Genetic Connectivity and the Origins of Tropical Reef Biodiversity

GENETIC CONNECTIVITY AND THE ORIGINS OF TROPICAL REEF BIODIVERSITY

Brian Bowen, Luiz Rocha, Matt Craig, Jeff Eble, Christopher Bird, Jennifer Schultz, Rob Toonen, and the ToBo (Toonen/Bowen) lab at Hawaii Institute of Marine Biology

Pacific Science Inter-Congress March 3, 2009 Photo credits: Jack Randall, Luiz Rocha, UCSC Biology, Rich Seaman, and more THE ORIGINS OF REEF BIODIVERSITY: New Perspectives from Marine Phylogeography

• Reef Biodiversity: Often Misdiagnosed, but Higher Than Previously Known • Larval Dispersal Guides Speciation: Life History and Ecology Determine Dispersal as Much as Oceanography and Geography • Shallow Evolutionary History: Reef Inhabitants Show Recent Population Expansions or Colonizations • Speciation Mechanisms: Conventional Allopatric Speciation is not Consistent with the Extensive Dispersal of Many Reef Organisms • Phylogeography: Speciation Occurs both in the Biodiversity Hotspots and the Isolated Archipelagos, and this Biodiversity Feedback promotes species richness Marine Phylogeography: Convict Surgeonfish Acanthurus triostegas

Planes and Fauvelot 2002 Evolution 56:378-399 Marine Phylogeography of Lutjanus kasmira and L. fulvus show extreme isolation of Marquesas Gaither, Planes et al. 2009 J. Biogeo. Accepted Pending Revision 1

2 D

D N

N RNA

16S

O C RNA

12S

I I

p O

o C

s T

a A

y DNA C

COIII

D N Mitochondrial ND3 Two rRNA, 22 tRNA, 13 proteins, one control region ND4L ND4 Mitochondrial DNA Primary Hotspot: Coral Triangle between Philippines, Indonesia, New Guinea

Modified from Allen 2002 Secondary Hotspot in the Caribbean ~400 Fish Species Two theories to Explain Biodiversity Hotspots in the Oceans Biodiversity Hotspots are Centers of Speciation: Intense Competition Forges New Species with High Fitness that Radiate Out and Replace Older Species (Briggs 1999 J Biogeo)

Biodiversity Hotspots are Centers of Accumulation: Speciation Occurs Under the Ecological Release of Depauperate Outer Archipelagos, and New Species Accumulate in the Center Of the Range Allopatric Speciation vs. Sympatric (Ecological) Speciation

Island A Island B

See Leray et al. 11:30 am Reef Biodiversity Higher than Expected Ophioblennius atlanticus

Redlip blenny

Muss et al. 2001. Evolution 55:561-572 Ophioblennius steindachneri and O. atlanticus

Grenada

Galapagos

St. Helena

Springer 1962 Neighbor-Joining 91 Azores Tree 93 Gulf of 99 Guinea 87

99 Mid-Atlanti

100 Caribbean

100 100 Brazil

Pacific 100

13 10 7.5 5 0 % sequence divergence Coloration is an uncertain basis for counting species and biodiversity Centropyge loricula distinct color morph

Centropyge loriculus

ST = 0.011, P = 0.147 Schultz et al. 2007 Atlantic Pygmy Angelfishes Distingished Primarily by Coloration

Centropyge argi Caribbean (N=14)

Centropyge aurantonotus Brazil and southern Caribbean (N=17) Centropyge resplendens Mid-Atlantic Ridge (N=15) IUCN Red List Atlantic Pygmy Angelfish Distribution Atlantic Centropyge species

C. resplendens Mid-Atlantic Ridge

C. argi Caribbean

C. aurantonotus Bowen et al. 2006 Brazil and southern Caribbean J. Heredity Emerging Species? Regional Color Morphs? Conclusion: Reef Biodiversity is usually higher, but sometimes lower than taxonomy would indicate

Sargassum Biodiversity: Lydiane Matio et al. 10:45 Room 1 Ecology Shapes Biodiversity The case of three Atlantic Surgeonfishes

Acanthurus bahianus

Acanthurus coeruleus Acanthurus chirurgus

Rocha et al. 2002, Molecular Ecology 11:243-252 Amazon Barrier Freshwater floats over salt water The Ocean Surgeonfish

Brazil

Caribbean These may be two species The Blue Tang

Acanthurus coeruleus The Doctorfish

Acanthurus chirurgus Atlantic Acanthurus spp. Very similar PLD (52-55 days) Very different levels of genetic structure

A. Bahianus d = 0.024

A. coeruleus

ST = 0.356; p < 0.001

A. chirurgus

ST = 0.001; N.S.

Note Differences in Ecology Sponge corridor (Collette & Rützler 1977) Ecosystem level connectivity Fauvelot et al. 9:15 am Room 1 Iacchei and Toonen 10:30 am Room 1 Skillings et al. 11:35 Room 1

? Planktonic larval duration (PLD) indicates dispersal ability? (Weersing and Toonen submitted) Good correlation Poor or no correlation Taylor and Hellberg (2003) Teske et al. (2007) Mar. Biol. Bohonak (1999) Quar. Rev. of Biol. Nishikawa and Sakai (2005) Zool. Sci. Zatcoff et al.(2005) Mar. Biol. Ayre et al. (1997) Mar. Biol. Murray-Jones & Ayre (1997) Mar. Biol. Rocha et al.(2005) Proc. Roy. Soc. Lon. B Waples (1987) Evolution Severance and Karl (2006) Mar. Biol. Lacson & Morizot (1991) Mar. Biol. Bowen et al. (2006) Mar. Biol Planes et al. (1996) J. Evol. Biol. Goldson et al. (2001) Mar. Biol. Duffy (1993) Mar. Biol. Borsa & Benzie (1996) Mar. Biol. Staton et al.(2000) J. Crust. Biol. Benzie & Williams (1997) Evolution Doherty et al. (1995) Ecology Shulman (1998) Aust. J. Ecol. Hellberg (1994) Evolution Planes (1993) Mar. Ecol. Prog. Ser. McMillan-Jackson et al. (1994) Mar. Biol. Gaarde & McClenaghan (1982) SW. Nat Addison and Hart (2004) Mar. Biol. Janson (1987) Bio. J. Linn. Soc. Hellberg (1996) Evolution Hunt & Ayre (1989) Mar. Biol. Todd et al. (1998) J. Exp. Mar. Biol. Ecol. Sole-Cava et al. (1994) J. Mar. Biol. Ass. Range / dispersal hypothesis

Red Sea and east coast of Africa to Central Pacific http://www.izuzuki.com/Zukan/Fish/niza/nagaNZ.html

Jay Hague Subtropical North Pacific

Eble et al. 2009 Mar Biol

Stan Shebs Hawaiian endemic Restricted Gene Flow in Island Endemics Comparisons across Hawaiian Archipelago: Acanthurus nigrofuscus

N: 298 Range: Indo-Pacific through Hawaii 0 significant pair-wise differences

Zebrasoma flavescens

N: 560 Range: North Pacific 5 significant pair-wise differences

Ctenochaetus strigosus

N: 513 Range: Hawaiian endemic 17 significant pair-wise differences

Eble et al. Marine Biology 2009 Hawaiian endemics vs. wide ranging spp.

Indo-Pacific Hawaiian endemic = high connectivity = reduced dispersal

Craig et al. 2007 Rivera et al. 2004 Ramon et al. 2008

Eble et al. 2009 Ramon et al. 2008 Eble et al. 2009

http://www.izuzuki.com/Zukan/Fish/niza/nagaNZ.html

Stan Shebs Eble et al. 2009 Hawaiian endemics exhibit lower dispersal relative to Indo-Pacific spp. After rare colonization event into Hawaii, they cannot maintain contact with parent population elsewhere in Jay Hague the Pacific. The Enigma of Shallow Population History in Many (but not all) Reef Fauna

Matthew Craig et al. In Prep Do Glacial Sea Level Changes Extirpate Shallow Reef Fauna? REDUCTIONS IN THE MITOCHONDRIAL DNA DIVERSITY OF CORAL REEF FISH PROVIDE EVIDENCE OF POPULATION BOTTLENECKS RESULTING FROM HOLOCENE SEA-LEVEL CHANGE C. FAUVELOT, G. BERNARDI, AND S. PLANES Evolution 2003, 57:1571-1583

Lagoons: Chaetodon citrinellus Pomacentrus pavo, Chrysiptera glauca, Dascyllus aruanus

Outer Slope: Chaetodon quadrimaculatus, Forcipiger flavissimus, Chromis xanthura Outer Slope Fauna Lagoon Fauna Older Younger

FAUVELOT, BERNARDI, PLANES 2003 Biodiversity Gradient May be Due to Post-Glacial Recolonization

Modified from Allen 2002 Test This Hypothesis on Deep (> 100 m) Reefs

Richard Pyle, Tonatiuh Trejo, Derek Skillings, Michelle Gaither, Robert Toonen, B.W. Bowen ongoing research Speciation in the Sea: The Case of Atlantic Wrasses Rocha 2004, Rocha et al. 2005

Haliochoeres radiatus and Haliochoeres braziliensis

Speciation along ecological barriers

Rocha et al. 2005 Proc Roy Soc B Historical biogeography and speciation in the reef fish genus Haemulon (Teleostei: Haemulidae) Rocha et al. 2008 Mol Phyogen Evol 48:918-928

Lindeman et al. 9:30 am Room 1

The case for sympatric or ecological speciation

Rocha et al. 2008 Does Allopatric Speciation Occur in the Transglobal Aquatic Medium? YES! Hawaiian Endemic Species Example (Eble et al. 2009) Negaprion spp. (Lemon sharks: Schultz et al. 9:00 am Room 1) Dascyllus trimaculatus complex (Matthieu Leray et al. 11:30 am Room 1)

Does Ecological or Sympatric Speciation Occur in the Ocean? YES! Atlantic wrasse example (Rocha et al. 2005) Grunts (genus Haemulon; Rocha et al. 2008, Lindeman et al. 9:30 am Room 1) Sympatric Speciation and Biodiversity Hotspots Populations do not have to be physically isolated to diverge and speciate Olive Ridley Turtle (Lepidochelys olivacea)

Recent Radiation from the IWP to Atlantic and East Pacific Bowen et al. 1998 Genetica Center of Accumulation in the Cowrie Monetaria caputserpentis species complex

This subset of the phylogeny supports the center of accumulation model. The peripheral subspecies in Hawaii and Easter Island are basal to the widespread Indo-Pacific lineage.

Paulay and Meyer 2002 Evolution Evidence from the Caribbean Hotspot

* * * Halichoeres bivittatus

Rocha et al. 2005 Proc Roy Soc B Chromis multilineata

Rocha et al. 2008 BMC Evolution C. Sparisoma axillare and S. rubripinne

D. S. chrysopterum, S. frondosum and S. griseorubra

Robertson et al. Mol Phylogenet Evol 2006, 40:795-807. Biodiversity in the Indo-Pacific hotspot may be enhanced by the extensive halo of archipelagos around the Coral Triangle, a feature nearly absent from the Atlantic hotspot

Implications for Evolution: Speciation at the Center, and Speciation at the Periphery, Operate as a Biodiversity Feedback to Enhance Species Richness in Both Habitats. Implications for Conservation: Both the Coral Triangle and Archipelagos are Crucial for Maintaining Biodiversity ALOHA MERCI