ARC Centre of Excellence Coral Reef Studies DATING THE ORIGINS OF CORAL REEF FISHES Supervisors: DR Bellwood L van Herwerden Peter F Cowman
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