Exploring the fitness consequences of whole-genome multiplication (WGM) is essential for understanding the establishment of autopolyploids in diploid parental populations, but suitable model systems are rare. We examined the impact of WGM on reproductive traits in three major cytotypes (2x, 3x, 4x) of Pilosella rhodopea, a species with recurrent formation of neo-autopolyploids in mixed-ploidy populations. We found that diploids had normal female sporogenesis and gametogenesis, high fertility, and produced predominantly euploid seed progeny. By contrast, autopolyploids had highly disturbed developmental programs that resulted in significantly lower seed set and a high frequency of aneuploid progeny. All cytotypes, but particularly triploids, produced gametes of varying ploidy, including unreduced ones, that participated in frequent intercytotype mating. Noteworthy, the reduced investment in sexual reproduction in autopolyploids was compensated by increased production of axillary rosettes and the novel expression of two clonal traits: adventitious rosettes on roots (root-sprouting), and aposporous initial cells in ovules which, however, do not result in functional apomixis. The combination of increased vegetative clonal growth in autopolyploids and frequent intercytotype mating are key mechanisms involved in the formation and maintenance of the largest diploid-autopolyploid primary contact zone ever recorded in angiosperms.

Department of Biology University of Fribourg Fribourg Switzerland

Herbarium Collections and Department of Botany Charles University Prague Czechia

Leibniz Institute of Plant Genetics and Crop Plant Research Gatersleben Germany

Plant Science and Biodiversity Centre Slovak Academy of Sciences Bratislava Slovakia

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Ren R, Wang H, Guo C, Zhang N, Zeng L, Chen Y, Ma H, Qi J. 2018. Widespread whole genome duplications contribute to genome complexity and species diversity in angiosperms. Molec. Plant 11, 414-428. ( 10.1016/j.molp.2018.01.002) PubMed DOI

Comai L. 2005. The advantages and disadvantages of being polyploid. Nat. Rev. Genet. 6, 836-846. ( 10.1038/nrg1711) PubMed DOI

Parisod C, Holderegger R, Brochmann C. 2010. Evolutionary consequences of autopolyploidy. New Phytol. 186, 5-17. ( 10.1111/j.1469-8137.2009.03142.x) PubMed DOI

Ramsey J. 2011. Polyploidy and ecological adaptation in wild yarrow. Proc. Natl Acad. Sci. USA 108, 7096-7101. ( 10.1073/pnas.1016631108) PubMed DOI PMC

Barker MS, Husband BC, Pires JC. 2016. Spreading winge and flying high: the evolutionary importance of polyploidy after a century of study. Amer. J. Bot. 103, 1139-1145. ( 10.3732/ajb.1600272) PubMed DOI

Van de Peer Y, Mizrachi E, Marchal K. 2017. The evolutionary significance of polyploidy. Nat. Rev. Genet. 18, 411-424. ( 10.1038/nrg.2017.26) PubMed DOI

Ramsey J, Ramsey TS. 2014. Ecological studies of polyploidy in the 100 years following its discovery. Proc. R. Soc. B 369, 20130352. ( 10.1098/rstb.2013.0352) PubMed DOI PMC

Spoelhof JP, Soltis PS, Soltis DE. 2017. Pure polyploidy: closing the gaps in autopolyploid research. J. Syst. Evol. 55, 340-352. ( 10.1111/jse.12253) DOI

Soltis DE, Soltis PS, Schemske DW, Hancock JF, Thompson JN, Husband BC, Judd WS. 2007. Autopolyploidy in angiosperms: have we grossly underestimated the number of species? Taxon 56, 13-30. ( 10.2307/25065732) DOI

Ramsey J, Schemske DW. 1998. Pathways, mechanisms, and rates of polyploid formation in flowering plants. Annu. Rev. Ecol. Evol. Syst. 29, 467-501. ( 10.1146/annurev.ecolsys.29.1.467) DOI

Ramsey J, Schemske DW. 2002. Neopolyploidy in flowering plants. Annu. Rev. Ecol. Evol. Syst. 33, 589-639. ( 10.1146/annurev.ecolsys.33.010802.150437) DOI

Cifuentes M, Grandont L, Moore G, Chèvre AM, Jenczewski E. 2010. Genetic regulation of meiosis in polyploid species: new insights into an old question. New Phytol. 186, 29-36. ( 10.1111/j.1469-8137.2009.03084.x) PubMed DOI

Levin D. 1975. Minority cytotype exclusion in local plant populations. Taxon 24, 35-43. ( 10.2307/1218997) DOI

Husband BC. 2000. Constraints on polyploid evolution: a test of the minority cytotype exclusion principle. Proc. R. Soc. Lond. B 267, 217-223. ( 10.1098/rspb.2000.0990) PubMed DOI PMC

Köhler C, Mittelsten Scheid O, Erilova A. 2010. The impact of the triploid block on the origin and evolution of polyploid plants. Trends Genet. 26, 142-148. ( 10.1016/j.tig.2009.12.006) PubMed DOI

Eliášová A, Trávníček P, Mandák B, Münzbergová Z. 2014. Autotetraploids of PubMed DOI PMC

Van Drunen WE, Friedman J. 2022. Autopolyploid establishment depends on life history strategy and the mating outcomes of clonal architecture. Evolution 76, 1953-1976. ( 10.1111/evo.14582) PubMed DOI

Koltunow M. 1993. Apomixis: embryo sacs and embryos formed without meiosis or fertilization in ovules. Plant Cell 5, 1425-1437. ( 10.1105/tpc.5.10.1425) PubMed DOI PMC

Klimeš L, Klimešová J, Hendriks R, van Groenendael J. 1997. Clonal plant architectures: a comparative analysis of form and function. In The ecology and evolution of clonal plants (eds de Kroon H., van Groenendael J), pp. 1-29. Leiden, The Netherlands: Backhuys Publishers.

Vallejo-Marín M, Dorken ME, Barrett SCH. 2010. The ecological and evolutionary consequences of clonality for plant mating. Annu. Rev. Ecol. Evol. Syst. 41, 193-213. ( 10.1146/annurev.ecolsys.110308.120258) DOI

Chrtek J, Herben T, Rosenbaumová R, Münzbergová Z, Dočkalová Z, Zahradníček J, Krejčíková J, Trávníček P. 2017. Cytotype coexistence in the field cannot be explained by inter-cytotype hybridization alone: linking experiments and computer simulations in the sexual species PubMed DOI PMC

Ortiz JP, et al. 2013. Harnessing apomictic reproduction in grasses: what we have learned from PubMed DOI PMC

Karunarathne P, Hojsgaard D. 2021. Single independent autopolyploidization events from distinct diploid gene pools and residual sexuality support range expansion of locally adapted tetraploid genotypes in a South American grass. Front. Genet. 12, 736088. ( 10.3389/fgene.2021.736088) PubMed DOI PMC

Beck BB, Windham MD, Pryer KM. 2011. Do asexual polyploid lineages lead short evolutionary lives? A case study from the fern genus PubMed DOI

Chrtek J, et al. 2020. Evolutionary history and genetic diversity of apomictic allopolyploids in PubMed DOI

Müntzing A. 1936. The evolutionary significance of autopolyploidy. Hereditas 21, 363-378. ( 10.1111/j.1601-5223.1936.tb03204.x) DOI

Gustafsson A. 1948. Polyploidy, life-form and vegetative reproduction. Hereditas 34, 1-22. ( 10.1111/j.1601-5223.1948.tb02824.x) DOI

Obeso JR. 2002. The costs of reproduction in plants. New Phytol. 155, 321-348. ( 10.1046/j.1469-8137.2002.00477.x) PubMed DOI

Herben T, Suda J, Klimešová J. 2017. Polyploid species rely on vegetative reproduction more than diploids: a re-examination of the old hypothesis. Ann. Bot. 120, 341-349. ( 10.1093/aob/mcx009) PubMed DOI PMC

Van Drunen WE, Husband BC. 2019. Evolutionary associations between polyploidy, clonal reproduction, and perenniality in the angiosperms. New Phytol. 224, 1266-1277. ( 10.1111/nph.15999) PubMed DOI

Eckert CG, Lui K, Bronson K, Corradini P, Bruneau A. 2003. Population genetic consequences of extreme variation in sexual and clonal reproduction in an aquatic plant. Molec. Ecol. 12, 331-344. ( 10.1046/j.1365-294X.2003.01737.x) PubMed DOI

Fialová M, Jandová M, Ohryzek J, Duchoslav M. 2014. Biology of the polyploid geophyte DOI

Baldwin SJ, Husband BC. 2013. The association between polyploidy and clonal reproduction in diploid and tetraploid PubMed DOI

Martínková J, Klimešová J, Doležal J, Kolář F. 2015. Root sprouting in DOI

Weiss-Schneeweiss H, Emadzade K, Jang TS, Schneeweiss GM. 2013. Evolutionary consequences, constraints and potential of polyploidy in plants. Cytogenet. Genome Res. 140, 137-150. ( 10.1159/000351727) PubMed DOI PMC

Van Drunen WE, Husband BC. 2018. Immediate vs. evolutionary consequences of polyploidy on clonal reproduction in an autopolyploid plant. Ann. Bot. 122, 195-205. ( 10.1093/aob/mcy071) PubMed DOI PMC

Husband BC, Ozimec B, Martin SL, Pollock L. 2008. Mating consequences of polyploid evolution in flowering plants: current trends and insights from synthetic polyploids. Int. J. Plant Sci. 169, 195-206. ( 10.1086/523367) DOI

Van Drunen WE, Husband BC. 2018. Whole genome duplication decreases clonal stolon production and genet size in the wild strawberry PubMed DOI

Blakeslee A, Avery A. 1937. Methods of inducing doubling of chromosomes in plants by treatment with colchicine. J. Hered. 28, 393-411. ( 10.1093/oxfordjournals.jhered.a104294) DOI

Münzbergová Z. 2017. Colchicine application significantly affects plant performance in the second generation of synthetic polyploids and its effects vary between populations. Ann. Bot. 120, 329-339. ( 10.1093/aob/mcx070) PubMed DOI PMC

Jaskani MJ, Kwon SW, Kim DH. 2005. Comparative study on vegetative, reproductive and qualitative traits of seven diploid and tetraploid watermelon lines. Euphytica 145, 259-268. ( 10.1007/S10681-005-1644-X) DOI

Cohen H, Fait A, Tel-Zur N. 2013. Morphological, cytological and metabolic consequences of autopolyploidization in PubMed DOI PMC

Bretagnolle F, Thompson JD. 1995. Gametes with the somatic chromosome number: mechanisms of their formation and role in the evolution of autopolyploid plants. New Phytol. 129, 1-22. ( 10.1111/j.1469-8137.1995.tb03005.x) PubMed DOI

Yamauchi A, Hosokawa A, Nagata H, Shimoda M. 2004. Triploid bridge and role of parthenogenesis in the evolution of autopolyploidy. Amer. Nat. 164, 101-112. ( 10.1086/421356) PubMed DOI

Mason AS, Pires JC. 2015. Unreduced gametes: meiotic mishap or evolutionary mechanism? Trends Genet. 31, 5-10. ( 10.1016/j.tig.2014.09.011) PubMed DOI

Šingliarová B, Hodálová I, Mráz P. 2011. Biosystematic study of the diploid-polyploid DOI

Šingliarová B, Zozomová-Lihová J, Mráz P. 2019. Polytopic origin and scale-dependent spatial segregation of cytotypes in primary diploid–autopolyploid contact zones of DOI

Šingliarová B, Mráz P, Chrtek J, Plačková I. 2011. Allozyme variation in diploid, polyploid and ploidy-mixed populations of the DOI

Krahulcová A, Krahulec F, Chapman HM. 2000. Variation in DOI

Šingliarová B, Šuvada R, Mráz P. 2013. Allopatric distribution, ecology and conservation status of the DOI

Otto F. 1990. DAPI staining of fixed cells for high-resolution flow cytometry of nuclear DNA. In Methods in cell biology (eds Crissman H, Darzynkiewicz Z), pp. 105-110. New York, NY: Academic Press. PubMed

Doležel J, Göhde W. 1995. Sex determination in dioecious plants PubMed DOI

Schönswetter P, Suda J, Popp M, Weiss-Schneeweiss H, Brochmann C. 2007. Circumpolar phylogeography of PubMed DOI

Loureiro J, Rodriguez E, Doležel J, Santos C. 2007. Two new nuclear isolation buffers for plant DNA flow cytometry: a test with 37 species. Ann. Bot. 100, 875-888. ( 10.1093/aob/mcm152) PubMed DOI PMC

Mráz P, Šingliarová B, Urfus T, Krahulec F. 2008. Cytogeography of PubMed DOI PMC

Hand ML, Vít P, Krahulcová A, Johnson SD, Oelkers K, Siddons H, Chrtek J, Fehrer J, Koltunow AM. 2015. Evolution of apomixis loci in PubMed DOI PMC

Matzk F, Meister A, Schubert I. 2000. An efficient screen for reproductive pathways using mature seeds of monocots and dicots. Plant J. 21, 97-108. ( 10.1046/j.1365-313x.2000.00647.x) PubMed DOI

R Core Team. 2023. R: A language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing. (http://www.r-project.org).

Pinheiro J, Bates D, DebRoy S, Sarkar D, Core Team R. 2017. Nlme: linear and nonlinear mixed effects models. R package version 3.1-131. Vienna, Austria: R Foundation for Statistical Computing.

Bates D, Maechler M, Bolker B, Walker S. 2015. Fitting linear mixed-effects models using lme4. J. Stat. Softw. 67, 1-48. ( 10.18637/jss.v067.i01) DOI

Hothorn T, Bretz F, Westfall P. 2008. Simultaneous inference in general parametric models. Biom. J. 50, 346-363. ( 10.1002/bimj.200810425) PubMed DOI

Stoffel MA, Nakagawa S, Schielzeth H. 2020. partR2: Partitioning R2 in generalized linear mixed models. DOI

Kolář F, Štech M, Trávníček P, Rauchová J, Urfus T, Vít P, Kubešová M, Suda J. 2009. Towards resolving the PubMed DOI PMC

Castro S, Münzbergová Z, Raabová J, Loureiro J. 2011. Breeding barriers at a diploid–hexaploid contact zone in DOI

Mráz P, Španiel S, Keller A, Bowmann G, Farkas A, Šingliarová B, Rohr RP, Broennimann O, Müller-Schärer H. 2012. Anthropogenic disturbance as a driver of microspatial and microhabitat segregation of cytotypes of PubMed DOI PMC

Hardy OJ, De Loose M, Vekemans X, Meerts P. 2001. Allozyme segregation and inter-cytotype reproductive barriers in the polyploid complex PubMed DOI

Koutecký P, Baďurová T, Štech M, Košnar J, Karásek J. 2011. Hybridization between diploid DOI

Morgan EJ, Čertner M, Lučanová M, Deniz U, Kubíková K, Venon A, Kovářík O, Lafon Placette C, Kolář F. 2021. Disentangling the components of triploid block and its fitness consequences in natural diploid–tetraploid contact zones of PubMed DOI

Lafon-Placette C, et al. 2017. Endosperm-based hybridization barriers explain the pattern of gene flow between PubMed DOI PMC

Santner A, Calderon-Villalobos LI, Estelle M. 2009. Plant hormones are versatile chemical regulators of plant growth. Nat. Chem. Biol. 5, 301-307. ( 10.1038/nchembio.165) PubMed DOI

Hojsgaard D, Pullaiah T. 2022. Apomixis in angiosperms: mechanisms, occurrences and biotechnology. Boca Raton, FL: CRC Press.

Böcher T. 1951. Cytological and embryological studies in the amphi-apomictic

Janas AB, Szeląg Z, Musiał K. 2021. In search of female sterility causes in the tetraploid and pentaploid cytotype of PubMed DOI PMC

Hojsgaard D. 2018. Transient activation of apomixis in sexual neotriploids may retain genomically altered states and enhance polyploid establishment. Front. Plant Sci. 9, 230. ( 10.3389/fpls.2018.00230) PubMed DOI PMC

Rosenberg O. 1906. Über die Embryobildung in der Gattung DOI

Rosenberg O. 1907. Cytological studies on the apogamy in

Koltunow AMG, Johnson SD, Okada T. 2011. Apomixis in hawkweed: Mendel's experimental nemesis. J. Exp. Bot. 62, 1699-1170. ( 10.1093/jxb/err011) PubMed DOI

Catanach AS, Erasmuson SK, Podivinsky E, Jordan BR, Bicknell R. 2006. Deletion mapping of genetic regions associated with apomixis in PubMed DOI PMC

Hojsgaard D, Hörandl E. 2019. The rise of apomixis in natural plant populations. Front. Plant Sci. 10, 358. ( 10.3389/fpls.2019.00358) PubMed DOI PMC

Zahn KH. 1930. Hieracium L. In Synopsis der mitteleuropäischen Flora XXII/1 (eds Graebner P, Graebner P). Liepzig, Germany: Borntraeger.

Peterson RL, Thomas AG. 1971. Buds on the roots of

Bomblies K. 2020. When everything changes at once: finding a new normal after genome duplication. Proc. R. Soc. B. 287, 2020215420202154. ( 10.1098/rspb.2020.2154) PubMed DOI PMC

Atta R, Laurens L, Boucheron-Dubuisson E, Guivarc'h A, Carnero E, Giraudat-Pautot V, Rech P, Chriqui D. 2009. Pluripotency of PubMed DOI

Rosspopoff O, et al. 2017. Direct conversion of root primordium into shoot meristem relies on timing of stem cell niche development. Development 144, 1187-1200. ( 10.1242/dev.142570) PubMed DOI

Martínková J, et al. 2023. What determines root-sprouting ability: injury or phytohormones? Am. J. Bot. 110, e16102. ( 10.1002/ajb2.16102) PubMed DOI

Martínková J, et al. 2023. Why is root-sprouting not more common among plants? Phytohormonal clues and ecological correlates. Environ. Exp. Bot. 205, 105147. ( 10.1016/j.envexpbot.2022.105147) DOI

Šingliarová B, Hojsgaard D, Müller-Schärer H, Mráz P. 2023. The novel expression of clonality following whole-genome multiplication compensates for reduced fertility in natural autopolyploids. Figshare. ( 10.6084/m9.figshare.c.6700004) PubMed DOI PMC

Multiple hybrid zones involving four Cardamine species and their triploid progeny: watching allopolyploid speciation in action?

The novel expression of clonality following whole-genome multiplication compensates for reduced fertility in natural autopolyploids

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