Luciano Beheregaray

Molecular Ecology Lab

School of Biological Sciences

A review of Phylogeography

and the integration between

biologists and Earth scientists

Outline

• Earth sciences and Phylogeography

• Perspectives

• A review of twenty years of Phylogeography

• The phylogeographer as a powerful naturalist

• Case Studies:- young radiation & ecological speciation in Brazil- history and conservation rescue in the Galápagos- comparative biogeography in Wallacea

www.bio.mq.edu.au/molecularecology (soon to be moved to Flinders)

Molecular Ecology Group for Marine Research

Our focus:

Understanding genetic and ecologic

connectivity in the sea

The Phylogeographer:

A Powerful Naturalist

• A nature admirer’s, an explorer

• A population biologist

• Integrative in essence:

- from genes to geosciences- from generations to millennia

Phylogeography, the Study of Population History

Phylogeography is concerned about patterns and processesat the tips of the Tree of Life (TOL)

Let’s zoom in the TOL

modified from Sunnucks (2000) TREE

Three ‘time slices’ in genetics

Dark = most informative

Genotypic

Allelic

Time (generations)Data type:

Phylogenetic

Work in progress… a review on:

2 - Identify achievements, trends and challenges for the field

Articles and citations in phylogeography*

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1987 1988 1989 1990 1991 1992 1993 1994 1995 1996 1997 1998 1999 2000 2001 2002 2003 2004 2005 2006 2007 2008 2009 2010

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Publication year

Articles

Citations

* 2010 (projections as in Nov 1st)

Distribution of articles in phylogeography by taxonomic group

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Mammals Fishes Plants

(terrestrial)

Invertebrates

(terrestrial)

Herps Invertebrates

(aquatic)

Birds Microorganisms Plants

(aquatic)

Fungi

% o

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Genetic markers in phylogeography: temporal trends

• mtDNA still reigns supreme (81% of all studies or 75% alone) • recently augmented by ever growing DNA barcode data…

• recent escalation of multilocus surveys (e.g. introns and microsatellites) improves inferences about population history:

- estimates of divergence time and Ne- accommodate for coalescence stochasticity

Some food for thought on genetic markers

• multilocus surveys can synergistically combine the power of POPULATION GENETICS with phylogeography:

- identify population units, hybridization and migrants (& their rates)- brings ecology (niche) and behaviour into phylogeography

• problems with multilocus (nuclear) markers:

- technical development can be difficult- coalescence tends to be less ‘convenient’ (much longer time)- rates of evolution more variable and unpredictable- population screening can be difficult and expensive (diploidy and

recombination)

Some food for thought on genetic markers

• Genomics provides solutions to many such problems and brings ‘new’ markers into play (exon capture, functional SNPs, etc)

Pattern? mtDNA (in animals)!

Processes? multilocus endeavour!

0.77

0.15

0.0240.06

Northern Hemisphere

Southern Hemisphere

Northern & Southern

Global

0.65

0.18

0.17 Terrestrial

Freshwater

Marine

The global geography of Phylogeography

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15

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35

Europe North

America

Asia Africa Australia South

America

Antarctica

Continent

% o

f art

icle

sThe global geography of Phylogeography

Mittermeier, Myers & Mittermeier

University of Chicago Press (2000)

Country Ranking based on endemism and

species diversity

Ranking based on papers in

phylogeography

Brazil 1 15

Indonesia 2 40

Colombia 3 65

Australia 4 5

Mexico 5 27

Madagascar 6 54

Conservation Biology is about prioritizing resources

RARITY RESTRICTED DISTRIBUTION CHARISMA

ECONOMICS ECOLOGICAL IMPORTANCE

EVOLUTIONARILY DISTINCT POPULATIONS

(as revealed by phylogeography)

Some food for thought on conservation & phylogeography

Historically isolated populations are not only genetically distinct

but also tend to be locally (ecologically) adapted

Comparative Phylogeography can help a lot here!

Genomics has jumped forwarded and moved into the wild!

Some food for thought on genomics & phylogeography

PROBLEM: Technological and analytical challenges can increase

(even more) the gap between phylogeographers from the

developed and developing world

Ecological Genomics & Phylogeography:

„Functional Phylogeography‟ – an integration to inform on the

origins and evolutionary trajectories of neutral and adaptive

genetic variation at landscape level

Functional (ecological) Genomics & Natural History:

„Mechanistic natural history‟ (Americ. Soc. Naturalists, 2002)

0.68

0.25

0.08

Single taxon

Multiple taxa

Comparative phylogeography

0.69

0.11

0.02

0.18 Quaternary (0 - 2 My)

Tertiary (2 - 66 My)

Quaternary & Tertiary

Undetermined

Nature of the study and timescale in Phylogeography

- Geology: Geomorphology PalaeontologyMineralogy and petrology Volcanology Geochemistry Sedimentology

- Geophysics- Hydrology:

Oceanography Limnology

- Glaciology- Atmospheric sciences:

Meteorology Climatology

Phylogeography is a historical discipline and relies on information from Earth Sciences

Most earth scientists have generally ignored anything different than physical records

Phylogeographers use other data sets (in addition to genetics) but…

…they have often inefficiently, simplistically (and sometimes incorrectly) explored and interpreted data about Earth’s history

Earth Sciences and Phylogeography:

Earth scientistsTaxonomists

Phylogeographers &

population geneticists

An integration to discover, document and understand

historical dimensions of biodiversity

Beheregaray & Caccone (2007) Journal of Biology

CASE STUDY 1:

When the branches of the Tree of Life are not well

formed

Time (generations)

O. argentinensis

• marine and estuarine

• estuarine speciationBeheregaray & Levy (2000) Copeia

A very young radiation?

O. perugiae species group

• freshwater lakes

• morphological divergence

Dyer & Malabarba (2003) Ichthyol. Explor. Freshwaters

75 km

ArgentinaUruguay

Southern Brazil

10 km

Freshwater group

+ +

- -

- -

80,000 ya

16,000 ya

6,000 ya

Beheregaray et al. (2002) Proc. Royal Soc. London B

500 km

Marine-estuarine group

+ +

marine pops

+ +

estuarine pops

+ +

Beheregaray & Sunnucks (2001) Molecular Ecology

• colonization of new habitats

• divergent natural selection

10 km

“ecological speciation with gene flow”

Isolation by adaptation in estuaries

Beheregaray & Sunnucks (2001) Molecular Ecology

mtDNA network – all coastal Odontesthes + riverine perugiae

marine sp

estuarine sp

O. mirinensis

O. sp A

O. piquava

O. ledae

O. perugiae

O. bicudo

Beheregaray (in prep)

Microsatellite tree (Dce genetic distance)

0.01

O. perugiae

O. bicudo PLEISTOCENE

O. sp A HOLOCENE 1

O. mirinensis HOLOCENE 1

O. piquava HOLOCENE 1

O. ledae HOLOCENE 2

O. sp C100

100

100

100

84

71

O. sp B

O. argentinensis

riverine

marine

estuarine

coastal

lakes

?

Beheregaray (in prep)

Processes responsible for adaptive radiation:

Divergent selection- estuarine pre-adaptation- trophic specializations - isolation by adaptation

Drift in small landlocked populations

CASE STUDY 2:

Population history and conservation rescue on

islands

Time (generations)

with Jeff Powell and Gisella Caccone (Yale)

male-biased dispersal

(Rasmann et al. 1997)

hybridization

(Grant & Grant 1996)

Biogeographic prediction:

“colonization and decreasing phylogeographic structure in E-W direction”

multiple colonization (Wright 1983)

DomedSaddleback

Giant Galápagos tortoises – Geochelone lineage

3 species finished off by zoo collectors and scientific expeditions!

Giant Galápagos tortoises – Geochelone lineage

PINZONephippium

SANTIAGO darwini

SAN CRISTOBALchatamensis

Cerro Fatal

La Caseta

PINTA abingdoni

ESPANOLA hoodensis

ISABELA

V. Wolfbecki

V. Darwinmicrophytes

V. Alcedovandenburghi

SANTA CRUZ porteri

V. Cerro Azul vicina

V. Sierra Negraguntheri

~†

†

†

†

Giant Galápagos tortoises – Geochelone lineage, 15 taxa

Caccone et al. (2002) Evolution

Galápagos

Mainland South America

Bayesian tree4750 bp of mtDNA

Galapagos taxa evolved in situ

Caccone et al. (1999) PNAS

Younger islands (<1.2 My) Older Islands (~ 3.0 – 1.5 My)

Archipelago-wide phylogeography of giant tortoises (n = 802)

Younger islands (<1.2 My) Older Islands (~ 3.0 – 1.5 My)

Beheregaray et al. (2004) PNAS

Archipelago-wide phylogeography of giant tortoises (n = 802)

Older Islands

(~ 3.0 – 1.5 Ma)

• 100% lineages: island endemics

• highly divergent

• deep history:

inter-island divergences

of ~ 2 – 0.8 Ma

PINTA

ESPANOLA

SANTA CRUZ (La Caseta and Cerro Fatal)

SAN CRISTOBAL

PINZON

29 steps

~

16 steps48 steps

30 steps

20 steps

Beheregaray et al. (2004) PNAS

Younger Islands

(< 1.2 Ma)

• volcano populations are not

monophyletic

• recent migration events

• shallow history:

expansions / colonizations

of ~ 0.6 – 0.1 Ma

25 steps

ISABELA

V. Darwin

V. Alcedo

V. Cerro Azul

V. Sierra Negra

SANTIAGO

V. Wolf (northern ISABELA)

Clade B

Clade A

Beheregaray et al. (2004) PNAS

• Inferences supported

by microsatellite analysis

Ciofi et al. (2006) Genetics

biogeographic consensus!

Main findings…

established knowledge for further studies on:

- demographic history

- conservation rescue

identification of evolutionary events

chronologically associated with volcano

evolution

V. Wolf beckih = 0.69

V. Darwin microphyesh = 0.50

V. Sierra Negra

guntheri

h = 0.83

V. Cerro Azul

vicina

h = 0.87

Diversity of maternal lineages on Isabela Island

V. Alcedo

vandenburghi

h = 0.17

• largest extant pop in the archipelago (~ 4,000 – 6,000)

• Alcedo was probably never exploited by whalers or pirates

Why reduced genetic variability in

Alcedo tortoises?

Geist et al. (1994) Bulletin of Volcanology

- 3.4 Km3 of rhyolitic tephra

- K-Ar dating: ~ 100 (±20) kya

Alcedo experienced a catastrophic volcano

eruption!

Used larger sample and multilocus data to:

• test for past population contraction

• date the population contraction

A = 7.3 (± 0.5)

A = 9.1 (± 0.6)

P = 0.01

P = 0.68

P = 0.51A = 8.9 (± 0.6)

Massive bottleneck in Alcedo tortoises

P = 0.01

P = 0.68

P = 0.51

Beheregaray et al. (2003) Science

DNA dating: ~ 88 kya (110-70 kya)

K-Ar dating: ~ 100 (±20) kya

Estimating the age of the population bottleneck

61

6161

61

62 63

64 65

• 61 is an „old‟ maternal lineage

Genes have recorded a prehistoric volcano eruption in the Galapagos!

Beheregaray et al. (2003) Science

Phylogeography and Conservation Rescue

A NEW and highly endangered species of giant tortoises

PINTA

ESPANOLA

SANTA CRUZ (La Caseta and Cerro Fatal)

SAN CRISTOBAL

PINZON

29 steps

~

16 steps48 steps

30 steps

20 steps

Beheregaray et al. (2003) Conservation Genetics

Russello et al. (2005) Biology Letters

The Cerro Fatal species (~ 70 left)

Extinct in the wild (IUCN 1996)

The story of a conservation icon:

„Lonesome George‟ (Geochelone abingdoni)

www.firstscience.com/home/blogs/George.html

The story of a conservation icon:

„Lonesome George‟ (Geochelone abingdoni)

The sexual problems of a conservation icon…

„Is he gay, impotent or just bored?‟

New Scientist

„Alien‟ matrilines found on Volcano Wolf

The fortunate phylogeographic twist…

New Scientist

(June 2007)

-7 Pinta museum specimens:

CAS (San Diego)

- 700 bp mtDNA

- 10 microsatellite loci

- all archipelago populations

- + 27 aliens from Wolf

Building an extinct nuclear DNA database…

Russello, Beheregaray et al. (2007) Current Biology

Lonesome George is not alone among Galápagos tortoises!

CASE STUDY 1:

Comparative population history in Wallacea: tying

geology with genetics

Time (generations)

0 500 1000 2000

kilometres

Equator

DISTRIBUTION

MAP

Charaxes

CethosiaDelias

FIELD WORK:

100+ sites,

13 countries

Solomon

Islands

Vanuatu

New

Caldeonia

Papua

New Guinea

Indonesia

Philippines

Malaysia

China

TaiwanMyanmar

Thailand

Vietnam

Laos

Cambodia

Brunei

Australia

020 1090 304060 507080

Millions of years

Oligocene Pli

oc

en

e

PleistoceneMioceneEocenePaleogeneCretaceous

Cethosia

Chronogram based on

Bayesian topology

C. mindanensis1

C. mindanensis2C. hypsea3

C. hypseabatu

C. penthesileapak

C. methypsea

C. hypseafruh

C. hypsea6

C. hypsea7

C. gabinia

C. penthesileatim

C. penthesilealom

C. luzonica4

C. luzonica3C. luzonica6

C. cyane3C. cyanenwC. cyane1

C. tambora3

C. tambora5

C. tambora1C. picta

C. biblis 1

C. lamarckiC. moestaC. nietneri

C. obscura1

C. obscura7C. obscuraantC. obscura3

C. obscura5

C. vasilia1C. vasilia4C. cydippeobian

C. cydippe4C. cydippe2

C. myrinanw

C. cydippecydippeC. cydippeanton

C. myrinamyrinaC. myrinaribbei

Acraea

ActinoteC. lechenaulti

Heliconius1

Vagrans

Argynnis

Heliconius2

WA

LL

AC

EA

WALLACEAN

DIVERSIFICATION

Muller & Beheregaray (2010) MPE

Millions of years

010 535 152030 25

Charaxes

Chronogram based on

Bayesian topology

Oligocene Pliocene PleistoceneMioceneEocene

C. borneensis

C. bernardus

C. repetitus

C. fervens

C. plateni

C. marmax

C. aristogiton

C. bajula

C. psaphon

C. durnfordi

C. bupalus

C. kahrubra

C. sangana

C. antonius

C. amycus

C. latona

C. affinis

C. setan

C. musashi

C. eurialus

C. madensis

C. orilus

C. ocellatus

C. marki

C. mars

C. nitebis

C. elwesi

C. distanti

C. harmodius

C. solon

C. castor

Polyura

Euxanthe

Archaeoprepona

Prothoe

Anaea

CalinagaW

AL

LA

CE

AN

DIV

ER

SIF

ICA

TIO

N

WA

LL

AC

EA

Muller, Wahlberg & Beheregaray (2010) Biol J Linnean

Soc

5 045 101525303540

Millions of years

Oligocene PleistoceneMioceneEocene

20

Pliocene

Delias

Chronogram based on

Bayesian topology

D. elongatusD. clathrataD. roepkeiD. naisD. albertisiD. discusD. meekiD. niepeltiD. iltisD. bakeriD. nigrinaD. eximiaD. leuciasD. harpalyceD. dixeyiD. kummeriD. messalinaD. madetesD. descombesiD. ellipsisD. diaphanaD. caeneusD. periboeaD. mysisD. salviniD. bagoeD. eileenaeD. hypareteD. cunningputiD. chimbuD. heroniD. flavissisimaD. aroaeD. stresemanniD. schassmanniD. geraldinaD. microstichaD. gilliardiD. eichhorniD. abrophoraD. aganippeD. totilaD. ladasD. woodiD. blancaD. ninusD. benasuD. subnubilaD. surprisaD. belladonnaD. enniaD. chrysomelaenaD. apetalaD. laknekeiD. hippodomiaD. baracasaD. agostinaD. narsesD. lemoultiD. yagashitaiD. nysaD. brandtiD. schoenigiD. viduaD. themisD. kuehniCeporaLeuciacriaAporiaPrioneris1Prioneris2Eurema

WALLACEAN

DIVERSIFICATION

WA

LL

AC

EA

Muller & Beheregaray (in review) J Biogeog

CethosiaO

rie

nta

lW

alla

ce

a

vasilia

bernsteini

hypsea

cyane penthesilea

obianabiblis

luzonica picta

myrinaobscura lamarcki

vasilialechenaulti

Orie

nta

lCharaxes

Walla

ce

a

amycus distantiantonius

harmodius latona

marmaxbajula kahrubra aristogiton schaderi

mars eurialus markisetan

ocellatus sulaensis nitebis orilus madensis

Long term isolation of Wallacean taxa was promoted by the progressive fragmentation of a micro-continent

Expanding Wallacea Theory

A Few Perspectives and ChallengesDo we have ‘virtual phylogeographers’ out there or is it just my imagination?

• computationally intensive, model driven researchers• use lots of markers and coalescence theory

• appear more interested in the theory than study system• good natural history experience?

• observation of Nature is the source of our hypotheses• never dump the biology! • without that the parameters that go into models are just guesswork,

and the interpretation may be equally blind• look for better ways to synergistically combine natural history and

computational biology

Statistically rigorous phylogeography is important, but what really matters are the quality of research questions

• Intellectual maturation of Phylogeography?

Recent developments in DNA technology, theory and statistics AND syntheses of comparative information across different regions of the globe

• Create strategies for developing in situ capacity

A Few Perspectives and Challenges

• A lot of the natural history has not been done yet: many more descriptive phylogeographic surveys are needed in the developing world

Acknowledgements

• MELFU PhD students and postdocs (current and alumni)

• Louis Bernatchez (Laval U, Canada)

• Paul Sunnucks (Monash U, Australia)

• Jeff Powell and Gisella Caccone (Yale U, USA)

• Luciana Moller (Flinders U, Australia)

Financial Support