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Genetic and morphometric markers are able to differentiate three morphotypes belonging to Section Algarobia of genus Prosopis (Leguminosae, Mimosoideae)

Abstract

The section Algarobia of genus Prosopis includes promising species for reforestation and afforestation programmes in arid and semiarid regions, mainly of the Americas. Many interspecific natural hybrid combinations have been described in this group. In this paper we analysed a hybrid zone in Chaco biogeographical province in Argentina, where P. ruscifolia and P. alba overlap and hybridise producing intermediate fertile hybrid forms. Eleven morphological traits and 76 loci RAPD were analysed to determine the effect of hybridization between these species. The comparison of morphological traits among groups yielded significant or highly significant differences for all traits. Estimates of H e in P. alba and P. ruscifolia did not differ from each other, but both showed significantly lower values than the hybrid group. The analysis of correlations between shared phenotypes and pair-wise relationships estimated from RAPD gave also strong support to the hypothesis that most of the phenotypic traits analysed have significant heritability. The analyses of population structure and clustering based on morphological and molecular data by DAPC and STRUCTURE were rather consistent and indicated that the three morphotypes studied here are differentiated with low overlapping. All results indicated that despite the occurrence of natural hybridization and introgression, interspecific gene flow would be limited by hybrid breakdown or natural selection favouring the maintenance of species integrity.

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References

  • Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with the hybrids: setting conservation guidelines. Trends Ecol Evol 16(11):613–622

    Article  Google Scholar 

  • Anderson E (1949) Introgressive hybridization. Wiley, New York

    Google Scholar 

  • Arnold M (1997) Natural hybridization and evolution. Oxford University press, Oxford

    Google Scholar 

  • Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568

    Article  PubMed  CAS  Google Scholar 

  • Bassam BJ, Caetano-Anollés G, Gresshoff PM (1991) Fast and sensitive silver staining of DNA in polyacrylamide gels. Anal Biochem 80:81–84

    Google Scholar 

  • Black WC IV (1996) FORTRAN programs for the analysis of RAPD-PCR markers in populations. Colorado State University, Fort Collins

    Google Scholar 

  • Burkart A (1976) A monograph of the genus Prosopis (Leguminosae, Mimosoideae). J Arnold Arb 57(3 and 4):219–249, 450–525

    Google Scholar 

  • Cabrera AL, Willink A (1973) Biogeografía de América Latina. The General Secretaria of the Organization of American States, Washington, DC

    Google Scholar 

  • Catalano SA, Vilardi JC, Tosto D, Saidman BO (2008) Molecular phylogeny and diversification history of Prosopis (Fabaceae: Mimosoideae). Biol J Linn Soc 93:621–640

    Article  Google Scholar 

  • Coart E, Lamote V, De Loose M, Van Bockstaele E, Lootens P, Roldan-Ruiz I (2002) AFLP markers demonstrate local genetic differentiation between two indigenous oak species [Quercus robur L. and Quercus petraea (Matt.) Liebl.] in Flemish populations. Theor Appl Genet 105:431–439

    Article  PubMed  CAS  Google Scholar 

  • Curtu AL, Gailing O, Finkeldey R (2007) Evidence for hybridization and introgression within a species-rich oak (Quercus spp.) community. BMC Evol Biol 7:2–18

    Article  Google Scholar 

  • Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Soft 22(4):1–20

    Google Scholar 

  • Dutton RW (1989) Prosopis sp.: a justification for their future research and development. In: Dutton R (ed) A Research and development strategy for Prosopis. Center for Overseas Research and Development, Durham, pp 33–40

    Google Scholar 

  • Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164:1567–1587

    PubMed  CAS  Google Scholar 

  • Ferreyra LI, Bessega C, Vilardi JC, Saidman BO (2004) First report on RAPD patterns able to differentiate some Argentinean species of section Algarobia (Prosopis, Leguminosae). Genetica 121:33–42

    Article  PubMed  CAS  Google Scholar 

  • Ferreyra LI, Bessega C, Vilardi JC, Saidman BO (2007) Consistency of population genetics parameters estimated from isozyme and RAPDs dataset in species of genus Prosopis (Leguminosae, Mimosoideae). Genetica 131:217–230

    Article  PubMed  CAS  Google Scholar 

  • González-Pérez MA, Caujapé-Castells J, Sosa PA (2004) Molecular evidence of hybridization between the endemic Phoenix canariensis and the widespread P. dactylifera with Random Amplified Polymorphic DNA (RAPD) markers. Plant Syst Evol 247:165–175

    Article  Google Scholar 

  • González-Rodriguez A, Arias D, Valencia S, Oyama K (2004) Morphological and RAPD analysis of hybridization between Quercus affinis and Quercus Laurina (Fagaceae), two Mexican red oaks. Am J Bot 91(3):401–409

    Article  PubMed  Google Scholar 

  • Harrison RG (1990) Hybrid zones: window on evolutionary process. Oxf Surv Evol Biol 7:69–128

    Google Scholar 

  • Hothorn T, Hornik K (2007) The exactRankTests Package. (http://www.r-project.org)

  • Hothorn T, Hornik K, Van de Wiel M, Zeileis A (2007) COIN: conditional inference procedures in a permutation test framework. (http://www.r-project.org)

  • Hunziker J, Poggio L, Palacios RA, Andrada AB (1975) Cytogenetic of some species and natural hybrids in Prosopis (Leguminosae). Can J Genet Cytol 17:253–262

    Google Scholar 

  • Hunziker J, Naranjo C, Palacios RA, Poggio L (1977) Chromosomal cytology and hybridization. In: Simpson B (ed) Mesquite, its biology in two desert ecosystems, US/IBP, Series 4, Dowden, Hutchinson and Ross, Inc, pp 56–59

  • Hunziker JH, Saidman BO, Naranjo CA, Palacios RA, Poggio L, Burghardt AD (1986) Hybridization and genetic variation of Argentine species of Prosopis. For Ecol Manag 16:301–315

    Article  Google Scholar 

  • Jakobsson M, Rosenberg NA (2007) CLUMPP: a cluster matching and permutation program for dealing with label switching and multimodality in analysis of population structure. Bioinformatics 23:1801–1806

    Article  PubMed  CAS  Google Scholar 

  • Jombart T (2008) adegenet: a R package for the multivariate analysis of genetic markers. Bioinformatics 24:1403–1405. doi:10.1093/bioinformatics/btn129

    Article  PubMed  CAS  Google Scholar 

  • Jombart T, Ahmed I (2011) adegenet 1.3-1: new tools for the analysis of genome-wide SNP data. Bioinformatics 27:3070–3071. doi:10.1093/bioinformatics/btr521

    Article  PubMed  CAS  Google Scholar 

  • Jombart T, Devillard S, Balloux F (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genet 11:94. http://www.biomedcentral.com/1471-2156/11/94

  • Joseph L, Kuriachan P, Thomas G (2008) Is Oryza malampuzhaensis Krish. et Chand. (Poaceae) a valid species? Evidence from morphological and molecular analyses. Plant Syst Evol 270:75–94

    Article  Google Scholar 

  • Li F, Gan S, Wenga Q, Zhao X, Huang S, Li M, Chenb S, Wang Q, Shib F (2008) RAPD and morphological diversity among four populations of the tropical tree species Paramichelia baillonii (Pierre) Hu in China. For Ecol Manage 255:1793–1801

    Article  Google Scholar 

  • Lynch M, Milligan BG (1994) Analysis of population genetic structure with RAPD markers. Mol Ecol 3:91–99

    Article  PubMed  CAS  Google Scholar 

  • Mallet J (2007) Hybrid speciation. Nature 446:280–283

    Article  Google Scholar 

  • Naranjo C, Poggio L, Enus Zeiger S (1984) Phenol chromatography, morphology and cytogenetic in three species and natural hybrids of Prosopis (Leguminosae, Mimosoidae). Plant Syst Evol 144:276–2577

    Article  Google Scholar 

  • Nei M (1978) Estimation of average heterozygosity and genetic distance from a small numbers of individuals. Genetics 89:583–590

    PubMed  CAS  Google Scholar 

  • Otha T (1982) Linkage disequilibria due to random genetic drift in finite subdivided populations. Proc Nat Acad Sc 79:1940–1944

    Article  Google Scholar 

  • Palacios RA, Bravo LD (1981) Hibridización natural en Prosopis (Leguminosae) en la región chaqueña Argentina. Evidencias morfológicas y cromatográficas. Darwiniana 23:3–35

    Google Scholar 

  • Pasiecznic NM, Harris PJC, Smith SJ (2004) Identifying tropical Prosopis species. Field guide. HIDRA, Coventry (ISBN 0 905343 34 4)

    Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    PubMed  CAS  Google Scholar 

  • Pritchard JK, Wen X, Falush D (2010) STRUCTURE ver. 2.3. University of Chicago, Chicago. http://pritch.bsd.uchicago.edu/structure.html

  • R Development Core Team (2012) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna. ISBN 3-900051-07-0. http://www.R-project.org/

  • Ramírez L, De La Vega A, Razkin N, Luna V, Harris JC (1999) Analysis of the relationships between species of the genus Prosopis revealed by the use of molecular markers. Agronomie 19:31–43

    Article  Google Scholar 

  • Riesberg LH (1997) Hybrid origin of a plant species. Ann Rev Ecol Syst 28:359–389

    Article  Google Scholar 

  • Riesberg LH, Ellstrand NC (1993) What can molecular and morphological markers tell us about plant hybridization. Crit Rev Plant Sci 12:213–241

    Google Scholar 

  • Rieseberg LH, Carney SE (1998) Plant hybridization. New Phytol 140:599–624

    Article  Google Scholar 

  • Rieseberg LH, Gerber D (1995) Hybridization in the Catalina Island Mountain mahogany (Cercocarpus traskiae): RAPD evidence. Cons Biol 9:199–203

    Article  Google Scholar 

  • Ritland K (1996) A marker-based method for inferences about quantitative inheritance in natural populations. Evolution 50:1062–1073

    Article  Google Scholar 

  • Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Mol Ecol Notes 4(1):137–138

    Article  Google Scholar 

  • Saidman BO (1986) Isoenzymatic studies of alcohol dehydrogenase and glutamate oxalacetate transaminase in four Southamerican species of Prosopis and their natural hybrids. Silvae Genet 35:3–10

    Google Scholar 

  • Saidman BO (1990) Isozyme studies on hybrid swarms on Prosopis caldenia and sympatric species. Silvae Genet 39:5–8

    Google Scholar 

  • Saidman BO, Vilardi JC (1993) Genetic variability and germoplasm conservation in the genus Prosopis. In: Puri S (ed) Nursery technology of forest tree species of arid and semiarid regions. Winrock-Oxford & IBH Publishing Co., New Delhi, pp 187–198

  • Saidman BO, Bessega C, Ferreyra LI, Vilardi JC (1998a) Random amplified polymorphic DNA (RAPDS) variation in hybrid swarms and pure population of the genus Prosopis (Leguminosae). In: Bruns S, Sinclair MC, Viana AM (eds) Recent advances in biotechnology for tree conservation and management. Tragardh International Foundation for Science, Stockholm, pp 122–134

    Google Scholar 

  • Saidman BO, Vilardi JC, Montoya S, Dieguez MJ, Hopp HE (1998b) Molecular Markers: A tool for the understanding of the relationships among species of Prosopis (Leguminosae, Mimosoideae). In: Puri S (ed) Tree improvement: applied research and technology transfer. Science Publishers, Inc., Enfield, pp 312–324. ISBN 1-57808-027-4

  • Saidman BO, Bessega C, Ferreyra LI, Julio N, Vilardi JC (2000) The use of genetic markers to assess population structure and relationships among species of the genus Prosopis (Leguminosae). Bol Soc Arg Bot 35(3–4):315–324

    Google Scholar 

  • Soltis P, Soltis D (2009) The role of hybridization. Annu Rev Plant Biol 60:561–588

    Article  PubMed  CAS  Google Scholar 

  • Stewart CN, Excoffier L (1996) Assessing population genetic structure and variability with RAPD data: application to Vaccinum macrocarpon (American cranberry). J Evol Biol 9:153–171

    Article  CAS  Google Scholar 

  • Templeton AR (1989) The meaning of species and speciation: a genetic perspective. In: Otte D, Endler JA (eds) Speciation and its consequences. Sinauer Associates Inc, Sunderland

    Google Scholar 

  • Tovar-Sánchez E, Oyama K (2004) Natural hybridization and hybrid zones between Quercus crassifolia and Quercus crassipes (Fagaceae) in Mexico: morphological and molecular evidence. Am J Bot 91:1352–1363

    Article  PubMed  Google Scholar 

  • Väha JP, Primmer CR (2006) Efficiency of model-based Bayesian methods for detecting hybrid individuals under different hybridization scenarios and with different numbers of loci. Mol Ecol 15:63–72. doi:10.1111/j.1365-294X.2005.02773

    Article  PubMed  Google Scholar 

  • Vázquez-Garcidueñas S, Palacios RA, Segovia-Quiroz J, Frías-Hernandez JT, Olalde-Portugal V, Martínez-de la Vega O, Mollard FPO, Vázquez-Marrufo G (2003) Morphological and molecular data to determine the origin and taxonomic status of Prosopis chilensis var. riojana (Fabaceae, Mimosoideae). Can J Bot 81:905–917

    Article  Google Scholar 

  • Vega M, Hernandez P (2005) Molecular evidence for natural interspecific hybridization in Prosopis. Agrofor Syst 64:197–202

    Article  Google Scholar 

  • Vekemans X, Beauwens T, Lemaire M, Roldan-Ruiz I (2002) Data from amplified fragment length polymorphism (AFLP) markers show indication of size homoplasy and of a relationship between degree of homoplasy and fragment size. Mol Ecol 11:139–151

    Article  PubMed  CAS  Google Scholar 

  • Verga A (1995) Genetische untersuchungen an Prosopis chilensis und Prosopis flexuosa (Mimosaceae) in trockenen Chaco Argentiniens. Gottingen Research Notes in Forest Genetics19. Abteilung fur Forstgenetik und Forstpflanzenzuchtung der Universitat Gottingen, Gottingen

  • Weising K, Nybom H, Wolff K, Kahl G (2005) DNA fingerprinting in plants. Principles, methods and applications. CRC Press, USA

    Book  Google Scholar 

  • Williams JGK, Kubelik AR, Livak KJ, Rafalski JA, Tingey SV (1990) DNA polymorphism amplified by arbitrary primers are useful as genetic markers. Nucl Acid Res 18:6531–6535

    Article  CAS  Google Scholar 

  • Wu CI (2001) The genetic view of the process of speciation. J Evol Biol 14:851–865

    Article  Google Scholar 

  • Yuzbasioglu E, Dadandi MY, Ozcan S (2008) Natural hybridization between Phlomis lycia D. Don P. Bourgaei Boiss, (Lamiaceae) revealed by RAPD markers. Genetica 133:13–20

    Article  PubMed  CAS  Google Scholar 

  • Zhivotovsky LA (1999) Estimating population structure in diploids with multilocus dominant DNA markers. Mol Ecol 8(6):907–913

    Article  PubMed  CAS  Google Scholar 

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Acknowledgments

This study was financed by Universidad de Buenos Aires (Grant UBACYT 20020100100008 to B.O.S.) and Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET) (Grant PIP No 11220090100147 to J.C.V.). BOS and JCV are members of the Carrera del Investigador Científico, Consejo Nacional de Investigaciones Científicas y Técnicas (CIC-CONICET).

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Correspondence to Laura I. Ferreyra.

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Ferreyra, L.I., Vilardi, J.C., Verga, A. et al. Genetic and morphometric markers are able to differentiate three morphotypes belonging to Section Algarobia of genus Prosopis (Leguminosae, Mimosoideae). Plant Syst Evol 299, 1157–1173 (2013). https://doi.org/10.1007/s00606-013-0786-x

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  • DOI: https://doi.org/10.1007/s00606-013-0786-x

Keywords

  • Prosopis
  • RAPD markers
  • Morphometry
  • Hybridization
  • DAPC
  • Structure