shores. We expected that, along the central Chilean coast, D. antarctica would show considerable phylogeographic structure as a consequence of the isolating effects of distance and habitat discontinuities. In contrast, we hypothesised that further south--throughout the region affected by the Patagonian Ice Sheet at the Last Glacial Maximum (LGM)--D. antarctica would show relatively little genetic structure, reflecting postglacial recolonisation.

Results: Mitochondrial (COI) and chloroplast (rbcL) DNA analyses of D. antarctica from 24 Chilean localities (164 individuals) revealed two deeply divergent (4.5 - 6.1% for COI, 1.4% for rbcL) clades from the centre and south of the country, with contrasting levels and patterns of genetic structure. Among populations from central Chile (32 degrees-44 degrees S), substantial phylogeographic structure was evident across small spatial scales, and a significant isolation-by-distance effect was observed. Genetic disjunctions in this region appear to correspond to the presence of long beaches. In contrast to the genetic structure found among central Chilean populations, samples from the southern Chilean Patagonian region (49 degrees-56 degrees S) were genetically homogeneous and identical to a haplotype recently found throughout the subantarctic region.

Conclusions: Southern (Patagonian) Chile has been recolonised by D. antarctica relatively recently, probably since the LGM. The inferred trans-oceanic ancestry of these Patagonian populations supports the notion that D. antarctica is capable of long-distance dispersal via rafting. In contrast, further north in central Chile, the correspondence of genetic disjunctions in D. antarctica with long beaches indicates that habitat discontinuity drives genetic isolation among established kelp populations. We conclude that rafting facilitates colonisation of unoccupied shores, but has limited potential to enhance gene-flow among established populations. Broadly, this study demonstrates that some taxa may be considered to have either high or low dispersal potential across different temporal and geographic scales.

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The effect of beach length on phylogeographic structure in bull-kelp in central Chile. Maximum length of beaches between pairs of adjacent sampled localities in central Chile [data estimated from Google Earth satellite images]. Upper: locality pairs between which there is a marked mitochondrial (COI) genetic disjunction (Nei's raw average pairwise difference, D, > 1.0) are shown in black, whereas genetically-similar locality pairs (D < 1.0) are shown in grey. Lower: Nei's raw average pairwise differences (D) for COI, plotted against maximum uninterrupted beach length, between all adjacent locality pairs in central Chile.
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Figure 5: The effect of beach length on phylogeographic structure in bull-kelp in central Chile. Maximum length of beaches between pairs of adjacent sampled localities in central Chile [data estimated from Google Earth satellite images]. Upper: locality pairs between which there is a marked mitochondrial (COI) genetic disjunction (Nei's raw average pairwise difference, D, > 1.0) are shown in black, whereas genetically-similar locality pairs (D < 1.0) are shown in grey. Lower: Nei's raw average pairwise differences (D) for COI, plotted against maximum uninterrupted beach length, between all adjacent locality pairs in central Chile.

Mentions: The Mantel test revealed a significant relationship between genetic and geographic distance (P = 0.015 for 999 permutations) (Fig. 4). Detailed geographic analyses based on maximum uninterrupted beach length between pairs of adjacent sampling locations in central Chile revealed a clear relationship between rocky shore habitat continuity and genetic connectivity along the central Chilean coast (Fig. 5). Under the definition of genetic disjunction corresponding to Nei's D ≥1.0, no 'disjunct' locality pairs shared any haplotypes. Notably, all phylogeographic disjunctions in central Chilean D. antarctica were associated with extensive (> 20 km) beaches (Fig. 5). The only adjacent locality pair separated by a beach > 20 km long that did not show a genetic disjunction was Lebu/Tirua (locality pair J in Fig. 5), separated by 62 km of uninterrupted beach. Logistic regression (with the binomial response variable of 'genetically disjunct or not', and the continuous fixed effects 'maximum beach length between adjacent localities' and 'coastal distance between adjacent localities') revealed that maximum beach length was a significant predictor of genetic disjunction (β = 0.05; P = 0.035; N = 15), whereas total coastal distance was not (β = 0.01; P = 0.608; N = 15). The outlier formed by Lebu/Tirua (locality pair J, Fig. 5) is, however, likely having a strong effect on the analysis; indeed, removing this locality pair from the analyses greatly strengthens the effect of long beaches in the logistic regression (β = 0.23; P = 0.002; N = 14). With or without the outlier, these results indicate that habitat discontinuity influences genetic connectivity among populations of central Chilean bull-kelp.


Contemporary habitat discontinuity and historic glacial ice drive genetic divergence in Chilean kelp.

Fraser CI, Thiel M, Spencer HG, Waters JM - BMC Evol. Biol. (2010)

The effect of beach length on phylogeographic structure in bull-kelp in central Chile. Maximum length of beaches between pairs of adjacent sampled localities in central Chile [data estimated from Google Earth satellite images]. Upper: locality pairs between which there is a marked mitochondrial (COI) genetic disjunction (Nei's raw average pairwise difference, D, > 1.0) are shown in black, whereas genetically-similar locality pairs (D < 1.0) are shown in grey. Lower: Nei's raw average pairwise differences (D) for COI, plotted against maximum uninterrupted beach length, between all adjacent locality pairs in central Chile.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3020628&req=5

Figure 5: The effect of beach length on phylogeographic structure in bull-kelp in central Chile. Maximum length of beaches between pairs of adjacent sampled localities in central Chile [data estimated from Google Earth satellite images]. Upper: locality pairs between which there is a marked mitochondrial (COI) genetic disjunction (Nei's raw average pairwise difference, D, > 1.0) are shown in black, whereas genetically-similar locality pairs (D < 1.0) are shown in grey. Lower: Nei's raw average pairwise differences (D) for COI, plotted against maximum uninterrupted beach length, between all adjacent locality pairs in central Chile.
Mentions: The Mantel test revealed a significant relationship between genetic and geographic distance (P = 0.015 for 999 permutations) (Fig. 4). Detailed geographic analyses based on maximum uninterrupted beach length between pairs of adjacent sampling locations in central Chile revealed a clear relationship between rocky shore habitat continuity and genetic connectivity along the central Chilean coast (Fig. 5). Under the definition of genetic disjunction corresponding to Nei's D ≥1.0, no 'disjunct' locality pairs shared any haplotypes. Notably, all phylogeographic disjunctions in central Chilean D. antarctica were associated with extensive (> 20 km) beaches (Fig. 5). The only adjacent locality pair separated by a beach > 20 km long that did not show a genetic disjunction was Lebu/Tirua (locality pair J in Fig. 5), separated by 62 km of uninterrupted beach. Logistic regression (with the binomial response variable of 'genetically disjunct or not', and the continuous fixed effects 'maximum beach length between adjacent localities' and 'coastal distance between adjacent localities') revealed that maximum beach length was a significant predictor of genetic disjunction (β = 0.05; P = 0.035; N = 15), whereas total coastal distance was not (β = 0.01; P = 0.608; N = 15). The outlier formed by Lebu/Tirua (locality pair J, Fig. 5) is, however, likely having a strong effect on the analysis; indeed, removing this locality pair from the analyses greatly strengthens the effect of long beaches in the logistic regression (β = 0.23; P = 0.002; N = 14). With or without the outlier, these results indicate that habitat discontinuity influences genetic connectivity among populations of central Chilean bull-kelp.

Bottom Line: Among populations from central Chile (32 degrees-44 degrees S), substantial phylogeographic structure was evident across small spatial scales, and a significant isolation-by-distance effect was observed.In contrast to the genetic structure found among central Chilean populations, samples from the southern Chilean Patagonian region (49 degrees-56 degrees S) were genetically homogeneous and identical to a haplotype recently found throughout the subantarctic region.We conclude that rafting facilitates colonisation of unoccupied shores, but has limited potential to enhance gene-flow among established populations.

View Article: PubMed Central - HTML - PubMed

Affiliation: Allan Wilson Centre for Molecular Ecology and Evolution, Department of Zoology, University of Otago, 340 Great King St, Dunedin 9016, New Zealand. ceridwen.fraser@gmail.com

ABSTRACT

Background: South America's western coastline, extending in a near-straight line across some 35 latitudinal degrees, presents an elegant setting for assessing both contemporary and historic influences on cladogenesis in the marine environment. Southern bull-kelp (Durvillaea antarctica) has a broad distribution along much of the Chilean coast. This species represents an ideal model taxon for studies of coastal marine connectivity and of palaeoclimatic effects, as it grows only on exposed rocky coasts and is absent from beaches and ice-affected shores. We expected that, along the central Chilean coast, D. antarctica would show considerable phylogeographic structure as a consequence of the isolating effects of distance and habitat discontinuities. In contrast, we hypothesised that further south--throughout the region affected by the Patagonian Ice Sheet at the Last Glacial Maximum (LGM)--D. antarctica would show relatively little genetic structure, reflecting postglacial recolonisation.

Results: Mitochondrial (COI) and chloroplast (rbcL) DNA analyses of D. antarctica from 24 Chilean localities (164 individuals) revealed two deeply divergent (4.5 - 6.1% for COI, 1.4% for rbcL) clades from the centre and south of the country, with contrasting levels and patterns of genetic structure. Among populations from central Chile (32 degrees-44 degrees S), substantial phylogeographic structure was evident across small spatial scales, and a significant isolation-by-distance effect was observed. Genetic disjunctions in this region appear to correspond to the presence of long beaches. In contrast to the genetic structure found among central Chilean populations, samples from the southern Chilean Patagonian region (49 degrees-56 degrees S) were genetically homogeneous and identical to a haplotype recently found throughout the subantarctic region.

Conclusions: Southern (Patagonian) Chile has been recolonised by D. antarctica relatively recently, probably since the LGM. The inferred trans-oceanic ancestry of these Patagonian populations supports the notion that D. antarctica is capable of long-distance dispersal via rafting. In contrast, further north in central Chile, the correspondence of genetic disjunctions in D. antarctica with long beaches indicates that habitat discontinuity drives genetic isolation among established kelp populations. We conclude that rafting facilitates colonisation of unoccupied shores, but has limited potential to enhance gene-flow among established populations. Broadly, this study demonstrates that some taxa may be considered to have either high or low dispersal potential across different temporal and geographic scales.

Show MeSH