Research Paper

Genetic diversity and differentiation in Zamia furfuracea (Zamiaceae): an endangered, endemic and restricted Mexican Cycad

Enrique Favian-Vega, Alan W. Meerow, Pablo Octavio-Aguilar, Lourdes G. Iglesias-Andreu

Published on: 21 May 2022

Page: 302 - 310

DOI: 10.6165/tai.2022.67.302

Abstract

Zamia furfuracea is a cycad endemic to coastal habitats of southeast Mexico and of high ecological and horticultural importance. It is threatened with extinction due to the declining population size, caused mainly by livestock raising, urban development, and poor environmental management. This work aimed to determine the genetic diversity and structure of six natural populations of Z. furfuracea throughout their known distribution range. To determine the genetic variation, ten molecular markers of repeated simple sequences (SSR) were used. A Bayesian assignment model, molecular variance analysis and bottleneck tests, and identification of loci with non-neutral heritage were also performed. A lower genetic diversity was identified in the southern population (Capulteolt). Four genetic groups were identified (K = 4). Ancestral polymorphism and management resulted in an increased genetic similarity between the populations of "Ciénega del Sur," "Toro Prieto," and "Playa Escondida". "Capulteolt" was the most differentiated population; a historical reduction in the population size was observed, leading to the loss of some alleles by putative directional natural selection. This study reveals the "Capulteolt" population's low genetic diversity as well as the presence of increased differentiation in the geographical limits of the species' distribution range.

Keyword: Bottleneck, genetic flow, genetic structure, natural selection, SSR markers

Literature Cited

Anderson, E.C. and K.K. Dunham. 2008. The influence of family groups on inferences made with the program Structure. Mol. Ecol. Resour. 8(6): 1219?1229.
DOI: 10.1111/j.1755-0998.2008.02355.xView Article Google Scholar

Baldo-Romero, M.A., L.G. Iglesias-Andreu, M. Va?zquez-Torres, L.R. Sa?nchez-Vela?squez, M. Luna-Rodri?guez and P. Octavio-Aguilar. 2013. Morphometric markers for gender identification in Zamia furfuracea L. f. (Zamiaceae). Rev. Chapingo Ser. Cienc. For. Ambient 19(3): 425?434.
DOI: 10.5154/r.rchscfa.2013.03.010View Article Google Scholar

Beaumont, M.A. and D.J. Balding. 2004. Identifying adaptive genetic divergence among populations from genome scans. Mol. Ecol. 13(4): 969?980.
DOI: 10.1111/j.1365-294X.2004.02125.xView Article Google Scholar

Bernard, J.M. 2005. An introduction to the imprecise Dirichlet model for multinomial data. Int. J. Approx. Reasoning 39(2-3): 123?150.
DOI: 10.1016/j.ijar.2004.10.002View Article Google Scholar

Calonje, M., A.W. Meerow, L. Knowles, D. Knowles, M.P. Griffith, K. Nakamura and J. Francisco-Ortega. 2013. Cycad biodiversity in the Bahamas Archipelago and conservation genetics of the threatened Zamia lucayana (Zamiaceae). Oryx 47(2): 190?198.
DOI: 10.1017/S0030605312000129View Article Google Scholar

Caro, T.M. and M.K. Laurenson. 1994. Ecological and genetic factors in conservation: a cautionary tale. Science 263(5146): 485?486.
DOI: 10.1126/science.8290956View Article Google Scholar

Chemnick, J. and T. Gregory. 2010. Zamia furfuracea. The IUCN Red List of Threatened Species 2010. Available from: http://dx.doi.org/10.2305/IUCN.UK.2010-3.RLTS.T42152A10668734.en (accesed 10 Feb 2019).

Chybicki, I.J. and J. Burczyk. 2009. Simultaneous estimation of null alleles and inbreeding coefficients. J. Hered. 100(1): 106?113.
DOI: 10.1093/jhered/esn088View Article Google Scholar

CITES. 2008. Convention on International Trade in Endangered Species of Wild. Available from: https://cites.org/esp/node/3298 (accessed 4 May 2017).

Cornuet, J.M. and G. Luikart. 1996. Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144(4): 2001?2014.
DOI: 10.1093/genetics/144.4.2001View Article Google Scholar

Dobson, A.P., G. Mace, M. Poole and R.A. Brett. 1992. Conservation biology: the ecology and genetics of endangered species. In: Berry R.J., et al. (eds.), Genes in ecology. Oxford, Blackwell, pp. 405?430.

Eckenwalder, J.E. 1980 Dispersal of the West Indian cycad Zamia pumila L. Biotropica 12(1): 79?80.
DOI: 10.2307/2387779View Article Google Scholar

Ellstrand, N.C. and D.R. Elam. 1993. Population genetic consequences of small population size; Implications for plant conservation. Annu. Rev. Ecol. Syst. 24(1): 217-242.
DOI: 10.1146/annurev.es.24.110193.001245View Article Google Scholar

Evanno, G., S. Regnaut and J. Goudet. 2005. Detecting the number of clusters of individuals using the software STRUCTURE: a simulation study. Mol. Ecol. 14(8): 2611?2620.
DOI: 10.1111/j.1365-294X.2005.02553.xView Article Google Scholar

Excoffier, L., P.E. Smouse and J.M. Quattro. 1992. Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131(2): 479?491.
DOI: 10.1093/genetics/131.2.479View Article Google Scholar

Falush, D., M. Stephens and J.K. Pritchard. 2003. Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164(4): 1567?1587.
DOI: 10.1093/genetics/164.4.1567View Article Google Scholar

Feng, X., Y. Wang and X. Gong. 2014. Genetic diversity, genetic structure and demographic history of Cycas simplicipinna (Cycadaceae) assessed by DNA sequences and SSR markers. BMC Plant. Biol. 14(1): 187.
DOI: 10.1186/1471-2229-14-187View Article Google Scholar

Foll, M. and O. Gaggiotti. 2008. A genome-scan method to identify selected loci appropriate for both dominant and codominant markers: a bayesian perspective. Genetics 180(2): 977?993.
DOI: 10.1534/genetics.108.092221View Article Google Scholar

Garc?a, E. 1970. Climates of the State of Veracruz (according to the climatic classification of Koppen modified by the author. Anales del Instituto de Biolog?a. Ser. Bot. 41(1): 3?41.

Garc?a-Montes, M.A., C.A. Rubio-Tob?n, Y. Islas-Barrios, A. Serrato-D?az, C.J. Figueredo-Urbina, D.M. Galv?n-Hern?ndez and P. Octavio-Aguilar. 2020. The influence of anthropogenic disturbance on the genetic diversity of Ceratozamia fuscoviridis (Zamiaceae). Int. J. Plant Sci. 181(5): 497?508.
DOI: 10.1086/707108View Article Google Scholar

Gitzendanner, M.A. and P.S. Soltis. 2000. Patterns of genetic variation in rare and widespread plant congeners. Am. J. Bot. 87(6): 783?792.
DOI: 10.2307/2656886View Article Google Scholar

Gong, Y.Q., Q.Q. Zhan, K.S. Nguyen, H.T. Nguyen, Y.H. Wang and X. Gong. 2015. The historical demography and genetic variation of the endangered Cycas multipinnata (Cycadaceae) in the red river region, examined by chloroplast DNA sequences and microsatellite markers. Plos One 10(2): e0117719.
DOI: 10.1371/journal.pone.0117719View Article Google Scholar

Gonza?lez-Astorga, J., A.P. Vovides, P. Octavio-Aguilar, D. Aguirre-Fey, F. Nicolalde-Morejo?n and C. Iglesias. 2006. Genetic diversity and structure of the cycad Zamia loddigesii Miq. (Zamiaceae): implications for evolution and conservation. Bot. J. Linnean Soc. 152(4): 533?544.
DOI: 10.1111/j.1095-8339.2006.00579.xView Article Google Scholar

Griffith, M.P., M. Calonje, A.W. Meerow, F. Tut, A.T. Kramer, A. Hird, T.M. Magellan and C. Husby. E. 2015. Can a botanic garden cycad collection capture the genetic diversity in a wild population? Int. J. Plant Sci. 176(1): 1?10.
DOI: 10.1086/678466View Article Google Scholar

Hall, J.A. and G.H. Walter. 2011. Does pollen aerodynamics correlate with pollination vector? Pollen settling velocity as a test for wind versus insect pollination among cycads (Gymnospermae: Cycadaceae: Zamiaceae). Biol. J. Linnean Soc. 104(1): 75?92.
DOI: 10.1111/j.1095-8312.2011.01695.xView Article Google Scholar

Hamada, T., L.I. Terry and T.E. Marler. 2015. Habitats, trade winds, and pollination of the endangered Cycas micronesica: Is there a role for wind as pollen vector on the Island of Guam? Int. J. Plant Sci. 176(6): 525?543.
DOI: 10.1086/681821View Article Google Scholar

Hamrick, J.L. and M.J.W. Godt. 1996. Conservation genetics of endemic plant species. In: Rieseberg L.H. and S.M. Swensen (eds.) Conservation genetics case histories from nature, Chapman & Hall New York, pp. 281?304.

IUCN. 2010. International Union for Conservation of Nature and Natural Resources. The IUCN Red List of Threatened Species. Available from: https://www.iucnredlist.org/search?query=zamia%20furfuracea&searchType=species (accessed 20 May 2019).

Kalinowski, S.T. 2011. The computer program STRUCTURE does not reliably identify the main genetic clusters within species: simulations and implications for human population structure. Heredity 106(4): 625?632.
DOI: 10.1038/hdy.2010.95View Article Google Scholar

Kaulfu?, F. and C. Reisch. 2017. Reintroduction of the endangered and endemic plant species Cochlearia bavarica-Implications from conservation genetics. Ecol. Evol. 7(24): 11100?11112.
DOI: 10.1002/ece3.3596View Article Google Scholar

Larios-Tlali, H., E. Torres-Benites, A. Quevedo-Nolasco, M.R. Marti?nez-Menes and J.A. Salgado-Tra?nsito. 2015. Riesgo de inundacio?n en la subcuenca del ri?o La Antigua, Veracruz, Me?xico. Tecnol. Cienc. Agua 6(3): 39?56.

Larson, W.A., L.W. Seeb, M.V. Everett, R.K. Waples, W.D. Templin and J.E. Seeb. 2014. Genotyping by sequencing resolves shallow population structure to inform conservation of Chinook salmon (Oncorhynchus tshawytscha). Evol. Appl. 7(3): 355?369.
DOI: 10.1111/eva.12128View Article Google Scholar

Leinonen, T., R.B. O'Hara, J.M. Cano and J. Merila. 2008. Comparative studies of quantitative trait and neutral marker divergence: a meta-analysis. J. Evol. Biol. 21(1): 1?17.
DOI: 10.1111/j.1420-9101.2007.01445.xView Article Google Scholar

Li, Y.L. and J.X. Liu. 2018. Structure_Selector: A web-based software to select and visualize the optimal number of clusters using multiple methods. Mol. Ecol. Resour. 18(1): 176?177.
DOI: 10.1111/1755-0998.12719View Article Google Scholar

Limo?n-Salvador, F. 2009. Gen?tica de poblaciones de Zamia furfuracea L. f. (Zamiaceae): una c?cada end?mica al estado de Veracruz, M?xico. Dissertation, Universidad Veracruzana, Xalapa, Veracruz, M?xico.

Liu, Y., S. Wang, L. Li, T. Yang, S. Dong, T. Wei, S. Wu, Y. Liu, Y. Gong, X. Feng, J. Ma, G. Chang, J. Huang, Y. Yang, H. Wang, M. Liu, Y. Xu, H. Liang, J. Yu, Y. Cai, Z. Zhang, Y. Fan, W. Mu, S.K. Sahu, S. Liu, X. Lang, L. Yang, N. Li, S. Habib, Y. Yang, A.J. Lindstrom, P. Liang, B. Goffinet, S. Zaman, J.L. Wegrzyn, D. Li, J. Liu, J. Cui, E.C. Sonnenschein, X. Wang, J. Ruan, J.-Y. Xue, Z.-Q. Shao, C. Song, G. Fan, Z. Li, L. Zhang, J. Liu, Z.-J. Liu, Y. Jiao, X.-Q. Wang, H. Wu, E. Wang, M. Lisby, H. Yang, J. Wang, X. Liu, X. Xu, N. Li, P.S. Soltis, Y.V. de Peer, D.E. Soltis, X. Gong, H. Liu and S. Zhang. 2022. The Cycas genome and the early evolution of seed plants. Nat. Plants 8: 389–401.

Meerow, A.W. and K. Nakamura. 2007. Ten microsatellite loci from Zamia integrifolia (Zamiaceae). Mol. Ecol. Notes 7(5): 824?826.
DOI: 10.1111/j.1471-8286.2007.01716.xView Article Google Scholar

Meerow, A.W., J. Francisco-Ortega, T. Ayala-Silva, D.W. Stevenson and K. Nakamura. 2012. Population genetics of Zamia in Puerto Rico, a study with ten SSR loci. Mem. N. Y. Bot. Gard. 106: 204?223.
DOI: 10.21135/893275150.015View Article Google Scholar

Miller, M. 1997. Tools for populations genetics analysis (TFPGA v 1.3): a windows program for the analysis of allozymes and molecular population genetic data. Department of Biological Sciences, Northern Arizona University, Flagstaff. Available from: https://www.ccg.unam.mx/~vinuesa/tlem09/docs/TFPGADOC.PDF

NOM-059-SEMARNAT. 2010. Protecci?n ambiental. Especies nativas de M?xico de flora y fauna silvestres. Categor?as de riesgo y especificaciones para su inclusi?n, exclusi?n o cambio. Lista de especies en riesgo. Secretar?a de Medio Ambiente y Recursos Naturales, M?xico 50 p. Availble from: https://www.profepa.gob.mx/innovaportal/file/435/1/NOM_059_SEMARNAT_2010.pdf (accesed 10 Feb 2019).

Norstog, K.J., D.W. Stevenson and K.J. Niklas. 1986. The role of beetles in the pollination of Zamia furfuracea L. fil. (Zamiaceae). Biotropica 18(4): 300?306.
DOI: 10.2307/2388573View Article Google Scholar

Norstog, K.J. and T.J., Nicholls. 1997. The Biology of cycads. Comstock Publishing Associates, Cornell University Press: Ithaca, NY, USA. 363p. https://lib.ugent.be/catalog/rug01:000504706

Octavio-Aguilar, P., L.G. Iglesias-Andreu, F.F. Nu?n?ez de Ca?ceres-Gonza?lez and D.M. Galva?n-Herna?ndez. 2017. Fine-Scale Genetic Structure of Zamia furfuracea: Variation with Life-Cycle Stages. Int. J. Plant Sci. 178(1): 57?66.
DOI: 10.1086/689200View Article Google Scholar

Osborne, R. and A.P. Vovides. 2007. The cardboard palms, or Zamia furfuracea. Palms and Cycads 97: 23?30.

Paetkau, D., R. Slade, M. Burden and A. Estoup. 2004. Genetic assignment methods for the direct, real?time estimation of migration rate: a simulation-based exploration of accuracy and power. Mol. Ecol. 13(1): 55?65.
DOI: 10.1046/j.1365-294X.2004.02008.xView Article Google Scholar

Peakall, R. and P.E. Smouse. 2006. GenAlEx 6.5: genetic analysis in Excel. Population genetic software for teaching and research. Bioinformatics 28(19): 2537?2539.
DOI: 10.1093/bioinformatics/bts460View Article Google Scholar

Pierson, J.C., D.J. Coates, J.G.B. Oostermeijer, S.R. Beissinger, J.G. Bragg, P. Sunnucks, N.H. Schumaker and A.G. Young. 2016. Genetic factors in threatened species recovery plans on three continents. Front. Ecol. Environ. 14(8): 433?440.
DOI: 10.1002/fee.1323View Article Google Scholar

Pina-Martins, F., D.N. Silva, J. Fino and O.S. Paulo. 2017. Structure_threader: an Improved Method for Automation Parallelization of Programs STRUCTURE, FASTSTRUCTURE and MavericK on Multi Core CPU systems. Mol. Ecol. Resour. 17(6): 268?274.
DOI: 10.1111/1755-0998.12702View Article Google Scholar

Piry, S., A. Alapetite, J.M., Cornuet, D., Paetkau, L., Baudouin and A. Estoup. 2004. GENECLASS2: a software for genetic assignment and first-generation migrant detection. J. Hered. 95(6): 536?539.
DOI: 10.1093/jhered/esh074View Article Google Scholar

Puechmaille, S.J. 2016. The program structure does not reliably recover the correct population structure when sampling is uneven: subsampling and new estimators alleviate the problem. Mol. Ecol. Resour. 16(3): 608?627.
DOI: 10.1111/1755-0998.12512View Article Google Scholar

Rodri?guez-Ramilo, S., M. Toro, J. Wang and J. Fern?ndez. 2014. Improving the inference of population genetic structure in the presence of related individuals. Genet. Res. 96: e003.
DOI: 10.1017/S0016672314000068View Article Google Scholar

Schwartz, M.K. and K.S. McKelvey. 2009. Why sampling scheme matters: the effect of sampling scheme on landscape genetic results. Conserv. Genet. 10(2): 441?452.
DOI: 10.1007/s10592-008-9622-1View Article Google Scholar

Stewart, C.N. and L.E. Via. 1993. A rapid CTAB DNA isolation technique useful for RAPD fingerprinting and other PCR applications. Biotechniques 14(5): 748?750.

Va?zquez-Torres, S.M. 2001. Distribuci?n, abundancia, estructura poblacional y potencial reproductor de Zamia furfuracea L. Instituto de Investigaciones Biol?gicas. Universidad Veracruzana. Bases de datos SNIB-CONABIO, proyecto R176. M?xico, D. F. Available from: https://www.snib.mx/iptconabio/resource?r=SNIB-R176 (accesed 10 Feb 2019).

Vovides, A.P., C. Iglesias, M.A., Pe?rez-Farrera, M. Va?zquez and U. Schippmann. 2002. Peasant nurseries: a concept for an integrated conservation strategy for cycads in Mexico. In: Maunder M., C. Clubbe, C. Hankamer and M. Groves (eds.) Plant conservation in the tropics: perspectives and practice. Royal Botanic Gardens, London, England, pp. 421?444.

Vovides, A.P., M.A. Pe?rez-Farrera and C. Iglesias. 2010. Cycad propagation by rural nurseries in Mexico as an alternative conservation strategy: 20 years on. Kew Bull. 65(4): 603?611.
DOI: 10.1007/s12225-010-9240-1View Article Google Scholar

Whitlock, M.C. and D.E. Mccauley. 1999. Indirect measures of gene flow and migration: FST ≠ 1/(4Nm+1). Heredity 82(2): 117?125.
DOI: 10.1038/sj.hdy.6884960View Article Google Scholar

Wright, S. 1969. Evolution and the Genetics of Populations, Vol. 2. The Theory of Gene Frequencies. Univ. Chicago Press, Chicago, IL

Xiao, L.Q., X.J. Ge, X. Gong, G. Hao and S.X. Zheng. 2004. ISSR variation in the endemic and endangered plant Cycas guizhouensis (Cycadaceae). Ann. Bot. 94(1): 133?138.
DOI: 10.1093/aob/mch119View Article Google Scholar