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Do plants evolve differently?. Thorsten Reusch IFM-GEOMAR Kiel. Eelgrass megaclone, Aland Islands. Fotograph: Chris Boström,. Genetic variation as fuel for evolution. selection recombination drift ultimate input: mutation. usual estimates of mutation rates

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Do plants evolve differently?

Thorsten Reusch

IFM-GEOMAR Kiel

Eelgrass megaclone, Aland Islands. Fotograph: Chris Boström,


Genetic variation as fuel for evolution

  • selection

  • recombination

  • drift

  • ultimate input: mutation

  • usual estimates of mutation rates

  • 10-7 -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 Weismann

1834-1914

zygote

embyo

  • soma cell lines are separate from germline from the onset of ontogeny

  • only germline cells keep totipotency


The Weismann ‘barrier’

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

soma

germline

protein

genetic information

John Maynard Smith:

The theory of evolution 1993


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


apical

meristem

producing

leaves

flower bud

Botany online Univ Hamburg

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)


moreover plants are modular

Genetic individual or genet (=clone)

Module or ramet

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


somatic mutation may affect one module

mutation

tree

clone

...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

pink Fosters grapefruit

normal


Genetic mosaics also possible

Rio red ‘chimera’ Texas, 1990


Meristem composed of (two) different genotypes

somatic mutation leads to genetic mosaic

meristemtic tissue

of vascular plants is stratified,

i.e. consisting of independently dividing sublineages


spatial arrangement of meristematic tissues...

...determines type of mosaic

Variegated

Pelargonium


Genetic detection of mosaics with microsatellites

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

allele (TC)11

allele (TC)10

DNA-Sequence


Genetic mosaics in grapevine ....

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

Moncada et al Genome 2006


Mosaic genotypes as mixtures of bi-allelic genotypes

125:131:133

125:133

125:131

step-wise

Mutation


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


marine angiosperm Zostera marina

female flowers

pollen

vegetative propoagation

seeds in

inflorescens

sexual reproduction


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

High clonal richness

Low clonal richness


Detection of mosaics using 2 hypervariable microsats

site Kolaviken, Archipelago Sea, Finnland

mosaic genotype

locus GA17H

normal bi-allelic genotype

normal bi-allelic genotype

mosaic genotype

normal bi-allelic genotype

locus 35

normal bi-allelic genotype



‘normal’ bi-allelic genotypes can be recovered

seagrass leaf

basal meristematic tissue

step-wise

Mutation


The data set: 36 European populations

Nramets = 20-60

Aland-Islands

5

ArchipelagoSea

12

NorthSea

8

SW Baltic

5

South Portugal

4

Sampling together with Chris Boström, Jeanine Olsen, Ester Serrao


The less sex, the more mutations

Exponential function,

R2 = 0.64; P < 0.001

4

3

2

Minimal Mutations per clone

1

0

1

.8

.6

.4

.2

0

Clonal Richness

Sex

No sex

Reusch & Boström, Evol Ecol in press


Correlation also present on the basis of subregions

1.5

Exponential function,

R2 = 0.97; P = 0.007

Aland

5

Archipleago,

12

1

Minimal Mutations per clone

0.5

SW Baltic

5

North Sea

8

Portu

4

0

1

.8

.6

.4

.2

0

Mean Clonal Richness

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


1

1

0

0

Isolation-by-distance in 4 European coastal regions

S Portugal

Finland

p<0.01

p<0.01

genetic distance (theta)

SW Baltic

Wadden Sea

clonal richness

ns

ns

geographic distance between pop pairs (log-scale)


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



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

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

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

  • hierarchical levels of selection needs more attention in population genetics


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

FINLAND

Äppelö

Rankoskär

Turku/Åbo

Sandö

Kakskerta, Eerikinvallanniemi

Kollinpää

Åland

Prästö

Lökholm

Ängsö

Hinderbengtsviken

Sandö

Högsåra

Ryssholm

Vänö

Fårö

Utö

Holma

Plagen

Husskär, Långören, Sandskär

Henriksberg

The old Danish itinerary in the1250s

Other medieval sailing routes, just marked one of very many


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