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Phylogeographic history of the wild ancestor of the domesticated common bean (Phaseolus vulgaris L.) Maria Chacon February 14 2003

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Phylogeographic history of the wild ancestor of the domesticated common bean ( Phaseolus vulgaris L.). Maria Chacon. February 14 2003. Plant domestication. - PowerPoint PPT Presentation

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Page 1: Maria Chacon

Phylogeographic history of the wild ancestor of the domesticated common

bean (Phaseolus vulgaris L.)

Maria Chacon

February 14 2003

Page 2: Maria Chacon

Plant domestication

. Evolutionary history of wild relatives of our crops

. Domestication history of the crop: single event? Multiple events? A single or multiple geographic regions?

. Impact of domestication on genetic diversity

. Analysis of the genetic basis of the domestication syndrome

Our crops were selected under a human-driven process called domestication. Plant domestication is an evolutionary process by which conscious (and unconscious) human selection on certain useful characters result in changes in the population’s genotypic frequencies that make plants more useful to humans, better adapted to human environments and sometimes fully dependent on man for dispersion

Page 3: Maria Chacon

Hunting and gathering Agriculture

Highlands

10,000 years ago

Page 4: Maria Chacon

Mesoamerican crops South American crops

Cucurbita argyrosperma Cucurbita ficifoliaCucurbita maximaCucurbita moschataCucurbita pepo

Phaseolus vulgaris small-seeded Phaseolus vulgaris, big-seeded Phaseolus lunatus. Lima type

Capsicum frutescens Capsicum baccatumCapsicum annuum Capsicum pubescens

Squashes

Chilli peppers

Beans

Page 5: Maria Chacon

Isthmus of Tehuantepec

Nicaraguan Depression

Darien Gap

Geographic distribution of wild common bean

Page 6: Maria Chacon

Nama dichotomum Phacelia crenulata Phacelia magellanica

Disjunct distributions of plant taxa in the AmericasFamily (Hydrophyllaceae)

Page 7: Maria Chacon

The rise of the Isthmus of Panama: The Great American Biotic Interchange

Moving into South America were 1) fox; 2) deer; 3) tapir; 4) spectacled bear; 5) spotted cat; and 6) llama. Flying north were 7) parrot; and 8) toucan. Following on foot were 9) armadillo; 10) giant sloth; 11) toxodont; 12) howler monkey; 13) paca; 14) giant predatory bird; 15) anteater; and 16) capybara.

Page 8: Maria Chacon

Historical causes of disjunct biogeographic distributions

Disjunct distributions are of interest because they demand an historical explanation: Dispersal and Vicariance

1. Dispersal: Species was present in only one area and was able to cross intervening barrier regions and colonize other areas. For example: climatic changes in the Pleistocene glaciations may have created “corridors” (with suitable climates) through which species could disperse to other areas.

2. Vicariance: changes in the position of continents, known as continental drift, or mountain building may have divided an originally continuous distribution.

3. In the case of wild relatives of domesticated plants, humans may have played a role in their distribution

Page 9: Maria Chacon

Wild common bean may have a relatively recent history

Population structure of the species may have been determined by recent historical events:

1. The species seems to have originated recently according to molecular clock calculations (Gepts and co-workers) that suggest an origin of the species at about 2 million years ago

2. The geological history of many of the units that wild beans occupy is a recent one, for example, many of them presented uplift and/or vulcanism in the Pleistocene (at about 2 million years ago).

3. The last glaciation in the Pleistocene (called the ice ages) caused global climatic change and ended about 10,000 years ago.

Page 10: Maria Chacon

Sierra Madre Occidental

Trans-Mexican Volcanic Belt

Sierra Madre del Sur

Chiapas-Guatemala -Honduras Highlands

Talamancan Cordillera

Eastern Cordillera of Colombia

Central Andes of Colombia and Eastern Andes of Ecuador

Cordillera Oriental of the Andes

Geological units of Latin America where wild common bean is distributed

Page 11: Maria Chacon

No fossil record of wild beans to indicate when or where P. vulgaris originated and directionality of expansion from Mesoamerica to South America or vice-versa

Phylogeography reconstructs phylogenetic lineages from molecular data and provides a framework to test the processes that most likely have led to the present-day distribution of those lineages: range fragmentation, range expansion and long distance colonization

Phylogeography

Phylogeographic methods are based on associations on the geographic extent of alleles and their genealogical relationships

Page 12: Maria Chacon

With DNA sequence variation or restriction site data we can build the evolutionary relationships among the different variants, alleles or haplotypes that occur within a species in the form of a gene tree or haplotype tree

If the tree may be rooted one could indicate the direction or the temporal polarity of the mutation or changes

Haplotype networks are a suitable way of representing the evolutionary relationships among alleles or haplotypes at the intraspecific level

Phylogeography (cont.)

Page 13: Maria Chacon

Most of the phylogeographic studies have focused on animals where sequences or RFLP data of the rapidly evolving mitochondrial genome are used to build phylogenies

Phylogeographic studies in plants have been limited by the lack of an appropriate source of variation. The few examples in the literature have used chloroplast DNA but this molecule have not proved useful for all the taxa

Phylogeography (cont.)

Page 14: Maria Chacon

Objectives

In this research, a genealogical approach was used to:

1. Understand the evolutionary history of the wild relative of an important crop: the common bean

2. Investigate the cause (s) of its current disjunct distribution

Page 15: Maria Chacon

The common bean as a model

1. The common bean offers an opportunity to study the processes that shape the natural distribution of lineages in plants: it presents an interesting disjunct and intercontinental distribution

2. This is a species that was domesticated several times in different places along its range and so the role that humans played in its dispersal can also be investigated

Page 16: Maria Chacon

Phylogeographic study

I. Survey of chloroplast DNA polymorphisms

II. Haplotype network: Built by using the method of Templeton, Crandall and Sing

III. Nested cladistic analysis: Using the method developed by Templeton and co-workers

IV. Proposed demographic processes in wild common bean

Page 17: Maria Chacon

1. Five individual plants of a representative sample of 158 accessions of wild common bean and 160 accessions of domesticated common bean from the Phaseolus germplasm collection held at CIAT were analysed

2. A survey of chloroplast DNA polymorphisms was conducted on 16 accessions and 10 non-coding chloroplast regions by sequencing. Seven regions showed polymorphisms

I. Survey of chloroplast DNA polymorphisms

Phylogeographic study

Page 18: Maria Chacon

Large single copy (LSC) Large single copy (LSC) (from left to right):(from left to right):rpl16 intron, accD-psaI spacertrnL-trnF spacer, trnL introntrnT-trnL spacer, rps14-psaB spacer

IR

SSC

LSC

IR

Small single copy (SSC):Small single copy (SSC):ndhA intron

Approximate positions of the seven polymorphic chloroplast DNA regions based on the map of the chloroplast genome of Nicotiana tabacum.

Page 19: Maria Chacon

5. Accessions differing by one or more changes were assigned to different chloroplast haplotypes (16 in total)

5’- TCGATTGACTGCAT -TCAGTCTCC- 3’

5’- TCGA TTAACTGCATTTCAGTTTCC -3’

TaqI MseI BsmI

3. Changes detected in the survey were of three sorts: point mutations conferring gain or loss of a restriction site (16), point mutations not detectable by any restriction enzyme (16) and indels (2)

4. A combination of sequencing and PCR-RFLP was used to genotype the

whole sample

Page 20: Maria Chacon

II. Haplotype network

1− 2i

i + rθi =1

n−1

∏ ⎧ ⎨ ⎩

⎫ ⎬ ⎭

i + rθi =1

n−1

∑ ⎧ ⎨ ⎩

⎫ ⎬ ⎭

i + rθ−

i

i + rθi =1

n−1

∏ ⎫ ⎬ ⎭i =1

n−1

∑ ⎧ ⎨ ⎩

H = r= length of the recognition sequence (r= 1 for sequence data)= 4N, N=effective population size, =mutation raten=number of haplotypes

a. An absolute distance matrix is calculated

b. The minimum number of mutational connections between haplotypes is calculated. H parameter from Hudson (1989) is calculated for a pair of randomly chosen haplotypes

c. Haplotypes are connected via justified minimum connections in one or more networks

Construction of a haplotype network: the method of Templeton, Crandall and Sing (1993) was used:

A B CA 0 2 1B 0 3C 0

Page 21: Maria Chacon

C

K

E

F

HG

J

L M

IAB

O

D

P

N

P. costaricensis

P. polyanthus

7 mutational steps

13 mutational steps

9 mutational steps

Tip haplotypes or younger

Interior haplotypes or older

Page 22: Maria Chacon

Tests of geographical associations of haplotypes were conducted following the procedures developed by Templeton and co- workers.

III. Nested cladistic analysis

next

1. The haplotypes in the network were grouped in a series of nested clades (design)

2. Dc, the clade distance, and Dn, the nested clade distance, were calculated for each clade (example)

3. The distributions of these two distances under the null hypothesis of no geographical associations within clades were determined by recalculating both distances after each of 1,000 random permutations of clades against sampling locations.

4. These randomization procedures allows to test for significantly large and small distances (both Dc and Dn) with respect to the null hypothesis

Page 23: Maria Chacon

O

K

J

L M

I

E

F

HG

C

AB

P

D

1-1

1-2

1-3

1-4

1-5

1-6

1-7

1-8 1-9

1-13

1-15

1-14

2-1

2-2

2-3

2-4

2-5

2-6

3-1

3-2

3-3

N

2-7

1-16

1-11

1-10

1-12

Close

The nesting arrangement resulted in a total of 26 hierarchically arranged clades, with higher level nesting correlating with more distant evolutionary time

Page 24: Maria Chacon

AA

AA

A

A

A

A great circle distance is the length of the SHORTEST arc on the surface of the Earth connecting two locations.

A

B

B

B

B

B

B

B

B

A

a1

a2

a3

a4

a5

a8

a7

a6

a9

Bb1

b2

b3

b4

b5

b8

b7

b6

b9

1-1

A9

A5A6A4 A7 A3

A2

A1

A1

B9

B1

B2

B3

B4

B5

B6

B7

B8

DcA=

ainAi=1

nA∑

bi

nBi=1

nB

∑DcB=

Ai

nAi =1

nA

∑DnA=

Bi

nBi =1

nB

∑DnB=

Great circle distances of hapotypes and clades

Close

Page 25: Maria Chacon

Under coalescent theory, different demographic models have different expectations regarding the relationship between the genealogical and

geographical distances between haplotypes

Contemporary factors

Restricted gene flow with isolation by distance . Significantly small Dcs for tip clades and large Dcs for interior clades.

Historical population events

Past population fragmentation. Small Dcs for both tip and interior clades. Significant restriction of Dcs at high level clades

Range expansions. Large Dcs and Dns for tip clades. Small Dcs for some interior clades.

Long distance colonization. Small Dcs for some tip clades.

Patterns of Dc and Dn distances for tip and interior clades are characteristic of different demographic models:

Dc(I)−Dc(T) significantly large

Dc(I)−Dc(T) significantly small

Dn(I)−Dn(T) significantly small

Page 26: Maria Chacon

1-2

1-3

1-4

1-5

1-6

1-7

1-8 1-9

1-10

1-11

1-121-13

1-15

1-14

2-1

2-2

2-3

2-4

2-5

2-6

3-1

3-2

3-3

2-7

1-16

Mutational step

Inferred haplotype

1-1

P

C

D N

O

F

E

G H

J

L M

I K

1-step clades

2-step clades

3-step clades

Observed haplotype

B A

Geographic distribution of haplotypes and evolutionary relationships

Page 27: Maria Chacon

Clade Final inference1-3 Restricted gene flow/dispersal but with some long distance dispersal1-13 Restricted gene flow with isolation by distance2-1 Restricted gene flow/dispersal but with some long distance dispersal2-3 Fragmentation or isolation by distance*2-4 Contiguous range expansion2-5 Contiguous range expansion2-7 Restricted gene flow with isolation by distance3-2 Contiguous range expansion or long distance colonisation*3-3 Contiguous range expansionTotalcladogram

Restricted gene flow with isolation by distance

IV. Proposed demographic processes in wild common bean

Page 28: Maria Chacon

Disjunct distribution of haplotype A: a biogeographical problem that deserves further study

1-2

1-3

2-1

1-1

P

C

D

B A

Dispersion by humans? Convergent evolution? Short-distance dispersal followed by extinction in the intermediate area? Direction of dispersal, north to south or south to north?

Haplotypes in domesticated beans

CIK

L

Haplotypes in wild beans

Page 29: Maria Chacon

Range expansion across current natural barriers: the Isthmus of Tehuantepec in Mesoamerica and the Nicaraguan depression and Darien Gap in Central America

1-10

1-11

1-12 1-13

2-4

2-5

3-3

J

L M

I K

Tehuantepec

Nicaraguan DepresionDarien Gap

Page 30: Maria Chacon

Dispersion from northern Andes to Central America: Contiguous range expansion or long distance colonization?

1-4

1-5

1-6

1-7

2-2

2-3

3-2

F

E

G H

Fragmentation or isolation by distance of clade 2-3?Lack of sampling or extinctions in Central America?

Page 31: Maria Chacon

Lack of sampling or extinctions in Central America?

0.62-0.750.75-0.87> 0.87

Probability scale

Nicaragua

Costa Rica

Panama

Honduras

Climates suitable for wild beans in Central America. The probability scale reflects increasing likelihood of wild beans occurring in these areas. Open circles indicate accessions included in this study. Filled circles indicate accessions not included in this study.

Page 32: Maria Chacon

Conclusions

. At least three dispersion events may have been taken place:One from Mesoamerica to northern South America (clade 3-3),another one from northern South America to Central America (clade 3-2) and a third one between Mesoamerica and South America of uncertain direction (haplotype A)

. Much of the early history of the species is missing as suggested by deep positions of missing intermediate haplotypes within the network. Lack of sampling and extinctions may explain the absence of these haplotypes in the sample

Page 33: Maria Chacon

Acknowledgments

Dr Barbara Pickersgill, School of Plant Sciences, University of Reading, England

Dr Daniel Debouck, Genetic Resources Unit, CIAT, Colombia

COLCIENCIAS, Colombia for funding this research