Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage

Aim Most reef fishes are site‐attached, but can maintain a broad distribution through their highly dispersive larval stage. The whitetip reef shark (Triaenodon obesus) is site‐attached, yet maintains the largest Indo‐Pacific distribution of any reef shark while lacking the larval stage of bony (tele...

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Veröffentlicht in:Journal of biogeography 2012-06, Vol.39 (6), p.1144-1156
Hauptverfasser: Whitney, Nicholas M, Robbins, William D, Schultz, Jennifer K, Bowen, Brian W, Holland, Kim N
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container_issue 6
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creator Whitney, Nicholas M
Robbins, William D
Schultz, Jennifer K
Bowen, Brian W
Holland, Kim N
description Aim Most reef fishes are site‐attached, but can maintain a broad distribution through their highly dispersive larval stage. The whitetip reef shark (Triaenodon obesus) is site‐attached, yet maintains the largest Indo‐Pacific distribution of any reef shark while lacking the larval stage of bony (teleost) fishes. Here we use mitochondrial DNA (mtDNA) sequence data to evaluate the enigma of the sedentary reef shark that maintains a distribution across two‐thirds of the planet. Location Tropical Pacific and Indian Oceans. Methods We analysed 1025 base pairs of the mtDNA control region in 310 individuals from 25 locations across the Indian and Pacific Oceans. Phylogeographic and population genetic analyses were used to reveal the dispersal and recent evolutionary history of the species. Results We resolved 15 mtDNA control region haplotypes, but two comprised 87% of the specimens and were detected at nearly every location. Similar to other sharks, genetic diversity was low (h = 0.550 ± 0.0254 and π = 0.00213 ± 0.00131). Spatial analyses of genetic variation demonstrated strong isolation across the Indo‐Pacific Barrier and between western and central Pacific locations. Pairwise ΦST comparisons indicated high connectivity among archipelagos of the central Pacific but isolation across short distances of contiguous habitat (Great Barrier Reef) and intermittent habitat (Hawaiian Archipelago). In the eastern Pacific only a single haplotype (the most common one in the central Pacific) was observed, indicating recent dispersal (or colonization) across the East Pacific Barrier. Main conclusions The shallow haplotype network indicates recent expansion of modern populations within the last half million years from a common ancestor. Based on the distribution of mtDNA diversity, this began with an Indo‐West Pacific centre of origin, with subsequent dispersal to the Central Pacific and East Pacific. Genetic differences between Indian and Pacific Ocean populations are consistent with Pleistocene closures of the Indo‐Pacific Barrier associated with glacial cycles. Pairwise population comparisons reveal weak but significant isolation by distance, and notably do not indicate the high coastal connectivity observed in other shark species. The finding of population structure among semi‐contiguous habitats, but population connectivity among archipelagos, may indicate a previously unsuspected oceanic dispersal behaviour in whitetip reef sharks.
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The whitetip reef shark (Triaenodon obesus) is site‐attached, yet maintains the largest Indo‐Pacific distribution of any reef shark while lacking the larval stage of bony (teleost) fishes. Here we use mitochondrial DNA (mtDNA) sequence data to evaluate the enigma of the sedentary reef shark that maintains a distribution across two‐thirds of the planet. Location Tropical Pacific and Indian Oceans. Methods We analysed 1025 base pairs of the mtDNA control region in 310 individuals from 25 locations across the Indian and Pacific Oceans. Phylogeographic and population genetic analyses were used to reveal the dispersal and recent evolutionary history of the species. Results We resolved 15 mtDNA control region haplotypes, but two comprised 87% of the specimens and were detected at nearly every location. Similar to other sharks, genetic diversity was low (h = 0.550 ± 0.0254 and π = 0.00213 ± 0.00131). Spatial analyses of genetic variation demonstrated strong isolation across the Indo‐Pacific Barrier and between western and central Pacific locations. Pairwise ΦST comparisons indicated high connectivity among archipelagos of the central Pacific but isolation across short distances of contiguous habitat (Great Barrier Reef) and intermittent habitat (Hawaiian Archipelago). In the eastern Pacific only a single haplotype (the most common one in the central Pacific) was observed, indicating recent dispersal (or colonization) across the East Pacific Barrier. Main conclusions The shallow haplotype network indicates recent expansion of modern populations within the last half million years from a common ancestor. Based on the distribution of mtDNA diversity, this began with an Indo‐West Pacific centre of origin, with subsequent dispersal to the Central Pacific and East Pacific. Genetic differences between Indian and Pacific Ocean populations are consistent with Pleistocene closures of the Indo‐Pacific Barrier associated with glacial cycles. Pairwise population comparisons reveal weak but significant isolation by distance, and notably do not indicate the high coastal connectivity observed in other shark species. The finding of population structure among semi‐contiguous habitats, but population connectivity among archipelagos, may indicate a previously unsuspected oceanic dispersal behaviour in whitetip reef sharks.</description><identifier>ISSN: 0305-0270</identifier><identifier>EISSN: 1365-2699</identifier><identifier>DOI: 10.1111/j.1365-2699.2011.02660.x</identifier><identifier>CODEN: JBIODN</identifier><language>eng</language><publisher>Oxford, UK: Blackwell Publishing Ltd</publisher><subject>Agnatha. 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Psychology ; General aspects ; genetic variation ; habitats ; Haplotypes ; Indo-Pacific Barrier ; larvae ; marine biogeography ; Marine ecology ; marine fish ; Mitochondrial DNA ; mtDNA ; Oceans ; phylogeography ; Population ; Population genetics ; population structure ; Reefs ; Sharks ; Synecology ; Triaenodon obesus ; Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution</subject><ispartof>Journal of biogeography, 2012-06, Vol.39 (6), p.1144-1156</ispartof><rights>Copyright © 2012 Blackwell Publishing Ltd.</rights><rights>2011 Blackwell Publishing Ltd</rights><rights>2015 INIST-CNRS</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4550-905ef1813817745359e33aa18337e0c594a2000f0bf293e3c8361a475aa37ff03</citedby><cites>FETCH-LOGICAL-c4550-905ef1813817745359e33aa18337e0c594a2000f0bf293e3c8361a475aa37ff03</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/23258801$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/23258801$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,776,780,799,1411,27903,27904,45553,45554,57995,58228</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&amp;idt=25906868$$DView record in Pascal Francis$$Hfree_for_read</backlink></links><search><creatorcontrib>Whitney, Nicholas M</creatorcontrib><creatorcontrib>Robbins, William D</creatorcontrib><creatorcontrib>Schultz, Jennifer K</creatorcontrib><creatorcontrib>Bowen, Brian W</creatorcontrib><creatorcontrib>Holland, Kim N</creatorcontrib><title>Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage</title><title>Journal of biogeography</title><description>Aim Most reef fishes are site‐attached, but can maintain a broad distribution through their highly dispersive larval stage. The whitetip reef shark (Triaenodon obesus) is site‐attached, yet maintains the largest Indo‐Pacific distribution of any reef shark while lacking the larval stage of bony (teleost) fishes. Here we use mitochondrial DNA (mtDNA) sequence data to evaluate the enigma of the sedentary reef shark that maintains a distribution across two‐thirds of the planet. Location Tropical Pacific and Indian Oceans. Methods We analysed 1025 base pairs of the mtDNA control region in 310 individuals from 25 locations across the Indian and Pacific Oceans. Phylogeographic and population genetic analyses were used to reveal the dispersal and recent evolutionary history of the species. Results We resolved 15 mtDNA control region haplotypes, but two comprised 87% of the specimens and were detected at nearly every location. Similar to other sharks, genetic diversity was low (h = 0.550 ± 0.0254 and π = 0.00213 ± 0.00131). Spatial analyses of genetic variation demonstrated strong isolation across the Indo‐Pacific Barrier and between western and central Pacific locations. Pairwise ΦST comparisons indicated high connectivity among archipelagos of the central Pacific but isolation across short distances of contiguous habitat (Great Barrier Reef) and intermittent habitat (Hawaiian Archipelago). In the eastern Pacific only a single haplotype (the most common one in the central Pacific) was observed, indicating recent dispersal (or colonization) across the East Pacific Barrier. Main conclusions The shallow haplotype network indicates recent expansion of modern populations within the last half million years from a common ancestor. Based on the distribution of mtDNA diversity, this began with an Indo‐West Pacific centre of origin, with subsequent dispersal to the Central Pacific and East Pacific. Genetic differences between Indian and Pacific Ocean populations are consistent with Pleistocene closures of the Indo‐Pacific Barrier associated with glacial cycles. Pairwise population comparisons reveal weak but significant isolation by distance, and notably do not indicate the high coastal connectivity observed in other shark species. The finding of population structure among semi‐contiguous habitats, but population connectivity among archipelagos, may indicate a previously unsuspected oceanic dispersal behaviour in whitetip reef sharks.</description><subject>Agnatha. Pisces</subject><subject>Animal and plant ecology</subject><subject>Animal, plant and microbial ecology</subject><subject>Archipelagos</subject><subject>Below the waterline</subject><subject>Biogeography</subject><subject>Biological and medical sciences</subject><subject>center of origin</subject><subject>Connectivity</subject><subject>Control region</subject><subject>Coral reefs</subject><subject>dispersal</subject><subject>dispersal behavior</subject><subject>East Pacific Barrier</subject><subject>Ecological genetics</subject><subject>elasmobranch</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>General aspects</subject><subject>genetic variation</subject><subject>habitats</subject><subject>Haplotypes</subject><subject>Indo-Pacific Barrier</subject><subject>larvae</subject><subject>marine biogeography</subject><subject>Marine ecology</subject><subject>marine fish</subject><subject>Mitochondrial DNA</subject><subject>mtDNA</subject><subject>Oceans</subject><subject>phylogeography</subject><subject>Population</subject><subject>Population genetics</subject><subject>population structure</subject><subject>Reefs</subject><subject>Sharks</subject><subject>Synecology</subject><subject>Triaenodon obesus</subject><subject>Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution</subject><issn>0305-0270</issn><issn>1365-2699</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><recordid>eNqNkd1u0zAUxyMEEmXwCAhLCIldJNhx7CRIXLCJdUOFIbGJS8tzjzuXzC6227XPwEtzSqZyi29s6fw_7J-LgjBaMVzvlhXjUpS17PuqpoxVtJaSVttHxeQweFxMKKeipHVLnxbPUlpSSnvBm0nx-9KA9s6QuUsriEkPxHmiSYI5-KzjjkQAS9Ktjj_J26voNPgwD56EG0jrdPyeLMBDxgDYOLQYIDZEAtsMPrkNEBO8B5PdxuUduXf5Nqwz5q9g0At0DTpusDNlvYDnxROrhwQvHvaj4vrs09XpeTm7nF6cfpyVphGClj0VYFnHeMfathFc9MC51qzjvAVqRN_oGt9n6Y2tew7cdFwy3bRCa95aS_lR8XrMXcXwaw0pq2VYR4-VinVSNj3CkajqRpWJIaUIVq2iu0MiilG1R6-Wak9Y7QmrPXr1F73aovXNQ4FORg82am9cOvhr0VPZyQ51H0bdvRtg99_56vPJxf6E_pejf5lyiP_yeS26jjKcl-PcpQzbwxy_UsmWt0L9-DpVs2nz7ayVX9Q56l-NequD0ouId77-js0N4qQcYfM_UKm5WA</recordid><startdate>201206</startdate><enddate>201206</enddate><creator>Whitney, Nicholas M</creator><creator>Robbins, William D</creator><creator>Schultz, Jennifer K</creator><creator>Bowen, Brian W</creator><creator>Holland, Kim N</creator><general>Blackwell Publishing Ltd</general><general>Blackwell Publishing</general><general>Blackwell</general><general>Wiley Subscription Services, Inc</general><scope>FBQ</scope><scope>BSCLL</scope><scope>IQODW</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7SN</scope><scope>7SS</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>RC3</scope></search><sort><creationdate>201206</creationdate><title>Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage</title><author>Whitney, Nicholas M ; Robbins, William D ; Schultz, Jennifer K ; Bowen, Brian W ; Holland, Kim N</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4550-905ef1813817745359e33aa18337e0c594a2000f0bf293e3c8361a475aa37ff03</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Agnatha. Pisces</topic><topic>Animal and plant ecology</topic><topic>Animal, plant and microbial ecology</topic><topic>Archipelagos</topic><topic>Below the waterline</topic><topic>Biogeography</topic><topic>Biological and medical sciences</topic><topic>center of origin</topic><topic>Connectivity</topic><topic>Control region</topic><topic>Coral reefs</topic><topic>dispersal</topic><topic>dispersal behavior</topic><topic>East Pacific Barrier</topic><topic>Ecological genetics</topic><topic>elasmobranch</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>General aspects</topic><topic>genetic variation</topic><topic>habitats</topic><topic>Haplotypes</topic><topic>Indo-Pacific Barrier</topic><topic>larvae</topic><topic>marine biogeography</topic><topic>Marine ecology</topic><topic>marine fish</topic><topic>Mitochondrial DNA</topic><topic>mtDNA</topic><topic>Oceans</topic><topic>phylogeography</topic><topic>Population</topic><topic>Population genetics</topic><topic>population structure</topic><topic>Reefs</topic><topic>Sharks</topic><topic>Synecology</topic><topic>Triaenodon obesus</topic><topic>Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Whitney, Nicholas M</creatorcontrib><creatorcontrib>Robbins, William D</creatorcontrib><creatorcontrib>Schultz, Jennifer K</creatorcontrib><creatorcontrib>Bowen, Brian W</creatorcontrib><creatorcontrib>Holland, Kim N</creatorcontrib><collection>AGRIS</collection><collection>Istex</collection><collection>Pascal-Francis</collection><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Journal of biogeography</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Whitney, Nicholas M</au><au>Robbins, William D</au><au>Schultz, Jennifer K</au><au>Bowen, Brian W</au><au>Holland, Kim N</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage</atitle><jtitle>Journal of biogeography</jtitle><date>2012-06</date><risdate>2012</risdate><volume>39</volume><issue>6</issue><spage>1144</spage><epage>1156</epage><pages>1144-1156</pages><issn>0305-0270</issn><eissn>1365-2699</eissn><coden>JBIODN</coden><abstract>Aim Most reef fishes are site‐attached, but can maintain a broad distribution through their highly dispersive larval stage. The whitetip reef shark (Triaenodon obesus) is site‐attached, yet maintains the largest Indo‐Pacific distribution of any reef shark while lacking the larval stage of bony (teleost) fishes. Here we use mitochondrial DNA (mtDNA) sequence data to evaluate the enigma of the sedentary reef shark that maintains a distribution across two‐thirds of the planet. Location Tropical Pacific and Indian Oceans. Methods We analysed 1025 base pairs of the mtDNA control region in 310 individuals from 25 locations across the Indian and Pacific Oceans. Phylogeographic and population genetic analyses were used to reveal the dispersal and recent evolutionary history of the species. Results We resolved 15 mtDNA control region haplotypes, but two comprised 87% of the specimens and were detected at nearly every location. Similar to other sharks, genetic diversity was low (h = 0.550 ± 0.0254 and π = 0.00213 ± 0.00131). Spatial analyses of genetic variation demonstrated strong isolation across the Indo‐Pacific Barrier and between western and central Pacific locations. Pairwise ΦST comparisons indicated high connectivity among archipelagos of the central Pacific but isolation across short distances of contiguous habitat (Great Barrier Reef) and intermittent habitat (Hawaiian Archipelago). In the eastern Pacific only a single haplotype (the most common one in the central Pacific) was observed, indicating recent dispersal (or colonization) across the East Pacific Barrier. Main conclusions The shallow haplotype network indicates recent expansion of modern populations within the last half million years from a common ancestor. Based on the distribution of mtDNA diversity, this began with an Indo‐West Pacific centre of origin, with subsequent dispersal to the Central Pacific and East Pacific. Genetic differences between Indian and Pacific Ocean populations are consistent with Pleistocene closures of the Indo‐Pacific Barrier associated with glacial cycles. Pairwise population comparisons reveal weak but significant isolation by distance, and notably do not indicate the high coastal connectivity observed in other shark species. The finding of population structure among semi‐contiguous habitats, but population connectivity among archipelagos, may indicate a previously unsuspected oceanic dispersal behaviour in whitetip reef sharks.</abstract><cop>Oxford, UK</cop><pub>Blackwell Publishing Ltd</pub><doi>10.1111/j.1365-2699.2011.02660.x</doi><tpages>13</tpages></addata></record>
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source Wiley Online Library Journals Frontfile Complete; Jstor Complete Legacy
subjects Agnatha. Pisces
Animal and plant ecology
Animal, plant and microbial ecology
Archipelagos
Below the waterline
Biogeography
Biological and medical sciences
center of origin
Connectivity
Control region
Coral reefs
dispersal
dispersal behavior
East Pacific Barrier
Ecological genetics
elasmobranch
Fundamental and applied biological sciences. Psychology
General aspects
genetic variation
habitats
Haplotypes
Indo-Pacific Barrier
larvae
marine biogeography
Marine ecology
marine fish
Mitochondrial DNA
mtDNA
Oceans
phylogeography
Population
Population genetics
population structure
Reefs
Sharks
Synecology
Triaenodon obesus
Vertebrates: general zoology, morphology, phylogeny, systematics, cytogenetics, geographical distribution
title Oceanic dispersal in a sedentary reef shark (Triaenodon obesus): genetic evidence for extensive connectivity without a pelagic larval stage
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