The mixed mating system of a widespread weed: the case of Argemone ochroleuca Sweet (Papaveraceae)

  • Sandra Rios-Carrasco Laboratorio de Desarrollo en Plantas. Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México
  • Sonia Vázquez-Santana Laboratorio de Desarrollo en Plantas. Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México
keywords: inbreeding depression, invasive weed, pseudocleistogamy, reproductive assurance, self-compatibility


Background: Argemone ochroleuca is a worldwide invasive weed but is also highly valuable for their chemical compounds. Knowledge about its reproduction will help create plans for its control or its propagation.

Questions: Does A. ochroleuca has an incompatibility system like other Papaveraceae species? Which are the reproductive strategies that favor the seed formation in A. ochroleuca?

Studied species: A. ochroleuca is an annual species with bisexual flowers.

Study site and dates: Mexico City, Mexico. The fieldwork was performed from February to May in 2013, 2014, and 2017.

Methods: Direct observations were made to describe the flower cycle of A. ochroleuca. We used self-pollinated flowers to analyze if this species is self-incompatible by following the pollen tube growth through gynoecium. Controlled pollinations were made to quantify and compare the number of seeds produced per treatment to know the mating system and explore if the species presents a mechanism of reproductive assurance through autogamy, or exhibits inbreeding depression.

Results: A. ochroleuca is self-compatible and exhibits a mixed mating system. Although outcrossing is how more seeds are produced, both autogamy and pseudocleistogamy are present as reproductive assurance mechanisms. Naturally pollinated flowers produce the maximum number of seeds, but inbreeding depression is present in the population. Thus, the number of seeds will be affected by continuous selfing.

Conclusions: This study highlights the mixed mating system and reproductive assurance mechanisms as successful strategies for A. ochroleuca, a common pattern in invasive weeds.


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Author Biography

Sonia Vázquez-Santana, Laboratorio de Desarrollo en Plantas. Departamento de Biología Comparada, Facultad de Ciencias, Universidad Nacional Autónoma de México, Ciudad de México




The mixed mating system of a widespread weed: the case of <em>Argemone ochroleuca</em> Sweet (Papaveraceae)


Allen AM, Hiscock SJ. 2008. Evolution and phylogeny of self-incompatibility systems in angiosperms. In: Franklin-Tong VE, ed. Self-incompatibility in Flowering Plants: Evolution, Diversity, and Mechanisms. Berlin: Springer-Verlag, pp. 73-102. ISBN: 978-354-0684-855

Anic V, Henríquez CA, Abades SR, Bustamante RO. 2015. Number of conspecifics and reproduction in the invasive plant Eschscholzia californica (Papaveraceae): is there a pollinator?mediated Allee effect? Plant Biology 17: 720-727. DOI:

Arredondo-Núñez A. 2011. Diferenciación de los sistemas reproductivos y despliegues florales en Eschscholzia californica (Papaveraceae) en un gradiente altitudinal. MSc Thesis, University of Chile.

Assaeed AM, Al-Rowaily SL, El-Bana MI, Hegazy AK, Dar BA, Abd-ElGawad AM. 2020. Functional traits plasticity of the invasive herb Argemone ochroleuca Sweet in different arid habitats. Plants 9: 1268. DOI:

Barrett SCH. 1995. Mating-system evolution in flowering plants: micro- and macroevolutionary approaches. Acta Botanica Neerlandica 44: 385-402. DOI:

Barrett SCH. 1998. The evolution of mating strategies in flowering plants. Trends in Plant Science 3: 335-341. DOI:

Barrett SCH. 2002. The evolution of plant sexual diversity. Nature Reviews Genetics 3: 274-284. DOI:

Barrett SCH. 2011. Why Reproductive systems matter for the invasion biology of plants. In: Richardson DM, ed. Fifty Years of Invasion Ecology: The Legacy of Charles Elton. West Sussex: John Wiley and Sons, pp. 195-210. ISBN: 978-1-4443-3585-9

Barrett SCH. 2014. Evolution of mating systems: outcrossing versus selfing. In: Losos J, ed. The Princeton Guide to Evolution. New Jersey: Princeton University Press, pp. 356-362 ISBN: 978-0-6911-4977-6

Bilinski P, Kohn J. 2012. Sites of self-pollen tube inhibition in Papaveraceae (sensu lato). Plant Systematics and Evolution 298: 1239-1247. DOI:

Bretagnolle V, Gaba S. 2015. Weeds for bees? A review. Agronomy for Sustainable Development 35: 891-909. DOI:

Busch JW, Delph LF. 2012. The relative importance of reproductive assurance and automatic selection as hypotheses for the evolution of self-fertilization. Annals of Botany 109: 553-562. DOI:

Busch JW, Herlihy CR, Gunn L, Werner WJ. 2010. Mixed mating in a recently derived self-compatible population of Leavenworthia alabamica (Brassicaceae). American Journal of Botany 97: 1005-13. DOI:

Calderón de Rzedowski G. 1991. Flora del bajío y de regiones adyacentes. Fascículo 1: Familia Papaveraceae. Xalapa: Instituto de Ecología. ISBN: 970-709-038-3

Carr DE, Dudash MR. 1996. Inbreeding depression in two species of Mimulus (Scrophulariaceae) with contrasting mating systems. American Journal of Botany 83: 586-593. DOI:

Carrió E, Güemes J. 2013. The role of a mixed mating system in the reproduction of a Mediterranean subshrub (Fumana hispidula, Cistaceae). Journal of Plant Research 126: 33-40. DOI:

Cheptou PO. 2019. Does the evolution of self-fertilization rescue populations or increase the risk of extinction? Annals of Botany 123: 337-345. DOI:

Cruden RW. 1976. Intraspecific variation in pollen-ovule ratios and nectar secretion-preliminary evidence of ecotypic adaptation. Annals of the Missouri Botanical Garden 63: 277-289. DOI:

Cruden RW. 1977. Pollen-ovule ratios: a conservative indicator of breeding systems in flowering plants. Evolution 31: 32-46. DOI:

Dar BA, Al-Rowaily SL, Assaeed AM, El-Bana MI, Hegazy AK, Malik JA. 2017. Allelopathic potential of Argemone ochroleuca from different habitats on seed germination of native species and cultivated crops. Pakistan Journal of Botany 49: 1841-1848.

de Nettancourt D. 1977. Incompatibility in angiosperms. Monographs on theoretical and applied genetics. Berlin: Springer-Verlag. ISBN: 978-0387081120

de Nettancourt D. 2001. Incompatibility and incongruity in wild and cultivated plants. Berlin: Springer-Verlag. ISBN: 978-3-662-04502-2

Galen C, Plowright RC. 1987. Testing the accuracy of using peroxidase activity to indicate stigma receptivity. Canadian Journal of Botany 65: 107-111. DOI:

Godinez-Álvarez H, Jiménez M, Mendoza M, Pérez F, Roldán P, Ríos-Casanova L, Lira R. 2008. Densidad, estructura poblacional, reproducción y supervivencia de cuatro especies de plantas útiles en el Valle de Tehuacán, México. Revista Mexicana de Biodiversidad 79: 393-403. DOI:

Goodwillie C, Kalisz S, Eckert CG. 2005. The evolutionary enigma of mixed mating systems in plants: occurrence, theoretical explanations, and empirical evidence. Annual Review of Ecology, Evolution, and Systematics 36: 47-79. DOI:

Güemes J, Boscaiu M. 2001. The breeding system of Fumana ericifolia: first evidence of autogamy in woody Cistaceae. Nordic Journal of Botany 21: 467-474. DOI:

Herlihy CR, Eckert CG. 2002. Genetic cost of reproductive assurance in a self-fertilizing plant. Nature 416: 320-323. DOI:

Hidalgo O, Gleissberg S. 2010. Evolution of reproductive morphology in the Papaveraceae s. l. (Papaveraceae and Fumariaceae, Ranunculales). International Journal of Plant Developmental Biology 4: 76-85.

Husband BC, Schemske DW. 1996. Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50: 54-70. DOI:

INEGI [Instituto Nacional de Estadística y Geografía]. 2021. Aspectos geográficos. CDMX. (accessed November 2021)

Kalisz S, Vogler DW, Hanley KM. 2004. Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430: 884-887. DOI:

Karlsson LM, Tamado T, Milberg P. 2003. Seed dormancy pattern of the annuals Argemone ochroleuca and A. mexicana (Papaveraceae). Flora 198: 329-339. DOI:

Kassambara A. 2020. rstatix: pipe-friendly framework for basic statistical tests. R package version 0.4.0.

Kephart SR, Brown E, Hall J. 1999. Inbreeding depression and partial selfing: evolutionary implications of mixed-mating in a coastal endemic Silene douglasii var. oraria (Caryophyllaceae). Heredity 82: 543-554. DOI:

Knight TM, Steets JA, Vamosi JC, Mazer SJ, Burd M, Campbell DR, Dudash MR, Johnston MO, Mitchel RJ, Ashman TL. 2005. Pollen limitation of plant reproduction: pattern and process. Annual Review of Ecology, Evolution and Systematics 36: 467-497. DOI:

Kumar S, Rohatgi N. 1999. The role of invasive weeds in changing floristic diversity. Annals of Forestry 7: 147-150.

Kwiatkowska M, Bohdanowicz J, Cuba?a M, S?omka A, ?abicka J, ?abicki P, Migda?ek G, Marcussen T, Thiele K, Kuta E. 2019. A new pollination system in non-cleistogamous species of Viola results from nyctinastic (night-closing) petal movements-A mixed outcrossing-selfing strategy. Flora 253: 1-9. DOI:

Lande R, Schemske DW. 1985. The evolution of self-fertilization and inbreeding depression in plants. I. Genetic Models. Evolution 39: 24-40. DOI:

León-Martínez G, Vielle-Calzada JP. 2019. Apomixis in flowering plants: Developmental and evolutionary considerations. Current topics in developmental biology 131: 565-604. DOI:

Lord EM. 1981. Cleistogamy: a tool for the study of floral morphogenesis, function and evolution. The Botanical Review 47: 421-449. DOI:

Lundqvist A. 1964. Frequency of specific incompatibility alleles in a population of Festaca pratensis Huds. Hereditas 52:189-196.

Lyon DL. 1992. Bee pollination of facultatively xenogamous Sanguinaria canadensis L. Bulletin of the Torrey Botanical Club 119: 368-375. DOI:

Márquez J, Wong R, Pérez M, López L, Munguía G. 2016. Técnicas de laboratorio para el estudio del desarrollo en angiospermas. Ciudad de México: Universidad Nacional Autónoma de México. ISBN: 978-607-02-8252-2.

Martin FW. 1959. Staining and observing pollen tubes in the style by means of fluorescence. Stain Technology 34: 125-128. DOI:

Martínez-Delgado AA, de Anda J, León-Morales JM, Mateos JC, Gutiérrez-Mora A, Castañeda-Nava JJ. 2022. Argemone species: Potential source of biofuel and high-value biological active compounds. Environmental Engineering Research 27: 200619. DOI:

McClure B, Cruz-García F, Romero C. 2011. Compatibility and incompatibility in S-RNase-based systems. Annals of Botany 108: 647-658. DOI:

Mitchell RJ. 1997. Effects of pollination intensity on Lesquerella fendleri seed set: variation among plants. Oecologia 109: 382-388. DOI:

Munoz F, Violle C, Cheptou P. 2016. CSR ecological strategies and plant mating systems: outcrossing increases with competitiveness but stress-tolerance is related to mixed mating. Oikos 125: 1296-1303. DOI:

Ohara M, Higashi S. 1994. Effects of inflorescence size on visits from pollinators and seed set of Corydalis ambigua (Papaveraceae). Oecologia 98: 25-30. DOI:

Paape T, Miyake T, Takebayashi N, Wolf D, Kohn JR. 2011. Evolutionary genetics of an S-like polymorphism in Papaveraceae with putative function in self-incompatibility. Plos One 6: e23635. DOI:

Porcher E, Lande R. 2005. Reproductive compensation in the evolution of plant mating systems. New Phytologist 166: 673-684. DOI:

R Core Team. 2019. R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. URL

Radosevich SR, Holt JS, Ghersa C. 1997. Weed ecology: implications for management. New York: John Wiley & Sons.

Reyes FD, Peña CJ, Canales M, Jiménez M, Meraz S, Hernández T. 2011. Antimicrobial activity of Argemone ochroleuca Sweet (Chicalote). Boletín Latinoamericano y del Caribe de Plantas Medicinales y Aromáticas 10: 139-146.

Ruan C-J, Li H, Mopper S. 2009. Kosteletzkya virginica displays mixed mating in response to the pollinator environment despite strong inbreeding depression. Plant Ecology 203: 183-193. DOI:

Ruan C-J, Qin P, Teixeira da Silva JA. 2011. Relationship between reproductive assurance and mixed mating in perennial Kosteletzkya virginica. South African Journal of Botany 77: 280-291. DOI:

Ruiz de Clavijo E, Jimenez MJ. 1993. Cleistogamy and chasmogamy in Ceratocapnos heterocarpa (Fumariaceae). International Journal of Plant Sciences 154: 325-333. DOI:

Salinas MJ, Suárez V. 2003. Reproductive biology of Sarcocapnos pulcherrima Morales & Romero (Fumariaceae), a threatened species. Acta Botanica Gallica 150: 137-146. DOI:

Sauquet H. 2021. Evolution: Cleistogamy to the rescue of zygomorphic flowers. Current Biology 31: R332-R335. DOI:

Schwarzbach AE, Kadereit JW. 1999. Phylogeny of prickly poppies, Argemone (Papaveraceae), and the evolution of morphological and alkaloid characters based on ITS nrDNA sequence variation. Plant Systematics and Evolution 218: 257-279. DOI:

Shivanna KR. 2014. Reproductive assurance through autogamy in some annual weed species. Proceedings of the National Academy of Sciences, India Section B: Biological Sciences 84: 681-687. DOI:

Tepedino VJ, Mull J, Griswold TL, Bryant G. 2014. Reproduction and pollination of the endangered dwarf bear-poppy Arctomecon humilis (Papaveraceae) across a quarter century: unraveling of a pollination web? Western North American Naturalist 74: 311-324. DOI:

van Doorn WG, Van Meeteren U. 2003. Flower opening and closure: A review. Journal of Experimental Botany 54: 1801-1812. DOI:

Veena V, Nampy S. 2019. Induced cleistogamy: A strategy for reproductive assurance in Murdannia nudiflora (Commelinaceae). Botany 97: 547-557. DOI:

Van Etten ML, Conner JK, Chang SM, Baucom RS. 2017. Not all weeds are created equal: A database approach uncovers differences in the sexual system of native and introduced weeds. Ecology and Evolution 7: 2636-2642. DOI:

Weiping L, Shengxiang L. 1997. Reproductive ecology of Corydalis sheareri var. bulbillifera (Papaveraceae). Journal of Central China Normal University 31: 87-91.

Whitehead MR, Lanfear R, Mitchell RJ, Karron JD. 2018. Plant mating systems often vary widely among populations. Frontiers in Ecology and Evolution 6: 38. DOI:

Winn A, Elle E, Kalisz S, Cheptou P, Eckert GC, Goodwillie C, Johnston MO, Moeller DA, Ree RH, Sargent RD, Vallejo-Marín M. 2011. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution 65: 3339-3359. DOI:

Xiao Y, Chen X, Hu X, Dong M. 2016. Pollination ecology of Eomecon chionantha Hance (Papaveraceae), an endemic species in China. Russian Journal of Ecology 47: 249-258. DOI:

Yang S, Chu G, Shi X, Wang S. 2019. Elaborated pollen packaging and dispensing mechanism induced by petal architecture from a Papaveraceae species. PeerJ 7: e7066. DOI:

Yun W, Yu-Rong L, Han P, Yong Y, Guang-Li L, Guo-Xing C, Qiang Z. 2015. Pollination ecology of alpine herb Meconopsis integrifolia at different altitudes. Chinese Journal of Plant Ecology 39: 1-13. DOI:

Zhang Y, Wu H., Hörandl E, de Oliveira Franca R, Wang L, Hao J. 2021. Autonomous apomixis in Praxelis clematidea (Asteraceae: Eupatorieae), an invasive alien plant. AoB Plants 13: plab007. DOI:

How to Cite
Rios-Carrasco, S., & Vázquez-Santana, S. (2022). The mixed mating system of a widespread weed: the case of Argemone ochroleuca Sweet (Papaveraceae). Botanical Sciences, 100(4), 814-826.