Asexual organisms often differ in their geographic distributions from their sexual relatives. This phenomenon, termed geographic parthenogenesis, has long been known, but the underlying factors behind its diverse patterns have been under dispute. Particularly problematic is an association between asexuality and polyploidy in most taxa. Here, we present a new system of geographic parthenogenesis on the tetraploid level, promising new insights into this complex topic. We used flow cytometric seed screen and microsatellite genotyping to characterise the patterns of distribution of sexuals and apomicts and genotypic distributions in Rubus ser. Glandulosi across its range. Ecological modelling and local-scale vegetation and soil analyses were used to test for niche differentiation between the reproductive groups. Apomicts were detected only in North-western Europe, sexuals in the rest of the range in Europe and West Asia, with a sharp borderline stretched across Central Europe. Despite that, we found no significant differences in ecological niches. Genotypic richness distributions suggested independence of the reproductive groups and a secondary contact. We argue that unless a niche differentiation (resulting from polyploidy and/or hybridity) evolves, the main factors behind the patterns of geographic parthenogenesis in plants are phylogeographic history and neutral microevolutionary processes, such as clonal turnover.

Centre of the Region Haná for Biotechnological and Agricultural Research Crop Research Institute Šlechtitelů 29 Olomouc 78371 Czech Republic

Plant Biosystematics and Ecology Research Group Department of Botany Faculty of Science Palacký University Šlechtitelů 27 Olomouc 78371 Czech Republic

Station of Apple Breeding for Disease Resistance Institute of Experimental Botany Czech Academy of Sciences Rozvojová 313 Prague 6 Lysolaje 16502 Czech Republic

Zobrazit více v PubMed

Asker S. 1970. Apomixis and sexuality in the Potentilla argentea complex II. Crosses within the complex. Hereditas 66: 189–204.

Asker SE, Jerling L. 1992. Apomixis in plants. Boca Raton, FL, USA; Ann Arbor, MI, USA; London, UK; Tokyo, Japan: CRC Press.

Atwater DZ, Ervine C, Barney JN. 2018. Climatic niche shifts are common in introduced plants. Nature Ecology & Evolution 2: 34–43.

Bachman S, Moat J, Hill AW, de la Torre J, Scott B. 2011. Supporting red list threat assessments with GeoCAT: geospatial conservation assessment tool. ZooKeys 150: 117–126.

Baniaga AE, Marx HE, Arrigo N, Barker MS. 2020. Polyploid plants have faster rates of multivariate niche differentiation than their diploid relatives. Ecology Letters 23: 68–78.

Bayer RJ, Stebbins GL. 1983. Distribution of sexual and apomictic populations of Antennaria parlinii. Evolution 37: 555–561.

Bell G. 1982. The masterpiece of nature: the evolution and genetics of sexuality. Berkeley, CA, USA: University of California Press.

Bengtsson BO. 2009. Asex and evolution: a very large‐scale overview. In: Schön I, Martens K, van Dijk P, eds. Lost sex: the evolutionary biology of parthenogenesis. Dordrecht, the Netherlands; Heidelberg, Germany; London, UK; New York, NY, USA: Springer, 1–19.

Bierzychudek P. 1985. Patterns in plant parthenogenesis. Experientia 41: 1255–1264.

Booth TH, Nix HA, Busby JR, Hutchinson MF. 2014. Bioclim: the first species distribution modelling package, its early applications and relevance to most current MaxEnt studies. Diversity and Distributions 20: 1–9.

Borcard D, Legendre P. 2002. All‐scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecological Modelling 153: 51–68.

ter Braak C, Šmilauer P. 2012. Canoco reference manual and user's guide: software of ordination (v.5.0). Ithaca, NY, USA: Microcomputer Power.

Broennimann O, Fitzpatrick MC, Pearman PB, Petitpierre B, Pellissier L, Yoccoz NG, Thuiller W, Fortin M‐J, Randin C, Zimmermann NE et al. 2012. Measuring ecological niche overlap from occurrence and spatial environmental data. Global Ecology and Biogeography 21: 481–497.

Brukhin V, Osadtchiy JV, Florez‐Rueda AM, Smetanin D, Bakin E, Nobre MS, Grossniklaus U. 2019. The Boechera genus as a resource for apomixis research. Frontiers in Plant Science 10: 392.

Burns JH, Strauss SY. 2011. More closely related species are more ecologically similar in an experimental test. Proceedings of the National Academy of Sciences, USA 108: 5302–5307.

Chytrý M, Danihelka J, Kaplan Z, Wild J, Holubová D, Novotný P, Řezníčková M, Rohn M, Dřevojan P, Grulich V et al. 2021. Pladias database of the Czech flora and vegetation. Preslia 93: 1–87.

Di Cola V, Broennimann O, Petitpierre B, Breiner FT, D'Amen M, Randin C, Engler R, Pottier J, Pio D, Dubuis A et al. 2017. Ecospat: an R package to support spatial analyses and modeling of species niches and distributions. Ecography 40: 774–787.

Dorken ME, Eckert CG. 2001. Severely reduced sexual reproduction in northern populations of a clonal plant, Decodon verticillatus (Lythraceae). Journal of Ecology 89: 339–350.

Ellenberg H, Weber HE, Düll R, Wirth V, Werner W, Paulissen D. 1992. Zeigerwerte von Pflanzen in Mitteleuropa. Scripta Geobotanica 18: 1–258.

Forejtová V. 2021. Apomixe v komplexu Rubus ser. Glandulosi: geografické vzorce a důsledky pro vnitropopulační diverzitu [Apomixis in the complex of Rubus ser. Glandulosi: geographical patterns and consequences for intrapopulation diversity]. Master thesis. Olomouc, Czechia: Palacký University Olomouc.

Graham J, Smith K, MacKenzie K, Jorgenson L, Hackett C, Powell W. 2004. The construction of a genetic linkage map of red raspberry (Rubus idaeus subsp. idaeus) based on AFLPs, genomic‐SSR and EST‐SSR markers. Theoretical and Applied Genetics 109: 740–749.

Graham J, Smith K, Tierney I, MacKenzie K, Hackett CA. 2006. Mapping gene H controlling cane pubescence in raspberry and its association with resistance to cane botrytis and spur blight, rust and cane spot. Theoretical and Applied Genetics 112: 818–831.

Grossniklaus U, Nogler GA, van Dijk PJ. 2001. How to avoid sex: the genetic control of developmental aspects. Plant Cell 13: 1491–1497.

Guisan A, Petitpierre B, Broennimann O, Daehler C, Kueffer C. 2014. Unifying niche shift studies: insights from biological invasions. Trends in Ecology & Evolution 29: 260–269.

Gustafsson Å. 1943. The genesis of the European blackberry flora. Lunds Universitets Årsskrift 39: 1–199.

Hammer Ø, Harper D, Ryan P. 2001. Past: paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 1–9.

Hartmann M, Chrtek J, Fér T, Choler P, Taberlet P, Mráz P. 2019. When triploids take over: phylogeography of geographical parthenogenesis in Hieracium alpinum. International Conference on Polyploidy. Ghent, Belgium, 11–14 June 2019.

Haveman R, Bijlsma R‐J, de Ronde I, Schaminée JHJ. 2016. Capricious, or tied to history's apron strings? Floristic regions in north‐west European brambles (Rubus subgenus Rubus, Rosaceae). Journal of Biogeography 43: 1360–1371.

Hengl T, Mendes de Jesus J, Heuvelink GBM, Ruiperez Gonzalez M, Kilibarda M, Blagotić A, Shangguan W, Wright MN, Geng X, Bauer‐Marschallinger B et al. 2017. SoilGrids250m: global gridded soil information based on machine learning. PLoS ONE 12: e0169748.

Herben T, Chytrý M, Klimešová J. 2016. A quest for species‐level indicator values for disturbance. Journal of Vegetation Science 27: 628–636.

Hojsgaard D, Hörandl E. 2019. The rise of apomixis in natural plant populations. Frontiers in Plant Science 10: 358.

Holub J. 1997. Some considerations and thoughts on the pragmatic classification of apomictic Rubus taxa. Osnabrücker Naturwissenschaftliche Mitteilungen 23: 147–155.

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

Hörandl E. 2023. Geographical parthenogenesis in alpine and arctic plants. Plants 12: 844.

Hörandl E, Jakubowsky G, Dobeš C. 2001. Isozyme and morphological diversity within apomictic and sexual taxa of the Ranunculus auricomus complex. Plant Systematics and Evolution 226: 165–185.

Janko K. 2014. Let us not be unfair to asexuals: their ephemerality may be explained by neutral models without invoking any evolutionary constraints of asexuality. Evolution 68: 569–576.

Janko K, Drozd P, Flegr J, Pannell JR. 2008. Clonal turnover versus clonal decay: a null model for observed patterns of asexual longevity, diversity and distribution. Evolution 62: 1264–1270.

Jørgensen M. 2011. A poly approach to ploidy: polyploid evolution and taxonomic implications. PhD thesis. Oslo, Norway: University of Oslo.

Juzepczuk SV. 1941. Genus 734: Rubus. In: Komarov VL, ed. Flora of U.S.S.R, vol. 10. Moskva‐Leningrad, USSR: Izdatel'stvo Akademii Nauk SSSR, 5–58.

Karbstein K, Tomasello S, Hodač L, Lorberg E, Daubert M, Hörandl E. 2021. Moving beyond assumptions: polyploidy and environmental effects explain a geographical parthenogenesis scenario in European plants. Molecular Ecology 30: 2659–2675.

Karger DN, Conrad O, Böhner J, Kawohl T, Kreft H, Soria‐Auza RW, Zimmermann NE, Linder HP, Kessler M. 2017. Climatologies at high resolution for the earth's land surface areas. Scientific Data 4: 170122.

Kass JM, Pinilla‐Buitrago GE, Paz A, Johnson BA, Grisales‐Betancur V, Meenan SI, Attali D, Broennimann O, Galante PJ, Maitner BS et al. 2023. Wallace 2: a shiny app for modeling species niches and distributions redesigned to facilitate expansion via module contributions. Ecography 2023: e06547.

Kelley AM, Johnson PG, Waldron BL, Peel MD. 2009. A survey of apomixis and ploidy levels among Poa L. (Poaceae) using flow cytometry. Crop Science 49: 1395–1402.

Kirchheimer B, Schinkel CCF, Dellinger AS, Klatt S, Moser D, Winkler M, Lenoir J, Caccianiga M, Guisan A, Nieto‐Lugilde D et al. 2016. A matter of scale: apparent niche differentiation of diploid and tetraploid plants may depend on extent and grain of analysis. Journal of Biogeography 43: 716–726.

Kolář F, Čertner M, Suda J, Schönswetter P, Husband BC. 2017. Mixed‐ploidy species: progress and opportunities in polyploid research. Trends in Plant Science 22: 1041–1055.

Kurtto A, Weber HE, Lampinen R, Sennikov AN, eds. 2010. Atlas florae Europaeae. Distribution of vascular plants in Europe, vol. 15: Rosaceae (Rubus). Helsinki, Finland: Committee for Mapping the Flora of Europe and Societas Biologica Fennica Vanamo.

Lai J, Zou Y, Zhang J, Peres‐Neto PR. 2022. Generalizing hierarchical and variation partitioning in multiple regression and canonical analyses using the rdacca.hp R package. Methods in Ecology and Evolution 13: 782–788.

Lehtonen J, Jennions MD, Kokko H. 2012. The many costs of sex. Trends in Ecology & Evolution 27: 172–178.

Levin DA. 1975. Minority cytotype exclusion in local plant populations. Taxon 24: 35–43.

Levin DA. 2002. The role of chromosomal change in plant evolution. Oxford, UK: Oxford University Press.

van der Maarel E, Franklin J. 2013. Vegetation ecology. Chichester, UK: Wiley‐Blackwell.

Matzk F, Meister A, Schubert I. 2000. An efficient screen for reproductive pathways using mature seeds of monocots and dicots. The Plant Journal 21: 97–108.

Matzk F, Prodanovic S, Bäumlein H, Schubert I. 2005. The inheritance of apomixis in Poa pratensis confirms a five locus model with differences in gene expressivity and penetrance. Plant Cell 17: 13–24.

Mau M, Liiving T, Fomenko L, Goertzen R, Paczesniak D, Böttner L, Sharbel TF. 2021. The spread of infectious asexuality through haploid pollen. New Phytologist 230: 804–820.

Mau M, Lovell JT, Corral JM, Kiefer C, Koch MA, Aliyu OM, Sharbel TF. 2015. Hybrid apomicts trapped in the ecological niches of their sexual ancestors. Proceedings of the National Academy of Sciences, USA 112: e2357–e2365.

Meirmans PG. 2021. Niche divergence contributes to geographical parthenogenesis in two dandelion taxa. Journal of Evolutionary Biology 34: 1071–1086.

Meirmans PG, Van Tienderen PH. 2004. genotype and genodive: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes 4: 792–794.

Meirmans S, Meirmans PG, Kirkendall LR. 2012. The costs of sex: facing real‐world complexities. Quarterly Review of Biology 87: 19–40.

Michaels HJ, Bazzaz FA. 1986. Resource allocation and demography of sexual and apomictic Antennaria parlinii. Ecology 67: 27–36.

Nardi FD, Dobeš C, Müller D, Grasegger T, Myllynen T, Alonso‐Marcos H, Tribsch A. 2018. Sexual intraspecific recombination but not de novo origin governs the genesis of new apomictic genotypes in Potentilla puberula (Rosaceae). Taxon 67: 1108–1131.

Nardi FD, Hülber K, Moser D, Alonso‐Marcos H, Tribsch A, Dobeš C. 2020. Occurrence of apomictic conspecifics and ecological preferences rather than colonization history govern the geographic distribution of sexual Potentilla puberula. Ecology and Evolution 10: 7306–7319.

Neiman M, Meirmans PG, Schwander T, Meirmans S. 2018. Sex in the wild: how and why field‐based studies contribute to solving the problem of sex. Evolution 72: 1194–1203.

Niissalo MA, Leong‐Škorničková J, Šída O, Khew GS. 2020. Population genomics reveal apomixis in a novel system: uniclonal female populations dominate the tropical forest herb family, Hanguanaceae (Commelinales). AoB Plants 12: plaa053.

Normand S, Ricklefs RE, Skov F, Bladt J, Tackenberg O, Svenning J‐C. 2011. Postglacial migration supplements climate in determining plant species ranges in Europe. Proceedings of the Royal Society B: Biological Sciences 278: 3644–3653.

O'Connell LM, Eckert CG. 1999. Differentiation in sexuality among populations of Antennaria parlinii (Asteraceae). International Journal of Plant Sciences 160: 567–575.

O'Connell LM, Eckert CG. 2001. Differentiation in reproductive strategy between sexual and asexual populations of Antennaria parlinii (Asteraceae). Evolutionary Ecology Research 3: 311–330.

Petitpierre B, Kueffer C, Broennimann O, Randin C, Daehler C, Guisan A. 2012. Climatic niche shifts are rare among terrestrial plant invaders. Science 335: 1344–1348.

R Core Team. 2023. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Rice A, Šmarda P, Novosolov M, Drori M, Glick L, Sabath N, Meiri S, Belmaker J, Mayrose I. 2019. The global biogeography of polyploid plants. Nature Ecology & Evolution 3: 265–273.

Šarhanová P, Majeský L', Sochor M. 2024. A novel strategy to study apomixis, automixis, and autogamy in plants. Plant Reproduction, in press.

Šarhanová P, Sharbel TF, Sochor M, Vašut RJ, Dančák M, Trávníček B. 2017. Hybridization drives evolution of apomicts in Rubus subgenus Rubus: evidence from microsatellite markers. Annals of Botany 120: 317–328.

Šarhanová P, Vašut RJ, Dančák M, Bureš P, Trávníček B. 2012. New insights into the variability of reproduction modes in European populations of Rubus subgen. Rubus: how sexual are polyploid brambles? Sexual Plant Reproduction 25: 319–335.

Schinkel CCF, Kirchheimer B, Dellinger AS, Klatt S, Winkler M, Dullinger S, Hörandl E. 2016. Correlations of polyploidy and apomixis with elevation and associated environmental gradients in an alpine plant. AoB Plants 8: plw064.

Schwander T, Crespi BJ. 2009. Twigs on the tree of life? Neutral and selective models for integrating macroevolutionary patterns with microevolutionary processes in the analysis of asexuality. Molecular Ecology 18: 28–42.

Sochor M, Šarhanová P, Duchoslav M, Konečná M, Hroneš M, Trávníček B. 2024. Plant kleptomaniacs: geographic genetic patterns in the amphi‐apomictic Rubus ser. Glandulosi (Rosaceae) reveal complex reticulate evolution of Eurasian brambles. BioRxiv. doi: 10.1101/2024.01.16.575855.

Sochor M, Trávníček B, Király G. 2019. Ploidy level variation in the genus Rubus in the Pannonian Basin and the northern Balkans, and evolutionary implications. Plant Systematics and Evolution 305: 611–626.

Sochor M, Vašut RJ, Sharbel TF, Trávníček B. 2015. How just a few makes a lot: speciation via reticulation and apomixis on example of European brambles (Rubus subgen. Rubus, Rosaceae). Molecular Phylogenetics and Evolution 89: 13–27.

Sonnleitner M, Hülber K, Flatscher R, Escobar García P, Winkler M, Suda J, Schönswetter P, Schneeweiss GM. 2016. Ecological differentiation of diploid and polyploid cytotypes of Senecio carniolicus sensu lato (Asteraceae) is stronger in areas of sympatry. Annals of Botany 117: 269–276.

Tichý L. 2016. Field test of canopy cover estimation by hemispherical photographs taken with a smartphone. Journal of Vegetation Science 27: 427–435.

Tilquin A, Kokko H. 2016. What does the geography of parthenogenesis teach us about sex? Philosophical Transactions of the Royal Society, B: Biological Sciences 371: 20150538.

Title PO, Bemmels JB. 2018. Envirem: an expanded set of bioclimatic and topographic variables increases flexibility and improves performance of ecological niche modeling. Ecography 41: 291–307.

Vandel A. 1928. La parthénogenese geographique. Contribution a l'étude biologique et cytologique de la parthénogenese naturelle. Bulletin Biologique de la France et de la Belgique 62: 164–182.

Vorburger C. 2006. Geographic parthenogenesis: recurrent patterns down under. Current Biology 16: R641–R6433.

Warren DL, Glor RE, Turelli M. 2008. Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62: 2868–2883.

Williams G. 1975. Sex and evolution. Princeton, UK: Princeton University Press.

Woodhead M, McCallum S, Smith K, Cardle L, Mazzitelli L, Graham J. 2008. Identification, characterisation and mapping of simple sequence repeat (SSR) markers from raspberry root and bud ESTs. Molecular Breeding 22: 555–563.

Xu Y, Jia H, Tan C, Wu X, Deng X, Xu Q. 2022. Apomixis: genetic basis and controlling genes. Horticulture Research 9: uhac150.

Zilli AL, Acuña CA, Schulz RR, Brugnoli EA, Guidalevich V, Quarin CL, Martínez EJ. 2018. Widening the gene pool of sexual tetraploid bahiagrass: generation and reproductive characterization of a sexual synthetic tetraploid population. Crop Science 58: 762–772.

Plant kleptomaniacs: geographical genetic patterns in the amphi-apomictic Rubus ser. Glandulosi (Rosaceae) reveal complex reticulate evolution of Eurasian brambles