Do plants evolve differently?

Eelgrass megaclone, Aland Islands. Fotograph: Chris Boström,

Thorsten ReuschIFM-GEOMAR Kiel

Genetic variation as fuel for evolution

•selection•recombination•drift

•ultimate input: mutation

•usual estimates of mutation rates10-7 -10-9 per nucelotideper generation

Common views about mutation

•somatic mutation-evolutionary dead end-often deleterious, e.g. may cause cancer-will not be passed into next generation-no change of allele frequencies•meiotic (~germline) mutations-evolutionary change

animal centered view originating from

overinterpretation of Weismann’s germline

concept

Weismann’s germline concept 1892

Das Keimplasma: eine Theorie der Vererbung. The germ plasm: a theory of heredity 1892

August Weismann1834-1914

•soma cell lines are separate from germline from the onset of ontogeny•only germline cells keep totipotency

zygote embyo

The Weismann ‘barrier’

•during modern synthesis provided ‘final blow’ against Lamarckism and pangenesis ideas of Darwin

John Maynard Smith: The theory of evolution 1993

soma

germline

protein

genetic information

Darwin’s pangenesis theory

...was actually pretty close to Lamarckian ideas

•Pangenesis view introduces gemmules that are derived from all body cells and are the carrier of hereditary changes•gemmules collectively migrate to reproductive organs•information from gemmules is somehow tranferred to germ cells

the Weismann barrier

•central to Modern Evolutionary Synthesis!

“Weismann is the second most notable evolutionary theorist of the nineteenth century, after Charles

Darwin”.

Ernst Mayr

Weismann was instrumentalized to save Darwin from Lamarckism

But: the Weismann barrier is not general

... and this is why botanists never really liked it

plant meristematic tissue can re-differentiate into reproductive organs (flowers)

Botany online Univ Hamburg

flower bud

apical meristem producing leaves

Genetic individual or genet (=clone)

Module or ramet

moreover plants are modular

Many plants (+ animals) are facultative clonal asexuals to a degree

mutation

somatic mutation may affect one module

clone tree

...and thus defective mutants (e.g. chlorophyll-)may be nourished by neighboring twigs/modules

Consequences of plant modular growth

chlorophyll-defective somatic mutants in mangrove

Klekowski & Godfrey Nature 1989

=> plants may carry a ‘somatic’ genetic load

Evidence for other somatically derived variation?

Agricultural and horticultural varieties

normal

pink Fosters grapefruit

Genetic mosaics also possible

Rio red ‘chimera’ Texas, 1990

Meristem composed of (two) different genotypes

somatic mutation leads to genetic mosaic

meristemtic tissueof vascular plants is stratified,i.e. consisting of independently dividing sublineages

spatial arrangement of meristematic tissues...

Variegated Pelargonium

...determines type of mosaic

Genetic detection of mosaics with microsatellitesD

NA

-Seq

uen

ce

allele (TC)11

allele (TC)10

...because mutation rates much higher (10-3 - 10-4)

Genetic mosaics in grapevine ....

Moncada et al Genome 2006

...allow for the separation of different Cabernet Sauvignon cultivars

Mosaic genotypes as mixtures of bi-allelic genotypes

step-wiseMutation

125:131:133

125:133

125:131

Are there any genetic mosaics in the wild?

hypotheses

•the larger + older the plant, the more important become somatic mutations and genetic mosaics(and cultivars propgated by grafting are very old clones)

•because sexual reproduction restores genetic uniformity by introducing a single-cell phase (zygote), sexual reproduction should be negatively correlated with mosaics

vegetative propoagation

sexual reproduction

marine angiosperm Zostera marina

seeds ininflorescens

pollenfemale flowers

Z. marina may from very large + old clones

in Archipelago and Aland Sea (Baltic) clones are 160 m + in extension and possibly >1000 yr old

Reusch et al 1999

Using clonal richness as a surrogate for sexual /vegetative reproduction

Low clonal richness

High clonal richness

Detection of mosaics using 2 hypervariable microsats

site Kolaviken, Archipelago Sea, Finnland

mosaic genotype

normal bi-allelic genotype

normal bi-allelic genotype

mosaic genotype

normal bi-allelic genotype

normal bi-allelic genotype

locu

s G

A17H

locu

s 35

Detection of clones using 7 less polymorphic loci

genotypeA

B

C

D

C

C

‘normal’ bi-allelic genotypes can be recovered

step-wiseMutation

sea

gra

ss le

af

basal meristematic tissue

The data set: 36 European populations

ArchipelagoSea

12

Aland-Islands

5

South Portugal

4

NorthSea 8

SW Baltic 5

Nramets = 20-60

Sampling together with Chris Boström, Jeanine Olsen, Ester Serrao

The less sex, the more mutations

Sex No sex

Clonal Richness

Min

imal

Mut

atio

ns p

er c

lone

1 .8 .6 .4 .2 0

0

1

2

3

4 Exponential function, R2 = 0.64; P < 0.001

Reusch & Boström, Evol Ecol in press

Mean Clonal Richness

Min

imal

Mut

atio

ns p

er c

lone

1 .8 .6 .4 .2 0

0

0.5

1

1.5

Exponential function,R2 = 0.97; P = 0.007

SW Baltic5

Archipleago, 12

Aland5

North Sea8 Portu

4

Correlation also present on the basis of subregions

Sex No sex

Reusch & Boström, Evol Ecol in press

The less sex the fewer mutation-free genotypes

Sex No sex

Reusch & Boström, Evol Ecol in press

So what..

microsatellite loci are selectively neutral(tested for Zos mar Oetjen & Reusch Mol Ecol 2007)

nevertheless, microsatellite polymorphism may indicate potential of processes at level of selected genes

depending on the age of plants or plant clones, input by somatic mutations may be much larger than input by meiotic mutations (e.g. modelling by Orive J theor Biol 2001)

Mutation without meiosis and dispersal stages

...is expected to lead to high between-population differentiation

complete population separation

random walk allele length

0

0.1

0.2

0.3

0.4

0.1 1 10 100

0

0.1

0.2

0.3

0.4

1 10 100

0

0.1

0.2

0.3

0.4

1 10 100 1000

0

0.1

0.2

0.3

0.4

1 10 100

gene

tic

dist

ance

(th

eta)

geographic distance between pop pairs (log-scale)

SW Baltic

FinlandS Portugal

Wadden Sea

0

1

0

1

clon

al r

ichn

ess

Isolation-by-distance in 4 European coastal regions

ns

p<0.01p<0.01

ns

Adaptive implications

adaptive genetic variation may also arise by somatic mutations, and reside as mosaics within genets or plant modules (cf cultivars)

how come that oldest clones of Zostera marina can survive under drastical environmental change in past 4000 yrs in northern Baltic?

testable hypothesis: mutation + selection may have happened within clones

Trees are just three-dimensional clones

www.inkart.con

Genetic mosaic hypothesis

Why are large, long-lived trees not overrun by pests and pathogens?

hypothesis: somatic mutation create mosaics at the level of branches

Witham & Slobotkin 1981; Gill 1988

Do plants evolve differently?- Yes

....but many clonal animals (19 phyla) do so as well

Do plants evolve differently?- Yes

1 because they do not posses a germline

2 because many of them grow to very large size (i.e. have time to accumulate somatic mutations)

3 because plants grow in modular fashion, opening the possibility for within ‘individual’ selection + variation

4 hierarchical levels of selection needs more attention in population genetics

Kollinpää

Lökholm

Sandö

VänöRyssholm

Holma

Högsåra

Husskär, Långören, Sandskär

Kakskerta, Eerikinvallanniemi

Äppelö Rankoskär

Hinderbengtsviken

Sandö

Prästö

HenriksbergPlagen

Turku/Åbo

Fårö

Ängsö

Utö

Empty red circles indicate mutation sites, filled red circles indicate all(?) other sites that have been genotyped through the years...

Åland

FINLAND

The old Danish itinerary in the1250s

Other medieval sailing routes, just marked one of very many