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Cited by 191Genetic diversity and population structureCoral and Marine Ecosystems StudiesFish Biology and Ecology Studies

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Phylogeography of the reef fish Cephalopholis argus (Epinephelidae) indicates Pleistocene isolation across the indo-pacific barrier with contemporary overlap in the coral triangle

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Gaither, Michelle R, Bowen, Brian W, Bordenave, Tiana-Rae, Rocha, Luiz A, Newman, Stephen J, Gomez, Juan A, van Herwerden, Lynne, Craig, Matthew T·2011·BMC Evolutionary Biology
DOI 10.1186/1471-2148-11-189PMC PMC3145601
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Abstract

BACKGROUND: The Coral Triangle (CT), bounded by the Philippines, the Malay Peninsula, and New Guinea, is the epicenter of marine biodiversity. Hypotheses that explain the source of this rich biodiversity include 1) the center of origin, 2) the center of accumulation, and 3) the region of overlap. Here we contribute to the debate with a phylogeographic survey of a widely distributed reef fish, the Peacock Grouper (Cephalopholis argus; Epinephelidae) at 21 locations (N = 550) using DNA sequence data from mtDNA cytochrome b and two nuclear introns (gonadotropin-releasing hormone and S7 ribosomal protein). RESULTS: Population structure was significant (ΦST = 0.297, P < 0.001; FST = 0.078, P < 0.001; FST = 0.099, P < 0.001 for the three loci, respectively) among five regions: French Polynesia, the central-west Pacific (Line Islands to northeastern Australia), Indo-Pacific boundary (Bali and Rowley Shoals), eastern Indian Ocean (Cocos/Keeling and Christmas Island), and western Indian Ocean (Diego Garcia, Oman, and Seychelles). A strong signal of isolation by distance was detected in both mtDNA (r = 0.749, P = 0.001) and the combined nuclear loci (r = 0.715, P < 0.001). We detected evidence of population expansion with migration toward the CT. Two clusters of haplotypes were detected in the mtDNA data (d = 0.008), corresponding to the Pacific and Indian Oceans, with a low level of introgression observed outside a mixing zone at the Pacific-Indian boundary. CONCLUSIONS: We conclude that the Indo-Pacific Barrier, operating during low sea level associated with glaciation, defines the primary phylogeographic pattern in this species. These data support a scenario of isolation on the scale of 105 year glacial cycles, followed by population expansion toward the CT, and overlap of divergent lineages at the Pacific-Indian boundary. This pattern of isolation, divergence, and subsequent overlap likely contributes to species richness at the adjacent CT and is consistent with the region of overlap hypothesis.

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Crossref · 10.1186/1471-2148-11-189

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Figures

Figure 1 Map of study area. Pie charts represent the ratio of individuals at each location with either the Pacific or Indian Ocean lineage as defined in Figure 2 (Photo credit: Luiz Rocha).
Figure 1 Map of study area. Pie charts represent the ratio of individuals at each location with either the Pacific or Indian Ocean lineage as defined in Figure 2 (Photo credit: Luiz Rocha).CC BY · PubMed Central
Figure 2 Median-joining networks for Cephalopholis argus. Networks were constructed using the program NETWORK 4.5 [43] for (a) 550 cytochrome b sequences (b) alleles at GnRH intron from 488 individuals, and (c) alleles at S7 intron for 490 individuals. Each circle represents one mitochondrial haplotype or nuclear allele with the area of each circle proportional to the number of that particular haplotype or allele in the dataset; dashes represent hypothetical haplotypes or alleles; colors represent collection location (see key).
Figure 2 Median-joining networks for Cephalopholis argus. Networks were constructed using the program NETWORK 4.5 [43] for (a) 550 cytochrome b sequences (b) alleles at GnRH intron from 488 individuals, and (c) alleles at S7 intron for 490 individuals. Each circle represents one mitochondrial haplotype or nuclear allele with the area of each circle proportional to the number of that particular haplotype or allele in the dataset; dashes represent hypothetical haplotypes or alleles; colors represent collection location (see key).CC BY · PubMed Central
Figure 3 Phylogenetic tree of Cephalopholis argus cytochrome b haplotypes. The best maximum likelihood tree generated using program default settings in RAxML [44] and rooted using two congenerics (C. urodeta and C. taeniops). Bootstrap support values were calculated using default settings with 1000 replicates. For comparison neighbor-joining bootstrap values (1000 bootstrap replicates) and Bayesian posterior probabilities are presented. Colored bars delineate the Pacific and Indian Ocean lineages separated by three fixed differences (see figure 1).
Figure 3 Phylogenetic tree of Cephalopholis argus cytochrome b haplotypes. The best maximum likelihood tree generated using program default settings in RAxML [44] and rooted using two congenerics (C. urodeta and C. taeniops). Bootstrap support values were calculated using default settings with 1000 replicates. For comparison neighbor-joining bootstrap values (1000 bootstrap replicates) and Bayesian posterior probabilities are presented. Colored bars delineate the Pacific and Indian Ocean lineages separated by three fixed differences (see figure 1).CC BY · PubMed Central
Figure 4 Mismatch distribution for Cephalopholis argus. Mismatch distribution based on 550 cytochrome b sequences from twenty-one populations. The dark colored line represents the observed and light colored line is the simulated pairwise differences as reported by DnaSP 5.0 [39]. The Harpending's raggedness index as calculated in ARLEQUIN 3.5 [42] and corresponding P-value are shown.
Figure 4 Mismatch distribution for Cephalopholis argus. Mismatch distribution based on 550 cytochrome b sequences from twenty-one populations. The dark colored line represents the observed and light colored line is the simulated pairwise differences as reported by DnaSP 5.0 [39]. The Harpending's raggedness index as calculated in ARLEQUIN 3.5 [42] and corresponding P-value are shown.CC BY · PubMed Central
Figure 5 Migration rates for Cephalopholis argus. Migration rates (Nm: where N is effective female population size and m is migration rate) based on cytochrome b sequences calculated using MIGRATE 3.1.6 [54,55]. Locations with non-significant pairwise ΦST values were grouped (see Table 2). French Polynesia (FP) = Marquesas and Moorea; central-west Pacific (CW) = Kiritimati, Palmyra, Samoa/Tokelau, Baker/Howland, Kwajalein, Pohnpei, Saipan, Palau, Lizard Island, Philippines, and Scott Reef; Indo-Pacific boundary (IB) = Bali and Rowley Shoals; eastern Indian Ocean (EI) = Christmas Island and Cocos/Keeling; western Indian Ocean (WI) = Sumatra, Diego Garcia, Oman, and Seychelles. The direction of migration is indicated. Numbers of migrants per generation between geographic regions are reported with 95% confidence intervals in parentheses.
Figure 5 Migration rates for Cephalopholis argus. Migration rates (Nm: where N is effective female population size and m is migration rate) based on cytochrome b sequences calculated using MIGRATE 3.1.6 [54,55]. Locations with non-significant pairwise ΦST values were grouped (see Table 2). French Polynesia (FP) = Marquesas and Moorea; central-west Pacific (CW) = Kiritimati, Palmyra, Samoa/Tokelau, Baker/Howland, Kwajalein, Pohnpei, Saipan, Palau, Lizard Island, Philippines, and Scott Reef; Indo-Pacific boundary (IB) = Bali and Rowley Shoals; eastern Indian Ocean (EI) = Christmas Island and Cocos/Keeling; western Indian Ocean (WI) = Sumatra, Diego Garcia, Oman, and Seychelles. The direction of migration is indicated. Numbers of migrants per generation between geographic regions are reported with 95% confidence intervals in parentheses.CC BY · PubMed Central
Figure 6 Map of Indo-Malaysia region during glacial maxima. Map shows the effect of lowered sea level on habitat in the region during Pleisotocene glacial maxima (Figure credit: Eric Franklin).
Figure 6 Map of Indo-Malaysia region during glacial maxima. Map shows the effect of lowered sea level on habitat in the region during Pleisotocene glacial maxima (Figure credit: Eric Franklin).CC BY · PubMed Central

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Citations

Cites

Research works printed but not linked: 13

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Authors
Gaither, M. R., Bowen, B. W., Bordenave, T.-R., Rocha, L. A., Newman, S. J., Gomez, J. A., van Herwerden, L., & Craig, M. T.
Affiliations
  • University of Hawaii System (US)
  • University of Hawaiʻi at Mānoa (US)
  • California Academy of Sciences (US)
  • Government of Western Australia (AU)
  • James Cook University (AU)
  • University of Puerto Rico-Mayaguez (PR)
Corresponding author
Gaither, Michelle R
ORCID
Venue
BMC Evolutionary Biology
Publisher
Springer Science and Business Media LLC
Published
2011-07-01
Volume
11
Issue
1
Pages
189-189
ISSN
1471-2148 (ISSN-L)
DOI
10.1186/1471-2148-11-189
PMC
PMC3145601
OpenAlex
W1989413030
Cited by
191
References
110
Citations by year
2026: 12 · 2025: 12 · 2024: 11 · 2023: 5 · 2022: 11 · 2021: 13 · 2020: 15 · 2019: 9 · 2018: 14 · 2017: 8 · 2016: 16 · 2015: 14 · 2014: 12 · 2013: 17 · 2012: 17
FWCI
9.98
Type
journal article
Language
en
Open access
Licence
Locations
  • BMC Evolutionary Biology (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • ResearchOnline at James Cook University (James Cook University) (submittedVersion)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • eSpace (Curtin University) (submittedVersion)
Funders
  • National Science Foundation (2005-008/66882, 0554657, OCE#09‐29031, 8208-07, 0929031, 0453167)
  • U.S. Department of Commerce
  • National Geographic Society (0453167, 0929031, 8208-07)
  • Nature Conservancy
  • National Oceanic and Atmospheric Administration (09-29031, 2005-008/66882, OCE-0929031, 0453167, NA09OAR4170060)
  • U.S. Fish and Wildlife Service
  • Hawai'i Sea Grant, University of Hawai'i (NA09OAR4170060, 2005-008/66882)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Genetic diversity and population structure
  • Physical Sciences › Environmental Science › Ecology › Coral and Marine Ecosystems Studies
  • Life Sciences › Agricultural and Biological Sciences › Aquatic Science › Fish Biology and Ecology Studies
Keywords
Cephalopholis argus, phylogeography, Pleistocene isolation, Coral Triangle, reef fish, population structure, isolation by distance, population growth, introgression, center of origin, Epinephelidae, cytochrome b, nuclear introns
MeSH terms
Animals, Bass, DNA, Mitochondrial, Molecular Sequence Data, Pacific Ocean, Phylogeny, Evolution, Molecular, Indian Ocean, Animal Migration, Fish Proteins, Phylogeography

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