Skip to main content
SpringerLink
Log in

Allozyme diversity levels in two congeneric Dioon spp. (Zamiaceae, Cycadales) with contrasting rarities

  • Original Article
  • Published:
Plant Systematics and Evolution Aims and scope Submit manuscript

Abstract

Allozyme diversity and population genetic structure studies were conducted in populations of two Mexican cycad species occurring in adjacent and closely related biogeographic regions. We evaluated if rarity traits in Dioon caputoi, a micro-endemic species, and Dioon merolae, a regional endemic with a wider distribution, influence levels of genetic diversity in different ways. We also explored if genetic structure differs in these species, considering that they have similar population histories. Our results indicate that D. caputoi harbors lower levels of genetic diversity and allelic richness (H E = 0.358, P = 76.9, A r = 1.86) than D. merolae (H E = 0.446, P = 92.3, A r = 2). However, genetic structure does not differ between the two species despite their contrasting geographic distributions (F ST = 0.06 vs. 0.07; D. caputoi and D. merolae, respectively). The comparison of population genetic structure information with historical and geographical aspects of the populations suggests that the rarity of D. caputoi might be due to relatively recent local ecological factors.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Aguinagalde I, Hampe A, Mohanty A, Martín JP, Duminil J, Petit RJ (2005) Effects of life-history traits and species distribution on genetic structure at maternally inherited markers in European trees and shrubs. J Biogeogr 32:329–339

    Article  Google Scholar 

  • Avise JC (2009) Phylogeography: retrospect and prospect. J Biogeogr 36:3–15

    Article  Google Scholar 

  • Brenner ED, Stevenson DW, Twigg RW (2003) Cycads: evolutionary innovations and the role of plant-derived neurotoxins. Trends Plant Sci 8:446–452

    Article  CAS  PubMed  Google Scholar 

  • Cabrera-Toledo D (2009) Biología poblacional de dos cícadas mexicanas con distintos niveles de rareza. PhD thesis, Instituto de Ecología, A.C., Xalapa, México

  • Cabrera-Toledo D, González-Astorga J, Vovides AP (2008) Heterozygote excess in ancient populations of the critically endangered Dioon caputoi (Zamiaceae, Cycadales) from central Mexico. Bot J Linn Soc 158:436–447

    Article  Google Scholar 

  • Chiang YC, Huang KH, Moore SJ, Ge XJ, Huang S, Hsu TW, Schaal BA, Chiang TY (2009) Paraphyly of organelle DNAs in Cycas Sect. Asiorentales due to ancient ancestral polymorphism. BMC Evol Biol 9:161

    Article  PubMed  Google Scholar 

  • Cole CT (2003) Genetic variation in rare and common plants. Annu Rev Ecol Evol S34:213–237

    Article  Google Scholar 

  • Comps B, Gömöry D, Letouzey J, Thiébaut B, Petit RJ (2001) Diverging between heterozygosity and allelic richness during postglacial colonization in the European beech. Genetics 157:389–397

    CAS  PubMed  Google Scholar 

  • Contreras-Medina R, Luna-Vega I, Morrone JJ (2007) Application of parsimony analysis of endemicity to Mexican gymnosperm distributions: grid-cells, biogeographical provinces and track analysis. Biol J Linn Soc 92:405–417

    Article  Google Scholar 

  • Duminil J, Fineschi S, Hampe A, Jordano P, Salvini D, Vendramin GG, Petit RJ (2007) Can population genetic structure be predicted from life-history traits? Am Nat 169:662–672

    Article  PubMed  Google Scholar 

  • Ellis JR, Pashley CH, Burke JM, McCauley DE (2006) High genetic diversity in a rare and endangered sunflower as compared to a common congener. Mol Ecol 15:2345–2355

    Google Scholar 

  • Ellstrand NC, Ellam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 24:217–242

    Article  Google Scholar 

  • Espinosa D, Morrone JJ, Llorente J, Flores O (2002) Introducción al análisis de patrones en biogeografía histórica. Universidad Nacional Autónoma de México, Ciudad de México

    Google Scholar 

  • Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491

    CAS  PubMed  Google Scholar 

  • Ferrusquía-Villafranca I (1998) Geology of Mexico: a synopsis. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological diversity of Mexico. Origins and distribution. Oxford University, New York, pp 3–107

    Google Scholar 

  • Flores-Vázquez JC (2008). Dinámica de las fases tempranas de desarrollo y genética de poblaciones de las cícadas Dioon merolae en los Taviches, Oaxaca. PhD thesis, Universidad Nacional Autónoma de México, Mexico D.F.

  • Fortam R (1984) Diagnóstico municipal. Plan Chiapas, Gobierno Federal Estatal Municipal, Tuxtla Gutiérrez, México

    Google Scholar 

  • García E (2004) Modificaciones al sistema de clasificación climática de Köppen. Instituto de Geografía-UNAM, México D. F.

    Google Scholar 

  • Gaston KJ (1994) Rarity. Chapman & Hall, London

    Google Scholar 

  • Gitzendanner MA, Soltis PS (2000) Patterns of genetic variation in rare and widespread plant congeners. Am J Bot 87:783–792

    Article  PubMed  Google Scholar 

  • González D, Vovides AP, Bárcenas C (2008) Phylogenetic relationships of the neotropical genus Dioon (Cycadales, Zamiaceae) based on nuclear and chloroplast DNA sequence data. Syst Bot 33:229–236

    Article  Google Scholar 

  • González-Astorga J, Vovides AP, Ferrer MM, Iglesias C (2003) Population genetics of Dioon edule Lindl. (Zamiaceae, Cycadales): biogeographical and evolutionary implications. Biol J Linn Soc 80:457–467

    Article  Google Scholar 

  • González-Astorga J, Vergara-Silva F, Vovides AP, Nicolalde-Morejón F, Cabrera-Toledo D (2008) Diversity and genetic structure of three species of Dioon Lindl. (Zamiaceae, Cycadales) from the Pacific seaboard of Mexico. Biol J Linn Soc 94:765–776

    Article  Google Scholar 

  • Graham A (1998) Historical factors and biological diversity in Mexico. In: Ramamoorthy TP, Bye R, Lot A, Fa J (eds) Biological diversity of Mexico. Origins and distribution. Oxford University Press, New York, pp 109–127

    Google Scholar 

  • Hamrick JL (2004) Response of forest trees to global environmental changes. Forest Ecol Manag 197:323–335

    Article  Google Scholar 

  • Hamrick JL, Godt MJW (1996) Effects of the history traits on genetic diversity in plants. Philos Trans R Soc Lond Ser B 351:1291–1298

    Article  Google Scholar 

  • Hamrick JL, Godt MJW, Murawsky DA, Loveless MD (1991) Correlations between species traits and allozyme diversity: implications for conservation biology. In: Falk DA, Holsinger KE (eds) Genetics and conservation of rare plants. Oxford University Press, New York, pp 75–86

    Google Scholar 

  • Harper J (1981) The meanings of rarity. In: Synge H (ed) The biological aspects of rare plant conservation. Wiley, New York, pp 189–203

    Google Scholar 

  • Hedrick PW (2000) Genetics of populations. Jones and Bartlett, Sudbury

    Google Scholar 

  • Hewitt G (1996) Some genetic consequences of ice ages, and their role in divergence and speciation. Biol J Linn Soc 58:247–276

    Google Scholar 

  • Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913

    Article  CAS  PubMed  Google Scholar 

  • Huang S, Chiang YC, Schaal BA, Chou CH, Chiang TY (2001) Organelle DNA phylogeography of Cycas taitungensis, a relict species in Taiwan. Mol Ecol 10:2669–2681

    Article  CAS  PubMed  Google Scholar 

  • IUCN (2009) IUCN red list of threatened species. http://www.iucnredlist.org. Accessed 26 Feb 2009

  • Jianguang X, Shuguang J, Nian L (2005) genetic variation in the endemic plant Cycas debaoensis on the basis of ISSR analysis. Aust J Bot 53:141–145

    Article  Google Scholar 

  • Kalinowski ST (2004) Counting alleles with rarefaction: private alleles and hierarchical sampling designs. Conserv Genet 5:539–543

    Article  CAS  Google Scholar 

  • Kalinowski ST (2005) HP-RARE 1.0: a computer program for performing rarefaction on measures of allelic richness. Mol Ecol Notes 5:187–189

    Article  CAS  Google Scholar 

  • Karron JD (1987) A comparison of levels of genetic polymorphism and self-compatibility in geographical restricted and widespread plant congeners. Evol Ecol 1:47–50

    Article  Google Scholar 

  • Knowles LL, Carstens BC, Keat ML (2007) Coupling genetic and ecological-niche models to examine how past population distributions contribute to divergence. Curr Biol 17:940–946

    Article  CAS  PubMed  Google Scholar 

  • Kruckeberg AR, Rabinowitz D (1985) Biological aspects of endemism in higher plants. Annu Rev Ecol Syst 16:447–479

    Article  Google Scholar 

  • Kyoda S, Setoguchi (2010) Phylogeography of Cycas revoluta Thunb. (Cycadaceae) on the Ryukyu Islands: very low genetic diversity and geographical structure. Plant Syst Evol. doi:10.1007/s00606-010-0322-1

  • Lande R (1988) Genetics and demography in biological conservation. Science 241:1455–1459

    Article  CAS  PubMed  Google Scholar 

  • Lázaro-Zermeño J (2002) Dinámica poblacional de Dioon merolae De Luca, Sabato & Vazquez-Torres (Zamiaceae) en dos sitios de la depresión central de Chiapas, México. PhD thesis, Universidad de Ciencias y Artes de Chiapas, Tuxtla Gutiérrez, México

  • Leimu R, Mutikainen P, Koricheva J, Fischer M (2006) How general are positive relationships between plant population size, fitness and genetic variation. J Ecol 94:942–952

    Article  Google Scholar 

  • Li CL, Wang Q, Jiang SY, Ge S, Wang KQ (1999) Genetic diversity of allozymes in populations of Cycas panzhihuaensis L. Zhou & S.Y. Yang. In: Chen CJ (ed) Biology and conservation of cycads. Proceedings of the fourth international conference on cycad biology, Sichuan, May 1996. International Academic Publishers, Beijing, pp 323–327

  • Loveless MD, Hamrick JL (1984) Ecological determinants of genetic structure in plant populations. Annu Rev Ecol Syst 15:65–95

    Article  Google Scholar 

  • Maki M, Horie S, Yokoyama J (2002) Comparison of genetic diversity between narrowly endemic shrub Menziesia goyozanensis and its widespread congener M. pentandra (Ericaceae). Conserv Genet 3:421–425

    Article  CAS  Google Scholar 

  • Mateu-Andrés I, Segarra-Moragues JG (2000) Population subdivision and genetic diversity in two narrow endemics of Antirrhinum L. Mol Ecol 9:2081–2087

    Article  PubMed  Google Scholar 

  • Milkman R (1975) Heterozygote excess due to population mixing. Ann Hum Genet 38:505

    Article  CAS  PubMed  Google Scholar 

  • Miller MP (1997) Tools for population genetic analyses (TFPGA) 1.3: a Windows program for the genetic data. Computer software distributed by author

  • Moretti A, Caputo P, Cozzolino S, De Luca P, Gaudio L, Gigliano GS, Stevenson DW (1993) A phylogenetic analysis of Dioon (Zamiaceae). Am J Bot 80:204–214

    Article  Google Scholar 

  • Morjan CL, Rieseberg LH (2004) How species evolve collectively: implications of the gene flow and selection for the spread of advantageous alleles. Mol Ecol 13:1341–1356

    Article  CAS  PubMed  Google Scholar 

  • Morrone JJ, Espinosa D, Aguilar C, Llorente J (1999) Preliminary classification of the Mexican biogeographic provinces: a parsimony analysis of endemicity based on plant, insect, and bird taxa. Southwest Nat 44:507–514

    Article  Google Scholar 

  • Moyle LC (2006) Correlates of genetic differentiation and isolation by distance in 17 congeneric Silene species. Mol Ecol 15:1067–1081

    Article  CAS  PubMed  Google Scholar 

  • Nei M (1972) Genetic distances between populations. Am Nat 106:283–292

    Article  Google Scholar 

  • Nicolalde-Morejón F, Vergara-Silva F, González-Astorga J, Stevenson DW, Vovides AP, Sosa V (2010) A character-based approach in the Mexican cycads supports diverse multigene combinations for DNA barcoding. Cladistics. doi:10.1111/j.1090-0031.2010.00321.x

  • Norstog KJ, Nicholls TJ (1997) The biology of cycads. Cornell University Press, Ithaca

    Google Scholar 

  • Peakall R, Smouse PE (2006) GenAlex 6: genetic analysis in Excel. Population genetic software for teaching and research. Mol Ecol Notes 6:288–295

    Article  Google Scholar 

  • Rabinowitz D (1981) Seven forms of rarity. In: Synge H (ed) The biological aspects of rare plant conservation. Wiley, New York, pp 205–217

    Google Scholar 

  • Reveal JL (1981) The concepts of rarity and population threats in plant communities. In: Morse LE, Henifin MS (eds) Rare plant conservation: geographical data organization. New York Botanical Garden, New York, pp 41–47

    Google Scholar 

  • Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228

    CAS  PubMed  Google Scholar 

  • Rzedowski J (1978) Vegetación de México. Limusa, México D.F., p 432

  • Shapcott A (2007) Does species range and rarity affect population genetics? A case study of four Graptophyllum species from Queensland, Australia. Biotropica 39:447–458

    Article  Google Scholar 

  • Silva JRM, Fernandes W, Lovato MB (2007) Genetic variation in two Chamaecrista species (Leguminosae) one endangered and narrowly distributed and another widespread in the serra de Espinhaco, Brazil. Can J Bot 85:629–636

    Article  Google Scholar 

  • Slatkin M (1985) Gene flow in natural populations. Annu Rev Ecol Syst 16:393–430

    Article  Google Scholar 

  • Sneath PHA, Sokal RR (1973) Numerical taxonomy. W. H. Freeman, San Francisco

    Google Scholar 

  • StatSoft (2002) STATISTICA (data analysis software system), version 6. http://www.statsoft.com

  • Toledo VM (1982) Pleistocene changes of vegetation in tropical Mexico. In Prance GT (ed) Biological diversification in the tropics. Proceedings of the 5th international symposium of the Association for Tropical Biology, Caracas. Columbia University Press, New York, pp 93–111

  • Valiente-Banuet A, Casas A, Alcántara A, Dávila P, Flores-Hernández N, Arizmendi M, Villaseñor JL, Ortega J (2000) La vegetación del valle de Tehuacan-Cuicatlán. Bol Soc Bot México 67:24–74

    Google Scholar 

  • Weir BS (1990) Genetic data analysis. Sinauer Associates, Sunderland, p 377

    Google Scholar 

  • Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evolution 38:1358–1370

    Article  Google Scholar 

  • Wendel JF, Weeden NF (1989) Visualization and interpretation of plant isozymes. In: Soltis DE, Soltis PS (eds) Isozymes in plant biology. Discorides, Portland, pp 5–45

  • Wright S (1951) The genetic structure of populations. Ann Eugen 16:97–159

    Google Scholar 

  • Xiao LQ, Gong X (2006) Genetic differentiation and relationship of populations in the Cycas balansae complex (Cycadaceae) and its conservation implications. Ann Bot 97:807–812

    Article  CAS  PubMed  Google Scholar 

  • Xiao LQ, Ge XJ, Gong X, Hao G, Zheng SX (2004) ISSR variation in the endemic and endangered pant Cycas guizhouensis (Cycadales). Ann Bot 94:133–138

    Article  CAS  PubMed  Google Scholar 

  • Xiao LQ, Gong X, Hao G, Ge X, Tian B, Zheng S (2005) Comparison of genetic diversity in two species of cycads. Aust J Bot 53:219–223

    Article  Google Scholar 

  • Yang SL, Meerow AW (1996) The Cycas pectinata (Cycadaceae) complex: genetic structure and gene flow. Int J Plant Sci 157:468–483

    Article  Google Scholar 

  • Zgurski JM, Rai HS, Fai QM, Bogler DJ, Francisco-Ortega J, Graham SW (2008) How well do we understand the overall backbone of cycad phylogeny? New insights from a large, multigene plastid data set. Mol Phylogenet Evol 47:1232–1237

    Google Scholar 

Download references

Acknowledgments

This study was financed by two grants: CONACyT SEMARNAT no. 2002-CO1-0183 and CONABIO no. GE004. We thank Teresa Valverde Valdes, Juan Núñez-Farfán, Luis Ortíz-Catedral, and Daniel Ruzzante for the critical review of an earlier version of this manuscript. The authors also thank Miguel Angel Pérez-Farrera, Nayeli Martínez Meléndez, Pablo Carrillo-Reyes, Juan Carlos Flores-Vázquez, and Vania Jiménez-Lobato for assistance in the field and Julia Hernández Villa and Lilián Juárez Téllez for laboratory assistance. Our sincere gratitude to Pablo Carrillo-Reyes for the elaboration of the map. This study is part of the Ph.D. dissertation of the principal author.

Author information

Authors and Affiliations

  1. Laboratorio de Ecología y Evolución de Recursos Vegetales, Centro de Investigaciones en Ecosistemas, Universidad Autónoma de México, Campus Morelia, Antigua Carretera a Pátzcuaro No. 8701, 58190, Morelia, Michoacán, Mexico

    Dánae Cabrera-Toledo

  2. Laboratorio de Genética de Poblaciones, Red de Biología Evolutiva, Instituto de Ecología, A.C. km 2.5 Antigua Carretera a Coatepec No. 351, 91070, Xalapa, Veracruz, Mexico

    Jorge González-Astorga

  3. Instituto de Investigaciones Biológicas, Universidad Veracruzana, Av. Luis Castelazo Ayala s/n, Col. Industrial Ánimas, 91190, Xalapa, Veracruz, Mexico

    Fernando Nicolalde-Morejón

  4. Laboratorio de Sistemática Molecular (Jardín Botánico), Instituto de Biología, Universidad Nacional Autónoma de México, 3er Circuito Exterior, Ciudad Universitaria, Coyoacán, 04510, Mexico D.F., Mexico

    Francisco Vergara-Silva

  5. Laboratorio de Biología Evolutiva de Cycadales, Red de Biología Evolutiva, Instituto de Ecología, A.C. km 2.5 Antigua Carretera a Coatepec No. 351, 91070, Xalapa, Veracruz, Mexico

    Andrew P. Vovides

Authors
  1. Dánae Cabrera-Toledo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Jorge González-Astorga
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Fernando Nicolalde-Morejón
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Francisco Vergara-Silva
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrew P. Vovides
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dánae Cabrera-Toledo.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cabrera-Toledo, D., González-Astorga, J., Nicolalde-Morejón, F. et al. Allozyme diversity levels in two congeneric Dioon spp. (Zamiaceae, Cycadales) with contrasting rarities. Plant Syst Evol 290, 115–125 (2010). https://doi.org/10.1007/s00606-010-0354-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00606-010-0354-6

Keywords

Search

Navigation