Plant Ecology and Evolution 154(2): 217-230, doi: 10.5091/plecevo.2021.1773
Population expansion and genetic structure in Cephalocereus nizandensis (Cactaceae), a microendemic cactus of rocky outcrops of the Tehuantepec basin, Mexico
expand article infoAldo Isaac Juárez-Miranda, Amelia Cornejo-Romero§, Carlos Fabián Vargas-Mendoza|
‡ Departamento de Zoología, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional City, Mexico§ Departamento de Botánica, Escuela Nacional de Ciencias Biológicas, Instituto Politécnico Nacional City, Mexico| Escuela nacional de Ciencias Biológicas, Instituto Politécnico Nacional, Mexico, City, Mexico
Open Access

Background and aimsCephalocereus nizandensis is a microendemic columnar cactus that grows isolated in xerophytic enclaves associated with rocky outcrops in the Isthmus of Tehuantepec, in the south of Mexico. Its demographic history and genetic structure were assessed to determine the main events that shaped its current restricted distribution.

Material and methods – Chloroplast intergenic sequences of 40 individuals and inter simple sequence repeats (ISSRs) of 45 individuals from four isolated populations were used to estimate haplotypic and nucleotide diversity, using expected heterozygosity and the Shannon index. AMOVA, population pair-wise FST, and Bayesian clustering analyses were performed to explore the genetic structure. Demographic history was estimated with neutrality tests, mismatch distribution analysis, and Bayesian skyline plots. Phylogenetic relationships and divergence times were determined using a median joining network and a Bayesian molecular clock.

Key resultsC. nizandensis has a high diversity and moderate genetic differentiation. The lowest elevation locality was found to be the most genetically distinct. The species has undergone a process of population expansion that began 150,000 years ago and has remained without evidence of a population contraction in the transition from the Pleistocene to the Holocene (11,700 years ago).

ConclusionsC. nizandensis presents moderate but significant genetic differentiation, which may be due to an early divergence of its populations. Currently observed levels of genetic diversity are the result of historical maintenance of high population sizes and a population expansion approximately in the last 150,000 years, which was sustained independently of the climatic fluctuations of the Early Quaternary, due in part to the stability of the rocky habitat.

Cactaceae, historical population expansion, microendemism, Oaxaca, rocky outcrops


  • Alejos-Velázquez L.P. 2002. Estudio de la estructura poblacional de Neobuxbaumia macrocephala en Tehuacán-Cuicatlán, Puebla, mediante el uso de marcadores moleculares. Bachelor thesis. Facultad de Estudios Superiores Iztacala, UNAM, México. Available from [accessed 29 Mar. 2021].
  • Anderson E.F. 2001. The cactus family. Timber Press, Portland, USA.
  • Arakaki M., Christin P.A., Nyffeler R., et al. 2011. Contemporaneous and recent radiations of the world’s major succulent plant lineages. Proceedings of the National Academy of Sciences of the United States of America 108: 8379–8384.
  • Arbogast B.S., Edwards S.V., Wakeley J., Beerli P. & Slowinski J.B. 2002. Estimating divergence times from molecular data on phylogenetic and population genetic timescales. Annual Review of Ecology and Systematics 33: 707–740.
  • Arriaga L., Espinoza J.M., Aguilar C., Martínez E., Gómez L. & Loa E. 2000. Regiones terrestres prioritarias de México. Comisión Nacional para el Conocimiento y uso de la Biodiversidad, México.
  • Bárcenas-Argüello M.L., Gutiérrez-Castorena M.C., Terrazas T. & López-Mata L. 2010. Rock-soil preferences of three Cephalocereus (Cactaceae) species of tropical dry forests. Soil Science Society of America Journal 74: 1374–1382.
  • Bonatelli I.A.S., Perez M.F., Peterson A.T., et al. 2014. Interglacial microrefugia and diversification of a cactus species complex: phylogeography and palaeodistributional reconstructions for Pilosocereus aurisetus and allies. Molecular Ecology 23: 3044–3063.
  • Bravo-Hollis H. & Sánchez-Mejorada R. 1978. Las cactáceas de México, Vol. I. Second edition. UNAM, México.
  • Broadhurst L., Breed M., Lowe A., et al. 2017. Genetic diversity and structure of the Australian flora. Diversity and Distribution 23: 41–52.
  • Byrne M. 2008. Evidence for multiple refugia at different time scales during Pleistocene climatic oscillations in southern Australia inferred from phylogeography. Quaternary Science Reviews 27: 2576–2585.
  • Byrne M. & Hopper S.D. 2008. Granite outcrops as ancient islands in old landscapes: evidence from the phylogeography and population genetics of Eucalyptus caesia (Myrtaceae) in Western Australia. Biological Journal of the Linnean Society 93: 177–188.
  • Byrne M., Krauss S.L., Millar M.A., et al. 2019. Persistence and stochasticity are key determinants of genetic diversity in plants associated with banded iron formation inselbergs. Biological Reviews 94: 753–772.
  • Buxbaum F. 1965. Die Tribus Pachycereae F.Buxb. und ihre Entwicklungswege (Fortsetzung IV). Kakteen und Andere Sukkulenten 16(3): 42–45.
  • Castro-Felix P., Rosas-Espinoza V.C., Díaz-Cardenas B., Pérez-Valencia L.I., Huerta-Martínez F. & Santerre A. 2014. Genetic diversity within a declining natural population of Ferocactus histrix (DC) Lindsay. Plant Species Biology 29: e21–e30.
  • Clark-Tapia R. & Molina-Freaner F. 2003. The genetic structure of a columnar cactus with a disjunct distribution: Stenocereus gummosus in the Sonoran desert. Heredity 90: 443–450.
  • Clark‐Tapia R., Alfonso‐Corrado C., Eguiarte L.E. & Molina‐Freaner F. 2005. Clonal diversity and distribution in Stenocereus eruca (Cactaceae), a narrow endemic cactus of the Sonoran Desert. American Journal of Botany 92(2): 272–278.
  • Corander J., Waldmann P. & Sillanpää M.J. 2003. Bayesian analysis of genetic differentiation between populations. Genetics 163: 367–374. Available from [accessed 29 Mar. 2021].
  • Cornejo-Romero A. 2004. Diversidad genética y estructura clonal de Stenocereus stellatus (Cactaceae), en una cronosecuencia edáfica del valle de Tehuacán. MSc thesis, UNAM, Mexico.
  • Cornejo-Romero A., Medina-Sánchez J., Hernández-Hernández T., et al. 2014. Quaternary origin and genetic divergence of the endemic cactus Mammillaria pectinifera in a changing landscape in the Tehuacán Valley, Mexico. Genetics and Molecular Research 13: 73–88.
  • Cornejo-Romero A., Vargas-Mendoza C.F., Aguilar-Martínez G.F., et al. 2017. Alternative glacial-interglacial refugia demographic hypotheses tested on Cephalocereus columna-trajani (Cactaceae) in the intertropical Mexican drylands. PLOS ONE 12(4): e0175905.
  • Couper P.J. & Hoskin C.J. 2008. Litho-refugia: the importance of rock landscapes for the long-term persistence of Australian rainforest fauna. Australian Zoologist 34: 554–560.
  • Crowther J. 1982. Ecological observations in a tropical karst terrain, West Malaysia. I. Variations in topography, soils and vegetation. Journal of Biogeography 9(1): 65–78.
  • de Aguiar-Campos N., Maia V.A., da Silva W.B. de Souza C.R. & dos Santos R.M. 2020. Can fine-scale habitats of limestone outcrops be considered litho-refugia for dry forest tree lineages? Biodiversity and Conservation 29: 1009–1026.
  • Drummond A.J., Rambaut A., Shapiro B. & Pybus O.G. 2005. Bayesian coalescent inference of past population dynamics from molecular sequences. Molecular Biology and Evolution 22: 1185–1192.
  • Drummond A.J., Rambaut A. & Suchard M.A. 2018. BEAST. Bayesian evolutionary analysis sampling trees version v1.10.4 Prerelease #bc6cbd9. Available from [accessed 29 Mar. 2021].
  • Earl D.A. & von Holdt B.M. 2012. STRUCTURE HARVESTER: a website and program for visualizing STRUCTURE output and implementing the Evanno method. Conservation Genetics Resources 4: 359–361.
  • Excoffier L. & Lischer H.E.L. 2010. Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Molecular Ecology Resources 10: 564–567.
  • Figueredo C.J., Nassar J.M., García-Rivas A.E. & González-Carcacía J.A. 2010. Population genetic diversity and structure of Pilosocereus tillianus (Cactaceae, Cereeae), a columnar cactus endemic to the Venezuelan Andes. Journal of Arid Environments 11: 1392–1398.
  • Fluxus Technology 2014. Free Phylogenetic Network Software. Version Fluxus Technology Ltd. Available from [accessed 2 Apr. 2021].
  • Franco F.F., Silva G.A.R., Moraes E.M., et al. 2017. Plio-Pleistocene diversification of Cereus (Cactaceae, Cereeae) and closely allied genera. Botanical Journal of the Linnean Society 183: 199–210.
  • Fu Y.X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection. Genetics 147: 915–925. Available from [accessed 29 Mar. 2021].
  • Gámez N., Escalante T., Espinosa D., Eguiarte L.E. & Morrone J.J. 2014. Temporal dynamics of areas of endemism under climate change: a case study of Mexican Bursera (Burseraceae). Journal of Biogeography 41: 871–881.
  • Ganopoulos I.K., Xanthopoulou A., Mastrogianni A., Koubouris G. & Madesis P. 2015. Genetic diversity of Barbary fig (Opuntia ficus-indica) collection in Greece with ISSR molecular markers. Plant Gene 2: 29–33.
  • García M.B., Domingo D., Pizarro M., Font X., Gómez D. & Ehrlén J. 2020. Rocky habitats as microclimatic refuges for biodiversity. A close-up thermal approach. Environmental and Experimental Botany 170: 103886.
  • Gitzendanner M.A. & Soltis P.S. 2000. Patterns of genetic variation in rare and widespread plant congeners. American journal of botany 87: 783–792.
  • Good-Avila S.V., Souza V., Gaut B.S. & Eguiarte L.E. 2006. Timing and rate of speciation in Agave (Agavaceae). Proceedings of the National Academy of Sciences of the United States of America 103: 9124–9129.
  • Gutiérrez-Flores C., García-De León F.J., León-de la luz J.L. & Cota-Sánchez J.H. 2016. Microsatellite genetic diversity and mating systems in the columnar cactus Pachycereus pringlei (Cactaceae). Perspectives in Plant Ecology, Evolution and Systematics 22: 1–10.
  • Hamrick J.L. & Godt M.J. 1996. Effects of life history traits on genetic diversity in plant species. Philosophical Transactions of the Royal Society B: Biological Sciences 351: 1291–1298.
  • Hamrick J.L., Nason J.D., Fleming T.H. & Nassar J.M. 2002. Genetic diversity in columnar cacti. In: Fleming T.H. & Valiente-Banuet A. (eds) Columnar cacti and their mutualists: evolution, ecology, and conservation: 93–108. University of Arizona Press, Tucson, USA.
  • Hasegawa M., Kishino H. & Yano T. 1985. Dating of the human-ape splitting by a molecular clock of mitochondrial DNA. Journal of Molecular Evolution 22: 160–174.
  • Hernández‐Hernández T., Brown J.W., Schlumpberger B.O., Eguiarte L.E. & Magallón S. 2014. Beyond aridification: multiple explanations for the elevated diversification of cacti in the New world succulent biome. New Phytologist 202: 1382–1397. /
  • Khan G., Ribeiro P.M., Bonatelli I.A.S., Perez M.F., Franco F.F. & Moraes E.M. 2018. Weak population structure and no genetic erosion in Pilosocereus aureispinus: a microendemic and threatened cactus species from eastern Brazil. PLOS ONE 13(4): e0195475.
  • Khattab S., El Sherif F., El-Garhy H.A., Ahmed S. & Ibrahim A. 2014. Genetic and phytochemical analysis of the in vitro regenerated Pilosocereus robinii by ISSR, SDS-PAGE and HPLC. Gene 533: 313–321.
  • Kim E. & Donohue K. 2013. Local adaptation and plasticity of Erysimum capitatum to altitude: its implications for responses to climate change. Journal of Ecology 101: 796–805.
  • Kumar S., Stecher G. & Tamura K. 2016. MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Molecular Biology and Evolution 33: 1870–1874.
  • Ledig F.T., Conkle M.T., Bermejo‐Velázquez B., et al. 1999. Evidence for an extreme bottleneck in a rare Mexican pinyon: genetic diversity, disequilibrium, and the mating system in Pinus maximartinezii. Evolution 53: 91–99.
  • Ledig F.T., Capó‐Arteaga M.A., Hodgskiss P.D., et al. 2001. Genetic diversity and the mating system of a rare Mexican piñon, Pinus pinceana, and a comparison with Pinus maximartinezii (Pinaceae). American Journal of Botany 88: 1977–1987.
  • Locosselli G.M., Cardim R.H. & Ceccantini G. 2016. Rock outcrops reduce temperature-induced stress for tropical conifer by decoupling regional climate in the semiarid environment. International Journal of Biometeorology 60: 639–649.
  • Mandujano M. del C., Carrillo-Angeles I., Martínez-Peralta C. & Golubov J. 2010. Reproductive biology of cactaceae. In: Ramawat K. (ed.) Desert plants: 197–230. Springer, Berlin, Germany.
  • Millar M.A., Byrne M., Coates D.J. & Roberts J.D. 2017. Comparative analysis indicates historical persistence and contrasting contemporary structure in sympatric woody perennials of semi-arid south-west Western Australia. Biological Journal of the Linnean Society 120: 771–787.
  • Moraes E.M., Abreu A.G., Andrade S.C., Sene F.M. & Solferini V.N. 2005. Population genetic structure of two columnar cacti with a patchy distribution in eastern Brazil. Genetica 125: 311–323.
  • Nason J.D., Hamrick J.L. & Fleming T.H. 2002. Historical vicariance and postglacial colonization effects on the evolution of genetic structure in Lophocereus, a Sonoran Desert columnar cactus. Evolution 56: 2214–2226.
  • Nassar J.M., Hamrick J.L. & Fleming T.H. 2003. Population genetic structure of Venezuelan chiropterophilous columnar cacti (Cactaceae). American Journal of Botany 90: 1628–1637.
  • Nistelberger H.M., Byrne M., Coates D. & Roberts J.D. 2015. Phylogeography and population differentiation in terrestrial island populations of Banksia arborea (Proteaceae). Biological Journal of the Linnean Society 114: 860–872.
  • Ornelas J.F. & Rodríguez-Gómez F. 2015. Influence of Pleistocene glacial/interglacial cycles on the genetic structure of the mistletoe cactus Rhipsalis baccifera (Cactaceae) in Mesoamerica. Journal of Heredity 106: 196–210.
  • Palleiro-Dutrenit N. 2008. Estructura poblacional y genética del cactus columnar Cephalocereus totolapensis (Bravo et MacDougall) en el Estado de Oaxaca, México. MSc thesis, UNAM, Mexico. Available from [accessed 29 Mar. 2021].
  • Pérez-García E.A. 2002. Enclaves de vegetación xerofítica en regiones mésicas: caracterización, análisis de su diversidad florística e importancia en el mantenimiento de floras xerofíticas. MSc thesis, UNAM, Mexico. Available from [accessed 29 Mar. 2021].
  • Perez M., Bonatelli I., Moraes E. & Carstens M.E. 2016. Model-based analysis supports interglacial refugia over long-dispersal events in the diversification of two South American cactus species. Heredity 116: 550–557.
  • Pérez-García E.A. & Meave J.A. 2005. Heterogeneity of xerophytic vegetation of limestone outcrops in a tropical deciduous forest region in southern México. Plant Ecology 175: 147–163.
  • Pérez-García E.A., Meave J.A., Villaseñor J.L., Gallardo-Cruz J.A., & Lebrija-Trejos E.E. 2010. Vegetation heterogeneity and life-strategy diversity in the flora of the heterogeneous landscape of Nizanda, Oaxaca, Mexico. Folia Geobotanica 45: 143–161.
  • Pérez-García E.A., Sevilha A.C., Meave J.A. & Scariot A. 2009. Floristic differentiation in limestone outcrops of southern Mexico and central Brazil: a beta diversity approach. Boletín de la Sociedad Botánica de México 84: 45–58.
  • Pezoa A. 2001. Estrategias de conservación de la diversidad biológica. In: Squeo F.A., Arancio G. & Gutiérrez J.R. (eds) Libro rojo de la flora nativa y de los sitios prioritarios para su conservación: región de Coquimbo: 273–280. Ediciones Universidad de La Serena, La Serena, Chile. Available from [accessed 29 Mar. 2021].
  • Porembski S. & Barthlott W. 2000. Granitic and gneissic outcrops (inselbergs) as centers of diversity for desiccation-tolerant vascular plants. Plant Ecology 151: 19–28.
  • Pritchard J.K., Stephens M. & Donnelly P. 2000. Inference of population structure using multilocus genotype data. Genetics 155: 945–959.
  • Quipildor V.B., Kitzberger T., Ortega‐Baes P., Quiroga M.P. & Premoli A.C. 2017. Regional climate oscillations and local topography shape genetic polymorphisms and distribution of the giant columnar cactus Echinopsis terscheckii in drylands of the tropical Andes. Journal of Biogeography 45: 116–126.
  • Rambaut A. 2018. FigTree. Tree figure drawing toll version 1.4.4. Available from [accessed 9 Sep. 2019].
  • Rambaut A. & Drummond A.J. 2018. TREEANNOTATOR v1.10.4 Prerelease #bc6cbd9. In: BEAST package. Available from [accessed 29 Mar. 2021].
  • Rambaut A., Drummond A.J., Xie D., Baele G. & Suchard M.A. 2018. Posterior summarization in Bayesian phylogenetics using Tracer 1.7. Systematic Biology 67: 901–904.
  • Rivera-Montoya I. 2003. Estudio de la variabilidad genética de las cactácea columnar Neobuxbaumia mezcalaensis. Bachelor thesis, UNAM, Mexico.
  • Ruán-Tejeda I., Santerre A., Huerta-Martínez F.M., Iñiguez-Dávalos L.I. & Castro-Félix P. 2014. Genetic diversity and relationships among wild and cultivated Stenocereus queretaroensis populations in western Mexico. Biochemical Systematics and Ecology 55: 125–130.
  • Shaw J., Lickey E.B., Schilling E.E. & Small R.L. 2007. Comparison of whole chloroplast genome sequences to choose noncoding regions for phylogenetic studies in angiosperms: the tortoise and the hare III. American Journal of Botany 94: 275–288.
  • Silva G.A.R., Antonelli A., Lendel A, Moraes E.M. & Manfrin M.H. 2018. The impact of early Quaternary climate change on the diversification and population dynamics of a South American cactus species. Journal of Biogeography 45: 76–88.
  • Silva G.A.R., Khan G., Ribeiro-Silva S., et al. 2020. Extreme genetic structure in a relict cactus genus from campo rupestre landscapes: implications for conservation. Biodiversity and Conservation 29: 1263–1281.
  • Suchard M.A., Lemey P., Baele G., Ayres D.L., Drummond A.J. & Rambaut A. 2018. Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10. Virus Evolution 4(1): vey016.
  • Taberlet P., Gielly L., Pautou G. & Bouvet J. 1991. Universal primers for amplification of three non-coding regions of chloroplast DNA. Plant Molecular Biology 17: 1105–1109.
  • Tapia H.J., Bárcenas-Argüello M.L., Terrazas T. & Arias S. 2017. Phylogeny and circumscription of Cephalocereus (Cactaceae) based on molecular and morphological evidence. Systematic Botany 42: 709–723.
  • Tapper S.L., Byrne M., Yates C.Y., et al. 2017. Prolonged isolation and persistence of a common endemic on granite outcrops in both mesic and semi-arid environments in south-western Australia. Journal of Biogeography 41: 2032–2044.
  • Toro M.A. & Caballero A. 2005. Characterization and conservation of genetic diversity in subdivided populations. Philosophical transactions of the Royal society B 360: 1367–1378.
  • Torres-Ribeiro K., Opazo-Medina B.M. & Rubio-Scarano F. 2007. Species composition and biogeographic relations of the rock outcrop flora on the high plateau of Itatiaia, SE-Brazil. Revista Brasileira de Botânica 30: 623–639
  • Tripati A.K., Roberts C.D. & Eagle R.A. 2009. Coupling of CO2 and ice sheet stability over major climate transitions of the last 20 million years. Science 326: 1394–1397.
  • Twidale C.R. 1982. Granite landforms. Elsevier Scientific Publishing Company, Amsterdam, The Netherlands.
  • Valadez-Moctezuma E., Samah S. & Luna-Paez A. 2015. Genetic diversity of Opuntia spp. varieties assessed by classical marker tools (RAPD and ISSR). Plant Systematics and Evolution 2: 737–747.
  • Valiente-Banuet A., Arizmendi M.C., Rojas-Martínez A., Casas C., Silva C. & Dávila P. 2002. Biotic interactions and population dynamics of columnar cacti. In: Fleming T.H. & Valiente-Banuet A (eds) Columnar cacti and their mutualists: evolution, ecology, and conservation: 225–240. University of Arizona Press, Tucson, USA.
  • Vazquez-Montiel R.F. 2005. Diversidad genética de Cephalocereus columna-trajani en cuatro regiones del Valle de Tehuacán-Cuicatlán con diferentes rangos de temperatura. MSc thesis, UNAM, Mexico.
  • Wolfe K.H., Li W.H. & Sharp P.M. 1987. Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. Proceedings of the National Academy of Sciences of the United Stated of America 84: 9054–9058.
  • Yeh F.C., Yang R.C., Boyle T.B., Ye Z.H. & Mao J.X. 1997. POPGENE, the user-friendly shareware for population genetic analysis. Molecular Biology and Biotechnology Centre, University of Alberta, Canada. Available from [accessed 29 Mar. 2021].