Hidden in plain view: A genetic survey reveals high connectivity and a cryptic endemic surgeonfish species in the Hawaiian Archipelago

Cryptic surgeonfish species:Phylogeographic survey reveals hidden biodiversity in the Pacific OceanJ. DiBattista, C. Wilcox, M. Craig, L. Rocha, and B. Bowen Hawai’i Institute of Marine Biology, University of Hawaii

Genetic connectivity of reef fish Most have high dispersal potential: - pelagic larvae (weeks to months)

Genetic connectivity of reef fish Most have high dispersal potential: - pelagic larvae (weeks to months) Direct tagging logistically difficult:  Molecular tools important here

Genetic connectivity of reef fish Most have high dispersal potential: - pelagic larvae (weeks to months) Direct tagging logistically difficult:  Molecular tools important here Scale of dispersal fundamental for: - defining management units - designing marine reserves (MPAs) - Identifying sources versus sinks

Phylogeography of Indo-Pacific reef fish OK HI JO MA PN KI KA TI SE DG AS MO CM MA FJReef fish families CC AcanthuridaeChaetodontidae Labridae Lutjanidae Mullidae Pomacanthidae Serranidae

Phylogeography of Indo-Pacific reef fish OK HI Hawaiian archipelago JO MA PN KI KA TI SE DG AS MO CM MA FJReef fish families CC AcanthuridaeChaetodontidae Labridae Lutjanidae Mullidae Pomacanthidae Serranidae

Hawaiian archipelago 25% endemism (Randall 2007)One of the most isolated in the Pacific

Papahā naumokuā kea Marine National Monument ? ?One of the largest marine conservation areas in the world

Bluelined Surgeonfish(Acanthurus nigroris) • Reef generalist/herbivore • 542 specimens collected  2004 to 2007 • 18 locations sampled  Hawaii and Pacific islands • mtDNA, cytochrome b

Pacific locations Hawaiian Locations N = 98 Marshall Islands (N = 19, MI) Christmas Island Kiribati (N = 24, KI) American Samoa (N = 23, AS) Moorea (N = 32, MO)Photo by Jerker Tamelander, IUCN

Hawaiian locations N = 445 Midway (N = 30) Pearl & Hermes (N = 29)Kure (N = 41) Lisianski (N = 39) Gardner Main Hawaiian Islands (MHI) Laysan (N = 27) (N = 46) N = 96 Maro Reef Necker Island (N = 35) (N = 3) French Frigate Shoals Kauai (N = 34) (N = 33) Nihoa Oahu (N = 29) (N = 32) Lanai (N = 1) Northwest Hawaiian Islands (NWHI) N = 315 Hawaii (N = 32) Johnston Atoll (N = 34)

Study objectivesWe aim to address the following questions:(1) Is there genetic structure within the Hawaiian archipelago?(2) Is there genetic structure among other sampled Pacific populations?(3) Is there evidence of genetic exchange between Hawaii and the rest of the Pacific?

Analysis of genetic structure 1) Haplotype and nucleotide diversity 2) Neutrality test statistics: Tajima’s D and Fu’s Fs 3) Connectivity via φ ST values: – Between all populations – Between NWHI & MHI – Between Hawaii and Pacific 4) mtDNA sequence divergence 5) Mismatch distribution analysis:  Coalescence times (from τ estimates) 6) MIGRATE software analysis:  number of migrants per generation

Connectivity within Hawaiian islands NO genetic structure in Hawaii - O v e r a l l : φ S T = 0 . 0 1, P = 0 . 0 - MHI vs. NWHI: φ ST = -0.002, P = 0.65 - 38 haplotypes (HAP 1 + 2 every site) - mtDNA sequence divergence= 0.1%

Connectivity within Hawaiian islands φ ST = 0.01, P = 0.07 NO genetic structure in Hawaii - O v e r a l l : φ S T = 0 . 0 1, P = 0 . 0 - MHI vs. NWHI: φ ST = -0.002, P = 0.65 - 38 haplotypes (HAP 1 + 2 every site) - mtDNA sequence divergence= 0.1%

Connectivity within Hawaiian islands φ ST = -0.002, P = 0.65 NO genetic structure in Hawaii - O v e r a l l : φ S T = 0 . 0 1, P = 0 . 0 - MHI vs. NWHI: φ ST = -0.002, P = 0.65 - 38 haplotypes (HAP 1 + 2 every site) - mtDNA sequence divergence= 0.1%

Connectivity within Hawaiian islands NO genetic structure in Hawaii Nm = 22.99 - O v e r a l l : φ S T = 0 . 0 1, P = 0 . 0 - MHI vs. NWHI: φ ST = -0.002, P = 0.65 - 38 haplotypes (HAP 1 + 2 every site) - mtDNA sequence divergence= 0.1% Number of migrants/generation: From NWHI into MHI = 22.99 (0 to 132)Nm = 35.19 From MHI into NWHI = 35.19 (0 to 162)

Direction of exchange appears primarily to the NW rather than SE in Hawaii

Connectivity within Pacific islands NO genetic structure in Pacific MI - O v e r a l l : φ S T = 0 . 0 0 9 , P = 0 . 18 - 5 8 h a p lo t y p e s ( m a n y s in g le t o KI AS - mtDNA sequence divergence = 0.6% MOMI = Marshall IslandsAS = American SamoaKI = KiribatiMO = Moorea

Connectivity within Pacific islands φ ST = 0.009, P = 0.18 genetic structure in Pacific NO MI - O v e r a l l : φ S T = 0 . 0 0 9 , P = 0 . 18 - 5 8 h a p lo t y p e s ( m a n y s in g le t o KI AS - mtDNA sequence divergence = 0.6% MOMI = Marshall IslandsAS = American SamoaKI = KiribatiMO = Moorea

Connectivity within Pacific islands φ ST = 0.009, P = 0.18 genetic structure in Pacific NO MI - O v e r a l l : φ S T = 0 . 0 0 9 , P = 0 . 18 - 5 8 h a p lo t y p e s ( m a n y s in g le t o KI AS - mtDNA sequence divergence = 0.6% MO Number of migrants/generation:MI = Marshall Islands Mean migration rate within PacificAS = American SamoaKI = Kiribati = 13.36 (0 to 66 CI)MO = Moorea NO BIAS IN MIGRATION DIRECTION

Connectivity between Pacific regions Hawaii Oahu Lanai Kauai Nihoa Necker French Frigate Shoals Hawaiian Archipelago Gardner Pinnacles Maro Reef Laysan Lisianski Pearl & Hermes Atoll Midway Kure ns tio Johnston Atoll a ut m 2 5 Marshall Islands Moorea Kiribati Pacific Islands American Samoa Sequence divergence = 4.12 % φ ST = 0.96, P < 0.0001 (DiBattista, Wilcox et al., 2011 JMB)

Photos by Jack E. RandallHawaiian A. nigroris, from Oahu Pacific A. nigroris, from Enewetak Meristic Differences Hawaiian PacificDorsal Soft Rays 24 - 27 23 - 26Anal Soft Rays 22 - 25 22 - 24Anterior Gill Rakers 26 - 31 21 - 25Posterior Gill Rakers 24 - 27 19 - 24 Randall, JE (1956), Pacific Science, 10:159-235.

Species distribution map Randall et al. in press, Pacific Science Acanthurus nigros Günther Acanthurus nigroris

Conclusions• High gene flow over large distances:  Hawaiian region: ~2600 km  Pacific region: ~800 km• Distinct barrier to gene flow between Hawaii and the rest of the Pacific• Two proposed surgeonfish species:  Hawaiian endemic species  Widespread Pacific species

The bigger picture? Hawaiian endemics Widespread surgeonfish Eble et al. 2011: Indo-Pacific Eble et al. 2009: Acanthurus nigrofuscus Some genetic structure Strong genetic structureCtenochaetus strigosus Eble et al. 2009: North/West Pacific Zebrasoma flavescens Some genetic structure Present study: No genetic structure Present Study: Central Pacific Acanthurus nigroris No genetic structure Acanthurus nigros

AcknowledgementsThanks to Robert Toonen and Jeff Eble for multiple contributions to thisstudy.This research was supported by the National Science Foundation grantsOIA0554657, OCE-0453167 and OCE-0929031 (BWB), OCE-0623678 (RJT),and NOAA National Marine Sanctuaries Program MOA No. 2005-008/66882(BWB & RJT).We thank the Papahanaumokuakea Marine National Monument and co-trustees NOAAMarine Sanctuaries, U.S. Fish and Wildlife Service (USFWS), and the State of Hawaii.Paul Barber, Howard Choat, Pat Collins, Greg Concepcion, Jonathan Dale, Toby Daly-Engel, John Earle, Michelle Gaither, Brian Greene, Matt Iacchei, Stephen Karl, RandallKosaki, Carl Meyer, Yannis Papastamatiou, Joshua Reece, Jennifer Schultz, ZoltanSzabo, Tonatiuh Trejo-Cantwell, Jill Zamzow, and the crew of the R.V. Hi’ialakaihelped collect specimens. Aulani Wilhelm, Jo-Ann Leong, Hoku Johnson, DanielleCarter, Daniel Polhemus, Randall Kosaki, Ann Mooney, Elizabeth Keenen, KellyGleason, James Maragos, and the Coral Reef Research Foundation provided cruciallogistic assistance to this project. We thank Zoltan Szabo for valuable laboratoryassistance and protocol development, Sarah Daley, Rajesh Shrestha and MindyMizobe of the HIMB EPSCoR core facility for their assistance with DNA sequencing,John Randall, Stephen Karl, and all the members of the ToBo lab for their advice,assistance, and support.

Hidden in plain view: A genetic survey reveals high connectivity and a cryptic endemic surgeonfish species in the Hawaiian Archipelago

by Christie Wilcox

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Hidden in plain view: A genetic survey reveals high connectivity and a cryptic endemic surgeonfish species in the Hawaiian Archipelago Presentation Transcript