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Living in the past: phylogeography and population histories of Indo-Pacific wrasses (genus Halichoeres) in shallow lagoons versus outer reef slopes.

Ludt WB, Bernal MA, Bowen BW, Rocha LA - PLoS ONE (2012)

Bottom Line: The outer reef species showed significantly less population structure, consistent with longer pelagic larval durations.Mismatch distributions and significant negative Fu's F values indicate Pleistocene population expansion for all species, and (contrary to expectations) shallower histories in the outer slope species.We conclude that lagoonal wrasses may persist through glacial habitat disruptions, but are restricted to refugia during lower sea level stands.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Science, University of Texas, Austin, Texas, United States of America. wbludt@gmail.com

ABSTRACT
Sea level fluctuations during glacial cycles affect the distribution of shallow marine biota, exposing the continental shelf on a global scale, and displacing coral reef habitat to steep slopes on oceanic islands. In these circumstances we expect that species inhabiting lagoons should show shallow genetic architecture relative to species inhabiting more stable outer reefs. Here we test this expectation on an ocean-basin scale with four wrasses (genus Halichoeres): H. claudia (N = 194, with ocean-wide distribution) and H. ornatissimus (N = 346, a Hawaiian endemic) inhabit seaward reef slopes, whereas H. trimaculatus (N = 239) and H. margaritaceus (N = 118) inhabit lagoons and shallow habitats throughout the Pacific. Two mitochondrial markers (cytochrome oxidase I and control region) were sequenced to resolve population structure and history of each species. Haplotype and nucleotide diversity were similar among all four species. The outer reef species showed significantly less population structure, consistent with longer pelagic larval durations. Mismatch distributions and significant negative Fu's F values indicate Pleistocene population expansion for all species, and (contrary to expectations) shallower histories in the outer slope species. We conclude that lagoonal wrasses may persist through glacial habitat disruptions, but are restricted to refugia during lower sea level stands. In contrast, outer reef slope species have homogeneous and well-connected populations through their entire ranges regardless of sea level fluctuations. These findings contradict the hypothesis that shallow species are less genetically diverse as a consequence of glacial cycles.

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Haplotype diversities for each of four Halichoeres species.Haplotype diversities for each of four Halichoeres species with error bars. CO1 (dark grey) indicates diversities for the cytochrome oxidase subunit 1 fragment, CR (light grey) indicates diversities for the control region fragment.
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pone-0038042-g004: Haplotype diversities for each of four Halichoeres species.Haplotype diversities for each of four Halichoeres species with error bars. CO1 (dark grey) indicates diversities for the cytochrome oxidase subunit 1 fragment, CR (light grey) indicates diversities for the control region fragment.

Mentions: A 526–559 bp segment of CO1, depending on the species, was obtained from 787 individuals, as well as a 252–343 bp segment of the CR from 723 individuals. Slope inhabitant Halichoeres claudia had 31 haplotypes for CO1 and 110 haplotypes for CR with 18 and 102 unique haplotypes (observed in single individuals), respectively (Fig. 2a & 3a). The minimum spanning network for CO1 shows a star pattern with the majority of individuals (65%) belonging to one haplotype (Fig. 2a). Overall haplotype diversity was 0.572±0.049 for CO1, and 0.996±0.002 for CR. Nucleotide diversity was 0.0018±0.0014 for CO1 and 0.0256±0.0135 for CR. Slope inhabitant H. ornatissimus was sampled at 12 locations across the Hawaiian archipelago, plus adjacent Johnston Atoll. CO1 had 34 haplotypes (21 unique), and CR had 162 haplotypes (122 unique; Fig. 2b). Similar to H. claudia, CO1 minimum spanning networks for H. ornatissimus show a star like pattern dominated by a single haplotype (Fig. 2b). Overall haplotype diversity was 0.407±0.036 for CO1 and 0.981±0.004 for CR. Nucleotide diversity was 0.0011±0.0010 for CO1 and 0.0268±0.0140 for CR. Lagoon inhabitant H. trimaculatus had 32 haplotypes for CO1 (26 unique), and 100 haplotypes for CR (78 unique; Fig. 2c & 3b). The CO1 minimum spanning network for H. trimaculatus shows three common haplotypes, each separated by one transition (Fig. 2c). Overall haplotype diversity was 0.754±0.017 for CO1 and 0.967±0.007 for CR. Nucleotide diversity was 0.0058±0.0033 for CO1 and 0.0268±0.0140 for CR. Lagoon inhabitant H. margaritaceus had 27 haplotypes for CO1 (18 unique), and 75 haplotypes for CR (66 unique; Fig. 2d & 3c). Overall haplotype diversity was 0.821±0.030 for CO1 and 0.994±0.003 for CR. Nucleotide diversities were 0.0022±0.0016 for CO1 and 0.0400±0.0200 for CR. Haplotype diversity and nucleotide diversities by sampling locations are provided in Tables 1 and 2 and a visual representation of overall haplotype diversity between species is provided in Figure 4. Overall haplotype and nucleotide diversity, ΦST estimates, and effective population sizes (NE) can be found in Table S1. Samples have been uploaded in GenBank with accession numbers JQ724865-JQ725555.


Living in the past: phylogeography and population histories of Indo-Pacific wrasses (genus Halichoeres) in shallow lagoons versus outer reef slopes.

Ludt WB, Bernal MA, Bowen BW, Rocha LA - PLoS ONE (2012)

Haplotype diversities for each of four Halichoeres species.Haplotype diversities for each of four Halichoeres species with error bars. CO1 (dark grey) indicates diversities for the cytochrome oxidase subunit 1 fragment, CR (light grey) indicates diversities for the control region fragment.
© Copyright Policy
Related In: Results  -  Collection

Show All Figures
getmorefigures.php?uid=PMC3368945&req=5

pone-0038042-g004: Haplotype diversities for each of four Halichoeres species.Haplotype diversities for each of four Halichoeres species with error bars. CO1 (dark grey) indicates diversities for the cytochrome oxidase subunit 1 fragment, CR (light grey) indicates diversities for the control region fragment.
Mentions: A 526–559 bp segment of CO1, depending on the species, was obtained from 787 individuals, as well as a 252–343 bp segment of the CR from 723 individuals. Slope inhabitant Halichoeres claudia had 31 haplotypes for CO1 and 110 haplotypes for CR with 18 and 102 unique haplotypes (observed in single individuals), respectively (Fig. 2a & 3a). The minimum spanning network for CO1 shows a star pattern with the majority of individuals (65%) belonging to one haplotype (Fig. 2a). Overall haplotype diversity was 0.572±0.049 for CO1, and 0.996±0.002 for CR. Nucleotide diversity was 0.0018±0.0014 for CO1 and 0.0256±0.0135 for CR. Slope inhabitant H. ornatissimus was sampled at 12 locations across the Hawaiian archipelago, plus adjacent Johnston Atoll. CO1 had 34 haplotypes (21 unique), and CR had 162 haplotypes (122 unique; Fig. 2b). Similar to H. claudia, CO1 minimum spanning networks for H. ornatissimus show a star like pattern dominated by a single haplotype (Fig. 2b). Overall haplotype diversity was 0.407±0.036 for CO1 and 0.981±0.004 for CR. Nucleotide diversity was 0.0011±0.0010 for CO1 and 0.0268±0.0140 for CR. Lagoon inhabitant H. trimaculatus had 32 haplotypes for CO1 (26 unique), and 100 haplotypes for CR (78 unique; Fig. 2c & 3b). The CO1 minimum spanning network for H. trimaculatus shows three common haplotypes, each separated by one transition (Fig. 2c). Overall haplotype diversity was 0.754±0.017 for CO1 and 0.967±0.007 for CR. Nucleotide diversity was 0.0058±0.0033 for CO1 and 0.0268±0.0140 for CR. Lagoon inhabitant H. margaritaceus had 27 haplotypes for CO1 (18 unique), and 75 haplotypes for CR (66 unique; Fig. 2d & 3c). Overall haplotype diversity was 0.821±0.030 for CO1 and 0.994±0.003 for CR. Nucleotide diversities were 0.0022±0.0016 for CO1 and 0.0400±0.0200 for CR. Haplotype diversity and nucleotide diversities by sampling locations are provided in Tables 1 and 2 and a visual representation of overall haplotype diversity between species is provided in Figure 4. Overall haplotype and nucleotide diversity, ΦST estimates, and effective population sizes (NE) can be found in Table S1. Samples have been uploaded in GenBank with accession numbers JQ724865-JQ725555.

Bottom Line: The outer reef species showed significantly less population structure, consistent with longer pelagic larval durations.Mismatch distributions and significant negative Fu's F values indicate Pleistocene population expansion for all species, and (contrary to expectations) shallower histories in the outer slope species.We conclude that lagoonal wrasses may persist through glacial habitat disruptions, but are restricted to refugia during lower sea level stands.

View Article: PubMed Central - PubMed

Affiliation: Department of Marine Science, University of Texas, Austin, Texas, United States of America. wbludt@gmail.com

ABSTRACT
Sea level fluctuations during glacial cycles affect the distribution of shallow marine biota, exposing the continental shelf on a global scale, and displacing coral reef habitat to steep slopes on oceanic islands. In these circumstances we expect that species inhabiting lagoons should show shallow genetic architecture relative to species inhabiting more stable outer reefs. Here we test this expectation on an ocean-basin scale with four wrasses (genus Halichoeres): H. claudia (N = 194, with ocean-wide distribution) and H. ornatissimus (N = 346, a Hawaiian endemic) inhabit seaward reef slopes, whereas H. trimaculatus (N = 239) and H. margaritaceus (N = 118) inhabit lagoons and shallow habitats throughout the Pacific. Two mitochondrial markers (cytochrome oxidase I and control region) were sequenced to resolve population structure and history of each species. Haplotype and nucleotide diversity were similar among all four species. The outer reef species showed significantly less population structure, consistent with longer pelagic larval durations. Mismatch distributions and significant negative Fu's F values indicate Pleistocene population expansion for all species, and (contrary to expectations) shallower histories in the outer slope species. We conclude that lagoonal wrasses may persist through glacial habitat disruptions, but are restricted to refugia during lower sea level stands. In contrast, outer reef slope species have homogeneous and well-connected populations through their entire ranges regardless of sea level fluctuations. These findings contradict the hypothesis that shallow species are less genetically diverse as a consequence of glacial cycles.

Show MeSH
Related in: MedlinePlus