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Evolution and Diversity of Fishes
B. Venkatesh
Institute of Molecular and Cell Biology, A*STAR
Singapore
Lobe-finned fishes
and Tetrapods
Teleost fishesSpotted garSturgeon
Bichir
Bony Fishes (Osteichthyes)
https://commons.wikimedia.org/w/index.php?curid=24336974
Devonian – The Age of Fishes
Tetrapods
Teleost fishesSpotted garSturgeon
Bichir
Bony Fishes (Osteichthyes)
Lungfish
Coelacanth
Lobe-finned
fishes
Water to Land Transition
Tetrapods
Teleost fishesSpotted garSturgeon
Bichir
Bony Fishes (Osteichthyes)
Lungfish
Coelacanth
Lobe-finned
fishes
Which Living Fish is the Closest to Humans?
Coelacanth
Lungfish Coelacanth
Lungfish
Coelacanth
Lungfish
Genome size
3.0 Gb
2.9 Gb
40 - 130 Gb
1.0 GbSpotted gar
Coelacanth – A Living Fossil
Coelacanth genome sequenced in 2013
Closest fish to human
Amemiya et al., Nature 2013
Lungfish is the closest to land animals
Bayesian tree (251 genes)
Mammals
Birds
Amphibians
Ray-fin
fishes
Non-avian
reptiles
Cartilaginous
fishes
Lobe-fin
fishes
100200300400500 Myr
Tetrapods
Jawless
vertebrates
Transition from Aquatic to Terrestrial life
Fin-to-limb transition
zebrafish
fin raysdistal radials
mouse
stylopod
zeugopodautopod
Dogfish shark
“distal radials”ceratotrichia
HoxD cluster and long-range autopod enhancers
800 kb
Island1 Island2 Island3 Island4
Montavon T. et al. Cell 2011
Early phase HoxD gene expression: patterns the stylopod and zeugopod
Late phase HoxD gene expression: development of digits
HoxD cluster and long-range autopod enhancers
800 kb
Island1 Island2 Island3 Island4
Montavon T. et al. Cell 2011
Transgenic mouse embryos (E12.5)
Human
ChickenFrog
CoelacanthFugu
MedakaStickleback
Zebrafish
E shark
Atf2 Atp5g3 Lnp Evx2 Mtx2HoxdIs1 Is2 Is3 Is4 GCR ProxMouse
Amemiya et al., Nature 2013
Coelacanth Is1 expression in transgenic mouse (E12.5)
Limb budLimb buds
Conserved noncoding elements in HoxD locus
Teleost fishesSpotted garSturgeon
Bichir
Bony Fishes (Osteichthyes)
Lobe-finned fishes
and Tetrapods
https://commons.wikimedia.org/w/index.php?curid=24375559
Evolution of ray-finned fishes
Bony Fishes (Osteichthyes)
14 species27 species 8 species
33,200
species
30,500
species
Non-avian reptiles14.9%
Birds16.3%
Mammals9.2%
Amphibians11.6%
Teleosts: the largest group of vertebrates
Teleost fishes47.8%
What is the genetic basis of phenotypic variation?
Most diverse group of vertebrates
~30,500 species
Teleost fishesSpotted garSturgeon
Bichir
Bony fishes (Osteichthyes)
Lobe-finned fishes
and Tetrapods
Whole Genome
Duplication
WGD
Clarke JT et al. PNAS 2016
Phenotypic variation in Holosteans and Teleosts
Fossil+extant holosteans
(only 8 extant species)
Stem-group teleosts
Crown-group teleosts
(a) Teleosts do not show enhanced phenotypic evolution relative to holosteans
WGD
(b) Uneven diversification rate
Near et al. PNAS 2012; Santini et al. BMC Evol Biol 2009
WGD
8,900 species(Ostariophysi)
15,640 species(Percomorpha)
(c) Time lag between WGD
and major diversifications
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Cichlid Fishes(>2,200 species)
Tarang Mehta
No Whole-Genome Duplication in cichlid lineage
Colour patterns
Lake Tanganyika species Lake Malawi species
Julidochromis ornatus
Tropheus brichardi
Cyphotilapia frontosa
Melanochromis auratus
Pseudotropheus microstoma
Cyrtocara moorii
Lake Victoria Lake Malawi Lake Tanganyika Lake Nicaragua
H. chilotes M. labrosus L. labiatus A. labiatus
EV
OLU
TIO
NA
RY
PA
RA
LL
ELIS
M
Thick-lipped phenotype
Salzburger, W. (2009)
EAST AFRICAN CICHLIDSVictoria
Tanganyika
Malawi
Brawand et al. Nature 2014
15,000-100,000 years
10-12 million years
<5 million years
Lake Victoria (~500 species)
Lake Tanganyika (~250 species)
Lake Malawi (~500 species)
A. burtoniO. niloticus
Summary
‣ Accelerated evolution of protein-coding sequence
‣ Transposable element insertions altering gene
expression
‣ Increased gene duplication with new expression
patterns
‣ Regulatory sequence evolution
Genome sequence
Lake representatives
N. brichardiP. nyererei M. zebra
Lake Victoria Lake Tanganyika Lake Malawi
Riverine
Regulatory Sequence Evolution
Medaka
Medaka
Medaka
Alvin Ng, Zhi Wei Lim and Venkatesh
O. niloticus (Nile tilapia) CNE
P. nyererei (Lake Victoria) CNE
Phenotype:
Sexual dimorphism
Ecotype:
Ecological opportunities
Genotype:
Genome plasticity
Adapted from Seehausen, O. (2015)
MAJOR DRIVERS OF ADAPTIVE RADIATION OF AFRICAN CICHLIDS
seahorses
seadragons
pipefish
pipefish
Seahorses, pipefish and seadragon
Hamilton et al. 2016
‘Extreme phenotypes’
Dorsal fin
Pectoral finPelvic fin
Anal fin
Caudal fin
Specialized Morphology of Seahorse
Brood pouch
Male seahorse
Salmon
No pelvic fin
No teeth
Fused jawsTube-like mouth
No caudal fin
Prehensile tail
No scales
Bony plates
Mating seahorses
Photograph: George Grall/Getty Images/National Geographic
Birthing Father
Credit: Rudie Kuiter
Tiger tail seahorse (Hippocampus comes)
IUCN List of Threatened Species: “Vulnerable”
Seahorse Genome
Seahorse
Nile tilapia
Platyfish
Medaka
Stickleback
Fugu
Mudskipper
Zebrafish
Spotted gar
0.04
0.463
0.415
0.443
0.460
0.437
0.454
0.450
0.422
Seahorse protein sequences evolving faster
4,122 protein sequences; ML treeLin et al. Nature 2016
Seahorse
Nile tilapia
Platyfish
Medaka
Stickleback
Fugu
Zebrafish
Spotted gar
1.924
1.693
1.919
1.868
1.8885
1.748
1.818
1.622
0.2
Mudskipper
Seahorse nucleotide sequences evolving faster
Neutral tree based on four-fold degenerate (4D) sites)
• SCPP genes critical for skeletal mineralization
• Present in all bony vertebrates
• Two groups – Acidic SCPP and P/Q-rich SCPP
mineralization of bone
and dentin
Enamel or enameloid
formation
Secretory calcium-binding phosphoprotein
(SCPP) gene family
Secretory Calcium-binding Phosphoprotein (SCPP)
genes
Chr4ChrX
Human genome
Acidic SCPP genes – bone and dentine
Proline/Glutamine-rich SCPP genes – enamel
milk, saliva, tears
17 Mb
Fugu Chr17
Seahorse scaf51 scaf_232
Zebrafish Chr1 Chr10 Chr5
Chr4ChrXHuman
Seahorse has lost P/Q-rich SCPP genes
Acidic SCPP genes
P/Q-rich SCPP genes
Toothless vertebrates (‘edentulism’)
All turtles Baleen whaleAll birds Pangolin
Loss of all enamel-related and dentin-related genes
Seahorse
Mutations in some or all of enamel-related and dentin-related genes
Meredith et al. Science 2014
Pitx1/Pitx2, Tbx4/Tbx5
Tanaka et al. Dev Biol 2005
Pitx2
Forelimb (Pectoral fin)
Hindlimb (Pelvic fin)
Loss of pelvic fins
Marcil et al. Development 2003
tbx2 tbx4 brip1
Seahorse
Fugu
Stickleback
Zebrafish
Tbx4 gene is missing in seahorse
Lin et al. Nature 2016
Lin et al. Nature 2016
CRISPR-Cas9 mediated knockout of Tbx4 in zebrafish
Loss of pelvic fins
Wild type
ventral ventral
WT tbx4- / -
Tbx4 knockout
Loss of Tbx4
IntactTbx4
IntactTbx4
IntactTbx4
Loss of pelvic fins
Freshwater stickleback
Near et al. 2012
Male pregnancy
Astacin metalloprotease subfamily (C6AST)
High choriolytic enzyme (HCE)
Low choriolytic enzyme (LCE)
Hatching enzymes
Patristacin (pipefish)
Expansion of a gene family
Expansion of patristacin gene family
Patristacin genes express in male brood pouch
Lin et al. Nature 2016
Expansion of patristacin gene family
Platyfish – ovoviviparous (‘female pregnancy’)
Genetic basis for the specialized phenotype of seahorse
Higher molecular evolutionary rate
Loss of some crucial genes
Expansion of some gene families with novel expression pattern
High turnover of regulatory elements
‘Nature’s gift to Science’