Skip to main content
Log in

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

  • Original paper
  • Published:
Evolutionary Ecology Aims and scope Submit manuscript

Abstract

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.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Agrawal AF, Lively CM (2001) Parasites and the evolution of self-fertilization. Evolution 55:869–879

    Article  PubMed  CAS  Google Scholar 

  • Armbruster P, Reed DH (2005) Inbreeding depression in benign and stressful environments. Heredity 95:235-242

    Article  PubMed  CAS  Google Scholar 

  • Atsatt PR (1970) Hemiparasitic flowering plants: phenotypic canalization by hosts. Nature 225:1161–1163

    Article  PubMed  CAS  Google Scholar 

  • Atsatt PR, Guldberg LD (1978) Host influence on floral variability in Orthocarpus densiflorus (Scrophulariaceae). Plant Syst Evol 129:167–176

    Article  Google Scholar 

  • 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 73:525–531

    Google Scholar 

  • Bull JJ (1994) Virulence. Evolution 48:1423–1437

    Article  Google Scholar 

  • Charlesworth D, Charlesworth B (1979) The evolutionary genetics of sexual systems on flowering plants. Proc Roy Soc Lond B 205:513–530

    Article  CAS  Google Scholar 

  • Charlesworth D, Charlesworth B (1987) Inbreeding depression and its evolutionary consequences. Annu Rev Ecol Syst 18:237–268

    Article  Google Scholar 

  • 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 13:522–531

    Article  Google Scholar 

  • Christen M, Milinski M (2003) The consequences of self-fertilization and outcrossing of the cestode Schistocephalus solidus in its second intermediate host. Parasitology 126:369–378

    Article  PubMed  CAS  Google Scholar 

  • Christen M, Kurtz J, Milinski M (2002) Outcrossing increases infection success and competitive ability: experimental evidence from a hermaphrodite parasite. Evolution 56:2243–2251

    Article  PubMed  Google Scholar 

  • Clay K, Dement D, Rejmanek M (1985) Experimental evidence for host races in mistletoe (Phoradendron tomentosum). Am J Bot 72:1225–1231

    Article  Google Scholar 

  • Coltman DW, Pilkington JG, Smith JA, Pemberton JM (1999) Parasite-mediated selection against inbred soay sheep in a free-living, island population. Evolution 53:1259–1267

    Article  Google Scholar 

  • Crawley MJ (1993) GLIM for ecologists. Blacwell Scientific Publications, Oxford, UK

    Google Scholar 

  • Crnokrak P, Roff DA (1999) Inbreeding depression in the wild. Heredity 83:260–270

    Article  PubMed  Google Scholar 

  • Ebert D (1994) Virulence and local adaptation of a horizontally transmitted parasite. Science 265:1084–1086

    Article  PubMed  Google Scholar 

  • Ebert D, Herre EA (1996) The evolution of parasitic diseases. Parasitol Today 12:96–101

    Article  PubMed  CAS  Google Scholar 

  • Ebert D, Hamilton WD (1996) Sex against virulence: the coevolution of parasitic diseases. Trends Ecol Evol 11:A79-A82

    Article  Google Scholar 

  • Frank SA (1996) Models of parasite virulence. Quart Rev Biol 71:37–78

    Article  PubMed  CAS  Google Scholar 

  • Gemmill AW, Viney ME, Read AF (1997) Host immune status determines sexuality in a parasitic nematode. Evolution 51:393–401

    Article  Google Scholar 

  • Herre EA (1995) Factors affecting the evolution of virulence: nematode parasites of fig wasps as a case study. Parasitology 111:S179–S191

    Article  Google Scholar 

  • Husband BC, Schemske DW (1996) Evolution of the magnitude and timing of inbreeding depression in plants. Evolution 50:54–70

    Article  Google Scholar 

  • Jaksic FM (2001) Ecological effects of El Niño in terrestrial ecosystems of western South America. Ecography 24:241–250

    Article  Google Scholar 

  • Johnston MO, Schoen DJ (1994) On the measurement of inbreeding depression. Evolution 48:1735–1741

    Article  Google Scholar 

  • Kalisz S (1989) Fitness consequences of mating system, seed weight, and emergence date in a winter annual, Collinsia verna. Evolution 43:1263–1272

    Article  Google Scholar 

  • Kaltz O, Shykoff JA (1999) Selfing versus outcrossing propensity of the fungal pathogen Microbotryum violaceum across Silene latifolia host plants. J Evol Biol 12:340–349

    Article  Google Scholar 

  • Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241

    Article  Google Scholar 

  • Kuijt J (1969) The biology of parasitic flowering plants. University of California Press, Berkeley

    Google Scholar 

  • Kuijt J (1988) Revision of Tristerix (Loranthaceae). Syst Bot Monogr 19:1–61

    Google Scholar 

  • Kurtz J (2003) Sex, parasites and resistance: an evolutionary approach. Zoology 106:327–339

    Article  PubMed  Google Scholar 

  • Lamont B (1983) Germination of mistletoes. Calder M, Bernhardt P (eds) The biology of mistletoes. Academic Press, Sidney, pp 129–143

    Google Scholar 

  • Lande R, Schemske DW (1985) The evolution of the self-fertilization and inbreeding depression in plants. I. Genetic models. Evolution 39:24–40

    Article  Google Scholar 

  • Levin DA (1989) Inbreeding depression in partially self-fertilizing Phlox. Evolution 43:1417–1423

    Article  Google Scholar 

  • Littell RC, Milliken GA, Stroup WW, Wolfinger RD (1996) SAS System for mixed models. SAS Institute, Cary, NC

    Google Scholar 

  • Lloyd DG (1980) Sexual strategies in plants. I. A hypothesis of serial adjustment of maternal investment during one reproductive season. New Phytol 86:69–79

    Article  Google Scholar 

  • 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 77:912–921

    Article  Google Scholar 

  • 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 20:571–576

    Article  Google Scholar 

  • Mauseth JD (1990) Morphogenesis in a highly reduced plant: the endophyte of Tristerix aphyllus (Loranthaceae). Bot Gaz 151:348–353

    Article  Google Scholar 

  • Mauseth JD, Montenegro G, Walckowiak AM (1984) Studies of the holoparasite Tristerix aphyllus (Loranthaceae) infecting Trichocereus chilensis (Cactaceae). Can J Bot 62:847–857

    Article  Google Scholar 

  • Mauseth JD, Montenegro G, Walckowiak AM (1985) Host infection and flower formation by the parasite Tristerix aphyllus (Loranthaceae). Can J Bot 63:567–581

    Article  Google Scholar 

  • Maynard Smith J (1978) The evolution of sex. Cambridge University Press, Cambridge, UK

    Google Scholar 

  • Medel R (2000) Assessment of parasite-mediated selection in a host–parasite system in plants. Ecology 81:1554–1564

    Article  Google Scholar 

  • Medel R (2001) Assessment of correlational selection on tolerance and resistance traits in a host plant–parasitic plant interaction. Evol Ecol 15:37–52

    Article  Google Scholar 

  • 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 75:127–140

    Article  Google Scholar 

  • Medel R, Vergara E, Silva A, Kalin-Arroyo M (2004) Effects of vector behavior and host resistance on mistletoe aggregation. Ecology 85:120–126

    Google Scholar 

  • 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 87:493–501

    Article  PubMed  Google Scholar 

  • Musselman LJ, Press MC (1995) Introduction to parasitic plants. In Press MC, Graves JD (eds) Parasitic plants. Chapman and Hall, London, UK, pp 1–13

    Google Scholar 

  • Norton DA, Carpenter MA (1998) Mistletoes as parasites: host specificity and speciation. Trends Ecol Evol 13:101–105

    Article  Google Scholar 

  • Norton DA, Reid N (1997) Lessons in ecosystem management from management of threatened and pest loranthaceous mistletoes in New Zealand and Australia. Cons Biol 11:759–769

    Article  Google Scholar 

  • Ossa CG (2003) Selección mediada por frugívoros en un sistema mutualista estrecho. MSc Thesis, Facultad de Ciencias, Universidad de Chile

  • Press MC, Graves JD (1995) Parasitic plants. Chapman and Hall, London

    Google Scholar 

  • 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 16:976–985

    Article  PubMed  CAS  Google Scholar 

  • SAS institute (1997) SAS/STAT software: changes and enhancements through release 6.12. SAS Institute, Cary, NC

    Google Scholar 

  • Shields WM (1982) Philopatry, inbreeding and the evolution of sex. State University of New York Press, Albany, USA

    Google Scholar 

  • Smith-Ramírez C (1999) Selección fenotípica secuencial sobre rasgos reproductivos del muérdago Tristerix aphyllus. PhD Thesis, Facultad de Ciencias, Universidad de Chile

  • Sokal RR, Rohlf FJ (1995) Biometry. W. H. Freedman and Company, New York

    Google Scholar 

  • Stanton ML (1984) Seed variation in wild radish: effect of seed size on components of seedling and adult fitness. Ecology 6:1105–1112

    Article  Google Scholar 

  • Stephenson AG (1981) Flower and fruit abortion: proximate causes and ultimate functions. Annu Rev Ecol Syst 12:253–279

    Article  Google Scholar 

  • Stephenson AG (1984) The regulation of maternal investment in an indeterminate flowering plant (Lotus corniculatus). Ecology 65:113–121

    Article  Google Scholar 

  • Stephenson AG, Leyshon B, Travers SE, Hayes CN, Winsor JA (2004) Interrelationships among inbreeding, herbivory, and disease on reproduction in a wild gourd. Ecology 85:3023–3034

    Google Scholar 

  • Stevens L, Yan GY, Pray LA (1997) Consequences of inbreeding on invertebrate host susceptibility to parasitic infection. Evolution 51:2032–2039

    Article  Google Scholar 

  • Stöcklin J (1997) Competition and the compensatory regulation of fruit and seed set in the perennial herb Epilobium dodonaei (Onagraceae). Am J Bot 84:763–768

    Article  Google Scholar 

  • Thompson JN (1994) The coevolutionary process. University of Chicago Press, Chicago, USA

    Google Scholar 

  • Williams GC (1975) Sex and evolution. Princeton University Press, Princeton, NJ, USA

    Google Scholar 

  • Winn AA (1988) Ecological and evolutionary consequences of seed size in Prunella vulgaris. Ecology 69:1537–1544

    Article  Google Scholar 

  • Wolfe LM (1993) Inbreeding depression in Hydrophyllum appendiculatum role of maternal effects, crowding, and parental mating histry. Evolution 47:374–386

    Article  Google Scholar 

Download references

Acknowledgments

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).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Wilfredo L. Gonzáles.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Gonzáles, W.L., Suárez, L.H. & Medel, R. Outcrossing increases infection success in the holoparasitic mistletoe Tristerix aphyllus (Loranthaceae). Evol Ecol 21, 173–183 (2007). https://doi.org/10.1007/s10682-006-0021-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10682-006-0021-0

Keywords

Navigation