Plant Systematics and Evolution

, Volume 300, Issue 9, pp 1959–1972 | Cite as

Is the insular endemic Psidium socorrense (Myrtaceae) at risk of extinction through hybridization?

  • Alfredo López-Caamal
  • Zenón Cano-Santana
  • Jaime Jiménez-Ramírez
  • Rolando Ramírez-Rodríguez
  • Efraín Tovar-Sánchez
Original Article


Natural hybridization between an insular endemic species and a widely distributed congener may endanger the endemic through genetic assimilation or outbreeding depression. Furthermore, hybrids can exhibit complex morphological variation, causing taxonomic problems in the identification of the involved taxa. In this work, we used a combination of leaf morphological and molecular markers (RAPD) to establish the differentiation between Psidium sp. aff. sartorianum and the insular endemic P. socorrense. It was also determined if hybridization between these taxa occurs in the southern slope of Isla Socorro, Mexico. Plant collection was carried along an altitudinal gradient (100–800 m). We collected eight populations separated 100 m a.s.l. apart from each other; 25 individuals were collected per population. Psidium socorrense and P. sp. aff. sartorianum differed significantly in all but two morphological characters measured. Also, a high number of diagnostic RAPD markers were found for each taxon. These results suggest that two Psidium species occur at Isla Socorro. Furthermore, both morphological and RAPD markers revealed a hybrid zone located in the southern slope of Isla Socorro (400–700 m a.s.l.) with an asymmetrical pattern of gene flow towards P. socorrense. We suggest that the disturbance caused by the sheep population in the mixed stand favors the establishment of hybrids. We further discuss whether hybridization represents a threat to the insular endemic P. socorrense.


Disturbance Genetic assimilation Insular endemic species Morphology Psidium RAPD 



We thank Maribel Paniagua Ibañez, Leonardo Beltrán, Paulette Arellano Vignettes, Guadalupe Rangel Altamirano, L. Márquez Valdemar, and Elgar Castillo Mendoza for technical assistance. We also thank Mauricio Mora Jarvio for his field assistance and Ramiro Cruz-Durán for providing excellent Psidium illustrations.

Supplementary material

606_2014_1025_MOESM1_ESM.doc (143 kb)
Supplementary material Phenotype characterization (Schwarzbach et al. 2001) of 17 leaf morphological characters in mixed stands between Psidium sp. aff. sartorianum and P. socorrense in Socorro Island, Mexico. (DOC 143 kb)


  1. Anderson E (1948) Hybridization of the habitat. Evolution 2:1–9CrossRefGoogle Scholar
  2. Anderson E (1949) Introgressive hybridization. John Wiley, New YorkGoogle Scholar
  3. Anton KA, Ward JR, Cruzan MB (2013) Pollinator-mediated selection on floral morphology: evidence for transgressive evolution in a derived lineage. J Evol Biol 26:660–673PubMedCrossRefGoogle Scholar
  4. Arnold ML (2006) Evolution through genetic exchange. Oxford University Press, New YorkGoogle Scholar
  5. Barton NH (1992) On the spread of new gene combinations in the third phase of Wright’s shifting-balance. Evolution 46:447–551CrossRefGoogle Scholar
  6. Beatty GE, Philipp M, Provan J (2010) Unidirectional hybridization at a species’ range boundary: implications for habitat tracking. Divers Distrib 16:1–9CrossRefGoogle Scholar
  7. Brattstrom BH (1990) Biogeography of the Isles Revillagigedo, Mexico. J Biogeogr 17:177–183CrossRefGoogle Scholar
  8. Brennan AC, Bridle JR, Ai-Lan W, Hiscock SJ, Abbott RJ (2009) Adaptation and selection in the Senecio (Asteraceae) hybrid zone on Mount Etna, Sicily. New Phytol 183:702–717PubMedCrossRefGoogle Scholar
  9. Buerkle CA, Wolf DE, Rieseberg LH (2003) The origin and extinction of species through hybridization. In: Brigham CA, Schwartz MW (eds) Population viability in plants. Springer, Berlin, pp 117–141CrossRefGoogle Scholar
  10. Burguess KS, Morgan M, Deverno L, Husband BC (2005) Asymmetrical introgression between two Morus species (M. alba, M. rubra) that differ in abundance. Mol Ecol 14:3471–3483CrossRefGoogle Scholar
  11. Burguess KS, Morgan M, Husband BC (2007) Interspecific seed discounting and the fertility cost of hybridization in an endangered species. New Phytol 177:276–284Google Scholar
  12. Caraway V, Carr GD, Morden CW (2001) Assessment of hybridization and introgression in lava-colonizing Hawaiian Dubautia (Asteraceae: Madiinae) using RAPD markers. Am J Bot 88:1688–1694PubMedCrossRefGoogle Scholar
  13. Carlquist S (1974) Island biology. Columbia University Press, New YorkGoogle Scholar
  14. Chacón-Torres A, Villaroel MM, Zataray M, Carrillo MO, Corona JG, Chavarría MPG, Gutiérrez AH, Morales OR, Solorio MAA, Rivera R, Villegas RES (1993) Reconocimiento ecológico de la Isla Socorro, Archipiélago de Revillagigedo, Colima, México. Revista Universidad Michoacana 9:11–39Google Scholar
  15. Crawford DJ, Witkus R, Stuessy TF (1987) Plant evolution and speciation on oceanic islands. In: Urbanska KM (ed) Differentiation patterns in higher plants. Academic Press, London, pp 183–199Google Scholar
  16. Daehler C, Strong DR (1997) Hybridization between introduced smooth cordgrass (Spartina alterniflora; Poaceae) and native California cordgrass (S. foliosa) in San Francisco Bay, California, USA. Am J Bot 84:607–611PubMedCrossRefGoogle Scholar
  17. D’Andrea L, Felber F, Guadagnuolo R (2008) Hybridization rates between lettuce (Lactuca sativa) and its wild relative (L. serriola) under field conditions. Environ Biosaf Res 7:61–71CrossRefGoogle Scholar
  18. Dittrich-Reed DR, Fitzpatrick BM (2013) Transgressive hybrids as hopeful monsters. Evol Biol 40:310–315PubMedPubMedCentralCrossRefGoogle Scholar
  19. Ellstrand NC, Biggs D, Kaus A, Lubinsky P, McDade LA, Preston K, Prince LM, Regan HM, Rorive V, Ryder OA, Schierenbeck KA (2010) Got hybridization? A multidisciplinary approach for informing science policy. Bioscience 60:384–388CrossRefGoogle Scholar
  20. Ellstrand NC, Elam DR (1993) Population genetic consequences of small population size: implications for plant conservation. Annu Rev Ecol Syst 4:217–242CrossRefGoogle Scholar
  21. Flores-Palacios A, Martínez-Gómez JE, Curry RL (2009) La vegetación de Isla Socorro, Archipiélago de Revillagigedo, México. Bol Soc Bot Mex 84:13–23Google Scholar
  22. Gaskin JF, Schaal BA (2002) Hybrid Tamarix widespread in US invasion and undetected in native Asian range. Proc Natl Acad Sci USA 99:11256–11259PubMedPubMedCentralCrossRefGoogle Scholar
  23. González-Pérez MA, Caujapé-Castells J, Sosa PA (2004) Molecular evidence of hybridisation between the endemic Phoenix canariensis and the widespread P. dactylifera with Random Amplified Polymorphic DNA (RAPD) markers. Plant Syst Evol 247:165–175CrossRefGoogle Scholar
  24. González-Pérez MA, Sosa PA (2009) Hybridization and introgression between the endemic Phoenix canariensis and the introduced P. dactylifera in the Canary Islands. Open For Sci J 2:78–85CrossRefGoogle Scholar
  25. Hardig TM, Brunsfeld SJ, Fritz RS, Morgan M, Orians CM (2000) Morphological and molecular evidence for hybridization and introgression in a willow (Salix) hybrid zone. Mol Ecol 9:9–24PubMedCrossRefGoogle Scholar
  26. Hedge SG, Nason JD, Clegg JM, Ellstrand NC (2006) The evolution of California’s wild radish has resulted in the extinction of its progenitors. Evolution 60:1187–1197CrossRefGoogle Scholar
  27. Hoban SM, McCleary Schlarbaum E, Anagnostakis SL, Romero-Severson J (2012) Human-induced landscapes facilitate hybridization between a native and an introduced tree. Evol Appl 5:720–731PubMedPubMedCentralCrossRefGoogle Scholar
  28. Holman JS, Hughes JM, Fensham RJ (2003) A morphological cline in Eucalyptus: a genetic perspective. Mol Ecol 12:3013–3025PubMedCrossRefGoogle Scholar
  29. Howard DJ, Preszler RW, Williams J, Fenchel S, Boecklen WJ (1997) How discrete are oak species? Insights from a hybrid zone between Quercus grisea and Q. gambelli. Evolution 5:747–755CrossRefGoogle Scholar
  30. Johnston MI (1931) The Flora of the Revillagigedo II. Proc Calif Acad Sci 20:9–104Google Scholar
  31. Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2002) Plant Systematics, a phylogenetic approach. Sinauer Associates, MassachusettsGoogle Scholar
  32. Levin DA (2000) The origin, expansion, and demise of plant species. Oxford University Press, New YorkGoogle Scholar
  33. Levin DA, Francisco-Ortega J (1996) Hybridization and the extinction of rare plant species. Conserv Biol 10:10–16CrossRefGoogle Scholar
  34. Levin G, Moran R (1989) The vascular flora of Socorro Island, Mexico. San Diego Society of Natural History 16:1–71Google Scholar
  35. Liston A, Rieseberg LH, Mistretta O (1990) Ribosomal DNA evidence for hybridization between island endemic species of Lotus. Biochem Syst Ecol 18:239–244CrossRefGoogle Scholar
  36. Losos JB, Ricklefs RE (2009) Adaptation and diversification on islands. Nature 457:830–836PubMedCrossRefGoogle Scholar
  37. Mallet J (2005) Hybridization as an invasion of the genome. Trends Ecol Evol 20:229–237PubMedCrossRefGoogle Scholar
  38. Martínez-Gómez JE, Curry RL (1996) The conservation status of the Socorro Mockingbird Mimodes graysoni in 1993–1994. Bird Conserv Int 6:271–283CrossRefGoogle Scholar
  39. Mayr E (1942) Systematics and the origin of species from the viewpoint of a zoologist. Columbia University Press, New YorkGoogle Scholar
  40. Meyerson LA, Viola DV, Brown RN (2010) Hybridization of invasive Phragmites australis with a native subspecies in North America. Biol Invasions 12:103–111CrossRefGoogle Scholar
  41. Miranda F (1960) Vegetación. In: Adem J, Cobo E, Blázquez L, Miranda F, Villalobos A, Herrera T, Villa B, Vázquez L (eds) La isla Socorro, Archipiélago de las Revillagigedo. Monografías del Instituto de Geofísica. UNAM, México, pp 201–216Google Scholar
  42. Mondini L, Noorani A, Pagnotta MA (2009) Assessing plant genetic diversity by molecular tools. Diversity 1:19–35CrossRefGoogle Scholar
  43. Paulay G (1994) Biodiversity on oceanic islands: Its origin and extinction. Am Zool 34:134–144Google Scholar
  44. Ramírez-Rodríguez R, Tovar-Sánchez E, Jiménez Ramírez J, Vega Flores K, Rodríguez V (2011) Introgressive hybridization between Brahea dulcis and Brahea nítida (Arecaceae) in Mexico: evidence from morphological and PCR-RAPD patterns. Botany 89:545–557CrossRefGoogle Scholar
  45. Randell RA, Howarth DG, Morden CW (2004) Genetic analysis of natural hybrids between endemic and alien Rubus (Rosaceae) species in Hawai’i. Conserv Genet 5:217–230CrossRefGoogle Scholar
  46. Rieseberg LH, Archer MA, Wayne RK (1999) Transgressive segregation, adaptation, and speciation. Heredity 83:363–372PubMedCrossRefGoogle Scholar
  47. Rieseberg LH, Carney SE (1998) Plant hybridization. New Phytol 140:599–624CrossRefGoogle Scholar
  48. Rieseberg LH, Ellstrand NC (1993) What can morphological and molecular markers tell us about plant hybridization? Crit Rev Plant Sci 12:213–241Google Scholar
  49. Rieseberg LH, Gerber D (1995) Hybridization in the Catalina Island mountain mahogany (Cercocarpus traskiae): RAPD’s evidence. Conserv Biol 9:199–203CrossRefGoogle Scholar
  50. Salas-Pascual M, Acebes-Ginoves JR, Del Arco Aguilar M (1993) Arbutus × androsterilis, a new interspecific hybrid between A. canariensis and A. unedo from the Canary Islands. Taxon 42:789–792CrossRefGoogle Scholar
  51. Schwarzbach AE, Donovan LA, Rieseberg LH (2001) Transgressive character expression in a hybrid sunflower species. Am J Bot 88:270–277PubMedCrossRefGoogle Scholar
  52. Seehausen O, Takimoto G, Roy D, Jokela J (2008) Speciation reversal and biodiversity dynamics with hybridization in changing environments. Mol Ecol 17:30–44PubMedCrossRefGoogle Scholar
  53. Shasany AK, Darokar MP, Dhawan S, Gupta AK, Gupta S, Shukla AK, Patra NK, Khanuja SPS (2005) Use of RAPD and AFLP markers to identify inter- and intraspecific hybrids of Mentha. J Hered 96:542–549PubMedCrossRefGoogle Scholar
  54. Stace CA (1975) Hybridization and the flora of the British Isles. Academic Press, LondonGoogle Scholar
  55. Tovar-Sánchez E, Rodríguez-Carmona F, Aguilar-Mendiola V, Mussali-Galante P, López-Caamal A, Valencia-Cuevas L (2012) Molecular evidence of hybridization in two native invasive species: Tithonia tubaeformis and T. rotundifolia (Asteraceae) in Mexico. Plant Syst Evol 298:1947–1959CrossRefGoogle Scholar
  56. Triest L, de Greef B, De Bondt R, van Slyckenà J (2000) RAPD of controlled crosses and clones from the field suggests that hybrids are rare in the Salix alba-Salix fragilis complex. Heredity 84:555–563PubMedCrossRefGoogle Scholar
  57. van Hengstum T, Lachmuth S, Oostermeijer JGB, den Nijs HCM, Meirmans PG, van Tienderen PH (2012) Human-induced hybridization among congeneric endemic plants on Tenerife, Canary Islands. Plant Syst Evol 298:1119–1131CrossRefGoogle Scholar
  58. Vilà M, Weber E, D’Antonio CM (2010) Conservation implications of invasion by plant hybridization. Biol Invasions 2:207–217CrossRefGoogle Scholar
  59. Walter HS, Levin GA (2008) Feral sheep on Socorro Island: facilitators of alien plant colonization and ecosystem decay. Divers Distrib 14:422–431CrossRefGoogle Scholar
  60. Whitney KD, Ahern JR, Campbell LG, Albert LP, King MS (2010) Patterns of hybridization in plants. Perspect Plant Ecol 12:175–182CrossRefGoogle Scholar
  61. Williams JGK, Kubelik AR, Livak KL, Rafalski JA, Tingey SV (1990) DNA polymorphisms amplified by arbitrary primers are useful as genetic markers. Nucleic Acids Res 18:6531–6535PubMedPubMedCentralCrossRefGoogle Scholar
  62. Wilson P (1992) On inferring hybridity from morphological intermediacy. Taxon 41:11–23CrossRefGoogle Scholar
  63. Wolf DE, Takebayashi N, Rieseberg LH (2001) Predicting the risk of extinction through hybridization. Conserv Biol 15:1039–1053CrossRefGoogle Scholar
  64. Yüzbaşıoğlu E, Dadandı MY, Özcan S (2008) Natural hybridization between Phlomis lycia D. Don × P. bourgaei Boiss., (Lamiaceae) revealed by RAPD markers. Genetica 133:13–20PubMedCrossRefGoogle Scholar
  65. Zar JH (2010) Biostatistical analysis. Prentice Hall, New JerseyGoogle Scholar
  66. Zha XF, Srirama RD, Fernandez MG, Mistree F (2008) Knowledge-intensive collaborative decision support for design processes: A hybrid decision support model and agent. Comput Ind 59:905–922CrossRefGoogle Scholar

Copyright information

© Springer-Verlag Wien 2014

Authors and Affiliations

  • Alfredo López-Caamal
    • 1
  • Zenón Cano-Santana
    • 2
  • Jaime Jiménez-Ramírez
    • 3
  • Rolando Ramírez-Rodríguez
    • 1
  • Efraín Tovar-Sánchez
    • 1
  1. 1.Departamento de Sistemática y Evolución, Centro de Investigación en Biodiversidad y ConservaciónUniversidad Autónoma del Estado de MorelosCuernavacaMexico
  2. 2.Departamento de Ecología y Recursos Naturales, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoMexico, DFMexico
  3. 3.Departamento de Biología Comparada, Facultad de CienciasUniversidad Nacional Autónoma de MéxicoMexico, DFMexico

Personalised recommendations