The evolution of simultaneous progressive provisioning revisited: extending the model to overlapping generations

  • Oliver Mitesser
  • Hans-Joachim Poethke
  • Erhard Strohm
  • Thomas Hovestadt
Original Article

Abstract

“Simultaneous progressive provisioners” feed their offspring gradually as they develop—and typically feed more than one offspring simultaneously (SIM) at a time. In contrast, “sequential mass provisioners” supply offspring one after another (SEQ). Utilizing individual-based simulations, Field (Nature 404:869–871, 2005) compared the lifetime reproductive success of these strategies in different scenarios. Accordingly, SEQ should evolve in the majority of cases—SIM only has an evolutionary benefit if offspring depend on their mothers’ protection until adulthood even past the provisioning period. However, this is only one potential explanation for the evolution of SIM. Here, we present an alternative mechanism for solitary individuals with overlapping generations. We propose an analytical model (comprising Field’s former approach) utilizing growth rate instead of lifetime reproductive success as a measure of fitness. Our model shows that multiplicative geometric effects on fitness would typically compensate for the demographic disadvantages of SIM (due to prolonged dependency) and consequently support the evolution of SIM over SEQ for a wide range of life history parameters. The optimal level of SIM (i.e., the optimal number of eggs laid simultaneously) is determined by offspring development time, survival rates, and foraging efficiency of the mother. Only extreme values of these demographic parameters would favor a transition to SEQ behavior. Our model provides a coherent explanation of selective favoring of SIM over SEQ that may also contribute to understanding why SIM is the dominant strategy among social insect species.

Significance statement

Workers in social insects typically feed several offspring simultaneously while solitary species with parental care—apart from a few exceptions—provision brood cells one after another. The provisioning pattern might play a prominent role in the evolutionary pathway to higher social organization. Based on a novel theoretical approach, we show that geometric growth benefits increase selection pressure towards simultaneous progressive provisioning in species with generation overlap. Such geometric benefits may specifically emerge in seasonal eusocial species. This result alters former assessment of causal mechanisms and extends findings focusing on solitary insects. It adds a new and reasonable explanation for the dominance of simultaneous provisioning among social species.

Keywords

Parental care Simultaneous provisioning Optimal clutch size Evolutionary model Social insects 

References

  1. Abramowitz M, Stegun IA (eds) (1965) Handbook of mathematical functions: with formulas, graphs, and mathematical tables, 9. Revised edition. Dover Publications, New YorkGoogle Scholar
  2. Batra SWT (1964) Behavior of the social bee, Lasioglossum zephyrum, within the nest (Hymenoptera: Halictidæ). Insect Soc 11:159–185. doi:10.1007/BF02222935 CrossRefGoogle Scholar
  3. Beekman M, Lingeman R, Kleijne FM, Sabelis MW (1998) Optimal timing of the production of sexuals in bumblebee colonies. Entomol Exp Appl 88:147–154. doi:10.1046/j.1570-7458.1998.00356.x CrossRefGoogle Scholar
  4. Benton TG, Grant A (2000) Evolutionary fitness in ecology: comparing measures of fitness in stochastic, density-dependent environments. Evol Ecol Res 2:769–789Google Scholar
  5. Bohart RM, Menke AS (1976) Sphecid wasps of the world: a generic revision. University of California Press, BerkeleyGoogle Scholar
  6. Bosch J, Maeta Y, Rust R (2001) A phylogenetic analysis of nesting behavior in the genus Osmia (Hymenoptera: Megachilidae). Ann Entomol Soc Am 94:617–627. doi:10.1603/0013-8746(2001)094[0617:APAONB]2.0.CO;2 CrossRefGoogle Scholar
  7. Cartar RV, Dill LM (1991) Costs of energy shortfall for bumble bee colonies: predation, social parasitism, and brood development. Can Entomol 123:283–293. doi:10.4039/Ent123283-2 CrossRefGoogle Scholar
  8. Chadab R (1979) Early warning cues for social wasps attacked by army ants. Psyche J Entomol 86:115–123. doi:10.1155/1979/38164 CrossRefGoogle Scholar
  9. Core Team R (2014) R: a language and environment for statistical computing. R Foundation for Statistical Computing, ViennaGoogle Scholar
  10. Cowan D (1991) The solitary and presocial Vespidae. In: Ross K, Matthews R (eds) The social biology of wasps. Cornell University Press, Ithaca, pp 33–73Google Scholar
  11. Duchateau MJ, Velthuis HHW (1988) Development and reproductive strategies in Bombus terrestris colonies. Behaviour 107:186–207. doi:10.1163/156853988X00340 CrossRefGoogle Scholar
  12. Dyer FC, Seeley TD (1991) Nesting behavior and the evolution of worker tempo in four honey bee species. Ecology 72:156–170. doi:10.2307/1938911 CrossRefGoogle Scholar
  13. Eickwort GC, Eickwort JM, Gordon J et al (1996) Solitary behavior in a high-altitude population of the social sweat bee Halictus rubicundus (Hymenoptera: Halictidae). Behav Ecol Sociobiol 38:227–233. doi:10.1007/s002650050236 CrossRefGoogle Scholar
  14. Engen S, Sæther BE (2017) R- and K-selection in fluctuating populations is determined by the evolutionary trade-off between two fitness measures: growth rate and lifetime reproductive success. Evolution 71:167–173. doi:10.1111/evo.13104 CrossRefPubMedGoogle Scholar
  15. Ferton C (1902) Notes détachées suri ‘instinct des Hyménoptères mellifères et ravisseurs avec la description de quelques espèces. Ann Soc Entom Fr LXXI:499–529Google Scholar
  16. Field J (2005) The evolution of progressive provisioning. Behav Ecol 16:770–778. doi:10.1093/beheco/ari054 CrossRefGoogle Scholar
  17. Field J, Brace S (2004) Pre-social benefits of extended parental care. Nature 428:650–652. doi:10.1038/nature02427 CrossRefPubMedGoogle Scholar
  18. Field J, Shreeves G, Sumner S, Casiraghi M (2000) Insurance-based advantage to helpers in a tropical hover wasp. Nature 404:869–871. doi:10.1038/35009097 CrossRefPubMedGoogle Scholar
  19. Field J, Turner E, Fayle T, Foster WA (2007) Costs of egg-laying and offspring provisioning: multifaceted parental investment in a digger wasp. Proc R Soc Lond B Biol Sci 274:445–451. doi:10.1098/rspb.2006.3745 CrossRefGoogle Scholar
  20. Freeman BE (1980) A population study in Jamaica on adult Sceliphron assimile (Dahlbom) (Hymenoptera: Sphecidae). Ecol Entomol 5:19–30. doi:10.1111/j.1365-2311.1980.tb01120.x CrossRefGoogle Scholar
  21. Greene A (1984) Production schedules of vespine wasps: an empirical test of the bang-bang optimization model. J Kansas Entomol Soc 57:545–568Google Scholar
  22. Herre EA, Wcislo WT (2011) In defence of inclusive fitness theory. Nature 471:E8–E9. doi:10.1038/nature09835 CrossRefPubMedGoogle Scholar
  23. Hunt JH (1999) Trait mapping and salience in the evolution of eusocial vespid wasps. Evolution:225–237Google Scholar
  24. Hunt JH, Amdam GV (2005) Bivoltinism as an antecedent to eusociality in the paper wasp genus Polistes. Science 308:264–267. doi:10.1126/science.1109724 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jeanne RL (1979) A latitudinal gradient in rates of ant predation. Ecology 60:1211–1224. doi:10.2307/1936968 CrossRefGoogle Scholar
  26. Jeanne RL (1991) The swarm-founding Polistinae. 191–231. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, IthacaGoogle Scholar
  27. Kukuk PF, Ward SA, Jozwiak A (1998) Mutualistic benefits generate an unequal distribution of risky activities among unrelated group members. Naturwissenschaften 85:445–449. doi:10.1007/s001140050528 CrossRefGoogle Scholar
  28. Longair RW (2004) Tusked males, male dimorphism and nesting behavior in a subsocial afrotropical wasp, Synagris cornuta, and weapons and dimorphism in the genus (Hymenoptera: Vespidae: Eumeninae). J Kans Entomol Soc 77:528–557. doi:10.2317/E-38.1 CrossRefGoogle Scholar
  29. Macevicz S, Oster G (1976) Modeling social insect populations II: optimal reproductive strategies in annual eusocial insect colonies. Behav Ecol Sociobiol 1:265–282CrossRefGoogle Scholar
  30. Malyshev SI (1968) Genesis of the Hymenoptera and the phases of their evolution. Richard Clay (The Chaucer Press), Ltd., BungayGoogle Scholar
  31. Mead F, Habersetzer C, Gabouriaut D, Gervet J (1994) Dynamics of colony development in the paper wasp Polistes dominulus Christ (Hymenoptera, Vespidae): the influence of prey availability. J Ethol 12:43–51. doi:10.1007/BF02350079 CrossRefGoogle Scholar
  32. Michener CD (2000) The bees of the world. John Hopkins University PressGoogle Scholar
  33. Mitesser O, Weissel N, Strohm E, Poethke H-J (2006) The evolution of activity breaks in the nest cycle of annual eusocial bees: a model of delayed exponential growth. BMC Evol Biol 6:45CrossRefPubMedPubMedCentralGoogle Scholar
  34. Oster G, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, PrincetonGoogle Scholar
  35. Pesenko YA, Banaszak J, Radchenko VG, Cierzniak T (2000) Bees of the family Halictidae excluding Sphecodes of Poland: taxonomy, ecology, bionomics. Wydawnictwo Uczelniane, BydgoszczGoogle Scholar
  36. Queller DC (1994) Extended parental care and the origin of eusociality. Proc R Soc Lond B Biol Sci 256:105–111. doi:10.1098/rspb.1994.0056 CrossRefGoogle Scholar
  37. Queller DC (1996) The origin and maintenance of eusociality: the advantage of extended parental care. In: Turillazzi S, West-Eberhard MJ (eds) Natural history and evolution of paper-wasps. Oxford University Press, Oxford, pp 218–234Google Scholar
  38. Reeve HK (1991) Polistes. In: Ross KG, Matthews RW (eds) The social biology of wasps. Cornell University Press, London, pp 99–148Google Scholar
  39. Richards OW, Richards MJ (1951) Observations on the social wasps of South America (Hymenoptera Vespidae). Trans R Entomol Soc Lond 102:1–169. doi:10.1111/j.1365-2311.1951.tb01241.x CrossRefGoogle Scholar
  40. Roff DA (2001) Life history evolution, 1st edn. Sinauer Associates, Inc., SunderlandGoogle Scholar
  41. Roubaud E (1916) Recherches biologiques sur les guêpes solitaires et sociales d’Afrique. Ann Sci Nat Zool 1:1–160Google Scholar
  42. Schatz B, Wcislo WT (1999) Ambush predation by the ponerine ant Ectatomma ruidum Roger (Formicidae) on a sweat bee Lasioglossum umbripenne (Halictidae), in Panama. J Insect Behav 12:641–663. doi:10.1023/A:1020927703689 CrossRefGoogle Scholar
  43. Seeley TD, Seeley RH, Akratanakul P (1982) Colony defense strategies of the honeybees in Thailand. Ecol Monogr 52:43–63. doi:10.2307/2937344 CrossRefGoogle Scholar
  44. Seger J (1983) Partial bivoltinism may cause alternating sex-ratio biases that favour eusociality. Nature 301:59–62. doi:10.1038/301059a0 CrossRefGoogle Scholar
  45. Spradbery JP (1973) Wasps. University of Washington Press, SeattleGoogle Scholar
  46. Strassmann JE, Orgren MCF (1983) Nest architecture and brood development times in the paper wasp, Polistes exclamans (Hymenoptera: Vespidae). Psyche J Entomol 90:237–248. doi:10.1155/1983/32347 CrossRefGoogle Scholar
  47. Strohm E, Marliani A (2002) The cost of parental care: prey hunting in a digger wasp. Behav Ecol 13:52–58. doi:10.1093/beheco/13.1.52 CrossRefGoogle Scholar
  48. Toft CA (1987) Population structure and survival in a solitary wasp (Microbembex cubana: Hymenoptera, Sphecidae, Nyssoninae). Oecologia 73:338–350. doi:10.1007/BF00385249 CrossRefPubMedGoogle Scholar
  49. Weissel N, Mitesser O, Liebig J et al (2006) The influence of soil temperature on the nesting cycle of the halictid bee Lasioglossum malachurum. Insect Soc 53:390–398. doi:10.1007/s00040-005-0884-7 CrossRefGoogle Scholar
  50. West-Eberhard MJ (2005) Behavior of the primitively social wasp Montezumia cortesioides Willink (Vespidae Eumeninae) and the origins of vespid sociality. Ethol Ecol Evol 17:201–215. doi:10.1080/08927014.2005.9522592 CrossRefGoogle Scholar
  51. Wilson EO (1971) The insects societies. Belknap Press of Harvard University PressGoogle Scholar
  52. Wilson EO (2008) One giant leap: how insects achieved altruism and colonial life. Bioscience 58:17–25. doi:10.1641/B580106 CrossRefGoogle Scholar
  53. Wolfram Research Inc. (2016) Mathematica, Version 10.4, Champaign, ILGoogle Scholar
  54. Yanega D (1997) Demography and sociality in halictine bees (Hymenoptera: Halictidae). In: Crespi BJ, Choe JC (eds) The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 293–315CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany 2017

Authors and Affiliations

  1. 1.Theoretical Evolutionary Ecology Group, Department of Animal Ecology and Tropical Biology, BiocenterUniversity of WürzburgWürzburgGermany
  2. 2.Field Station FabrikschleichachUniversity of WürzburgRauhenebrachGermany
  3. 3.Department for ZoologyUniversity of RegensburgRegensburgGermany

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