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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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Haplotype networks and global projection. COI haplotype network diagrams of D. antarctica for A) the 'central Chilean' clade and B) the 'Patagonian/subantarctic' clade (see also [19]), with circle size scaled approximately according to haplotype frequency, and small dots representing undetected, hypothetical haplotypes. Although the 'Patagonian/subantarctic' and 'New Zealand south' clades [19] joined parsimoniously using network analysis, the 'central Chilean' clade did not join to any other lineages at ≥90% confidence limit: a hypothetical, non-statistically supported connection between the major clades is indicated with a red dashed line. The most common (C-I/red) haplotype was found throughout Chilean Patagonia [this study] and the subantarctic [19]. C) Global projection showing locations of other (subantarctic) sites at which the Patagonian (C-I/red) haplotype has previously been detected [19]. The eastward flow of the Antarctic Circumpolar Current (ACC) is indicated.
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Figure 3: Haplotype networks and global projection. COI haplotype network diagrams of D. antarctica for A) the 'central Chilean' clade and B) the 'Patagonian/subantarctic' clade (see also [19]), with circle size scaled approximately according to haplotype frequency, and small dots representing undetected, hypothetical haplotypes. Although the 'Patagonian/subantarctic' and 'New Zealand south' clades [19] joined parsimoniously using network analysis, the 'central Chilean' clade did not join to any other lineages at ≥90% confidence limit: a hypothetical, non-statistically supported connection between the major clades is indicated with a red dashed line. The most common (C-I/red) haplotype was found throughout Chilean Patagonia [this study] and the subantarctic [19]. C) Global projection showing locations of other (subantarctic) sites at which the Patagonian (C-I/red) haplotype has previously been detected [19]. The eastward flow of the Antarctic Circumpolar Current (ACC) is indicated.

Mentions: Phylogenetic analyses of COI revealed that 13 of the D. antarctica haplotypes in Chile (C-II to C-XIV) were restricted to populations in central Chile, whereas all sampled Chilean Patagonian populations south of 44°S were fixed for a single haplotype (C-I), which was highly divergent from the others (Fig. 2). The widespread Patagonian haplotype, C-I, was previously detected at numerous subantarctic locations throughout the Southern Hemisphere [19] (Fig. 3). With the exception of the Patagonian haplotype (C-I), all (central) Chilean haplotypes (C-II - C-XIV) were closely related to one another (uncorrected distances 0.2 - 1.3%), together forming a strongly supported clade (Bayesian PP 1.00; Fig. 2a); by contrast, the Patagonian haplotype (C-I) was markedly divergent from all other Chilean haplotypes (C-II - C-XIV) (uncorrected distances 4.5 - 6.1%). The two chloroplast (rbcL) haplotypes detected in Chile were 1.4% divergent (uncorrected distance), with one (R-I) restricted to all sampled Patagonian populations, and the other (R-II) found only in central Chile (Cucao, Punta Loncoyen, Tumbes, Constitución, Montemar and Pichicuy). More broadly, the Patagonian rbcL haplotype R-I has a circum-subantarctic distribution, including the Falkland Islands and South Georgia (not shown; [19]).


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)

Haplotype networks and global projection. COI haplotype network diagrams of D. antarctica for A) the 'central Chilean' clade and B) the 'Patagonian/subantarctic' clade (see also [19]), with circle size scaled approximately according to haplotype frequency, and small dots representing undetected, hypothetical haplotypes. Although the 'Patagonian/subantarctic' and 'New Zealand south' clades [19] joined parsimoniously using network analysis, the 'central Chilean' clade did not join to any other lineages at ≥90% confidence limit: a hypothetical, non-statistically supported connection between the major clades is indicated with a red dashed line. The most common (C-I/red) haplotype was found throughout Chilean Patagonia [this study] and the subantarctic [19]. C) Global projection showing locations of other (subantarctic) sites at which the Patagonian (C-I/red) haplotype has previously been detected [19]. The eastward flow of the Antarctic Circumpolar Current (ACC) is indicated.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
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Figure 3: Haplotype networks and global projection. COI haplotype network diagrams of D. antarctica for A) the 'central Chilean' clade and B) the 'Patagonian/subantarctic' clade (see also [19]), with circle size scaled approximately according to haplotype frequency, and small dots representing undetected, hypothetical haplotypes. Although the 'Patagonian/subantarctic' and 'New Zealand south' clades [19] joined parsimoniously using network analysis, the 'central Chilean' clade did not join to any other lineages at ≥90% confidence limit: a hypothetical, non-statistically supported connection between the major clades is indicated with a red dashed line. The most common (C-I/red) haplotype was found throughout Chilean Patagonia [this study] and the subantarctic [19]. C) Global projection showing locations of other (subantarctic) sites at which the Patagonian (C-I/red) haplotype has previously been detected [19]. The eastward flow of the Antarctic Circumpolar Current (ACC) is indicated.
Mentions: Phylogenetic analyses of COI revealed that 13 of the D. antarctica haplotypes in Chile (C-II to C-XIV) were restricted to populations in central Chile, whereas all sampled Chilean Patagonian populations south of 44°S were fixed for a single haplotype (C-I), which was highly divergent from the others (Fig. 2). The widespread Patagonian haplotype, C-I, was previously detected at numerous subantarctic locations throughout the Southern Hemisphere [19] (Fig. 3). With the exception of the Patagonian haplotype (C-I), all (central) Chilean haplotypes (C-II - C-XIV) were closely related to one another (uncorrected distances 0.2 - 1.3%), together forming a strongly supported clade (Bayesian PP 1.00; Fig. 2a); by contrast, the Patagonian haplotype (C-I) was markedly divergent from all other Chilean haplotypes (C-II - C-XIV) (uncorrected distances 4.5 - 6.1%). The two chloroplast (rbcL) haplotypes detected in Chile were 1.4% divergent (uncorrected distance), with one (R-I) restricted to all sampled Patagonian populations, and the other (R-II) found only in central Chile (Cucao, Punta Loncoyen, Tumbes, Constitución, Montemar and Pichicuy). More broadly, the Patagonian rbcL haplotype R-I has a circum-subantarctic distribution, including the Falkland Islands and South Georgia (not shown; [19]).

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