On the origin of the two putative allopolyploids, Opuntia curvispina and O. martiniana (Cactaceae): A case of cryptic speciation in prickly pear cacti

  • Lucas C. Majure University of Florida Herbarium
Keywords: Haplotypes, Hybridization, Opuntia chlorotica, Phylogenetics, Polyploidy

Abstract

The putative allopolyploid taxon, Opuntia curvispina, is distributed from northeastern Arizona and southern Nevada to southeastern California, where it often grows in close proximity to, or sympatric with, O. chlorotica, O. engelmannii and O. phaeacantha. Another putative allopolyploid, O. martiniana, grows sympatrically with O. curvispina in only one area north of the Hualapai Mts., northwestern Arizona. Both of these taxa have previously been treated as either nothospecies or mere spontaneous hybrids by previous researchers. My objectives were to determine the origins of both O. curvispina and O. martiniana to test previous hypotheses of hybrid origin, with O. curvispina putatively derived from O. chlorotica and O. phaeacantha and O. martiniana putatively derived from O. chlorotica and O. engelmannii. I also wanted to determine the overall extent of the ranges of the two taxa by expanding collections and verifying existing herbarium collections, as numerous specimens identified as O. martiniana and O. curvispina have been reported from outside of their expected ranges. My data indicate that O. curvispina indeed is partially derived from O. chlorotica, as well as another putative parent, likely O. phaeacantha, while O. martiniana appears to be most likely derived from O. curvispina and O. macrorhiza, two taxa not before implicated in the origin of O. martiniana. The hexaploid O. phaeacantha also appears to be non-monophyletic and may have been derived several times from different hybridization events. Careful morphological study of O. martiniana clearly separates that species from O. curvispina, although it may be considered cryptically different, a likely result of its partial putative origin from O. curvispina. Given the very broad distribution and dominance of O. curvispina in parts of its range, it is most appropriate to recognize this allopolyploid as a species, rather than as a nothotaxon, as previously designated. The unique feature of an obovate or urceolate style in Opuntia martiniana appears to be a transgressive trait rather than a synapomorphy, given that the taxon is derived from reticulation, and neither putative parent exhibits that character state. This work provides a framework for species recognition using DNA sequence data, morphological characters, geography and cytological information—a total evidence approach clearly needed for taxonomically difficult taxa, such as many within the genus Opuntia. A treatment of O. curvispina and O. martiniana is given with updated descriptions, and O. martiniana is neotypified.

References

BAKER, M.A., D.J. PINKAVA, J.P. REBMAN, B.D. PARFITT, & A.D. ZIMMERMAN. 2009. Chromosome numbers in some cacti of western North America. VIII. Haseltonia 15:117–134.
BAKER, M.A. & M. CLOUD-HUGHES. 2014. Noteworthy collections. Madroño 61:411–412.
BAKER, M.A. & D.J. PINKAVA. 2018. Chromosome numbers in some cacti of western North America—IX. Haseltonia 25:5–29.
BAO, Y., J.F. WENDEL, & S. GE. 2010. Multiple patterns of rDNA evolution following polyploidy in Oryza. Molec. Phylogen. Evol. 55:136–142.
BENSON, L.D. 1950. The cacti of Arizona, 2nd Edition. University of Arizona Press, Tucson, AZ, U.S.A.
BENSON, L.D. 1982. The cacti of the United States and Canada. Stanford University Press, Stanford, CA, U.S.A.
BENSON, L.D. & D.L. WALKINGTON 1965. The southern Californian prickly pears—invasion, adulteration and trial by fire. Ann. Missouri Bot. Gard. 52:262–273.
BRITTON, N.L. & J.N. ROSE. 1920. The Cactaceae: Descriptions and illustrations of the cactus family. Publ. No. 248. The Carnegie Institution of Washington, Washington, U.S.A.
CROOK, R. & R. MOTTRAM. 1996. Opuntia Index Part 2: Nomenclatural note and C–E. Bradleya 14:99–144.
DOYLE, J.J. & J.L. DOYLE. 1987. A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem. Bull. Bot. Soc. Amer. 19:11–15.
ENGELMANN, G. 1856. Synopsis of the Cactaceae of the territory of the United States and adjacent regions. Proc. Amer. Acad. Arts. 3:259–311.
FELINER, G.N. & J.A. ROSELLÓ. 2007. Better the devil you know? Guidelines for insightful utilization of nrDNA ITS in species-level evolutionary studies in plants. Molec. Phylogen. Evol. 44:911–919.
FOSBERG, F.R. 1934. The southern California prickly pears. Bull. South. Calif. Acad. Sci. 33:93–104.
GRIFFITHS, D. 1916. New species of Opuntia. Bull. Torrey Bot. Club 43:83–92.
HODKINSON, T.R., M.W. CHASE, C. TAKAHASHI, I.J. LEITCH, M.D. BENNETT, & S.A. RENVOIZE. 2002. The use of dna sequencing (ITS and trnL-F), AFLP, and fluorescent in situ hybridization to study allopolyploid Miscanthus (Poaceae). Amer. J. Bot. 89:279–286.
JUDD, W.S. 2007. Revision of Miconia sect. Chaenopleura (Miconieae, Melastomataceae) in the Greater Antilles. Syst. Bot. Monogr. 81:1–235.
MAJURE, L.C. 2021. On the origin of the two putative allopolyploids, Opuntia curvispina and O. martiniana (Cactaceae): A case of cryptic speciation in prickly pear cacti. (Data available on FigShare: 10.6084/m9.figshare.15143877).
MAJURE, L.C. & R. PUENTE. 2014. Phylogenetic relationships and morphological evolution in Opuntia s. str. and closely related members of tribe Opuntieae. Succ. Pl. Res. 8:9–30.
MAJURE, L.C., W.S. JUDD, P.S. SOLTIS, & D.E. SOLTIS. 2012a. Cytogeography of the Humifusa clade of Opuntia s.s. Mill. 1754 (Cactaceae: Opuntioi-deae): Correlations with geographic distributions and morphological differentiation of a polyploid complex. Comp. Cytogen. 6:53–77.
MAJURE, L.C., R. PUENTE, M.P. GRIFFITH, W.S. JUDD, P.S. SOLTIS, & D.S. SOLTIS. 2012b. Phylogeny of Opuntia s.s. (Cactaceae): Clade delineation, geo-graphic origins, and reticulate evolution. Amer. J. Bot. 99:847–864.
MAJURE, L.C., R. PUENTE, & D.J. PINKAVA. 2012c. Miscellaneous chromosome counts in Opuntieae DC. (Cactaceae) with a compilation of counts for the group. Haseltonia 18:67–78.
MAJURE, L.C., R. PUENTE, M.P. GRIFFITH, D.E. SOLTIS, & W.S. JUDD. 2013. Opuntia lilae, another Tacinga hidden in Opuntia s.l. Syst. Bot. 38:444–450.
MAJURE, L.C., D.E. SOLTIS, P.S. SOLTIS, & W.S. JUDD. (2013). 2014. A case of mistaken identity, Opuntia abjecta, long-lost in synonymy under the Caribbean species, O. triacantha, and a reassessment of the enigmatic O. cubensis. Brittonia 66:118–130. DOI 10.1007/s12228-013-9307-z.
MAJURE, L.C., W.S. JUDD, P.S. SOLTIS, & D.E. SOLTIS. 2017. A taxonomic revision of the Opuntia humifusa complex (Opuntia s.s.: Cactaceae). Phytotaxa 290:1–65.
MAJURE, L.C., M. BAKER, M. CLOUD-HUGHES, A. SALYWON, & K.M. NEUBIG. 2019. Phylogenomics in Cactaceae: A case study using the chollas sensu lato (Cylindropuntieae, Opuntioideae) reveals a common pattern out of the Chihuahuan/Sonoran desert. Amer. J. Bot. 106:1–19.
MAJURE, L.C., T. CLASE, Y. ENCARNACIÓN, B. PEGUERO, K. HO, & D. BARRIOS. 2021. Phylogenetics of Leptocereus (Cactaceae) on Hispaniola: Clarifying species limits in the L. weingartianus complex and a new species from the Sierra de Bahoruco. Phytokeys 172:17–37. https://doi.org/10.3897/phytokeys.172.59497
NEUBIG, K.M, W.M. WHITTEN, J.R. ABBOTT, S. ELLIOTT, D.E. SOLTIS, & P.S. SOLTIS. 2014. Variables affecting DNA preservation in archival DNA speci-mens. In: W.L. Applequist and L.M. Campbell, eds. DNA banking in the 21st Century: Proceedings of the U.S. workshop on DNA banking. St. Louis: The WilliamL. Brown Center at the Missouri Botanical Garden, St. Louis, Missouri, U.S.A.
PARFITT, B.D. 1980. Origin of Opuntia curvospina (Cactaceae). Syst. Bot. 5:408–418.
PINKAVA, D.J., M.G. MCLEOD, L.A. MCGILL, & R.C. BROWN. 1973. Chromosome numbers in some cacti of western North America—II. Brittonia 25:2–9.
PINKAVA, D.J. 2002. On the evolution of the North American Opuntioideae. In: Hunt, D. & N. Taylor, eds. Studies in the Opuntioideae (Cac-taceae). David Hunt, The Manse. Pp. 59–98.
PINKAVA, D.J. 2003. Cactaceae Jussieau subfam. Opuntioideae Burnett. In Flora of North America Editorial Committee, eds. Flora of North American north of Mexico, Magnoliophyta: Caryophyllidae. Oxford University Press, NY, U.S.A. 4(1):102–150.
POWELL, A.M. & J.F. WEEDIN. 2004. Cacti of the Trans-Pecos and adjacent areas. Texas Tech University Press, Lubbock, TX, U.S.A.
RIPMA, L.A., M.G. SIMPSON, & K. HASENSTAB-LEHMAN. 2014. Geneious! Simplified genome skimming methods for phylogenetic systematic studies: a case study in Oreocarya (Boraginaceae). App. Pl. Sci. 2:1400062.
STAMATAKIS, A. 2014. RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies. Bioinformatics 30:1312–1313.
STAPLES, G. & J. PRADO. 2018. Clarification is needed in the Code for the nomenclatural status of type specimen photographs. Taxon 67:833–835.
STEBBINS, G.L. 1959. The role of hybridization in evolution. Proc. Amer. Philos. Soc. 103:231–251.
STRAUB, S.C.K., M. PARKS, K. WEITHMIER, M. FISHBEIN, R.C. CRONN, & A. LISTON. 2012. Navigating the tip of the genomic iceberg: next-generation sequencing for plant systematics. Amer. J. Bot. 99:349–364.
THIERS, B. 2017. Index Herbariorum: a global directory of public herbaria and associated staff. New York Botanical Garden’s Virtual Herbarium. Website: http://sweetgum.nybg.org/scien ce/ih/.
TURLAND N.J., J.H. WIERSEMA, F.R. BARRIE, W. GREUTER, D.L. HAWKSWORTH, P.S. HERENDEEN, S.KNAPP, W.-H. KUSBER, D.-Z. LI, K. MARHOLD, T.W. MAY, J. MCNEILL, A.M. MONRO, J. PRADO, M.J. PRICE, & G.F. SMITH, EDS. 2018: International Code of Nomenclature for algae, fungi, and plants (Shenzhen Code) adopted by the Nineteenth International Botanical Congress Shenzhen, China, Jul 2017. Koeltz Botanical Books, Glashütten, Germany.
WHEELER, Q.D. & N.I. PLATNICK. 2000. The phylogenetic species concept (sensu Wheeler and Platnick). In: Q.D. Wheeler and R. Meier, eds. Species concepts and phylogenetic theory: A debate. Colombia University Press, New York, U.S.A. Pp. 55–69.
WHITE T.J., T. BRUNS, S. LEE, & J.W. TAYLOR. 1990. Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics. In: M.A. Innis, D.H. Gelfand, J.J. Sninsky, and T.J. White, eds. PCR protocols: A guide to methods and applications. Academic Press, San Diego, California, U.S.A. Pp. 315–322.
Published
2022-07-15
How to Cite
Majure, L. C. (2022). On the origin of the two putative allopolyploids, Opuntia curvispina and O. martiniana (Cactaceae): A case of cryptic speciation in prickly pear cacti. Journal of the Botanical Research Institute of Texas, 16(1), 317-333. https://doi.org/10.17348/jbrit.v16.i1.1235