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

Cryptic surgeonfish species: Cryptic surgeonfish species: Phylogeographic survey reveals hidden Phylogeographic survey reveals hidden

biodiversity in the Pacific Oceanbiodiversity in the Pacific Ocean

J. DiBattista, C. Wilcox, M. Craig, L. Rocha, and B. BowenJ. DiBattista, C. Wilcox, M. Craig, L. Rocha, and B. BowenHawai’i Institute of Marine Biology, University of Hawaii Hawai’i Institute of Marine Biology, University of Hawaii

Genetic connectivity of reef fishGenetic connectivity of reef fish

Most have high dispersal potential:- pelagic larvae (weeks to months)



Direct tagging logistically difficult: Molecular tools important hereMolecular tools important here



Direct tagging logistically difficult: Molecular tools important hereMolecular tools important here

Scale of dispersal fundamental for: - defining management units- designing marine reserves (MPAs)- Identifying sources versus sinks

Phylogeography of Indo-Pacific reef fishPhylogeography of Indo-Pacific reef fish

SE DG

CC

CM

OK

HI

KI

MAMOAS

FJ

PN

MA

TIKA

JO

Reef fish familiesReef fish families AcanthuridaeAcanthuridae ChaetodontidaeChaetodontidae LabridaeLabridae LutjanidaeLutjanidae MullidaeMullidae PomacanthidaePomacanthidae SerranidaeSerranidae

Phylogeography of Indo-Pacific reef fishPhylogeography of Indo-Pacific reef fish

SE DG

CC

CM

OK

HI

JO

KI

MAMOAS

FJ

PN

MA

TIKA

Hawaiian archipelagoHawaiian archipelago

Reef fish familiesReef fish families AcanthuridaeAcanthuridae ChaetodontidaeChaetodontidae LabridaeLabridae LutjanidaeLutjanidae MullidaeMullidae PomacanthidaePomacanthidae SerranidaeSerranidae

Hawaiian archipelagoHawaiian archipelago25% endemism (Randall 2007)25% endemism (Randall 2007)

One of the most isolated in the PacificOne of the most isolated in the Pacific

?

?

PapahPapahāānaumokunaumokuāākea kea Marine National MonumentMarine National Monument

One of the largest marine conservation areas in the worldOne of the largest marine conservation areas in the world

Bluelined SurgeonfishBluelined Surgeonfish((Acanthurus nigrorisAcanthurus nigroris))

• Reef generalist/herbivore

• 542 specimens collected

2004 to 2007

• 18 locations sampled

Hawaii and Pacific islands

• mtDNA, cytochrome b

Pacific locationsPacific locationsHawaiian LocationsHawaiian Locations

Marshall Islands(N = 19, MI)

Christmas IslandKiribati

(N = 24, KI)

American Samoa(N = 23, AS)

Moorea(N = 32, MO)

NN = 98 = 98

Photo by Jerker Tamelander, IUCNPhoto by Jerker Tamelander, IUCN

Kure (N = 41)

Midway (N = 30)

Pearl & Hermes (N = 29)

Lisianski (N = 39)

Laysan(N = 46)

Maro Reef(N = 35)

Gardner(N = 27)

French Frigate Shoals(N = 33)

Necker Island(N = 3)

Nihoa(N = 32)

Kauai (N = 34)

Oahu (N = 29)

Lanai(N = 1)

Hawaii(N = 32)

Johnston Atoll(N = 34)

Northwest Hawaiian Islands (NWHI)Northwest Hawaiian Islands (NWHI)NN = 315 = 315

Main Hawaiian Islands (MHI)Main Hawaiian Islands (MHI) N = 96N = 96

Hawaiian locationsHawaiian locationsNN = 445 = 445

Study objectivesStudy objectives

We aim to address the following questions:We 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 ST values:– Between all populations– Between NWHI & MHI– Between Hawaii and Pacific

4) mtDNA sequence divergence

5) Mismatch distribution analysis:

Coalescence times (from estimates)

6) MIGRATE software analysis:

number of migrants per generation

Analysis of genetic structure

1) Haplotype and nucleotide diversity

2) Neutrality test statistics:

Tajima’s D and Fu’s Fs

3)3) Connectivity via Connectivity via STST values: values:– Between all populationsBetween all populations– Between NWHI & MHIBetween NWHI & MHI– Between Hawaii and PacificBetween Hawaii and Pacific

4) mtDNA sequence divergence4) mtDNA sequence divergence

5) Mismatch distribution analysis:

Coalescence times (from estimates)

6) MIGRATE software analysis:6) MIGRATE software analysis:

number of migrants per generationnumber of migrants per generation

NO genetic structure in HawaiiNO genetic structure in Hawaii

- Overall: ST = 0.01, P = 0.07

- MHI vs. NWHI: ST = -0.002, P = 0.65

- 38 haplotypes (HAP 1 + 2 every site)

- mtDNA sequence divergence= 0.1%

Connectivity within Hawaiian islandsConnectivity within Hawaiian islands


- Overall: ST = 0.01, P = 0.07

- MHI vs. NWHI: ST = -0.002, P = 0.65




STST = 0.01, = 0.01, PP = 0.07 = 0.07


- Overall: ST = 0.01, P = 0.07

- MHI vs. NWHI: ST = -0.002, P = 0.65




STST = -0.002, = -0.002, PP = 0.65 = 0.65


- Overall: ST = 0.01, P = 0.07

- MHI vs. NWHI: ST = -0.002, P = 0.65



Number of migrants/generation: Number of migrants/generation: From NWHI into MHI = 22.99 (0 to 132) From MHI into NWHI = 35.19 (0 to 162)


NmNm = 22.99 = 22.99

NmNm = 35.19 = 35.19

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

http://images.google.com/imgres?imgurl=http://www.norman.noaa.gov/publicaffairs/images/logos/noaa.gif&imgrefurl=http://www.norman.noaa.gov/publicaffairs/logos.html&h=426&w=426&sz=13&hl=en&start=7&tbnid=kDmTASSS1o7wJM:&tbnh=126&tbnw=126&prev=/images%3Fq%3DNOAA%26gbv%3D2%26svnum%3D10%26hl%3Den%26safe%3Doff

Connectivity within Pacific islandsConnectivity within Pacific islands

AS

KI

MO

MI

NO genetic structure in PacificNO genetic structure in Pacific

- Overall: ST= 0.009, P = 0.18

- 58 haplotypes (many singletons)

- mtDNA sequence divergence = 0.6%

MI = Marshall IslandsMI = Marshall IslandsAS = American SamoaAS = American SamoaKI = KiribatiKI = KiribatiMO = MooreaMO = Moorea


AS

KI

MO

MI


- Overall: ST= 0.009, P = 0.18



STST = 0.009, = 0.009, PP = 0.18 = 0.18



AS

KI

MO

MI


- Overall: ST= 0.009, P = 0.18



Number of migrants/generation: Number of migrants/generation: Mean migration rate within Pacific = 13.36 (0 to 66 CI) NO BIAS IN MIGRATION DIRECTIONNO BIAS IN MIGRATION DIRECTION

STST = 0.009, = 0.009, PP = 0.18 = 0.18


HawaiiOahuLanaiKauaiNihoaNeckerFrench Frigate ShoalsGardner PinnaclesMaro ReefLaysanLisianskiPearl & Hermes AtollMidwayKureJohnston Atoll

Pacific IslandsPacific Islands

Hawaiian ArchipelagoHawaiian Archipelago

Sequence divergence = 4.12 % ST = 0.96, P < 0.0001

25 muta

tions

25 muta

tions

Connectivity between Pacific regionsConnectivity between Pacific regions

Marshall IslandsMooreaKiribatiAmerican Samoa

(DiBattista, Wilcox et al., 2011(DiBattista, Wilcox et al., 2011 JMB) JMB)

Meristic DifferencesHawaiian Hawaiian A. nigroris,A. nigroris, from Oahu from Oahu Pacific Pacific A. nigrorisA. nigroris, from Enewetak, from Enewetak

Randall, JE (1956), Pacific Science, 10:159-235.

Hawaiian Pacific

Dorsal Soft Rays 24 - 27 23 - 26

Anal Soft Rays 22 - 25 22 - 24

Anterior Gill Rakers 26 - 31 21 - 25

Posterior Gill Rakers 24 - 27 19 - 24

Photos by Jack E. Randall

Meristic DifferencesHawaiian Pacific

Dorsal Soft Rays 24 - 27 23 - 26

Anal Soft Rays 22 - 25 22 - 24

Anterior Gill Rakers 26 - 31 21 - 25

Posterior Gill Rakers 24 - 27 19 - 24

Photos by Jack E. Randall

Hawaiian Hawaiian A. nigroris,A. nigroris, from Oahu from Oahu Pacific Pacific A. nigrorisA. nigroris, from Enewetak, from Enewetak

Randall, JE (1956), Pacific Science, 10:159-235.

Acanthurus nigros GüntherAcanthurus nigroris

Randall et al. Randall et al. in pressin press,, Pacific Science Pacific ScienceSpecies distribution mapSpecies distribution map

ConclusionsConclusions

• 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?The bigger picture?

Hawaiian endemicsHawaiian endemics Widespread surgeonfishWidespread surgeonfish

Eble et al. 2009:

Strong genetic structure

Eble et al. 2011:

Indo-Pacific

Some genetic structureAcanthurus Acanthurus nigrofuscusnigrofuscus

Ctenochaetus strigosusCtenochaetus strigosus Eble et al. 2009:

North/West Pacific

Some genetic structureZebrasoma flavescensZebrasoma flavescens

Present study:

No genetic structure

Acanthurus nigrorisAcanthurus nigroris

Acanthurus nigrosAcanthurus nigros

Present Study:

Central Pacific

No genetic structure

AcknowledgementsAcknowledgements

Thanks to Robert Toonen and Jeff Eble for multiple contributions to this study.This research was supported by the National Science Foundation grants OIA0554657, 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 NOAA Marine 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, Randall Kosaki, Carl Meyer, Yannis Papastamatiou, Joshua Reece, Jennifer Schultz, Zoltan Szabo, Tonatiuh Trejo-Cantwell, Jill Zamzow, and the crew of the R.V. Hi’ialakai helped collect specimens. Aulani Wilhelm, Jo-Ann Leong, Hoku Johnson, Danielle Carter, Daniel Polhemus, Randall Kosaki, Ann Mooney, Elizabeth Keenen, Kelly Gleason, James Maragos, and the Coral Reef Research Foundation provided crucial logistic assistance to this project. We thank Zoltan Szabo for valuable laboratory assistance and protocol development, Sarah Daley, Rajesh Shrestha and Mindy Mizobe 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.

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