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Biota-FAPESP International Symposium on Phylogeography Comparative phylogeography of Neotropical carnivores: congruence vs. uniqueness of historical patterns Eduardo Eizirik Faculdade de Biociências, PUCRS, Brasil Instituto Pró-Carnívoros, Brasil Laboratory of Genomic Diversity, NIH, USA

Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

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Page 1: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Biota-FAPESP International Symposium on Phylogeography

Comparative phylogeography of Neotropical

carnivores:congruence vs. uniqueness of historical patterns

Eduardo Eizirik

Faculdade de Biociências, PUCRS, Brasil

Instituto Pró-Carnívoros, Brasil

Laboratory of Genomic Diversity, NIH, USA

Page 2: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Neotropical carnivores

Page 3: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

The Great American Biotic

Interchange and the

diversification of Neotropical

carnivores

Meta-analysis of molecular phylogenies

and divergence dates derived from

nuclear gene supermatrices.

Contrasting patterns of diversification

among carnivoran families.

Eizirik (in press)

Page 4: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Eizirik (in press)

Page 5: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Ocelot (L. pardalis)

Mexico,

Central America

N. northwest SA

N. northeast SA

Brasil, Bolivia,

Paraguai

Margay (Leopardus wiedii)

N. Mexico

S. Mexico,

Guatemala

Costa Rica,

Nicaragua

Northern SA

Bolivia e Peru

Brasil e Paraguai

Page 6: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Historical Distribution

Current Distribution

Panthera onca

16, 26

2021, 22

23, 24, 25

30, 3731

40, 41

42, 4443

46

47

49,50

51,52

54

56,58

59 60, 62, 63

6465, 66

68

75

Markers:

- mtDNA control region

- 29 microsatellite loci

Page 7: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Pco P. concolor

Mexico,

Guatemala

Venezuela

Brazil

Argentina

Puma yagouaroundi1142 bp mtDNA

(CR, ATP8, ND5, 16S)

ML

Hya11 Mexico

Hya21 Mexico

Hya28 Mexico

Hya29 Mexico

Hya24 Mexico

Hya13 Guatemala

Hya14 Guatemala

Hya18 Mexico

Hya23 Mexico

Hya25 Mexico

Hya15 Guatemala

Hya45 Venezuela

Hya47 Venezuela

Hya49 Venezuela

Hya32 Brasil

Hya34 Brasil

Hya35 Brasil

Hya36 Brasil

Hya37 Brasil

Hya40 Argentina

Hya41 Argentina

Hya42 Argentina

Hya16 Argentina

Hya17 ArgentinaHya43 Argentina

*

*

*

**

**

Page 8: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Puma concolor

Leopardus pardalis

Leopardus wiedii

Panthera onca

Puma

yagouaroundi

Page 9: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

L. tigrinus, L. geoffroyi, L. colocolo and L. guigna

Leopardus tigrinus

Leopardus geoffroyi

?

L. guina

L. colocolo

L. tigrinus

L. geoffroyi

Trigo et al. (in prep.)

Page 10: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

mtDNA Control Region

bLti301 bLge06

bLti133 bLti60 bLti134 bLti110 bLge46 bLge79 bLti71 bLge11 Lco02 bLti47 bLti68 bLti30 bLti29 bLti74 bLti89 bLti100

bLti93 bLti95

bLti50 bLti46 bLti80 bLti113 bLti114 bLti59 bLti131

bLti119 bLti106 bLge07 bLti98

bLti108 bLti51 bLti92 bLti75 bLge02 bLge80

bLti10 bLti102 bLti04 bLti76 bLti62 bLti44 bLti72

bLge08 bLti87 bLti124 bLti05 bLti31 bLti61 bLge27

bLti56 bLti109 bLti69 bLge01 bLti117 bLti48 bLti135

bLti132 bLti99

bLti90 Ogu03

bLge63 bLge64

bLge52 bLti09 bLge10 bLti49 bLti79 bLge57 bLge35 bLge71 bLge13g bLti01

bLge20 bLge03 bLti121 bLge05 bLge56 bLge42 bLge29 bLge31 bLge04 bLge33

bLge66 bLge51 bLge50 bLge53

bLge61 bLge67 bLge68 bLge62

bLti65 bLge73 bLge37 bLge43 bLge44 bLge40 bLge70 bLge41 bLge89 bLge12 bLge39

bLco07 bLco06

bLco30 bLco13

bLti85 bLti24

bLti28

*

Trigo et al. (2008) Mol. Ecol.

Page 11: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

bLco07

bLco06

bLco30

bLco13

bLti85

bLti24

bLti28

70

bLti301 SPbLge06 RS

bLti133 RSbLti60 SPbLti134 RSbLti110 RSbLge46 RSbLge 79 RSbLti71 SPbLge11 RSLco02bLti47 RS bLti68 RSbLti30 PARbLti29 PARbLti74 SPbLti89 PRbLti100 RS

bLti93 PRbLti95 RS

bLti50 RSbLti46 RSbLti80 RSbLti113 RSbLti114 RSbLti59 SPbLti131 RS

bLti119 RSbLti106 RSbLge07 RSbLti98 RS

bLti108 RSbLti51 RSbLti92 PRbLti75 SPbLge02 RSbLge80 RS

bLti10 RSbLti102 RSbLti04 RSbLti76 SPbLti62 SPbLti44 SCbLti72 MS

bLge08 RSbLti87 SPbLti124 RSbLti05 RSbLti31 PRbLti61 SPbLge27 RS

bLti56 SPbLti109 MGbLti69 RSbLge01 RSbLti117 RSbLti48 RSbLti135 RSbLti132 RS

bLti99 RSbLti90 PR

98

62

Ogu03

bLge63 BOL

bLge64 BOL

bLge52 ARG

bLti09 RS

bLge10 RS

bLti49 RS

bLti79 RS

bLge57 URU

bLge35 RS

bLge71 RS

bLge13 RS

bLti01 RS

bLge20 URU

bLge03 RS

bLti121 RS

bLge05 RS

bLge56 URU

bLge42 RS

bLge29 RS

bLge31 RS

bLge04 RS

bLge33 RS

bLge66 BOL

bLge51 ARG

bLge50 ARG

bLge53 ARG

bLge61 ARG

bLge67 BOL

bLge68 BOL

bLge62 BOL

bLti65 SP

bLge73 RS

bLge37 RS

bLge43 RS

bLge44 RS

bLge40 RS

bLge70 RS

bLge41 RS

bLge89 RS

bLge12 RS

bLge39 RS

95

73

65

62 Brazilian populations of L.

tigrinus may have mtDNA

lineages from three

distinct species!

Page 12: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

L. tigrinus

clade

L. geoffroyi clade

L. colocolo clade

L. guigna

L. pardalis

L. wiedii

mtDNA haplotype network

Trigo et al. (in prep.)

Page 13: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

L. tigrinus

clade

L. geoffroyi clade

L. colocolo clade

L. guigna

L. pardalis

L. wiedii

mtDNA haplotype network

L. tigrinus

(C, NE Brasil)

Trigo et al. (in prep.)

Page 14: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

L. guigna

L. pardalis + L. wiedii

Haplotype network (intron 2, PLP1 gene, X chromosome)

L. colocolo

L. geoffroyi

Trigo et al. (in prep.)

Page 15: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

L. guigna

L. pardalis + L. wiedii

L. tigrinus

(S, SE Brasil)

L. tigrinus

(C, NE Brazil)

Haplotype network (intron 2, PLP1 gene, X chromosome)

Trigo et al. (in prep.)

Page 16: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

L. wiedii

L. colocolo

L. tigrinus

(C, NE Brazil)

L. geoffroyi

L. tigrinus

(S, SE Brasil)

Haplotype network (intron 2, ZFY and SMCY3 genes, Y chromosome)

Trigo et al. (in prep.)

Page 17: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Eizirik (in press)

Page 18: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Phylogeographic Patterns and Evolutionary History of the

Neotropical otter (Lontra longicaudis)

Cristine Silveira Trinca

Molecular markers

mtDNA sequences

- Control region

- ND5

-ATP8

10 microsatellite loci

Page 19: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

mtDNA haplotype network

Signal for a recent demographic expansion in eastern SA

Tajima’s D: -2.31891; p = 0.000

Fu’s F = -7.96204; p = 0.001

Eastern SA

French Guiana

Brazilian Amazon

Peru

Bolivia

Colombia

Page 20: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence
Page 21: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Comparative phylogeography and demographic history of two South American procyonids:

Nasua nasua and Procyon cancrivorus

Mirian T. N. Tsuchiya-Jerep

Page 22: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

LBGM samples

Skin samples (MZUSP)

N. nasua

UCLA samples

(Dr. Klaus Peter-Koepfli)

Page 23: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

LBGM Samples

Skin samples (MZUSP)

P. cancrivorus

Page 24: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

-2500

-2400

-2300

-2200

-2100

-2000

-1900

-1800

0 2 4 6 8 10

Number of clusters (K )

Ln

P(X

|D)

-1500

-1450

-1400

-1350

-1300

-1250

-1200

0 2 4 6 8 10

Number of clusters (K )

Ln

P(X

|D)

Nasua nasua Procyon cancrivorus

Page 25: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Eizirik (in press)

Page 26: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Tchaicka et al. (2007). Mol. Ecol.

Cerdocyon thous

Page 27: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Tchaicka et al. (2007). Mol. Ecol.

Cerdocyon thous

Page 28: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Eizirik (no prelo)

Genus Lycalopex

Page 29: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Genus Lycalopex

L. culpaeus

L. griseus L. gymnocercus

L. sechurae

L. vetulus

L. fulvipes

Tchaicka et al. (in prep)

Page 30: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

bCth184

bCth228

bPcu001

bPcu002

DC18

bPcu003

bPcu004

Df20

Df27

bPgr001

bPgr002

Dgr18

Dgr19

bPgy50

bPgy64

bPgy72

bPgy66

bPgy77

bPve328

bPve353

bPgy83

bPse001

bPse002

bPse003

bPse004

bPve10

Pve307

Pve310

bPve322

bPve14

bPve15

bPve16

0.005 substitutions/site

ML phylogeny for 3

concatenated mtDNA

segments (2.5 kb)

99

96

75

58

100

57

95

10096

100

L. vetulus

L. gymnocercus

L. griseus

L. fulvipes

L. sechurae

L. culpaeus

Genus Lycalopex

M. Favarini et al. (in prep)

Page 31: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

bCth184

bCth228

bPcu001

bPcu002

DC18

bPcu003

bPcu004

bPgr001

bPgr002

Dgr18

Dgr19

bPgy50

bPgy64

bPgy72

bPgy66

bPgy77

bPve328

bPve353

bPgy83

Df20

Df27

bPse001

bPse002

bPse003

bPse004

bPve10

Pve307

Pve310

bPve322

bPve14

bPve15

bPve16

5 changes

100

bCth184

bCth228

bPcu001

bPcu002

DC18

bPcu003

bPcu004

Df20

Df27

bPgr001

bPgr002

Dgr18

Dgr19

bPgy50

bPgy64

bPgy72

bPgy66

bPgy77

bPve328

bPve353

bPgy83

bPse001

bPse002

bPse003

bPse004

bPve10

Pve307

Pve310

bPve322

bPve14

bPve15

bPve16

0.005 substitutions/site

L. vetulus and L. gymnocercus in Brazil

Page 32: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

Steve O’Brien

Warren Johnson

Robert Wayne

Klaus Koepfli

Kris Helgen

Juliana Vianna

Mauro Lucherini

Fabiana Rocha

Gitana Cavalcanti

Fabio Mazim

Cladinara R. Sarturi

AcknowledgementsTatiane C. Trigo

Taiana Haag

Cristine S. Trinca

Renata Bornholdt

Alexsandra Schneider

Manoel F. Rodrigues

Ezequiel Fabiano

Eunice M. Matte

Carlos Benhur Kasper

Marina O. Favarini

Anelisie S. Santos

Taiz L. Simão

Carla B. Pires

Gabriel M. Souza

Livia Lehugeur

Vanessa G. Dias

Letícia K. Freitas

Eduarda C. Freitas

Support: CNPq, CAPES, FAPERGS, NIH, NSF, FNMA,

CESP, WCS, WWF, CVRD, PETROBRAS, PUCRS

Thales R. Freitas

Francisco M. Salzano

Sandro L. Bonatto

Ligia Tchaicka

Larissa Oliveira

Flávio H. Rodrigues

Juliana Vianna

Laury Cullen

Tadeu Oliveira

Cibele Indrusiak

Ronaldo G. Morato

Page 33: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

The Great American Biotic

Interchange and the

diversification of Neotropical

carnivores

Meta-analysis of molecular phylogenies

and divergence dates derived from

nuclear gene supermatrices.

Contrasting patterns of diversification

among carnivoran families.

Eizirik (in press)

Page 34: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

GHR

Lycalopex culpaeus

Lycalopex vetulus

Lycalopex fulvipes

Lycalopex griseus

Lycalopex gymnocercus

Lycalopex sechurae

Canis latrans

Cerdocyon thous

Chrysocyon brachyurus

TCP1

ATP7A E3

FES

CYP1A1

Page 35: Comparative phylogeography of Neotropical …The Great American Biotic Interchange and the diversification of Neotropical carnivores Meta-analysis of molecular phylogenies and divergence

DGKG

Leopardus pardalis

Leopardus wiedii

Leopardus colocolo

Leopardus geoffroyi

Leopardus tigrinusPLP1I2

CHRNA1

SILV