Breeding system in a population of the globose cactus Mammillaria magnimamma at Valle del Mezquital, Mexico

keywords: floral morphometry, germination rate, gynodioecy, pollinator, scanning electron microscopy

Abstract

Background: The breeding system of Mammillaria magnimamma was initially described as hermaphroditic. However, some individuals in a natural population at Valle del Mezquital exhibited a seemingly non-functional androecium.

Objectives: To determine the breeding system of M. magnimamma through morphological characterization of floral types.

Study site and years: The study was conducted at Valle del Mezquital, Mexico, during the 2019 reproductive season.

Methods: We characterized floral polymorphism by means of scanning electron microscopy and morphometric analysis of 18 floral traits. Pollinator frequency, size and number of seeds, and germination rate were compared between flower types.

Results: 87.85 % of the plants were hermaphrodites, and 12.15 % were females with non-functional androecium, with significantly smaller stamens, indehiscent anthers, and malformed pollen. Female flowers were shorter (14.007 ± 0.742 mm) and had smaller (1.856 ± 0.151 mm) nectar chambers than hermaphroditic flowers (15.821 ± 0.450 and 2.194 ± 0.090 mm, respectively). Although pollinators visited hermaphrodites (124 visits) about twice as often as pistillate flowers (60 visits), the latter produced more numerous (F1,26 = 8.320, P = 0.003) and larger  (Hc = 4.637, P = 0.031) seeds that also germinated faster (Hc = 70.59, P < 0.0001).

Conclusions: This M. magnimamma population exhibits a gynodioecious breeding system with both hermaphroditic and male sterile female plants. Females produce more, higher quality seeds, which favour their maintenance in the population.

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Breeding system in a population of the globose cactus <em>Mammillaria magnimamma</em> at Valle del Mezquital, Mexico

References

Addinsoft. 2019. Statistical and data analysis solution XLSTAT. New York, USA. USA. (accessed 28 May 2019).
Agren J, Elmqvist T, Tunlid A.1986. Pollination by deceit, floral sex ratios and seed set in dioecious Rubus chamaemorus L. Oecologia 70: 332-338. DOI: 10.1007/BF00379493.
Almeida OJG, Cota-Sánchez JH, Paoli AAS. 2013. The systematic significance of floral morphology, nectaries, and sugar nectar concentration in epiphytic cacti of tribes Hylocereeae and Rhipsalideae (Cactaceae). Perspectives in Plant Ecology Evolution and Systematics 15: 255–268. http://dx.doi.org/10.1016/j.ppees.2013.08.001
Armstrong JE. 1997. Pollination by deceit in nutmeg (Myristicainsipida, Myristicaceae): floral displays and beetle activity at male and female trees. American Journal of Botany 84: 1266-1274. https://doi.org/10.2307/2446051
Ashman TL. 2006. The evolution of separate sexes: a focus on the ecological context. In: Harder L.D. and Barrettt S.C.H. Eds. Ecology and evolution of flowers, pp. 204-222, Oxford University Press, UK. ISBN-13: 978-0198570868, ISBN-10: 0198570864
Baker M. 2006. A new florally dimorphic hexaploid, Echinocereus yavapaiensis sp.nov. (section Triglochidiatus, Cactaceae) from central Arizona. Plant Systematic and Evolution 258: 63-83. DOI: 10.1007/s00606-005-0390-9
Baker MA and Cloud-Hughes MA. 2014. Cylindropuntia chuckwallensis (Cactaceae), a new species from Riverside and Imperial Counties, California. Madroño 61: 231-243. https://doi.org/10.3120/0024-9637-61.2.231
Barrett SCH, Harder LD, Worley AC. 1996. The comparative biology of pollination and mating in flowering plants. Philosophical Transactions of the Royal Society of London B 351: 1271-1280. https://doi.org/10.1098/rstb.1996.0110
Barrett SCH. 2002. The evolution of plant sexual diversity. Nature Reviews Genetics 3: 274-284. DOI: 10.1038/nrg776
Barrett SCH and Hough J. 2013. Sexual dimorphism in flowering plants. Journal of Experimental Botany 64: 67-82. DOI:10.1093/jxb/ers308
Barrett SCH. 2015. Influences of clonality on plant sexual reproduction. Proceedings of the National Academy of Sciences 112: 8859-8866. doi/10.1073/pnas.1501712112
Camacho VA, Ríos CS, and Vázquez SS. 2016. Reproductive biology of the subfamily Cactoideae (Cactaceae). Cactáceas y Suculentas Mexicanas 61: 100-127.
ISSN 0526-717X
Case AL and Barrett SC. 2004. Environmental stress and the evolution of dioecy: Wurmbea dioica (Colchicaceae) in Western Australia. Evolutionary Ecology 18:145–164. https://doi.org/10.1023/B:EVEC.0000021152.34483.77
Charlesworth D and Charlesworth B. 1981. Allocation of resources to male and female functions in hermaphrodites. Biological Journal of the Linnean Society 15: 57-74. https://doi.org/10.1111/j.1095-8312.1981.tb00748.x
Charlesworth D and Charlesworth B. 1987. Inbreeding depression and its evolutionary consequences. Annual Review of Ecology and Systematics 18: 237-268. https://doi.org/10.1146/annurev.es.18.110187.001321
Costich DE. 1995. Gender specialization across a climatic gradient: Experimental comparison of monoecious and dioecious Ecballium. Ecology 76: 1036-1050. https://doi.org/10.2307/1940914
Del Castillo RF and Trujillo-Argueta S. 2009. Reproductive implications of combined and separate sexes in a trioecious population of Opuntia robusta (Cactaceae). American Journal of Botany 96: 1148-1158. DOI:10.3732/ajb.0800301
Delph LF and Wolf DE. 2005. Evolutionary consequences of gender plasticity in genetically dimorphic breeding systems New Phytologist 166: 119-128.
DOI: 10.1111/j.1469-8137.2005.01339.x
Diaz L and Cocucci AA. 2003. Funcional gynodioecy in Opuntia quimilo (Cactaceae), a tree cactus pollinated by bees and hummingbirds. Plant Biology 5: 531-539.
https://doi.org/10.1055/s-2003-44783
Fleming TH, Maurice S, Buchmann SL, and Tuttle MD. 1994. Reproductive biology and relative male and female fitness in a trioecious cactus, Pachycereus pringlei (Cactaceae). American Journal of Botany 81: 858-867. https://doi.org/10.1002/j.1537-2197.1994.tb15567.x
Geber MA. 1999. Theories of the evolution of sexual dimorphism. In: Geber M.A., Dawson T.E., and Delph L.F. Eds. Gender and sexual dimorphism in flowering plants, pp. 97-122, Springer-Verlag Berlin Heidelberg, New York. ISBN-10: 3540645977 ISBN-13: 978-3540645979
Gutiérrez-Flores C, Cota-Sánchez JH, León-de la Luz JL, and Garcia-de León FJ. 2017. Disparity in floral traits and breeding systems in the iconic columnar cactus Pachycereus pringlei (Cactaceae). Flora 235: 18-28. https://doi.org/10.1016/j.flora.2017.08.007
Hammer, Ø., D. A. T. Harper, and P. D. Ryan. 2001. PAST: Paleontological statistics software package for education and data analysis. Palaeontologia Electronica 4: 19.

Hernández H.M. and Gómez-Hinostrosa C. 2015. Mapping the cacti of Mexico. Part II. Mammillaria. Succulent Plant Research, DH Books, Milborne Port England. 189 pp. ISBN 13: 9780993311314, ISBN 10: 0993311318
Hoffman MT. 1992. Functional dioecy in Echinocereus coccineus (Cactaceae): breeding systems, sex ratios, and geographic range of floral dimorphism. American Journal of Botany 79: 1382-1388. https://doi.org/10.1002/j.1537-2197.1992.tb13748.x
Kaul M. 1988. Male sterility in higher plants. Monographs on Theoretical and Applied Genetics, vol. 10 Springer- Verlag, Berlin-Heidelberg. ISBN 978-3-642-83141-6, eISBN 978-3-642-83139-3
Lindsay G, and Dawson EY. 1952. Mammillarias of the islands of Northwestern Baja California, México. Cactus and Succulent Journal 24: 76-84. ISSN: 0007-9367. eISSN: 1938-288X
Lloyd DG and Webb CJ. 1977. Secondary sex characters in plants. The Botanical Review 43: 177-216. https://doi.org/10.1007/BF02860717
Mandujano MC, Carrillo AI, Martínez PC and Golubov J. 2010. Reproductive biology of Cactaceae. In: Ramawat K.G. Ed. Desert Plants: Biology and biotechnology, pp. 197-230, Springer-Verlag Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02550-1_10
Martínez-Peralta C, Molina-Freaner F, Golubov J, Vázquez-Lobo A and Mandujano MC. 2014. A comparative study of the reproductive traits and floral morphology of a genus of geophytic cacti. International Journal of Plant Sciences 175: 663-680. http://www.jstor.org/stable/10.1086/676302 .
Martínez-Ramos M, Arroyo-Cosultchi G, Golubov J and Mandujano MC. 2015. Fenología y sistema de apareamiento de Mammillaria humboldtii: una especie en peligro de extinción. Cactáceas y Suculentas Mexicanas, 60: 80-90. ISSN 0526-717X
Parfitt BD. 1985. Dioecy in North American Cactaceae: a review. SIDA Contributions of Botany 11: 200-206. ISSN: 0036-1488
Ramsey and Glenda Vaughton G. 2001. Sex expression and sexual dimorphism in subdioecious Wurmbea dioica (Colchicaceae). International Journal of Plant Sciences 162: 589-597. DOI: 10.1086/320142
Rebman JP. 1998. A new cholla (Cactaceae) from Baja California, Mexico. Haseltonia 6: 17-21
Rebman JP. 2001. The succulents of Islote Toro, Baja California, Mexico. Cactaceas y Suculentas Mexicanas 46: 52-55. ISSN 0526-717X
Sánchez D and Vázquez SS. 2018. Embryology of Mammillaria dioica (Cactaceae) reveals a new male sterility phenotype. Flora 241: 16-26. https://doi.org/10.1016/j.flora.2018.02.007
SEMARNAT. 2013. Programa de Ordenamiento Ecológico de la Región de Río San Juan, en los municipios de Tecozautla, Huichapan, Nopala de Villagran, Chapantongo y Alfajayucan en el Estado de Hidalgo. SEMARNAT, Ordenamiento Ecológico Territorial, Universidad Autónoma de Morelos. Hidalgo, México.
Shykoff JA, Kolokotronis SO, Collin CL and López VM. 2003. Effects of male sterility on reproductive traits in gynodioecious plants: a meta-analysis. Oecologia 135: 1-9.
DOI: 10.1007/s00442-002-1133-z
Spigler RB and Ashman TL. 2012. Gynodioecy to dioecy: are we there yet? Annals of Botany 109: 531-543. DOI:10.1093/aob/mcr170
Valverde T, Quijas S, López-Villavicencio M and Castillo S. 2004. Population dynamics of Mammillaria magnimamma Haworth. (Cactaceae) in a lava-field in central Mexico. Plant Ecology 170: 167-184. https://doi.org/10.1023/B:VEGE.0000021662.78634.de
Zar J.H. 2001. Biostatical Analysis, second edition. Prentice Hall, New York, New York, USA. ISBN: 978-0-13-100846-5
Published
2021-02-14
How to Cite
Callejas-Chavero, A., Vargas-Mendoza, C. F., Gomez-Hinostrosa, C., Arriola-Padilla, V. J., & Cornejo-Romero, A. (2021). Breeding system in a population of the globose cactus Mammillaria magnimamma at Valle del Mezquital, Mexico. Botanical Sciences, 99(2), 229-241. https://doi.org/10.17129/botsci.2654
Section
ECOLOGY / ECOLOGÍA