Skip to main content
Log in

Inbreeding influences herbivory in Cucurbita pepo ssp. texana (Cucurbitaceae)

  • Plant Animal Interactions
  • Published:
Oecologia Aims and scope Submit manuscript

Abstract

In a series of field experiments Diabrotica beetle herbivory was found to influence the magnitude of inbreeding depression in Cucurbita pepo ssp. texana, an annual monoecious vine. Beetles damage flowers and fruits and chew dime-sized holes in leaf tissue between major veins. Inbred plants were found to be more likely to be damaged by beetles and to have more leaves damaged per plant than outcrossed plants. A positive linear association was found between the coefficient of inbreeding and the magnitude of leaf damage, whereas a negative association was found between coefficient of inbreeding and several male and female fitness traits. When pesticides were used to control beetle herbivory, the interaction between coefficient of inbreeding and pesticide treatment was significant for fruit production and marginally significant for pollen quantity per anther. Therefore, the magnitude of inbreeding depression in C. pepo ssp . texana varies depending on the severity of beetle herbivory.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4

Similar content being viewed by others

References

  • Agrios GN (1978) Plant pathology, 2nd edn. Academic, New York

  • Aizen MA, Raffaele E (1998) Flowering-shoot defoliation affects pollen grain size and postpollination pollen performance in Alstroemeria aurea. Ecology 79:2133–2142

    Google Scholar 

  • Allison TD (1990) The influence of deer browsing on the reproductive biology of Canada Yew (Taxus canadensis). Oecologia 83:523–529

    Google Scholar 

  • Avila-Sakar G, Krupnick GA, Stephenson AG (2001) Growth and resource allocation in Cucurbita pepo ssp. texana: Effects of fruit removal. Int J Plant Sci 162:1089–1095

    Article  Google Scholar 

  • Bach CE (1989) Chrysomelid beetle movements in relation to host-plant size and surrounding non-host vegetation. Ecology 70:1679–1690

    Google Scholar 

  • Barber HS (1947) Diabrotica and two new genera. Proc Entomol Soc Wash 49:151–161

    Google Scholar 

  • Barrett SCH, Eckert CG (1990) Variation and Evolution of mating system in seed plants. In: Kawano S (ed) Biological approaches and evolutionary trends in plants. Academic, London, pp 229–254

  • Bergelson J, Purrington CB (1996) Surveying patterns in the cost of resistance in plants. Am Nat 148:536–558

    Article  Google Scholar 

  • Brewbaker JL, Kwack BH (1963) The essential role of calcium ion in pollen germination and pollen tube growth. Am J Bot 50:859–865

    CAS  Google Scholar 

  • Carr DE, Dudash MR (1995) Inbreeding depression under a competitive regime in Mimulus guttatus: consequences for potential male and female function. Heredity 75:437–445

    Google Scholar 

  • Carr DE, Eubanks MD (2002) Inbreeding alters resistance to insect herbivory and host plant quality in Mimulus guttatus (Scrophulariaceae). Evolution 56:22–30

    PubMed  Google Scholar 

  • Chambliss OL, Jones CM (1966) Chemical and genetic basis for insect resistance in cucurbits. Proc Am Soc Hortic Sci 89:394–405

    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 C-O, 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 

  • Crnokrak P, Barrett SCH (2002) Perspective: purging the genetic load: a review of the experimental evidence. Evolution 56:2347–2358

    PubMed  Google Scholar 

  • Da Costa CP, Jones CM (1971) Resistance of cucumber, Cucumis sativus L., to three species of cucumber beetles. HortScience 6:340–343

    Google Scholar 

  • Decker DS, Wilson HD (1987) Allozyme variation in Cucurbita pepo complex C. pepo var overifera vs C. texana. Syst Bot 12:263–273

    Google Scholar 

  • Decker-Walters DS (1990) Evidence for multiple domestication of Cucurbita pepo. In: Bates DM, Robinson, RW, Jeffrey C (eds) Biology and utilization of the Cucurbitaceae. Cornell University Press, Ithaca, pp 96–101

  • Decker-Walters DS, Straub JE, Chung SM, Nakata E, Quemada HD (2002) Diversity in free-living populations of Cucurbita pepo (Cucurbitaceae) as assessed by random amplified polymorphic DNA. Syst Bot 27:19–28

    Google Scholar 

  • Delph LF, Johannsson MH, Stephenson AG (1997) How environmental factors affect pollen performance: ecological and environmental perspectives. Ecology 78:1632–1639

    Google Scholar 

  • Dudash M (1990) Relative fitness of selfed and outcross progeny in a self-compatible, protandrous species, Sabatia angularis L. (Gentianaceae): a comparison in three environments. Evolution 44:1129–1139

    Google Scholar 

  • Hauser TP, Loeschcke V (1996) Drought stress and inbreeding depression in Lychnis flos-cuculi (Caryophyllaceae). Evolution 50:1119–1126

    Google Scholar 

  • Hendrix SD, Trapp EJ (1981) Plant-herbivore interactions: insect induced changes in host plant sex expression and fecundity. Oecologia 49:119–122

    Google Scholar 

  • Hendrix SD, Trapp EJ (1989) Floral herbivory in Pastinaca sativa: Do compensatory responses offset reductions in fitness? Evolution 43:891–895

    Google Scholar 

  • Hoffman MP, Robinson RW, Kyle MM, Kirkwyland JJ (1996) Defoliation and infestation by Cucurbita pepo genotypes by diabroticite beetles. HortScience 31:439–442

    Google Scholar 

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

    Google Scholar 

  • Jaworski A, Gorski PM, Shannon S, Robinson RW (1985) Cucurbitacin concentrations in different plant parts of Cucurbita species as a function of age. Cucurbit Genet Coop Rpt 8:71–73

    Google Scholar 

  • Kennedy GG, Barbour JD (1992) Resistance variation in natural and managed systems. In: Fritz RS, Simm EL (eds) Plant resistance to herbivores: ecology, evolution, and genetics. University of Chicago Press, Chicago, pp 13–41

  • Lee TD (1988) Patterns of fruit and seed production. In: Lovett Doust J, Lovett Doust L (eds) Plant reproductive ecology: patterns and strategies. University Press, New York, pp 179–202

  • Lira R, Andrès TC, Nee M (1995) Cucurbita. In: Lira R (ed) Systematic and ecogeographic studies on crop genepools, vol 9. Estudios taxonómicos y ecogeográficos de las Cucurbitaceae latino-americanas de importancia económica: Cucurbita, Sechium, Sicana y Cyclanthera. International Plant Genetic Resources Institute. Instituto deo Biología, México D.F. and Rome, pp 1–115

  • Lloyd DG, Webb CJ (1997) Secondary sex characters in plants. Bot Rev 43:177–216

    Google Scholar 

  • Louda SM, Keeler KH, Holt RD (1989) Herbivore influences on plant performance and competitive interactions In: Grace JB, Tilman D (eds) Perspectives in plant competition. Academic, New York, pp 413–444

    Google Scholar 

  • Marquis RJ (1984) Leaf herbivores decrease fitness of a tropical plant. Science 226:537–539

    Google Scholar 

  • Marquis RJ (1988) Phenological variation in the neotropical understory shrub Piper arieianum: causes and consequences. Ecology 69:1552–1565

    Google Scholar 

  • Marquis RJ (1992) The selective impact of herbivores. In: Fritz RS, Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. University of Chicago Press, Chicago, pp 301–325

  • Matheson AC, White TL, Powell GR (1995) Effects of inbreeding on growth, stem form and rust resistance in Pinus elliottii. Silvae Genet 44:37–46

    Google Scholar 

  • McCall CT, Mitchell-Olds T, Waller D (1989) Fitness consequences of outcrossing in Impatiens capensis: tests of the frequency-dependent and sib-competition models. Evolution 43:1075–1084

    Google Scholar 

  • Metcalf RL, Rhodes AM (1990) Coevolution of the Cucurbitaceae and Luperini (Coleoptera: Chrysomelidae): Basic and applied aspects. In: Bates DM, Robinson RW, Jeffrey C (eds) Biology and utilization of the Cucurbitaceae. Comstock and Cornell University Press, Ithaca, pp 167–182

  • Mutikainen P, Delph LF (1996) Effects of herbivory on male reproductive success in plants. Oikos 75:353–358

    Google Scholar 

  • Nunez-Farfan J, Cabrales-Vargas RA, Dirzo R (1996) Mating system consequences on resistance to herbivory and life history traits in Datura stramonium. Am J Bot 83:1041–1049

    Google Scholar 

  • Obeso JR (1993) Does defoliation affect reproductive output in herbaceous perennials and woody plants in different ways? Funct Ecol 7:150–155

    Google Scholar 

  • Ouborg NJ, Biere A, Mudde CL (2000) Inbreeding effects on resistance and transmission-related traits in the Silene Microbotryum pathosystem. Ecology 81:520–531

    Google Scholar 

  • Pedersen DG (1968) Environmental stress, heterozygote advantage and genotype-environment interaction in Arabidopsis. Heredity 23:127–138

    PubMed  Google Scholar 

  • Quesada M, Bollman K, Stephenson AG (1995) Leaf damage decreases pollen production and hinders pollen performance in Cucurbitatexana. Ecology 16:437–443

    Google Scholar 

  • Ramsey M, Vaughton G (1998) Effect of environment on the magnitude of inbreeding depression in seed germination in a partially self-fertile perennial herb (Blandifolia grandiflora, Liliaceae). Int J Plant Sci 159:98–104

    Article  Google Scholar 

  • Rich PM, Ranken DM, George JS (1989) A manual for microcomputer image analysis: Los Alamos National Laboratory, Los Alamos

    Google Scholar 

  • Roach DA, Wulff RD (1987) Maternal effects in plants. Annu Rev Ecol Syst 18:209–235

    Article  Google Scholar 

  • Roff DA (1997) Evolutionary quantitative genetics. Chapman and Hall, New York

  • Schmitt J, Ehrhardt DW (1990) Enhancement of inbreeding depression by dominance and suppression in Impatiens D.W. capensis. Evolution 44:269–278

    Google Scholar 

  • Schmitt J, Gamble SE (1990) The effect of distance from the parental site on offspring performance and inbreeding depression in Impatiens capensis: a test of the local adaptation hypothesis. Evolution 44:2022–2030

    Google Scholar 

  • Simms EL, Rausher MD (1987) Costs and benefits of plant defense to herbivory. Am Nat 130:570–581

    Article  Google Scholar 

  • Simms EL, Rausher MD (1989) The evolution of resistance to herbivory in Ipomoea purpurea. II. Natural selection by insects and costs of resistance. Evolution 43:573–585

    Google Scholar 

  • Smith CM (1989) Plant resistance to insects: a fundamental approach. Wiley, New York

    Google Scholar 

  • Snyder MA (1993) Interactions between Abert’s squirrel and ponderosa pine: the relationship between selective herbivory and host plant fitness. Am Nat 141:866–879

    Article  Google Scholar 

  • Stephenson AG (1982) The role of extrafloral nectaries of Catalpa speciosa in limiting herbivory and increasing fruit production. Ecology 63:663–669

    Google Scholar 

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

    Google Scholar 

  • Stephenson AG, Lau T-C, Quesada M, Winsor JA (1992) Factors that affect pollen performance. In: Wyatt R (ed) Ecology and evolution of plant reproduction. Chapman and Hall, New York, pp 119–136

  • Strauss SY, Karban R (1994) The significance of outcrossing in an intimate plant-herbivore relationship. 1. Does outcrossing provide an escape from herbivores to the parent plant? Evolution 48:454–464

    Google Scholar 

  • Strauss SY, Conner JK, Rush SL (1996) Foliar herbivory affects floral characters and plant attractivness to pollinators: implications for male and female plant fitness. Am Nat 147:1098–1107

    Article  Google Scholar 

  • Strauss SY, Conner JK, Lehtila KP (2001) Effects of foliar herbivory by insects on the fitness of Raphanus raphanistrum: damage can increase male fitness. Am Nat 158:496–504

    Article  Google Scholar 

  • Strauss SY, Rudgers JA, Lau JA, Irwin RE (2002) Direct and ecological costs of resistance to herbivory. Trends Ecol Evol 17:278–285

    Article  Google Scholar 

  • Tallamy DW, Krischik VA (1989) Variation and function of cucurbitacins in Cucurbita: an examination of current hypotheses. Am Nat 133:766–786

    Article  Google Scholar 

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

    Google Scholar 

Download references

Acknowledgements

We thank Robert Oberheim and the Department of Horticulture for use of The Pennsylvania State University Agricultural Experimental Station at Rock Springs, Pa., USA. We thank Tony Omeis, Steve Breault, Mike Westerman, Brian Clark, Sara Simmers, and Laura Leist for field and lab assistance. This work was supported by NSF grants DEB 93–18224 and DEB 98–06691 to A.G.S.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to C. Nelson Hayes.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Hayes, C.N., Winsor, J.A. & Stephenson, A.G. Inbreeding influences herbivory in Cucurbita pepo ssp. texana (Cucurbitaceae). Oecologia 140, 601–608 (2004). https://doi.org/10.1007/s00442-004-1623-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00442-004-1623-2

Keywords

Navigation