PhD exit seminar - 2011

ARC Centre of Excellence

Coral Reef Studies

DATING THE ORIGINS OF CORAL REEF

FISHES

Supervisors:

DR Bellwood

L van Herwerden

Peter F Cowman

BACKGROUND: MARINE BIODIVERSITY HOTSPOT

•Patterns of biodiversity

•Studies of maintenance

•Less emphasis on origin and evolution of taxa

•The Indo-Australia Archipelago (IAA)

•>500 spp corals; > 5,000 spp fish

•Gradient of declining richness

BACKGROUND: THE HOPPING HOTSPOT

Renema et al. 2008

THESIS QUESTIONS

1. What are the temporal origins of trophicmodes on coral reefs?

2. What roles have coral reefs played through time?

3. How has historical biogeography shaped coral reef diversity?

MATERIALS & METHODS

Alignment/Supermatrix constructionModel testing, partitioning

ABC

D

MY

Age estimationMCMC Bayes I BEAST PackageFossil Data (+ biogeographic)

AB

C

D

Phylogenetic reconstructionMP, ML, BI. Bootstrapping etc.

Garli MrBayes

Labridae

(wrasses)

DNA for reef fish families GenBankMax taxa, gene regions (Mt, Nuc)

ABC

D

MY

ABC

D

MY

ABC

D

MY

ABC

D

MY

MATERIALS & METHODS

Labridae

(wrasses)

Chaetodontidae

(butterflyfish)Pomacentridae

(damselfish)

AB

C

D

AB

C

D

Apogonidae

(cardinalfish)

AB

C

D

AB

C

D

Temporal Framework

LTTMY

CHAPTER 1&2: TROPHIC EVOLUTION

Labridae

• 600 spp, 80 genera

• Diverse specialized feeding modes

• Moderate fossil record

• Little info on origins of novel feeding modes

Chaetodontidae

• 130 spp, 10 genera

• 63% of all corallivores

• Little info on origins of corallivory

• Effect of coral feeding of speciation

Q1: What are the temporal origins of trophic modes on coral reefs?

I. Patterns of trophic evolution? (wrasses)

II. Origins of corallivory? Effect? (butterflyfishes)

Chapter 1&2: QUESTIONS & AIMS

a) Trophic chronology, explore patterns (wrasses, butterflyfishes)

b) Corallivory and significant cladogenesis (butterflyfishes)

CHAPTER 1&2: TROPHIC EVOLUTION

Labridae Chaetodontidae hard coral feedersoft

coral feeder

General InvertGastropodFishPlanktonHerbivoreCleanerForamsExcavatorBrowsingScrapersCoral Mucus

70.0 60.0 50.0 40.0 30.0 20.0 10.0 0.0

Cr Palae Eocene Oligo. Miocene Pl

Hypsigenyines

Labrines

Cheilines

Scarines

Labrichth.

Julidines

CHAPTER 1&2: TROPHIC EVOLUTION

Palaeo. Eocene Oligo. Miocene Pli Plt/Recent

Small invertebrates

Large gastropods

Piscivory

Coral mucus

Plankton

Foraminifera

Cleaner

Chaetodon Corallivory

7.5 million years?

CHAPTER 1&2: TROPHIC EVOLUTION

Chaetodontidae

Significantly more diverse than expectedCrown ChaetodonClade C1+C2+C3+C4Clade C2+C3+C4Clade C3+C4Clade C2Clade C4

Clade C3, not significantly more diverseBut contains most corallivores

Move onto coral reefs underpins cladogenesis in Chaetodon

Labridae

• Multiple origins

• Escalation of novelty

• Miocene NB

• ~7.5 MY in place

Chaetodontidae

• Multiple independent origins (5)

• Miocene NB

• Significantly diverse Chaetodon

• Move onto coral reefs underpinned diversification

CONCLUSIONS

Palaeo. Eocene Oligo. Miocene Pli Plt/Recent

Small invertebrates

Large gastropods

Piscivory

Coral mucus

Plankton

Foraminifera

Cleaner

CHAPTER 3: CORAL REEFS AS DRIVERS OF CLADOGENESIS

Q2: What roles have coral reefs played through time?

Labridae

(wrasses)

Chaetodontidae

(butterflyfish)Pomacentridae

(damselfish)

Apogonidae

(cardinalfish)

(More data) (More data) (First time) (First time)ABC

D

MY

ABC

D

MY

ABC

D

MY

ABC

D

MY

LTT

Tempo

Moments estimator

Significantly more diverse

I. Temporal concordance in reef fish origins?

II. Does reef use increase diversification?

Chapter 3: QUESTIONS & AIMS

a) ID congruent periods of elevated diversification

b) % Reef vs Rate of Diversification (reefs as drivers) % Reef vs Extinction (reefs as refuge)

0.0

10.0

20.0

30.0

40.0

50.0

60.0

70.0

Pa

leo

.Eo

cen

eO

ligo

.M

ioce

ne

Pl.

Cr.

ORIGIN AND TEMPO

K/T boundary

Expanding reefs

Log

# L

ine

ag

es

1

2

5

10

20

50

100

200

Time before present (MY)6070 50 40 30 20 10 0

Paleo. Eocene Oligo. Miocene Pl.Cr

ORIGIN AND TEMPO

LINEAGE THROUGH TIME

Fossil

Phylogeny

Lin

eag

es

Foss

il d

iver

sity

(Crisp & Cook 2009)

Time before present (MY)

‘hopping hotspot’ (Renema et al 2008)

CRYPTIC EXTINCTION?

Log

# L

ine

ag

es

1

2

5

10

20

50

100

200

Time before present (MY)6070 50 40 30 20 10 0

Paleo. Eocene Oligo. Miocene Pl.Cr

Fossil

Phylogeny

Hopping hotspot

ELEVATED CLADOGENESIS

Moments

SIGNIFICANT EXPANSION

Alfaro et al. (2007)Bellwood et al. (2004)Williams and Duda (2008)

Pomacentridae

Labridae

Apogonidae

Chaetodontidae

Significantly more diverse lineage

Time before present (MY)6070 50 40 30 20 10 0

Paleo. Eocene Oligo. Miocene Pl.Cr

ROLE OF CORAL REEFS

Significant relationship between % reef occupancy (of a family) and the global rate of diversification (of a family)

ROLE OF CORAL REEFS

CORAL REEFS ACT AS A DRIVER OF CLADOGENESIS

Ability of lineages to maintain high diversification rate even with high simulated extinction

ROLE OF CORAL REEFS

Higher % reef High resilience against extinction

CORAL REEFS ACT AS A REFUGE

CONCLUSIONS

• Congruent patterns

• Cryptic extinction event

• Expanding coral reef habitat

Supporting high diversification

Refuge from high extinctionLo

g #

Lin

ea

ge

s

1

2

5

10

20

50

100

200

Time before present (MY)6070 50 40 30 20 10 0

Paleo. Eocene Oligo. Miocene Pl.Cr

CHAPTER 4: HISTORIC BIOGEOGRAPHY OF FISHES ON

CORAL REEFS

Q3: How have historical biogeographic patterns resulted in current coral reef diversity?

Labridae

(wrasses)

Pomacentridae

(damselfish)

Chaetodontidae

(butterflyfish)

Global Dist.Widespread Indo-PacificEndemics

Barriers divide marine realms

EPB ??

??

IOPTTE3.1 MY

~12 MY

METHODS: ANCESTRAL RANGE RECONSTRUCTION

LAGRANGE (REE AND SMITH 2008)

5 biogeography regions1. East Pacific (EP)2. Atlantic (Atl.)3. Indian Ocean (In)4. Indo-Australian Archipelago (IAA)5. Central Pacific (CP)

METHODS: ANCESTRAL RANGE RECONSTRUCTION

Bannerfishes (Chaetodontidae)

ORIGINATION & DISPERSAL

Extant Lineages

EP Atl. In IAA CP

ORIGINATION & BIODIVERSITY

Regional origination/Regional RichnessTukey-Kramer Post-hoc:

EP, Atl, IAA HigherIn, CP Lower

ORIGINATION AND BIODIVERSITY

Regional origination/Family RichnessTukey-Kramer Post-hoc:

IAA HigherEP, Atl., In, CP Lower

ORIGINATION AND DISPERSAL THROUGH TIME: ANCESTRAL LINEAGES

Paleo-Eocene (65-33)Global pamixiaAccumulated ranges in IAA

Oligocene (33-23)Regional VicarianceRestricted dispersalSurvival in IAA

Miocene (23-5 MY)Leap in IAA OriginationSome Dispersal

Pliocene-Recent (5-0 MY)Some originationIncreasing dispersal

Accumulation

Survival

Origination

Expansion

BARRIERS & VICARIANCE

East Pacific Barrier (EPB)•Periodically breached

•West-East

•Multiple causes

Isthmus of Panama (IOP)•Wide distribution (~10MY)

•More near final closure

Terminal Tethyan Event (TTE)•No temporal congruence

•Pre-TTE (Paratethys?)

•Post-TTE (around Africa)

Hard Barriers not that hard

BARRIERS & VICARIANCE

Indian Ocean/IAA (In/IAA)•Temporal Concordance (2.5-5MY)

•Bidirection dispersal

•Barrier/Barriers?

IAA/Central Pacific (IAA/CP)•Temporal concordance (~6MY)

•Unidirection dispersal, IAA to CP

•Vicariance both side of IAA

•Global event?

Soft Barriers have more influence?Changing Ocean Currents?

CONCLUSIONS

Patterns of Origination and dispersal

East Pacific & Atlantic Isolated and Independent

IAAAccumulation, Survival, Origin, Expansion

Indian Ocean & Central Pacific Recipient/evolutionary sink

Vicariance and Barriers Hard barriers are temporally diffuse Soft barriers are temporally concordant

THESIS CONCLUSIONS

Trophic Evolution:• Miocene Important for novel feeding

modes

Role of Coral Reef:• Drivers of claodogenesis (Miocene)

• Refuge during high extinction

Biogeography & coral reef diversity• IAA – Centre of Accumulation,

Survival, Origin & Expansion

Palaeo. Eocene Oligo. Miocene Pli Plt/Recent

Small invertebrates

Large gastropods

Piscivory

Coral mucus

Plankton

Foraminifera

Cleaner

Fossil

Phylogeny

PUBLICATIONS

Cowman, P.F., D. R. Bellwood, and L. van Herwerden. 2009. Dating the evolutionary origins of wrasse lineages and the rise of trophic novelty on coral reefs. Molecular Phylogenetics & Evolution. 52:621-631.

Bellwood, D. R., S. Klanten, P. F. Cowman, M. S. Pratchett, N. Konow, and L. van Herwerden. 2010. Evolutionary history of the butterflyfishes (f: Chaetodontidae) and the rise of coral feeding fishes. Journal of Evolutionary Biology. 23:335-349.

Cowman, P. F., D. R. Bellwood. In press. Coral reefs as drivers of cladogenesis: expanding coral reefs, cryptic extinction events and the development of biodiversity hotspots. Journal of Evolutionary Biology.

Cowman, P. F., D. R. Bellwood. In prep. Historical biogeography of teleosts on coral reefs: patterns of origination and dispersal. Journal of Biogeography

Cowman, P. F., D. R. Bellwood. In prep. Vicariance of teleosts lineages on coral reefs: nature of historical hard and soft barriers to dispersal. Journal of Global Ecology and Biogeography

ARC Centre of Excellence

Coral Reef Studies

ACKNOWLEDGMENTS

• Prof. DR Bellwood, Dr. L van Herwerden• ARC Centre of Excellence, International Student Centre, G.R.S.• Colleagues: A. Hoey, S. Wismer, R. Bonaldo, C. LeFerve, S. Klanten, C. Goatley, J. Tanner.• Photos: R. Bonaldo, C. LeFevre , A. Hoey, J. Krajewski• HPC support staff, Tech support, BEAST user group members• Staff and students at Bodega Bay Applied Phylogenetics workshop• Professors, staff and students from School of Marine and Tropical Biology• Family & friends

FINANCIAL SUPPORT:• Tuition fees – Endeavour International Postgraduate Research Scholarship• Stipend – JCU scholarship• Project funding – ARC Centre of Excellence (DRB), JCU Internal Research Award, Graduate

Research Scheme

• Conference travel – ARC Centre of Excellence, Australian Coral Reef Society, ANNiMS.

• Virginal Chadwick Award for publication

ARC Centre of Excellence

Coral Reef Studies

QUESTIONS?

EVOLUTIONARY TEMPO