Do plants evolve differently?
Thorsten Reusch
IFM-GEOMAR Kiel
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
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)
apical
meristem
producing
leaves
flower bud
Botany online Univ Hamburg
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
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
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
DNA-Sequence
allele (TC)10
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
vegetative propoagation
sexual reproduction
seeds in
inflorescens
pollen
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
locus GA17H
site Kolaviken, Archipelago Sea, Finnland
mosaic genotype
normal bi-allelic genotype
normal bi-allelic genotype
locus 35
mosaic genotype
normal bi-allelic genotype
normal bi-allelic genotype
Detection of clones using 7 less polymorphic loci
genotypeA
B
C
C
C
D
seagrass leaf
‘normal’ bi-allelic genotypes can be recovered
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,
Minimal Mutations per clone
4
R2 = 0.64; P < 0.001
3
2
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
Minimal Mutations per clone
Exponential function,
R2 = 0.97; P = 0.007
1
Archipleago,
12
Aland
5
0.5
North Sea
8
0
1
.8
SW Baltic
5
Portu
4
.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
Isolation-by-distance in 4 European coastal regions
0.4
S Portugal
0.3
0.3
0.2
0.2
0.1
p<0.01
0
0.1
1
10
1
Finland
0
0.1
p<0.01
0
100
1
10
100
1000
0.4
0.4
1
SW Baltic
0.3
0.3
0.2
0.2
ns
0.1
Wadden Sea
0
ns
0.1
0
0
1
10
100
1
10
geographic distance between pop pairs (log-scale)
100
clonal richness
genetic distance (theta)
0.4
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
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
Vänö
Fårö
Ryssholm
Utö
Holma
Plagen
Husskär, Långören, Sandskär
The old Danish itinerary in the1250s
Other medieval sailing routes, just marked one of very many
Henriksberg