Qu’a apporté la génomique à la phylogénie des animaux ?
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Qu’a apporté la génomique à la phylogénie des animaux ? Hervé Philippe Département de Biochimie, Centre Robert Cedergren, Université de Montréal, Succursale Centre-Ville, Montréal, Québec H3C3J7, Canada. Cambrian explosion: a paleontological perspective. Marrella. Aysheaia. Halkieria.

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Qu’a apporté la génomique à la phylogénie des animaux ? Hervé Philippe

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Qu a apport la g nomique la phylog nie des animaux herv philippe

Qu’a apporté la génomique à la phylogénie des animaux ?

Hervé Philippe

Département de Biochimie, Centre Robert Cedergren, Université de Montréal, Succursale Centre-Ville, Montréal, Québec H3C3J7, Canada


Qu a apport la g nomique la phylog nie des animaux herv philippe

Cambrian explosion: a paleontological perspective

Marrella

Aysheaia

Halkieria

Pikaia


Qu a apport la g nomique la phylog nie des animaux herv philippe

Cambrian explosion: a molecular perspective

Choanoflagellata

Porifera

Porifera

Porifera

Cnidaria

Cnidaria

Ecdysozoa

Ecdysozoa

Ecdysozoa

Lophotrochozoa

Lophotrochozoa

Lophotrochozoa

Lophotrochozoa

Deuterostomia

Deuterostomia

Deuterostomia

Deuterostomia

Molecular phylogenies should resolve series of speciation events separated by a few millions of years

MYa

700

600

500

400

300

200

100

0

Cambrian explosion


Qu a apport la g nomique la phylog nie des animaux herv philippe

Lack of resolution in molecular phylogenetics

(1)Inadequate selection of sequences (non-orthologous, saturated, etc.)

Inadequate tree reconstruction method

Inadequate taxon sampling

Rapid diversification of species

  • Points (1), (2) and (3) are always mixed:

    • A (simplistically) theoretical overview

    • Analyses of several case studies

    • A molecular dating approach


Qu a apport la g nomique la phylog nie des animaux herv philippe

Cambrian explosion: a molecular perspective

Choanoflagellata

Porifera

Porifera

Porifera

Cnidaria

Cnidaria

Ecdysozoa

Ecdysozoa

Ecdysozoa

Lophotrochozoa

Lophotrochozoa

Lophotrochozoa

Lophotrochozoa

Deuterostomia

Deuterostomia

Deuterostomia

Deuterostomia

Bootstrap support  95% requires 3 substitutions on the corresponding branch (Felsenstein, 1985)

T

MYa

700

600

500

400

300

200

100

0

Cambrian explosion

18S Ribosomal RNA (~1000 positions): ~100 substitutions over 500 MY

 resolution for branches with T  15 MY

146 genes (Delsuc et al. 2006, 33800 positions): ~7000 substitutions over 500 MY

 resolution for branches with T  0.25 MY

50 genes (Rokas et al. 2005, 12060 positions): ~2400 substitutions over 500 MY

 resolution for branches with T  0.7 MY


Qu a apport la g nomique la phylog nie des animaux herv philippe

Phylogenetic signal

Inferred

trees

3: 10%

3

2: 25%

1

2

3

1000 positions

1: 80%

1

2

12000

positions

3: 100%

2

1

3

2: 100%

Phylogenetic signal

1: 100%

true history


Qu a apport la g nomique la phylog nie des animaux herv philippe

Comparison of ML SSU and LSU trees (A and B, respectively)

Medina M. et.al. PNAS 2001;98:9707-9712


Qu a apport la g nomique la phylog nie des animaux herv philippe

50 genes (12,060 amino acid positions), ML RtREV+I+ / MP bootstrap support

Rokas et al. (2005) Animal evolution and the molecular signature of radiations compressed in time. Science, 310:1993-1998


Qu a apport la g nomique la phylog nie des animaux herv philippe

Phylogenetic signal

Inferred

trees

3: 10%

3

2: 25%

1

2

3

1000 positions

1: 80%

1

2

12000

positions

3: 100%

2

1

3

2: 100%

Phylogenetic signal

1: 100%

true history


Qu a apport la g nomique la phylog nie des animaux herv philippe

Non-phylogenetic signal

Sequence evolves according to a very complex and heterogeneous process that our tree reconstruction method approximates as best as they can using elaborated model of sequence evolution

Real complexities: mutation process is not homogeneous over time and across the genome, population structure is not homogeneous over time, selective pressures are not homogeneous over time and across the genome

 Nucleotide compositions are heterogeneous across species, evolutionary rate is heterogeneous across positions and over time (heterotachy), substitution process is heterogeneous across positions and over time, positions are inter-dependent, etc.

All the complexities that are not adequately handled by our oversimplified models of sequence evolution can imply systematic biases, which are referred here as non-phylogenetic signal


Qu a apport la g nomique la phylog nie des animaux herv philippe

Phylogenetic signal and non-phylogenetic signal

Inferred

trees

3: 10%

3

2: 5%

1

2

3

apparent

signal

1: 70%

1

2

3: 100%

2

1

3

2: 5%

1

2

3

Non-phylogenetic

signal

1: 100%

Phylogenetic signal

true history

1

2

3

1000 positions

12000

positions


Qu a apport la g nomique la phylog nie des animaux herv philippe

Systematic errors (inconsistency)

A

C

A

C

q

q

p<q2

p

B

D

B

D

Systematic error: the error in phylogenetic estimates that is due to the failure of the reconstruction method to account fully for multiple substitutions (in a probabilistic framework, the properties of the data)

Systematic errors will not disappear with phylogenomics, and may indeed become more apparent

A

A

B

C

C

B

D

D

LONG BRANCH ATTRACTION (Felsenstein, 1978)


Qu a apport la g nomique la phylog nie des animaux herv philippe

Multiple substitutions at the same position

C

C

GC

AC

AG

A

A

C

C

Tree building artefact

A

A


Qu a apport la g nomique la phylog nie des animaux herv philippe

MLMP

9956

9455

9751

7236

8454

10075

4374

50 genes (12,060 amino acid positions), ML RtREV+I+ / MP bootstrap support

Rokas et al. (2005) Science, 310:1993-1938


Qu a apport la g nomique la phylog nie des animaux herv philippe

Phylogenetic signal and non-phylogenetic signal

Inferred

trees

3: 84%

ML

3

2: 99%

1

2

3

apparent

signal

1: 100%

2

3: 54%

1

MP

2: 56%

1

2

3

Non-phylogenetic

signal

1: 75%

1

Phylogenetic signal

2

MLMP

9956

9455

9751

7236

8454

10075

4374

true history

3

12000 positions

1

12000

positions

2

3


Qu a apport la g nomique la phylog nie des animaux herv philippe

Phylogenomics yields incongruent results

PLoS Biology

Nature

Current Biology


Qu a apport la g nomique la phylog nie des animaux herv philippe

Single gene phylogeny of Schierwater et al. (2009)

Anthozoa

Amoebozoa

Hexapoda

Ascomycota

Crustacea

Basidomycota

Scyphozoa

Calcarea

Priapulida

Hexactinellida

Bivalvia

Demospongiae

Mitochondrial ATP synthase F0 subunit 6

Echinodermata

Scyphozoa

NON-HOMOLOGOUS

Hexactinellida

Anthozoa

Calcarea

Trichoplax adhaerens

Demospongiae

Choanoflagellata

PARALOGOUS

ER HSP70

Hydrozoa

Echinodermata

Mammalia

Mammalia

Ctenophora

Hexapoda

Trichoplax adhaerens

Crustacea

Choanoflagellata

Bivalvia

Amoebozoa

Annelida

Cytosolic HSP70

Excavata

Gastropoda

Ascomycota

Hemichordata

Basidomycota

0.1

Chromalveolata

Annelida

0.1


Qu a apport la g nomique la phylog nie des animaux herv philippe

Single gene phylogeny of Schierwater et al. (2009)

CDC42

Basidomycota

Amoebozoa

Ascomycota

Ascomycota

RAC1

Choanoflagellata

Basidomycota

Calcarea

Choanoflagellata

Anthozoa

Trichoplax_adhaerens

Small RAS-like GTPase

Hexactinellida

Excavata

Chromalveolata

Chromalveolata

Mammalia

Echinodermata

Echinodermata

Demospongiae

Hexapoda

Hexactinellida

Trichoplax adhaerens

Anthozoa

Mammalia

Demospongiae

Amoebozoa

Annelida

Hexapoda

0.1

Cubozoa

GTP-binding nuclear protein Ran

Calcarea

Priapulida

Gastropoda

Hydrozoa

0.1


Qu a apport la g nomique la phylog nie des animaux herv philippe

Single gene phylogeny of Schierwater et al. (2009)

Demospongiae

Anthozoa

Cubozoa

Chromalveolata

Scyphozoa

Excavata

Anthozoa

Ascomycota

Trichoplax adhaerens

Mammalia

Pair box domain protein PAX-B

Mammalia

Hexapoda

Basidomycota

Trichoplax adhaerens

Pol II

Amoebozoa

Echinodermata

Hydrozoa

Hexapoda

0.1

0.1

Pol III

DNA directed RNA polymerase


Qu a apport la g nomique la phylog nie des animaux herv philippe

0.1

0.1

Excavata

Ciliophora

Contaminated dataset

Schierwater et al. (2009) PLoS Biol 7(1): e1000020

Amoebozoa

Basidiomycota

Ascomycota

Choanoflagellata

Placozoa

4

Calcarea

Porifera

Demospongiae

9

Hexactinellida

98

53

Ctenophora

Cnidaria

27

62

Bilateria

Excavata

Ciliophora

Amoebozoa

Ascomycota

Basidiomycota

Choanoflagellata

Calcarea

36

Porifera

Demospongiae

Clean dataset

Philippe et al. (2011) PLoS Biol in press

44

Hexactinellida

Ctenophora

40

4

9

Placozoa

Cnidaria

23

Bilateria

38


Qu a apport la g nomique la phylog nie des animaux herv philippe

Dunn et al. : 150 genes 24,708 positions

Contaminations:

Symsagitiferra: 13 genes (including 6 Chlorophyta, 2 Ciliophora, 2 Bacteria)

4 Neochildia (Microsporidia)

2 Saccoglossus (Mus)

2 Acanthoscurria (angiosperm)

2 Hydra (Artemia)

1 Oscarella (Pseudomonas)

1 Asterina (Bacteria)

1 Dugesia (Gallus)

1 Xiphinema (Lumbricus)

1 Monosiga (Rhizopus)

1 Macrostomum

2 Trichinella

2 Priapulus

1 Branchiostoma


Qu a apport la g nomique la phylog nie des animaux herv philippe

Dunn et al.: 150 genes 24,708 positions

Frameshifts: 63 concerned species

Drosophila2

Paraplanocera3

Echinoderes4

Xenoturbella4

Chaetopterus5

Cyanea5

Cristatella6

Platynereis6

Spinochordodes6

Cryptococcus8

Spadella8

Mnemiopsis9

Bugula10

Gnathostomula10

Hydra10

Sphaeroforma10

Turbanella10

Chaetoderma15

Myzostoma15

Scutigera16

Carcinus18

Lumbricus20

Ptychodera20

Euperipatoides21

Carcinoscorpius22

Symsagittifera22

Chaetopleura23

Homo25

Boophilus30

Hypsibius30

Richtersius30

Daphnia32

Asterina35

Anoplodactylus40

Argopecten43

Xiphinema43

Acropora45

Dugesia46

Brachionus50

Ciona50

Branchiostoma52

Hydractinia53

Haementeria54

Flaccisagitta55

Strongylocentrotus55

Acanthoscurria58

Aplysia58

Saccoglossus60

Capsaspora68

Gallus73

Phoronis87

Capitella93

Echinococcus100

Ferrenopenaeus112

Monosiga118

Schmidtea129

Oscarella141

Mytilus151

Euprymna201

Trichinella281

Crassostrea296

Macrostomum382

Biomphalaria384


Qu a apport la g nomique la phylog nie des animaux herv philippe

Frameshifts:3868 “invented” amino acids

5 introns:

Anoplodactylus

Chaetopterus

Ciona

Themiste

Trichinella

Many single point errors :

A total 970 errors

(in large part due to the use of

erroneous mitochondrial genetic code!)

Several genes with paralogy issues:

2-5 intractable problems

10-20 tractable problems

DUNN:150 genes 21,152 positions

55.6% of missing data

UPDUNN:150 genes 18,463 positions

35.6% of missing data


Qu a apport la g nomique la phylog nie des animaux herv philippe

Saccharomyces

Cryptococcus

Sphaeroforma

Amoebidium

Capsaspora

Monosiga

86

Amphimedon

62

Oscarella

mertensiid

Mnemiopsis

Hydractinia

Hydra

Cyanea

84

Nematostel

Acropora

Symsagittifera

Neochildia

58

Homo

Gallus

Ciona

Branchiostoma

Xenoturbella

Saccogloss

Ptychodera

30

Strongylocentrotus

Asterina

Gnathostomula

Spadella

Flaccisagitta

Philodina

Brachionus

Macrostomum

Paraplanocera

Echinococcus

Schmidtea

Dugesia

Pedicellina

Cristatella

Bugula

Phoronis

Turbanella

Terebratalia

Cerebratulus

Carinoma

Chaetopterus

Myzostoma

Themiste

Platynereis

Lumbricus

Haementeria

Urechis

Capitella

Chaetopleura

Chaetoderma

Euprymna

Mytilus

Crassostrea

BS=100%

Argopecten

Biomphalaria

Aplysia

70<BS<100

Priapulus

Echinoderes

Xiphinema

Trichinella

Spinochordodes

Richtersius

0.2

Hypsibius

Euperipatoides

Drosophila

Daphnia

Fenneropenaeus

Carcinus

Scutigera

Carcinoscorpius

Anoplodactylus

Acanthoscurria

Boophilus

Porifera

Ctenophora

Cnidaria

Clean Dunn et al. dataset

Bilateria

CAT+G model

150 genes 18,463 positions

35.6% of missing data


Qu a apport la g nomique la phylog nie des animaux herv philippe

Model of sequence evolution

+ 20 stationary probabilities (i)

+ 190 relative rates (ij = ji)

C

D

E

F

G

H

I

K

A C D E F G H I K L M N P Q R S T V W Y

L

M

N

P

,

Q

R

S

T

V

W

Y

A C D E F G H I K L M N P Q R S T V W

WAG matrix

l

a

b


Qu a apport la g nomique la phylog nie des animaux herv philippe

The CAT model of sequence evolution

Man

M A E I G R L I E F S A M V D F W Q N R C

Frog

M A E I G R L V E Y S A M V D F W Q N R C

Zebrafish

M A D L G K L I D Y S A L V D F W Q N R C

Fly

M S D I G K L V E F S P M V E F W Q Q K C

Yeast

M S E I G R L V E F T P M V E F W Q N R C

Amoeba

L S E L G R L V D F T A M V D F W N N R C

Paramecium

L A E L G K L V E Y A P M I D F W Q A R C

Green alga

L S D L G K L I D F S A M I N F W Q N K C

Homogeneous

(WAG) model

Heterogeneous (CAT) model : K distinct profiles

amino acid

profiles

1 substitution

matrix

ACD...VWY

ACD...VWY

ACD...VWY

ACD...VWY

Categories (modes): 1 2 3 … K

Lartillot & Philippe (2004) Mol Biol Evol. 21:1095-1109


Qu a apport la g nomique la phylog nie des animaux herv philippe

The CAT model of sequence evolution

A C D E F G H I K L M N P Q R S T V W Y

To keep the number of parameters low, a category is only defined by a set of stationary probabilities (the relative rates are uniform), and the number of categories is inferred from the alignment

+ 20 stationary probabilities (i)

+ uniform relative rates (ij=ji)

C

D

E

F

G

H

I

K

L

M

N

P

Q

R

S

T

V

W

Y

A C D E F G H I K L M N P Q R S T V W Y

A C D E F G H I K L M N P Q R S T V W

Lartillot & Philippe (2004) Mol Biol Evol. 21:1095-1109


Qu a apport la g nomique la phylog nie des animaux herv philippe

Stable categories inferred by the CAT model

E

Q

The size of an amino acid is proportional to its stationary probability

D

N


Qu a apport la g nomique la phylog nie des animaux herv philippe

Multiple substitutions between two amino acids

D

E

D

E

D

D

E

E

D

E

D

E

D

D

D

E

E

E

D

E

D

E

E

D

D

E

D

E

D

E

E

D

E

E

D


Qu a apport la g nomique la phylog nie des animaux herv philippe

What is predicted by evolutionary models?

GTR

WAG

CAT

# substitutions

0

1

2

3

4

5

6

7


Qu a apport la g nomique la phylog nie des animaux herv philippe

Multiple substitutions between two amino acids

D

E

D

E

D

D

These multiple substitutions are well handled by the CAT model because this position will be explained by this profile:

E

E

D

E

D

E

D

D

D

E

E

E

D

E

D

E

E

D

D

E

D

E

D

E

E

D

E

E

D


Qu a apport la g nomique la phylog nie des animaux herv philippe

What is predicted by WAG replacement matrix?

# substitutions


Qu a apport la g nomique la phylog nie des animaux herv philippe

Further reduction of non-phylogenetic signal

Human

Mouse

Zebrafish

Tunicate

Triclad platyhelminth

Trematode platyhelminth

Mollusk

Annelid

Priapulid

Arthropod

Nematode

Anthozoan cnidarian

Hydrozoan cnidarian

Hexactinelid poriferan

Calcareous poriferan

Demosponge

Choanoflagellate

100

100

100

95

63

100

49

99

52

98

76

78

76

55

74

0.02

Alignment of Rokas et al. (2005):50 genes (12,060 amino acid positions)

Model CAT+, inferred using phylobayes; 100 bootstrap replicates


Qu a apport la g nomique la phylog nie des animaux herv philippe

Reduction of non-phylogenetic signal

100

Chordates

90

Protostomes

80

Ecdysozoa

70

Lophotrochozoa

60

Bootstrap support

Bilaterians

50

Cnidarians

40

Poriferans

30

20

10

0

MP

rtREV+

CAT+


Qu a apport la g nomique la phylog nie des animaux herv philippe

3

5

3

Fungi

Ichthyosporea

Choanoflagellata

Homoscleromorpha

2

64

Porifera

Calcarea

4

90

2

Hexactinellida

Demospongiae

99

9

Placozoa

3

22

3

Ctenophora

78

62

Cnidaria

98

62

Bilateria

5

3

3

Fungi

Ichthyosporea

91

Choanoflagellata

Ctenophora

4

2

Homoscleromorpha

55

Hexactinellida

2

Demospongiae

80

99

9

22

Calcarea

Placozoa

38

98

Cnidaria

Bilateria

45

0.1

128 genes

30,257 positions

Philippe et al. (2009) Curr. Biol.

Model CAT+

0.1

Model WAG+

Philippe et al. (2011) PLOS Biol.


Qu a apport la g nomique la phylog nie des animaux herv philippe

Improvement of phylogenetic resolution

1

Phylogenetic signal

3

2

3

2

Non-phylogenetic

signal

1

true history

Phylogenomics: phylogenetic signal as well as non-phylogenetic signal are abundant

To improve resolution, one has to use the same methods as to avoid systematic errors:

Complex model of sequence evolution

Rich taxon sampling

Removal of fast evolving positions and taxa


Qu a apport la g nomique la phylog nie des animaux herv philippe

3

Choanoflagellata

2

Homoscleromorpha

91

4

Calcarea

96

2

Porifera

Hexactinellida

Demospongiae

9

Placozoa

22

3

Ctenophora

93

62

Cnidaria

94

90

Bilateria

0.1

0.1

Model CAT+

47 species

128 genes

30,257 positions

Philippe et al. (2009) Curr. Biol.

Choanoflagellata

Model CAT+

3

Ctenophora

70

Cnidaria

94

18 species

Same sampling as

Schierwater et al.

Calcarea

Placozoa

44

Demospongiae

56

9

86

Hexactinellida

53

Bilateria

Philippe et al. (2011) PLOS Biol.


Qu a apport la g nomique la phylog nie des animaux herv philippe

Hétérogénéité des modèles

M A D I G R L I E F S A M V D F W

M G E I G R L V E Y S A M V D F W

M A E L G K L I D Y S A L V D F W

M T D I G K L V E F S P M V E F W

M W D I G R L V E F T P M V E Y W

M S D L A R L V D F T A M V D F W

M Y D L G K L I D F S A M I N F W

M A D I G R L I E F S A M V D Y W

M E D I G R L V E Y S A M V D F W

M R D L G K L I D Y S A L V D F W

au cours du temps

états de caractères

entre les sites

  • Hétérogénéité des états de caractères

    • matrices d’échange : Dayhoff, WAG … LG, GTR

  • Hétérogénéité entre les sites

    • loi gamma, modèle CAT

  • Hétérogénéité au cours du temps

    • modèle covarion, points de changements


Qu a apport la g nomique la phylog nie des animaux herv philippe

Hypothèse

Hétéropécilie

variation temporelle du processus de substitution en acides aminés pour un site donné(poikillw= to vary)


Qu a apport la g nomique la phylog nie des animaux herv philippe

Retrait progressif des sites hétéropécilles

Protocole

Données

  • 13 protéines mitochondriales

    • 68 espèces

Bilateria

Deuterostomia

Protostomia

Cnidaria

Porifera

CAT+G4

Choanoflagellata

  • Inférence par CAT+Γ4 avec les jeux réduits

Sites retirés suivant une valeur croissante de PIPn

Roure & Philippe (2011) BMC Evol Biol 11:17


Qu a apport la g nomique la phylog nie des animaux herv philippe

Retrait progressif des sites hétéropécilles

probabilité postérieure

taille de l’alignement

Bilateria

Deuterostomia

Cnidaria

Choanoflagellata

Roure & Philippe (2011) BMC Evol Biol 11:17

41

Protostomia

Porifera


Qu a apport la g nomique la phylog nie des animaux herv philippe

Retrait progressif des sites hétéropécilles

probabilité postérieure

taille de l’alignement

Deuterostomia

Cnidaria

Choanoflagellata

Roure & Philippe (2011) BMC Evol Biol 11:17

Protostomia

Porifera


Qu a apport la g nomique la phylog nie des animaux herv philippe

Retrait progressif des sites hétéropécilles

probabilité postérieure

taille de l’alignement

Deuterostomia

Cnidaria

Cnidaria

Porifera

Choanoflagellata

Choanoflagellata

Roure & Philippe (2011) BMC Evol Biol 11:17

Deuterostomia

Protostomia

Protostomia

Porifera

Porifera


Qu a apport la g nomique la phylog nie des animaux herv philippe

Retrait progressif des sites hétéropécilles

probabilité postérieure

taille de l’alignement

Deuterostomia

Deuterostomia

Cnidaria

Cnidaria

Porifera

Choanoflagellata

Choanoflagellata

Choanoflagellata

Roure & Philippe (2011) BMC Evol Biol 11:17

Deuterostomia

Protostomia

Protostomia

Protostomia

Cnidaria

Porifera

Porifera

Porifera


Qu a apport la g nomique la phylog nie des animaux herv philippe

Retrait progressif des sites

Sites à évolution rapide

probabilité postérieure

probabilité postérieure

Sites hétéropéciles

taille de l’alignement

taille de l’alignement

Le regroupement incorrect des Cnidaires et des Porifères n’est pas dû à la présence de sites à évolution rapide, mais à la présence de sites hétéropéciles qui est erronément interprétée comme une synapomorphie pour regrouper Cnidaires et Porifères

Roure & Philippe (2011) BMC Evol Biol 11:17


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