Skip to main content
Log in

Costs of delayed dispersal and alloparental care in the fungus-cultivating ambrosia beetle Xyleborus affinis Eichhoff (Scolytinae: Curculionidae)

  • Original Paper
  • Published:
Behavioral Ecology and Sociobiology Aims and scope Submit manuscript

Abstract

Body reserves may determine the reproductive output of animals, depending on their resource allocation strategy. In insects, an accumulation of reserves for reproduction is often obtained before dispersal by pre-emergence (or maturation) feeding. This has been assumed to be an important cause of delayed dispersal from the natal nest in scolytine beetles. In the cooperatively breeding ambrosia beetles, this is of special interest because in this group delayed dispersal could serve two alternative purposes: “selfish” maturation feeding or “altruistic” alloparental care. To distinguish between these two possibilities, we have experimentally studied the effect of delayed dispersal on future reproductive output in the xyleborine ambrosia beetle Xyleborus affinis. Females experimentally induced to disperse and delayed dispersing females did not differ in their body condition at dispersal and in their founding success afterwards, which indicates that females disperse independently of condition, and staying adult females are fully mature and would be able to breed. However, induced dispersers produced more offspring than delayed dispersers within a test period of 40 days. This suggests that delayed dispersal comes at a cost to females, which may result primarily from alloparental care and leads to a reduced reproductive output. Alternatively, females might have reproduced prior to dispersal. This is unlikely, however, for the majority of dispersing females because of the small numbers of offspring present in the gallery when females dispersed, suggesting that mainly the foundress had reproduced. In addition, “gallery of origin” was a strong predictor of the reproductive success of females, which may reflect variation in the microbial complex transmitted vertically from the natal nest to the daughter colony, or variation of genetic quality. These results have important implications for the understanding of proximate mechanisms selecting for philopatry and alloparental care in highly social ambrosia beetles and other cooperatively breeding arthropods.

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

Similar content being viewed by others

References

  • Baker JM, Norris DM (1968) A complex of fungi mutualistically involved in nutrition of ambrosia beetle Xyleborus ferrugineus. J Inv Path 11:246–250

    Article  Google Scholar 

  • Batra LR (1979) Insect–fungus symbiosis. Nutrition, mutualism, and commensalism. Wiley, New York

    Google Scholar 

  • Beaver RA (1986) The taxonomy, mycangia and biology of Hypothenemus curtipennis (Schedl), the first known cryphaline ambrosia beetle (Coleoptera: Scolytidae). Ent Scand 17:131–135

    Google Scholar 

  • Beaver RA (1989) Insect–fungus relationships in the bark and ambrosia beetles. In: Wilding N, Collins NM, Hammond PM, Webber JF (eds) Insect–fungus interactions. Academic, London, pp 121–143

    Google Scholar 

  • Biedermann PHW (2007) Social behaviour in sib mating fungus farmers. Master thesis, University of Bern

  • Biedermann PHW, Klepzig KD, Taborsky M (2009) Fungus cultivation by ambrosia beetles: behavior and laboratory breeding success in three xyleborine species. Environ Entomol 38:1096–1105

    Article  PubMed  Google Scholar 

  • Bischoff LL (2004) The social structure of the haplodiploid bark beetle, Xylosandrus germanus. Diploma thesis, University of Bern

  • Bonte D, De La Pena E (2009) Evolution of body condition-dependent dispersal in metapopulations. J Evol Biol 22:1242–1251

    Article  PubMed  CAS  Google Scholar 

  • Botterweg PF (1982) Dispersal and flight behavior of the spruce bark beetle Ips typographus in relation to sex, size and fat-content. Z Angew Entomol 94:466–489

    Article  Google Scholar 

  • Bowler DE, Benton TG (2005) Causes and consequences of animal dispersal strategies: relating individual behaviour to spatial dynamics. Biol Rev 80:205–225

    Article  PubMed  Google Scholar 

  • Bruintjes R, Hekman R, Taborsky M (2010) Experimental global food reduction raises resource acquisition costs of brood care helpers and reduces their helping effort. Funct Ecol 24:1054–1063

    Article  Google Scholar 

  • Helms Cahan S, Blumstein DT, Sundström L, Liebig J, Griffin A (2002) Social trajectories and the evolution of social behaviour. Oikos 96:206–216

    Article  Google Scholar 

  • Choe JC, Crespi BJ (1997) The evolution of social behaviour in insects and arachnids. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Costa JT (2006) The other insect societies. Belknap Press of Harvard University Press, Cambridge

    Google Scholar 

  • Cote J, Clobert J, Fitze PS (2007) Mother–offspring competition promotes colonization success. PNAS 104:9703–9708

    Article  PubMed  CAS  Google Scholar 

  • Craig R (1983) Subfertility and the evolution of eusociality by kin selection. J Theor Biol 100:379–397

    Article  Google Scholar 

  • Dahlsten DL (1982) Relationship between bark beetles and their natural enemies. In: Mitton JB, Sturgeon KB (eds) Bark beetles in North American conifers. University of Texas Press, Austin, pp 140–182

    Google Scholar 

  • Eden SF (1987) When do helpers help—food availability and helping in the moorhen, Gallinula-chloropus. Behav Ecol Sociobiol 21:191–195

    Article  Google Scholar 

  • Eichhoff W (1881) Die Europäischen Borkenkäfer. Springer, Berlin

    Google Scholar 

  • Elkin CM, Reid ML (2005) Low energy reserves and energy allocation decisions affect reproduction by mountain pine beetles, Dendroctonus ponderosae. Funct Ecol 19:102–109

    Article  Google Scholar 

  • Farrell BD, Sequeira AS, O’Meara BC, Normark BB, Chung JH, Jordal BH (2001) The evolution of agriculture in beetles (Curculionidae: Scolytinae and Platypodinae). Evolution 55:2011–2027

    PubMed  CAS  Google Scholar 

  • Fischer M (1954) Untersuchungen über den kleinen Holzbohrer (Xyleborus saxeseni). Pflanzenschutzberichte 12:137–180

    CAS  Google Scholar 

  • Francke-Grosmann H (1956) Hautdrüsen als Träger der Pilzsymbiose bei Ambrosiakäfern. Z Morph Ökol Tiere 45:275–308

    Article  Google Scholar 

  • Francke-Grosmann H (1975) Zur epizoischen und endozoischen Übertragung der symbiotischen Pilze des Ambrosiakäfers Xyleborus saxeseni (Coleoptera: Scolitidae). Entomologica Ger 1:279–292

    Google Scholar 

  • French JRJ, Roeper RA (1975) Studies on the biology of the ambrosia beetle Xyleborus dispar. J Appl Entomol 78:241–247

    Google Scholar 

  • Graham K (1961) Air-swallowing—mechanism in photic reversal of the beetle Trypodendron. Nature 191:519–520

    Article  Google Scholar 

  • Gyllenberg M, Kisdi E, Utz M (2008) Evolution of condition-dependent dispersal under kin competition. J Math Biol 57:285–307

    Article  PubMed  Google Scholar 

  • Hager R, Jones CB (2009) Reproductive skew in vertebrates: proximate and ultimate causes. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Hamilton WD (1978) Evolution and diversity under bark. In: Mound LA, Waloff N (eds) Diversity of insect faunas. Blackwell, Oxford, pp 154–175

    Google Scholar 

  • Heg D, Bachar Z, Brouwer L, Taborsky M (2004) Predation risk is an ecological constraint for helper dispersal in a cooperatively breeding cichlid. Proc R Soc Lond B 271:2367–2374

    Article  Google Scholar 

  • Ims RA, Hjermann DO (2001) Condition-dependent dispersal. In: Clobert J, Danchin E, Dhondt AA, Nichols JD (eds) Dispersal. Oxford University Press, Oxford, pp 203–216

    Google Scholar 

  • Kajimura H, Hijii N (1994) Reproduction and resource utilization of the ambrosia beetle, Xylosandrus mutilatus, in-field and experiment populations. Entomol Exp Appl 71:121–132

    Article  Google Scholar 

  • Kalshoven LGE (1962) Note on the habits of Xyleborus destruens Bldf., the near-primary borer of teak trees on Java. Entomol Berichten 22:7–18

    Google Scholar 

  • Kawata M (1987) The effect of kinship on spacing among female red-backed voles, Clethrionomys rufocanus bedfordiae. Oecologia 72:115–122

    Article  Google Scholar 

  • Keller L, Reeve HK (1994) Partitioning of reproduction in animal societies. Trends Ecol Evol 9:98–102

    Article  PubMed  CAS  Google Scholar 

  • Kingsolver JG, Norris DM (1977) The interaction of Xyleborus ferrugineus Fabr. (Coleoptera: Scolytidae) behavior and initial reproduction in relation to its symbiotic fungi. Ann Entomol Soc Am 70:1–4

    Google Scholar 

  • Kirkendall LR, Kent DS, Raffa KF (1997) Interactions among males, females and offspring in bark and ambrosia beetles: the significance of living in tunnels for the evolution of social behavior. In: Choe JC, Crespi BJ (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 181–215

    Google Scholar 

  • Koenig WD, Pitelka FA, Carmen WJ, Mumme RL (1992) The evolution of delayed dispersal in cooperative breeders. Q Rev Biol 67:111–150

    Article  PubMed  CAS  Google Scholar 

  • Kok LT, Norris DM, Chu HM (1970) Sterol metabolism as a basis for a mutualistic symbiosis. Nature 225:661–662

    Article  PubMed  CAS  Google Scholar 

  • Kokko H, Ekman J (2002) Delayed dispersal as a route to breeding: territorial inheritance, safe havens, and ecological constraints. Am Nat 160:468–484

    Article  PubMed  Google Scholar 

  • Korb J, Heinze J (2008) The ecology of social life: a synthesis. In: Korb J, Heinze J (eds) Ecology of social evolution. Springer, Berlin, pp 245–259

    Chapter  Google Scholar 

  • Krausseopatz B, Kohler U, Schopf R (1995) The energetic state of Ips typographus L. (Coleoptera, Scolytidae) during the life-cycle. Z Angew Entomol 119:185–194

    Google Scholar 

  • Liang KY, Zeger SL (1986) Longitudinal data-analysis using generalized linear-models. Biometrika 73:13–22

    Article  Google Scholar 

  • Latty TM, Reid ML (2010) Who goes first? Condition and danger dependent pioneering in a group-living bark beetle (Dendroctonus ponderosae). Behav Ecol Sociobiol 64:639–646

    Article  Google Scholar 

  • McNee WR, Wood DL, Storer AJ (2000) Pre-emergence feeding in bark beetles (Coleoptera: Scolytidae). Environ Entomol 29:495–501

    Article  Google Scholar 

  • Milne DH, Giese RL (1970) Biology of the Columbian timber beetle, Corthylus columbianus (Coleoptera: Scolytidae). 10. Comparison of yearly mortality and dispersal losses with population densities. Entomol News 81:12–24

    Google Scholar 

  • Moore JC, Loggenberg A, Greeff JM (2006) Kin competition promotes dispersal in a male pollinating fig wasp. Biol Lett 2:17–19

    Article  PubMed  Google Scholar 

  • Mueller UG, Gerardo NM, Aanen DK, Six DL, Schultz TR (2005) The evolution of agriculture in insects. Ann Rev Ecol Evol Syst 36:563–595

    Article  Google Scholar 

  • Norusis M (2007) Generalized estimating equations. In: Norusis M (ed) SPSS 15.0 advanced statistical procedures companion. Prentice Hall, Upper Saddle River, pp 279–296

    Google Scholar 

  • Peer K, Taborsky M (2004) Female ambrosia beetles adjust their offspring sex ratio according to outbreeding opportunities for their sons. J Evol Biol 17:257–264

    Article  PubMed  CAS  Google Scholar 

  • Peer K, Taborsky M (2005) Outbreeding depression, but no inbreeding depression in haplodiploid ambrosia beetles with regular sibling mating. Evolution 59:317–323

    PubMed  Google Scholar 

  • Peer K, Taborsky M (2007) Delayed dispersal as a potential route to cooperative breeding in ambrosia beetles. Behav Ecol Sociobiol 61:729–739

    Article  Google Scholar 

  • R Development Core Team (2008) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • Reid RW (1958) The behaviour of the mountain pine beetle, Dendroctonus monticolae Hopk., during mating, egg laying, and gallery construction. Can Entomol 90:505–509

    Article  Google Scholar 

  • Roeper R, Treeful LM, O’Brien KM, Foote RA, Bunce MA (1980) Life history of the ambrosia beetle Xyleborus affinis (Coleoptera: Scolytidae) from in vitro culture. Great Lakes Entomol 13:141–144

    Google Scholar 

  • Roisin Y (1994) Intragroup conflicts and the evolution of sterile castes in termites. Am Nat 143:751–765

    Article  Google Scholar 

  • Schedl KE (1956) Breeding habits of arboricole insects in Central Africa. Verh 10 Int Kongr Entomol (Vienna) 1:183–197

    Google Scholar 

  • Schneider I (1987) Distribution, fungus-transfer and gallery construction of the ambrosia beetle Xyleborus affinis in comparison with X. mascarensis (Coleoptera, Scolytidae). Entomologia Generalis 12:267–275

    Google Scholar 

  • Stacey PB, Koenig WD (1990) Cooperative breeding in birds: long-term studies of ecology and behavior. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Stacey PB, Ligon JD (1991) The benefits-of-philopatry hypothesis for the evolution of cooperative breeding: variation in territory quality and group size effects. Am Nat 117:831–846

    Article  Google Scholar 

  • Sundstrom L (1995) Dispersal polymorphism and physiological condition of males and females in the ant, Formica truncorum. Behav Ecol 6:132–139

    Article  Google Scholar 

  • West-Eberhard MJ (1975) The evolution of social behaviour by kin selection. Q Rev Biol 50:1–33

    Article  Google Scholar 

  • Whitney HS (1971) Association of Dendroctonus ponderosae with blue stain fungi and yeasts during brood development in lodgepole pine. Can Entomol 103:1495–1503

    Article  Google Scholar 

  • Zeger SL, Liang KY (1986) Longitudinal data-analysis for discrete and continuous outcomes. Biometrics 42:121–130

    Article  PubMed  CAS  Google Scholar 

  • Zera AJ, Denno RF (1997) Physiology and ecology of dispersal polymorphism in insects. Ann Rev Entomol 42:207–230

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We are grateful to Stacy Blomqvist and Eric Ott for collecting X. affinis in the field and starting the first lab galleries. This manuscript benefitted greatly from comments of Tabea Turrini, Dik Heg and two anonymous reviewers. The study was supported by a cooperative agreement between the Department of Behavioral Ecology, University of Bern and the Southern Research Station, USDA Forest Service. PHWB is a recipient of a DOC fellowship of the Austrian Academy of Sciences at the Department of Behavioural Ecology, University of Bern, and was partly funded by a fellowship of the Roche Research Foundation.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Peter H. W. Biedermann.

Additional information

Communicated by N. Wedell

Appendix

Appendix

Fig. 3
figure 3

Total numbers of eggs produced by the two experimental groups of females 40 days after the treatment. Induced dispersers laid more eggs than delayed dispersers overall (GEE: P < 0.001). Numbers of daughter galleries included (induced dispersers/delayed dispersers): gallery1 (2/2), G2 (5/6), G3 (5/5), G4 (5/2), G5 (4/4) and G6 (12/11). Arithmetic means are shown with their standard errors

Fig. 4
figure 4

Comparison of the body weight of females from the two experimental groups collected in four galleries. There was no significant difference between induced and delayed dispersers (GEE: P = 0.95). Numbers of galleries included (induced dispersers/delayed dispersers): gallerya (9/2), Gb (12/7), Gc (4/1) and Gd (6/3). Arithmetic means of dry weight are shown with their standard errors

Rights and permissions

Reprints and permissions

About this article

Cite this article

Biedermann, P.H.W., Klepzig, K.D. & Taborsky, M. Costs of delayed dispersal and alloparental care in the fungus-cultivating ambrosia beetle Xyleborus affinis Eichhoff (Scolytinae: Curculionidae). Behav Ecol Sociobiol 65, 1753–1761 (2011). https://doi.org/10.1007/s00265-011-1183-5

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00265-011-1183-5

Keywords

Navigation