Gametophytic apomixis is a way of asexual plant reproduction by seeds. It should be advantageous under stressful high altitude or latitude environment where short growing seasons, low temperatures, low pollinator activity or unstable weather may hamper sexual reproduction. However, this hypothesis remains largely untested. Here, we assess the reproductive mode in 257 species belonging to 45 families from the world's broadest alpine belt (2800-6150 m) in NW Himalayas using flow cytometric seed screen. We found only 12 apomictic species, including several members of Poaceae (Festuca, Poa and Stipa), Rosaceae (Potentilla) and Ranunculaceae (Halerpestes, Ranunculus), which are families typical for high apomict frequency. However, several apomictic species were newly discovered, including the first known apomictic species from the family Biebersteiniaceae (Biebersteinia odora), and first apomicts from the genera Stipa (Stipa splendens) and Halerpestes (Halerpestes lancifolia). Apomicts showed no preference for higher elevations, even in these extreme Himalayan alpine habitats. Additional trait-based analyses revealed that apomicts differed from sexuals in comprising more rhizomatous graminoids and forbs, higher soil moisture demands, sharing the syndrome of dominant species with broad geographical and elevation ranges typical for the late-successional habitats. Apomicts differ from non-apomicts in greater ability of clonal propagation and preference for wetter, more productive habitats.

Department of Botany Faculty of Science University of South Bohemia Branišovská 1760 370 05 České Budějovice Czech Republic

Institute of Botany The Czech Academy of Sciences Dukelská 135 Třeboň 379 01 Czech Republic

Laboratory of Tree Ring Research University of Arizona 1215 E Lowell Street Tucson 85721 Arizona USA

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Bierzychudek P. Patterns in plantparthenogenesis. Experientia. 1985;41:1255–1264. doi: 10.1007/BF01952068. DOI

Gregor T. Apomicts in the vegetation of Central Europe. Tuexenia. 2013;33:233–257.

Kearney M. Hybridization, glaciation and geographical parthenogenesis. Trends Ecol. Evol. 2005;20:495–502. doi: 10.1016/j.tree.2005.06.005. PubMed DOI

Tilquin, A., & Kokko, H. What does the geography of parthenogenesis teach us about sex? Philos Trans R Soc Lond B Biol Sci. 371 (2016). PubMed PMC

Stebbins, G. L. Variation and Evolution in Plants. (New York: Columbia University Press, 1950).

Baker HG. Support for Baker’s law – as a rule. Evolution. 1967;21:853–856. doi: 10.1111/j.1558-5646.1967.tb03440.x. PubMed DOI

Hörandl E, Cosendai AC, Temsch EM. Understanding the geographic distributions of apomictic plants: a case for a pluralistic approach. Plant. Ecol. Divers. 2008;1:309–320. doi: 10.1080/17550870802351175. PubMed DOI PMC

Hörandl E, et al. Apomixis is not prevalent in subnival to nival plants of the European Alps. Ann. Bot-London. 2011;108:381–390. doi: 10.1093/aob/mcr142. PubMed DOI PMC

Hartmann M, et al. The Red Queen hypothesis and geographical parthenogenesis in the alpine hawkweed Hieracium alpinum (Asteraceae) Biol. J. Linn. Soc. 2017;122:681–696. doi: 10.1093/biolinnean/blx105. DOI

Paudel, B. R., Shrestha, M., Dyer, A. G., & Li, Q. J. Ginger and the beetle: Evidence of primitive pollination system in a Himalayan endemic alpine ginger (Roscoea alpina, Zingiberaceae). PloS one. 12 (2017). PubMed PMC

Kirchheimer B, et al. A matter of scale: apparent niche differentiation of diploid and tetraploid plants may depend on extent and grain of analysis. J. Biogeogr. 2016;43:716–726. doi: 10.1111/jbi.12663. PubMed DOI PMC

Schinkel, C. C. et al. Correlations of polyploidy and apomixis with elevation and associated environmental gradients in an alpine plant. AoB Plants, 8 (2016). PubMed PMC

Schinkel CC, et al. Pathways to polyploidy: indications of a female triploid bridge in the alpine species Ranunculus kuepferi (Ranunculaceae) Plant syst. Evol. 2017;303:1093–1108. doi: 10.1007/s00606-017-1435-6. PubMed DOI PMC

Kirchheimer B, et al. Reconstructing geographical parthenogenesis: effects of niche differentiation and reproductive mode on Holocene range expansion of an alpine plant. Ecol. Lett. 2018;21:392–401. doi: 10.1111/ele.12908. PubMed DOI PMC

Klatt S, Schinkel CC, Kirchheimer B, Dullinger S, Hörandl E. Effects of cold treatments on fitness and mode of reproduction in the diploid and polyploid alpine plant Ranunculus kuepferi (Ranunculaceae) Ann Bot. 2018;121:1287–1298. doi: 10.1093/aob/mcy017. PubMed DOI PMC

Warren, S. D., Harper, K. T. & Booth, G. M. Elevational distribution of insect pollinators. Am. Midl. Nat. 325–330 (1988).

McCall C, Primack RB. Influence of flower characteristics, weather, time of day, and season on insect visitation rates in three plant communities. Am. J. Bot. 1992;79:434–442. doi: 10.1002/j.1537-2197.1992.tb14571.x. DOI

Stenseth NC, Kirkendall LR. On the evolution of pseudogamy. Evolution. 1985;39:294–307. doi: 10.1111/j.1558-5646.1985.tb05667.x. PubMed DOI

Gornall, R. J. Population genetic structure in agamospermous plants in Syst. Assoc. Spec. Vol. (eds Hollingsworth, P. M., Bateman, R. M., Gornall, R. J.) 118–138 (London: Taylor & Francis, 1999).

Carman JG. Asynchronous expression of duplicate genes in angiosperms may cause apomixis, bispory, tetraspory, and polyembryony. Biol. J. Linn. Soc. 1997;61:51–94. doi: 10.1111/j.1095-8312.1997.tb01778.x. DOI

Lynch M. Destabilizing hybridisation, general purpose genotypes and geographic parthenogenesis. Q. Rev. Biol. 1984;59:257–290. doi: 10.1086/413902. DOI

Hörandl, E. Geographical parthenogenesis: Opportunities for asexuality in Lost Sex (eds Schön, I., Martens, K., Van Dijk, P.) 161–186 (Netherlands, Dordrecht: Springer, 2009).

Thompson SL, Whitton J. Patterns of recurrent evolution and geographic parthenogenesis within apomictic polyploid easter daises (Townsendia hookeri) Mol. Ecol. 2006;15:3389–3400. doi: 10.1111/j.1365-294X.2006.03020.x. PubMed DOI

Van Dijk PJ. Ecological and evolutionary opportunities of apomixis: insights from Taraxacum and Chondrilla. Philos. T. Roy. Soc. B. 2003;358:1113–1121. doi: 10.1098/rstb.2003.1302. PubMed DOI PMC

Cosendai AC, Rodewald J, Hörandl E. Origin and distribution of autopolyploids via apomixis in the alpine species Ranunculus kuepferi (Ranunculaceae) Taxon. 2011;60:355–364. doi: 10.1002/tax.602006. DOI

Baker HG. Dimorphism and monomorphism in the Plumbaginaceae: 1. A survey of the family. Ann. Bot-London. 1948;12:207–219. doi: 10.1093/oxfordjournals.aob.a083185. DOI

Baker HG. Self compatibility and establishment after long distance. Evolution. 1955;9:347–349.

Stebbins GL. Self fertilisation and population variability in the higher plants. Am. Nat. 1957;91:337–354. doi: 10.1086/281999. DOI

Hörandl E. The complex causality of geographical parthenogenesis. New Phytol. 2006;171:525–538. PubMed

Lefebvre V, Fontaine C, Villemant C, Daugeron C. Are empidine dance flies major flower visitors in alpine environments? A case study in the Alps, France. Biol. Letters. 2014;10:4. doi: 10.1098/rsbl.2014.0742. PubMed DOI PMC

Williams PH, Bystriakova N, Huang JX, Miao ZY, An J. Bumblebees, climate and glaciers across the Tibetan plateau (Apidae: Bombus Latreille) Syst. Biodivers. 2015;13:164–181. doi: 10.1080/14772000.2014.982228. DOI

Rutishauser A. Die Entwicklungserregung des Endosperms bei pseudogamen Ranunculusarten. Mitt. der Naturf. Ges. Schaffhausen. 1954;25:1–45.

Nybom H. Active self-pollination in blackberries (Rubus subgen. Rubus, Rosaceae) Nord. J. Bot. 1986;5:521–525. doi: 10.1111/j.1756-1051.1985.tb01689.x. DOI

Kollmann J, Steinger T, Roy BR. Evidence of sexuality in European Rubus (Rosaceae) species based on AFLP and allozyme analysis. Am. J. Bot. 2000;87:1592–1598. doi: 10.2307/2656735. PubMed DOI

Gregor T. Apomicts in the vegetation of Central. Europe. Tuexenia. 2013;33:233–257.

Smith GL. Studies in Potentilla L. II. Cytological aspects of apomixis in P. crantzii (Cr.) Beck ex Fritsch. New Phytol. 1963;62:283–300. doi: 10.1111/j.1469-8137.1963.tb06335.x. DOI

Doležal J, et al. Vegetation dynamics at the upper elevational limit of vascular plants in Himalaya. Sci. Rep-UK. 2016;6:24881. doi: 10.1038/srep24881. PubMed DOI PMC

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

Dobeš C, Luckl A, Hulber K, Paule J. Prospects and limits of the flow cytometric seed screen - insights from Potentilla sensu lato (Potentilleae, Rosaceae) New Phytol. 2013;198:605–616. doi: 10.1111/nph.12149. PubMed DOI PMC

Krahulcová A, Rotreklová O. Use of flow cytometry in research on apomictic plants. Preslia. 2010;82:23–39.

Matzk, F. Reproduction mode screening in Flow Cytometry with Plant Cells: Analysis of Genes, Chromosomes and Genomes (eds Doležel, J., Greilhuber, J., & Suda, J.) 131–152 (John Wiley & Sons, 2007).

Chiarugai A. Il gametofito femmineo dell Angiosperme nei suoi vari tipi di costruzione e di sviluppo. Nuovo G. Bot. Ital. 1927;34:5.

Koltunow AM, Grossniklaus U. Apomixis: A developmental perspective. Annu. Rev. Plant Biol. 2003;54:547–574. doi: 10.1146/annurev.arplant.54.110901.160842. PubMed DOI

Matzk F, Meister A, Brutkovska R, Schubert I. Reconstruction of reproductive diversity in Hypericum perforatum L. opens novel strategies to manage apomixis. Plant J. 2001;26:275–282. doi: 10.1046/j.1365-313X.2001.01026.x. PubMed DOI

Talent N, Dickinson TA. Endosperm formation in aposporous Crataegus (Rosaceae, Spiraeoideae, tribe Pyreae): parallels to Ranunculaceae and Poaceae. New Phytol. 2007;173:231–249. doi: 10.1111/j.1469-8137.2006.01918.x. PubMed DOI

Klimešová J, Doležal J, Dvorský M, de Bello F, Klimeš L. Clonal growth forms in eastern Ladakh, Western Himalayas: classification and habitat preferences. Folia Geobot. 2011;46:191–217. doi: 10.1007/s12224-010-9076-3. DOI

Barrett SC. Influences of clonality on plant sexual reproduction. P. Natl. Acad. Sci. USA. 2015;112:8859–8866. doi: 10.1073/pnas.1501712112. PubMed DOI PMC

Emadzade K, Lehnebach C, Lockhart P, Hörandl E. A molecular phylogeny, morphology and classification of genera of Ranunculeae (Ranunculaceae) Taxon. 2010;59:809–828. doi: 10.1002/tax.593011. DOI

Dvorský M, Doležal J, De Bello F, Klimešová J, Klimeš L. Vegetation types of East Ladakh: species and growth form composition along main environmental gradients. Appl. Veg. Sci. 2011;14:132–147. doi: 10.1111/j.1654-109X.2010.01103.x. DOI

Dvorský M, Macek M, Kopecký M, Wild J, Doležal J. Niche asymmetry of vascular plants increases with elevation. J. Biogeogr. 2017;44:1418–1425. doi: 10.1111/jbi.13001. DOI

Asker S. Chromosome studies in Potentilla. Hereditas. 1985;102:289–292. doi: 10.1111/j.1601-5223.1985.tb00628.x. DOI

Asker S. Polymorphism of Potentilla tamernaemontani and related taxa on Gotland. Hereditas. 1985;102:39–45. doi: 10.1111/j.1601-5223.1985.tb00463.x. DOI

Talent N, Dickinson TA. Chapter 16. Apomixis and hybridization in Rosaceae subtribe Pyrinae Dumort.: a new tool promises new insights. Regnum Veg. 2007;147:301.

Asker, S. & Jerling, L. Apomixis in Plants (CRC Press, 1992).

Dobeš C, et al. Parallel origins of apomixis in two diverged evolutionary lineages in tribe Potentilleae (Rosaceae) Bot. J. Linn. Soc. 2015;177:214–229. doi: 10.1111/boj.12239. DOI

Corner, E. J. H. The Seeds of Dicotyledons, Vol 1 (Cambridge University Press, 1976).

Martin AC. The comparative internal morphology of seeds. Am. Midl. Nat. 1946;36:513–660. doi: 10.2307/2421457. DOI

Kalkman, C. Rosaceae in The Families and Genera of Vascular Plants (ed. Kubitzki, K.) 343–386 (Berlin, Heidelberg, Germany & New York, NY, USA: Springer, 2004).

Jeelani SM, Kumari S, Gupta RC. Meiotic studies in some selected angiosperms from the Kashmir Himalayas. J. Syst. Evol. 2012;50:244–257. doi: 10.1111/j.1759-6831.2012.00183.x. DOI

Christoff M, Papasova G. Die genetischen Grundlagen der apomiktischen Fortpflanzung in der Gattung Potentilla. Mol. Gen. Genet. 1943;81:1–27. doi: 10.1007/BF01847440. DOI

Rani S, Kumar S, Jeelani SM, Gupta RC, Kumari S. Additions to the cytologically investigated species of Potentilla L. (Rosaceae) from India. Plant Syst. Evol. 2012;298:485–497. doi: 10.1007/s00606-011-0560-x. DOI

Eriksson T, Donughue MJ, Hibbs MS. Phylogenetic analysis of Potentilla using DNA sequences of nuclear ribosomal internal transcribed spacers (ITS), and implications for the classification of Rosoideae (Rosaceae) Plant Syst. Evol. 1998;211:155–179. doi: 10.1007/BF00985357. DOI

Nogler, G. A. Gametophytic apomixis in Embryology of Angiosperms (ed. Johri, B. M.) 475–518 (Berlin, Germany: Springer, 1984).

Nogler GA. Genetics of apospory in apomictic Ranunculus auricomus: 5. Conclusion. Bot. Helv. 1984;94:411–423.

Hörandl E, et al. Phylogenetic relationships and evolutionary traits in Ranunculus s.l. (Ranunculaceae) inferred from ITS sequence analysis. Mol. Phylogenet. Evol. 2005;36:305–327. doi: 10.1016/j.ympev.2005.02.009. PubMed DOI

Emadzade K, Lehnebach C, Lockhart P, Hörandl E. A molecular phylogeny, morphology and classification of genera of Ranunculeae (Ranunculaceae) Taxon. 2010;59:809–828. doi: 10.1002/tax.593011. DOI

Kelley AM, Johnson PG, Waldron BL, Peel MD. A Survey of apomixis and ploidy levels among Poa L. (Poaceae) using flow cytometry. Crop Sci. 2009;49:1395–1402. doi: 10.2135/cropsci2008.09.0553. DOI

Richards, A. J. Plant Breeding Systems (London: Allen & Unwin, 2nd edition, 1997).

Hojsgaard D, Klatt S, Baier R, Carman JG, Hörandl E. Taxonomy and biogeography of apomixis in angiosperms and associated biodiversity characteristics. Cr. Rev. Plant Sci. 2014;33:414–427. doi: 10.1080/07352689.2014.898488. PubMed DOI PMC

Soreng, R. J., Davis, J. I., Voionmaa, M. A. A phylogenetic analysis of Poaceae tribe Poeae sensu lato based on morphological characters and sequence data from three plastid-encoded genes: evidence for reticulation, and a new classification for the tribe. Kew Bull. 425–454 (2007).

Chapman, G. P. (ed.). Reproductive Versatility in the Grasses (Cambridge University Press, 1990).

Rutishauser A. Pseudogamie und Polymorphie in der Gattung Potentilla. Arch. Julius-Klaus-Srifr. Vererbungsforsch. 1948;23:267–424.

Asker S. Pseudogamy, hybridization and evolution in Potentilla. Hereditas. 1977;87:179–184. doi: 10.1111/j.1601-5223.1978.tb01260.x. DOI

Harlan JR, de Wet JMJ, On O. Winge and a prayer: the origin of polyploidy. Bot. Rev. 1975;41:361–390. doi: 10.1007/BF02860830. DOI

Whitton J, Sears CJ, Baack EJ, Otto SP. The dynamic nature of apomixis in the angiosperms. Int J Plant Sci. 2008;169:169–182. doi: 10.1086/523369. DOI

Maugini E. Morfologia fiorale embriologia ed embriog in Leontopodium alpinum Cass. var. α typicum fiori e Paoletti. Plant Biosystem. 1962;69:1–18.

Sokolowska-Kulczycka, A. Apomiksja u Leontopodium alpinum Cass: Apomixis in Leontopodium alpinum Cass. (1959).

Noyes RD. Apomixis via recombination of genome regions for apomeiosis (diplospory) and parthenogenesis in Erigeron (daisy fleabane, Asteraceae) Sex Plant Reprod. 2006;19:7–18. doi: 10.1007/s00497-005-0017-x. DOI

Noyes RD. Inheritance of apomeiosis (diplospory) in fleabanes (Erigeron, Asteraceae) Heredity. 2005;94:193. doi: 10.1038/sj.hdy.6800597. PubMed DOI

Noyes RD, Baker R, Mai B. Mendelian segregation for two-factor apomixis in Erigeron annuus (Asteraceae) Heredity. 2007;98:92. doi: 10.1038/sj.hdy.6800907. PubMed DOI

Noyes RD, Rieseberg LH. Two independent loci control agamospermy (apomixis) in the triploid flowering plant Erigeron annuus. Genetics. 2000;155:379–390. PubMed PMC

Stratton DA. Life history variation within populations of an asexual plant, Erigeron annuus (Asteraceae) Am. J. Bot. 1991;78:723–728. doi: 10.1002/j.1537-2197.1991.tb12596.x. DOI

Chiarugi A. Aposporiae apogamia in Artemisia nitida Bertol. Nuovo Giorn. Bot. Ital. 1926;33:501–626.

Noyes RD. Apomixis in the Asteraceae: diamonds in the rough. Funct. Plant. Sci. Biotechnol. 2007;1:207–222.

Richards AJ. The origin of Taraxacum agamospecies. Bot. J. Linn. Soc. 1973;66:189–211. doi: 10.1111/j.1095-8339.1973.tb02169.x. PubMed DOI PMC

Firetti, F. Apomixis in Neotropical Vegetation. Vegetation. 129–148 (2018).

Roy BA, Bierzychudek P. The potential for rust infection to cause natural selection in apomictic Arabis holboellii (Brassicaceae) Oecologia. 1993;95:533–541. doi: 10.1007/BF00317438. PubMed DOI

Schranz ME, Dobeš C, Koch MA, Mitchell‐Olds T. Sexual reproduction, hybridization, apomixis, and polyploidization in the genus Boechera (Brassicaceae) Am. J. Bot. 2005;92:1797–1810. doi: 10.3732/ajb.92.11.1797. PubMed DOI

Orellana MR, Rovira AM, Blanché C, Bosch M. Pollination and reproductive success in the gynodioecious endemic Thymus loscosii (Lamiaceae) Can. J. Bot. 2005;83:183–193. doi: 10.1139/b04-166. DOI

Hand ML, Koltunow AM. The genetic control of apomixis: asexual seed formation. Genetics. 2014;197:441–450. doi: 10.1534/genetics.114.163105. PubMed DOI PMC

Burt A. Perspective: sex, recombination and the efficacy of selection – was Weismann right? Evolution. 2000;54:337–351. PubMed

Karger DN, et al. Climatologies at high resolution for the earth’s land surface areas. Sci. data. 2017;4:170122. doi: 10.1038/sdata.2017.122. PubMed DOI PMC

Janatková K, et al. Community structure of soil phototrophs along environmental gradients in arid Himalaya. Environ. microbiol. 2013;15:2505–2516. doi: 10.1111/1462-2920.12132. PubMed DOI

Krahulcová A, Suda J. A modified method of flow cytometric seed screen simplifies the quantification of progeny classes with different ploidy levels. Biol. Plantarum. 2006;50:457–460. doi: 10.1007/s10535-006-0070-9. DOI

Doležel J, Greilhuber J, Suda J. Estimation of nuclear DNA content in plants using flow cytometry. Nat. Protoc. 2007;2:2233–2244. doi: 10.1038/nprot.2007.310. PubMed DOI

Doležel J, et al. Plant genome size estimation by flow cytometry: inter-laboratory comparison. Ann. Bot-London. 1998;82:17–26. doi: 10.1093/oxfordjournals.aob.a010312. DOI

Cornelissen JHC, et al. A handbook of protocols for standardised and easy measurement of plant functional traits worldwide. Aust. J. Bot. 2003;51:335–380. doi: 10.1071/BT02124. DOI

Doležal J, et al. Functionally distinct assembly of vascular plants colonizing alpine cushions suggests their vulnerability to climate change. Ann. Bot. 2019;123:569–578. doi: 10.1093/aob/mcy207. PubMed DOI PMC

ter Braak, C. J. & Šmilauer, P. Canoco Reference Manual and User’s Guide: Software for Ordination, Version 5.0. (Microcomputer power, 2012).