Do plants evolve differently?

1. Do plants evolve differently? Thorsten Reusch IFM-GEOMAR Kiel Eelgrass megaclone, Aland Islands. Fotograph: Chris Boström,

2. Genetic variation as fuel for evolution • selection • recombination • drift • ultimate input: mutation • usual estimates of mutation rates • 10-7 -10-9 per nucelotideper generation

3. 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

4. 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

5. 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

6. 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

7. 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

8. 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)

9. moreover plants are modular Genetic individual or genet (=clone) Module or ramet Many plants (+ animals) are facultative clonal asexuals to a degree

10. somatic mutation may affect one module mutation tree clone ...and thus defective mutants (e.g. chlorophyll-) may be nourished by neighboring twigs/modules

11. Consequences of plant modular growth chlorophyll-defective somatic mutants in mangrove Klekowski & Godfrey Nature 1989 => plants may carry a ‘somatic’ genetic load

12. Evidence for other somatically derived variation? Agricultural and horticultural varieties pink Fosters grapefruit normal

13. Genetic mosaics also possible Rio red ‘chimera’ Texas, 1990

14. 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

15. spatial arrangement of meristematic tissues... ...determines type of mosaic Variegated Pelargonium

16. Genetic detection of mosaics with microsatellites ...because mutation rates much higher (10-3 - 10-4) allele (TC)11 allele (TC)10 DNA-Sequence

17. Genetic mosaics in grapevine .... ...allow for the separation of different Cabernet Sauvignon cultivars Moncada et al Genome 2006

18. Mosaic genotypes as mixtures of bi-allelic genotypes 125:131:133 125:133 125:131 step-wise Mutation

19. 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

20. marine angiosperm Zostera marina female flowers pollen vegetative propoagation seeds in inflorescens sexual reproduction

21. 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

22. Using clonal richness as a surrogate for sexual / vegetative reproduction High clonal richness Low clonal richness

23. 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

24. Detection of clones using 7 less polymorphic loci genotypeA B C C C D

25. ‘normal’ bi-allelic genotypes can be recovered seagrass leaf basal meristematic tissue step-wise Mutation

26. 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

27. 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

28. 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

29. The less sex the fewer mutation-free genotypes Sex No sex Reusch & Boström, Evol Ecol in press

30. 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)

31. Mutation without meiosis and dispersal stages ...is expected to lead to high between-population differentiation complete population separation random walk allele length

32. 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)

33. 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

34. Trees are just three-dimensional clones www.inkart.con

35. 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

36. Do plants evolve differently? - Yes ....but many clonal animals (19 phyla) do so as well

37. 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

39. 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