Evolutionary Ecology

, 21:173 | Cite as

Outcrossing increases infection success in the holoparasitic mistletoe Tristerix aphyllus (Loranthaceae)

  • Wilfredo L. Gonzáles
  • Lorena H. Suárez
  • Rodrigo Medel
Original paper


Most studies on the fitness advantage of outbreeding in host–parasite systems have been assessed from the host rather than the parasite perspective. Here, we performed experimental pollination treatments to evaluate the consequences of outbreeding on fitness-related traits in the holoparasitic mistletoe Tristerix aphyllus in a 2-year field study. Results indicate that self-pollinated plants had a lower fruit production than outcrossed plants (20.4% and 29.5% reduction in 2002 and 2003, respectively), and resulting inbred fruits were smaller than outcrossed fruits in both years. No effect was detected for seed mass. The percentage of germination of inbred seeds was 15.1% and 6.0% lower than outcrossed seeds in 2002 and 2003, respectively. Inbred seedlings had shorter radicles, which translated to a 71.6% and 60.0% reduction in infection success compared with outcrossed plants in 2002 and 2003, respectively. Overall, our results revealed significant inbreeding depression on almost every trait that was examined. Although the mean value of traits varied from a year to another, the magnitude of inbreeding depression did not change significantly between years. Our findings constitute the first evidence that outcrossing increases infection success and probably virulence in parasitic plant populations.


Host–parasite interactions Inbreeding depression Radicle Selfing Outcrossing Chile Cacti 



We thank N. Peña, C. Neely, P. Caballero, and C. Ossa for their assistance during the fieldwork and E. Gianoli and three anonymous reviewers for helpful comments on a previous version of this manuscript. Special thanks to CONAF for allowing us to work at Las Chinchillas National Reserve and for logistic support provided during this research. WLG was supported by a CONICYT doctoral fellowship. This work was partially funded by FONDECYT 1010660, and the Center for Advanced Studies in Ecology and Research in Biodiversity supported by the Millennium Science Initiative (P99-103F ICM).


  1. Agrawal AF, Lively CM (2001) Parasites and the evolution of self-fertilization. Evolution 55:869–879PubMedCrossRefGoogle Scholar
  2. Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235-242PubMedCrossRefGoogle Scholar
  3. Atsatt PR (1970) Hemiparasitic flowering plants: phenotypic canalization by hosts. Nature 225:1161–1163PubMedCrossRefGoogle Scholar
  4. Atsatt PR, Guldberg LD (1978) Host influence on floral variability in Orthocarpus densiflorus (Scrophulariaceae). Plant Syst Evol 129:167–176CrossRefGoogle Scholar
  5. Botto-Mahan C, Medel R, Ginocchio R, Montenegro G (2000) Factors affecting the circular distribution of the leafless mistletoe Tristerix aphyllus (Loranthaceae) on the cactus Echinopsis Chilensis. Rev Chil Hist Nat 73:525–531Google Scholar
  6. Bull JJ (1994) Virulence. Evolution 48:1423–1437CrossRefGoogle Scholar
  7. Charlesworth D, Charlesworth B (1979) The evolutionary genetics of sexual systems on flowering plants. Proc Roy Soc Lond B 205:513–530CrossRefGoogle Scholar
  8. Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268CrossRefGoogle Scholar
  9. Cheptou PO, Imbert E, Lepart J, Escarre J (2000) Effects of competition on lifetime estimates of inbreeding depression in the outcrossing plant Crepis sancta (Asteraceae). J Evol Biol 13:522–531CrossRefGoogle Scholar
  10. Christen M, Milinski M (2003) The consequences of self-fertilization and outcrossing of the cestode Schistocephalus solidus in its second intermediate host. Parasitology 126:369–378PubMedCrossRefGoogle Scholar
  11. Christen M, Kurtz J, Milinski M (2002) Outcrossing increases infection success and competitive ability: experimental evidence from a hermaphrodite parasite. Evolution 56:2243–2251PubMedCrossRefGoogle Scholar
  12. Clay K, Dement D, Rejmanek M (1985) Experimental evidence for host races in mistletoe (Phoradendron tomentosum). Am J Bot 72:1225–1231CrossRefGoogle Scholar
  13. Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution 53:1259–1267CrossRefGoogle Scholar
  14. Crawley MJ (1993) GLIM for ecologists. Blacwell Scientific Publications, Oxford, UKGoogle Scholar
  15. Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270PubMedCrossRefGoogle Scholar
  16. Ebert D (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science 265:1084–1086CrossRefPubMedGoogle Scholar
  17. Ebert D, Herre EA (1996) The evolution of parasitic diseases. Parasitol Today 12:96–101PubMedCrossRefGoogle Scholar
  18. Ebert D, Hamilton WD (1996) Sex against virulence: the coevolution of parasitic diseases. Trends Ecol Evol 11:A79-A82CrossRefGoogle Scholar
  19. Frank SA (1996) Models of parasite virulence. Quart Rev Biol 71:37–78PubMedCrossRefGoogle Scholar
  20. Gemmill AW, Viney ME, Read AF (1997) Host immune status determines sexuality in a parasitic nematode. Evolution 51:393–401CrossRefGoogle Scholar
  21. Herre EA (1995) Factors affecting the evolution of virulence: nematode parasites of fig wasps as a case study. Parasitology 111:S179–S191CrossRefGoogle Scholar
  22. Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70CrossRefGoogle Scholar
  23. Jaksic FM (2001) Ecological effects of El Niño in terrestrial ecosystems of western South America. Ecography 24:241–250CrossRefGoogle Scholar
  24. Johnston MO, Schoen DJ (1994) On the measurement of inbreeding depression. Evolution 48:1735–1741CrossRefGoogle Scholar
  25. Kalisz S (1989) Fitness consequences of mating system, seed weight, and emergence date in a winter annual, Collinsia verna. Evolution 43:1263–1272CrossRefGoogle Scholar
  26. Kaltz O, Shykoff JA (1999) Selfing versus outcrossing propensity of the fungal pathogen Microbotryum violaceum across Silene latifolia host plants. J Evol Biol 12:340–349CrossRefGoogle Scholar
  27. Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241CrossRefGoogle Scholar
  28. Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, BerkeleyGoogle Scholar
  29. Kuijt J (1988) Revision of Tristerix (Loranthaceae). Syst Bot Monogr 19:1–61Google Scholar
  30. Kurtz J (2003) Sex, parasites and resistance: an evolutionary approach. Zoology 106:327–339PubMedCrossRefGoogle Scholar
  31. Lamont B (1983) Germination of mistletoes. Calder M, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sidney, pp 129–143Google Scholar
  32. Lande R, Schemske DW (1985) The evolution of the self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40CrossRefGoogle Scholar
  33. Levin DA (1989) Inbreeding depression in partially self-fertilizing Phlox. Evolution 43:1417–1423CrossRefGoogle Scholar
  34. Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS System for mixed models. SAS Institute, Cary, NCGoogle Scholar
  35. Lloyd DG (1980) Sexual strategies in plants. I. A hypothesis of serial adjustment of maternal investment during one reproductive season. New Phytol 86:69–79CrossRefGoogle Scholar
  36. Martinez del Río C, Silva A, Medel R, Hourdequin M (1996) Seeds dispersers as disease vectors: bird transmission of mistletoe seeds to plant hosts. Ecology 77:912–921CrossRefGoogle Scholar
  37. Martínez del Río C, Hourdequin M, Silva A, Medel R (1995) The influence of cactus size and previous infection on bird deposition of mistletoe seeds. Aust J Ecol 20:571–576CrossRefGoogle Scholar
  38. Mauseth JD (1990) Morphogenesis in a highly reduced plant: the endophyte of Tristerix aphyllus (Loranthaceae). Bot Gaz 151:348–353CrossRefGoogle Scholar
  39. Mauseth JD, Montenegro G, Walckowiak AM (1984) Studies of the holoparasite Tristerix aphyllus (Loranthaceae) infecting Trichocereus chilensis (Cactaceae). Can J Bot 62:847–857CrossRefGoogle Scholar
  40. Mauseth JD, Montenegro G, Walckowiak AM (1985) Host infection and flower formation by the parasite Tristerix aphyllus (Loranthaceae). Can J Bot 63:567–581CrossRefGoogle Scholar
  41. Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge, UKGoogle Scholar
  42. Medel R (2000) Assessment of parasite-mediated selection in a host–parasite system in plants. Ecology 81:1554–1564CrossRefGoogle Scholar
  43. Medel R (2001) Assessment of correlational selection on tolerance and resistance traits in a host plant–parasitic plant interaction. Evol Ecol 15:37–52CrossRefGoogle Scholar
  44. Medel R, Botto-Mahan C, Smith-Ramirez C, Mendez MA, Ossa CG, Caputo L, Gonzáles WL (2002) Historia natural cuantitativa de una relación parásito-hospedero: el sistema Tristerix-cactáceas en Chile semiárido. Rev Chil Hist Nat 75:127–140CrossRefGoogle Scholar
  45. Medel R, Vergara E, Silva A, Kalin-Arroyo M (2004) Effects of vector behavior and host resistance on mistletoe aggregation. Ecology 85:120–126Google Scholar
  46. Medrano M, Guitián P, Guitián J (2000) Patterns of fruit and seed set within inflorescences of Pancratium maritimum (Amaryllidaceae): nonuniform pollination, resource limitation, or architectural effects? Am J Bot 87:493–501PubMedCrossRefGoogle Scholar
  47. Musselman LJ, Press MC (1995) Introduction to parasitic plants. In Press MC, Graves JD (eds) Parasitic plants. Chapman and Hall, London, UK, pp 1–13Google Scholar
  48. Norton DA, Carpenter MA (1998) Mistletoes as parasites: host specificity and speciation. Trends Ecol Evol 13:101–105CrossRefGoogle Scholar
  49. Norton DA, Reid N (1997) Lessons in ecosystem management from management of threatened and pest loranthaceous mistletoes in New Zealand and Australia. Cons Biol 11:759–769CrossRefGoogle Scholar
  50. Ossa CG (2003) Selección mediada por frugívoros en un sistema mutualista estrecho. MSc Thesis, Facultad de Ciencias, Universidad de ChileGoogle Scholar
  51. Press MC, Graves JD (1995) Parasitic plants. Chapman and Hall, LondonGoogle Scholar
  52. Salathe P, Ebert D (2003) The effects of parasitism and inbreeding on the competitive ability in Daphnia magna: evidence for synergistic epistasis. J Evol Biol 16:976–985PubMedCrossRefGoogle Scholar
  53. SAS institute (1997) SAS/STAT software: changes and enhancements through release 6.12. SAS Institute, Cary, NCGoogle Scholar
  54. Shields WM (1982) Philopatry, inbreeding and the evolution of sex. State University of New York Press, Albany, USAGoogle Scholar
  55. Smith-Ramírez C (1999) Selección fenotípica secuencial sobre rasgos reproductivos del muérdago Tristerix aphyllus. PhD Thesis, Facultad de Ciencias, Universidad de ChileGoogle Scholar
  56. Sokal RR, Rohlf FJ (1995) Biometry. W. H. Freedman and Company, New YorkGoogle Scholar
  57. Stanton ML (1984) Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology 6:1105–1112CrossRefGoogle Scholar
  58. Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annu Rev Ecol Syst 12:253–279CrossRefGoogle Scholar
  59. Stephenson AG (1984) The regulation of maternal investment in an indeterminate flowering plant (Lotus corniculatus). Ecology 65:113–121CrossRefGoogle Scholar
  60. Stephenson AG, Leyshon B, Travers SE, Hayes CN, Winsor JA (2004) Interrelationships among inbreeding, herbivory, and disease on reproduction in a wild gourd. Ecology 85:3023–3034Google Scholar
  61. Stevens L, Yan GY, Pray LA (1997) Consequences of inbreeding on invertebrate host susceptibility to parasitic infection. Evolution 51:2032–2039CrossRefGoogle Scholar
  62. Stöcklin J (1997) Competition and the compensatory regulation of fruit and seed set in the perennial herb Epilobium dodonaei (Onagraceae). Am J Bot 84:763–768CrossRefGoogle Scholar
  63. Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago, USAGoogle Scholar
  64. Williams GC (1975) Sex and evolution. Princeton University Press, Princeton, NJ, USAGoogle Scholar
  65. Winn AA (1988) Ecological and evolutionary consequences of seed size in Prunella vulgaris. Ecology 69:1537–1544CrossRefGoogle Scholar
  66. Wolfe LM (1993) Inbreeding depression in Hydrophyllum appendiculatum role of maternal effects, crowding, and parental mating histry. Evolution 47:374–386CrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2006

Authors and Affiliations

  • Wilfredo L. Gonzáles
    • 1
  • Lorena H. Suárez
    • 1
  • Rodrigo Medel
    • 2
  1. 1.Departamento de BotánicaUniversidad de ConcepciónConcepciónChile
  2. 2.Departamento de Ciencias Ecológicas, Facultad de CienciasUniversidad de ChileSantiagoChile

Personalised recommendations