Skip to main content

Extreme polyandry in social Hymenoptera: evolutionary causes and consequences for colony organisation

  • Chapter

Abstract

Polyandry, the multiple mating of females with more than one male, is a behavioural pattern found throughout the animal kingdom. In eusocial Hymenoptera (the bees, wasps and ants) polyandry is present in many taxa, and also the species with the highest degrees of polyandry known so far are found in this group. Polyandry has evolved multiple times and the genera with polyandrous species provide excellent test systems to study the evolution of multiple mating and its consequences for natural selection. Polyandrous colonies are composed of many paternal subfamilies (= patrilines), creating conflict potential on the one hand, and a template for variability among the colony members on the other hand.

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

Buying options

Chapter
USD   29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD   49.99
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD   64.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD   99.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Learn about institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Alber M, Jordan M, Ruttner F, Ruttner H (1955) Von der Paarung der Honigbiene. Z Bienenforsch 3:1-28

    Google Scholar 

  • Amdam GV, Omholt SW (2003) The hive bee to forager transition in honeybee colonies: the double repressor hypothesis. J Theor Biol 223:451-64

    PubMed  CAS  Google Scholar 

  • Andersson M, Simmons LW (2006) Sexual selection and mate choice. Trends Ecol Evol 21:296-302

    PubMed  Google Scholar 

  • Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151-154

    CAS  Google Scholar 

  • Baer B, Morgan ED, Schmid-Hempel P (2001) A nonspecific fatty acid within the bumblebee mating plug prevents females from remating. Proc Natl Acad Sci USA 98:3926-3928

    PubMed  CAS  Google Scholar 

  • Beye M, Hasselmann M, Fondrk MK, Page RE Jr, Omholt SW (2003) The gene csd is the primary signal for sexual development in the honeybee and encodes an SR-type protein. Cell 114:419-429

    PubMed  CAS  Google Scholar 

  • Bonabeau E, Theraulaz G, Deneubourg J-L (1996) Quantitative study of the fixed threshold model for the regulation of division of labour in insect societies. Proc R Soc Lond B 263:1565-1569

    Google Scholar 

  • Boomsma JJ, Ratnieks FLW (1996) Paternity in eusocial Hymenoptera. Philos Trans R Soc Lond B 351:947-975

    Google Scholar 

  • Calderone NW, Page RE Jr (1988) Genotypic variability in age polyethism and task specialization in the honey bee, Apis mellifera (Hymenoptera: Apidae). Behav Ecol Sociobiol 22:17-25

    Google Scholar 

  • Calderone NW, Page RE Jr (1991) Evolutionary genetics of division-of-labour in colonies of the honeybee (Apis mellifera). Am Nat 138:69-92

    Google Scholar 

  • Campos LAO, Kerr WE, da Silva DLN (1979) Sex determination in bees. VIII. Relative action of genes xa and xb on sex determination in Melipona bees. Rev Bras Genet 2:267-280

    Google Scholar 

  • Cole BJ (1983) Multiple mating and the evolution of social behaviour in the Hymenoptera. Behav Ecol Sociobiol 12:191-201

    Google Scholar 

  • Crozier RH, Fjerdingstad EJ (2001) Polyandry in social Hymenoptera – disunity in diversity? Ann Zool Fenn 38:267-285

    Google Scholar 

  • Crozier RH, Page RE Jr (1985) On being the right size – male contributions and multiple mating in social Hymenoptera. Behav Ecol Sociobiol 18:105-115

    Google Scholar 

  • Darchen R, Delage-Darchen B (1971) Le déterminisme des castes chez les Trigones (Hyménoptères Apidés). Insect Soc 18:121-134

    Google Scholar 

  • Darchen R, Delage-Darchen B (1977) Sur le déterminisme des castes chez les Meliponinés (Hymenoptères: Apidés). Bull Biol Fr Belg 11:91-109

    Google Scholar 

  • Davidson DW (1982) Sexual selection in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex) Behav Ecol Sociobiol 10:245-250

    Google Scholar 

  • Denny AJ, Franks NR, Powell S, Edwards KJ (2004) Exceptionally high levels of multiple mating in an army ant. Naturwissenschaften 91:396-399

    PubMed  CAS  Google Scholar 

  • Estoup A, Solignac M, Harry M, Cornuet J-M (1993) Characterization of (GT)n and (CT)n microsatellites in two insect species: Apis mellifera and Bombus terrestris. Nuc Acids Res 21:1427-1431

    CAS  Google Scholar 

  • Estoup A, Garnery L, Solignac M, Cornuet J-M (1995) Microsatellite variation in honey bee (Apis mellifera L.) populations: hierarchical genetic structure and test of the infinite allele and stepwise mutation models. Genetics 140:679-695

    PubMed  CAS  Google Scholar 

  • Fewell JH, Page RE Jr (1999) The emergence of division of labour in forced associations of normally solitary ant queens. Evol Ecol Res 1:537-548

    Google Scholar 

  • Fewell JH, Page RE Jr (2000) Colony-level selection effects on individual and colony foraging task performance in honeybees, Apis mellifera L. Behav Ecol Sociobiol 48:173-181

    Google Scholar 

  • Franks NR (1985) Reproduction, foraging efficiency and worker polymorphism in army ants. In: Hölldobler B, Lindauer M (eds) Experimental Behavioral Ecology and Sociobiology: in Memoriam Karl von Frisch, 1886-1982, Vol 31. Sinauer Associates, Sunderland/MA, pp 91-107

    Google Scholar 

  • Frumhoff PС, Baker J (1988) A genetic component to division of labour within honey bee colonies. Nature 333:358-361

    Google Scholar 

  • Fuchs S, Moritz RFA (1999) Evolution of extreme polyandry in the honeybee Apis mellifera L. Behav Ecol Sociobiol 9:269-275

    Google Scholar 

  • Gotwald WH (1995) Army Ants: The Biology of Social Predation. Cornell University Press, Ithaca

    Google Scholar 

  • Greeff JM (1996) Effects of thelytokous worker reproduction on kin-selection and conflict in the Cape honeybee, Apis mellifera capensis. Philos Trans R Soc Lond B 351:617-625

    Google Scholar 

  • Haberl M, Tautz D (1998) Sperm usage in honey bees. Behav Ecol Sociobiol 42:247-255

    Google Scholar 

  • Hamilton WD (1964) The genetical evolution of social behaviour. J Theor Biol 7:1-16

    PubMed  CAS  Google Scholar 

  • Helanterä H, Strassmann JE, Carrillo J, Queller DC (2009) Unicolonial ants: where do they come from, what are they and where are they going? Trends Ecol Evol 24:341-349

    PubMed  Google Scholar 

  • Hillesheim E, Koeniger N, Moritz RFA (1989) Colony performance in honeybees (Apis mellifera capensis Esch) depends on the proportion of subordinate and dominant workers. Behav Ecol Sociobiol 24:291-296

    Google Scholar 

  • Hughes WOH, Sumner S, Van Borm S, Boomsma JJ (2003) Worker caste polymorphism has a genetic basis in Acromyrmex leaf-cutting ants. Proc Natl Acad Sci USA 100:9394-9397

    PubMed  CAS  Google Scholar 

  • Hughes WOH, Oldroyd BP, Beekman M, Ratnieks FLW (2008a) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213-1216

    CAS  Google Scholar 

  • Hughes WOH, Ratnieks FLW, Oldroyd BP (2008b) Multiple paternity or multiple queens: two routes to greater intracolonial genetic diversity in the eusocial Hymenoptera. J Evol Biol 21:1090-1095

    CAS  Google Scholar 

  • Jaffé R, Kronauer DJC, Kraus FB, Boomsma JJ, Moritz RFA (2007) Worker caste determination in the army ant Eciton burchellii. Biol Lett 3:513-516

    PubMed  Google Scholar 

  • Jennions MD, Petrie M (2000) Why do females mate multiply? A review of the genetic benefits. Biol Rev 75:21-64

    PubMed  CAS  Google Scholar 

  • Keller L, Genoud M (1997) Extraordinary lifespans in ants: a test of evolutionary theories of ageing. Nature 389:958-960

    CAS  Google Scholar 

  • Keller L, Reeve HK (1994) Genetic variability, queen number, and polyandry in social Hymenoptera. Evolution 48:694-704

    Google Scholar 

  • Keller L, Reeve HK (1995) Why do females mate with multiple males? The sexually selected sperm hypothesis. Adv Stud Behav 24:291-315

    Google Scholar 

  • Keller L, Ross KG (1995) Gene by environment interaction – effects of a singlegene and social environment on reproductive phenotypes of fire ant queens. Funct Ecol 9:667-676

    Google Scholar 

  • Kerr WE (1950) Genetic determination of castes in the genus Melipona. Genetics 35:143-152

    PubMed  CAS  Google Scholar 

  • Kolmes SA, Winston ML, Fergusson LA (1989) The division of labor among worker honey bees – the effects of multiple patrilines. J Kansas Entomol Soc 62:80-95

    Google Scholar 

  • Kraus FB, Neumann P, van Praagh J, Moritz RFA (2004) Sperm limitation and the evolution of extreme polyandry in honeybees (Apis mellifera L.). Behav Ecol Sociobiol 55:494-501

    Google Scholar 

  • Kronauer DJC, Boomsma JJ (2007) Multiple queens means fewer mates. Curr Biol 17:R753-R755

    PubMed  CAS  Google Scholar 

  • Kronauer DJC, Schöning C, Pedersen JS, Boomsma JJ, Gadau J (2004) Extreme queen-mating frequency and colony fission in African army ants. Mol Ecol 13:2381-2388

    PubMed  Google Scholar 

  • Kronauer DJC, Berghoff SM, Powell S, Denny AJ, Edwards KJ, Franks NR, Boomsma JJ (2006) A reassessment of the mating system characteristics of the army ant Eciton burchellii. Naturwissenschaften 93:402-406

    PubMed  CAS  Google Scholar 

  • Kronauer DJC, Johnson RA, Boomsma JJB (2007) The evolution of multiple mating in army ants. Evolution 61:413-422

    PubMed  Google Scholar 

  • Lattorff HMG, Moritz RFA, Fuchs S (2005) A single locus determines thelytokous parthenogenesis of laying honeybee workers (Apis mellifera capensis). Heredity 94:533-537

    PubMed  CAS  Google Scholar 

  • Lattorff HMG, Moritz RFA, Crewe RM, Solignac M (2007) Control of reproductive dominance by the thelytoky gene in honeybees. Biol Lett 3:292-295

    PubMed  CAS  Google Scholar 

  • Linksvayer TA, Fondrk MK, Page RE Jr (2009) Honeybee social regulatory networks are shaped by colony-level selection. Am Nat 173:E99-E107

    PubMed  Google Scholar 

  • Mattila HR, Seeley TD (2007) Genetic diversity in honey bee colonies enhances productivity and fitness. Science 317:362-364

    PubMed  CAS  Google Scholar 

  • Mays HL Jr, Hill GE (2004) Choosing mates: good genes versus genes that are a good fit. Trends Ecol Evol 19:554-559

    PubMed  Google Scholar 

  • Moritz RFA (1985) The effects of multiple mating on the worker-queen conflict in Apis mellifera L. Behav Ecol Sociobiol 16:375-377

    Google Scholar 

  • Moritz RFA (1986) Intracolonial worker relationship and sperm competition in the honeybee (Apis mellifera L). Experientia 42:445-448

    Google Scholar 

  • Moritz RFA, Haberl M (1994) Lack of meiotic recombination in thelytokous parthenogenesis of laying workers of Apis mellifera capensis (the Cape honeybee). Heredity 73:98-102

    Google Scholar 

  • Moritz RFA, Kryger P, Koeniger G, Koeniger N, Estoup A, Tingek S (1995) High degree of polyandry in Apis dorsata queens detected by DNA microsatellite variability. Behav Ecol Sociobiol 37:357-363

    Google Scholar 

  • Moritz RFA, Kryger P, Allsopp MH (1996) Competition for royalty in bees. Nature 384:31

    CAS  Google Scholar 

  • Moritz RFA, Simon UE, Crewe RM (2000) Pheromonal contest between honeybee workers (Apis mellifera capensis). Naturwissenschaften 87:395-397

    PubMed  CAS  Google Scholar 

  • Moritz RFA, Pflugfelder J, Crewe RM (2003) Lethal fighting between honeybee queens and parasitic workers (Apis mellifera). Naturwissenschaften 90:378-381

    PubMed  CAS  Google Scholar 

  • Moritz RFA, Lattorff HMG, Neumann P, Kraus FB, Radloff SE, Hepburn HR (2005) Rare royal families in honeybees, Apis mellifera. Naturwissenschaften 92:488-491

    PubMed  CAS  Google Scholar 

  • Nelson CM, Ihle KE, Fondrk MK, Page RE Jr, Amdam GV (2007) The gene vitellogenin has multiple coordinating effects on social organization. Plos Biol 5: 5:e62, doi: 10.1371/journal.pbio.0050062

    Google Scholar 

  • Neumann P, Moritz RFA (2002) The Cape honeybee phenomenon: the sympatric evolution of a social parasite in real time? Behav Ecol and Sociobiol 52:271-281

    Google Scholar 

  • O’Donnell S (1998) Dominance and polyethism in the eusocial wasp Mischocyttarus mastigophorus (Hymenoptera: Vespidae). Behav Ecol Sociobiol 43:327-331

    Google Scholar 

  • Oldroyd BP, Rinderer TE, Harbo JR, Buco SM (1992) Effects of intracolonial genetic diversity on honey-bee (Hymenoptera, Apidae) colony performance. Ann Entomol Soc Am 85:335-343

    Google Scholar 

  • Onions GW (1912) South African ‘fertile worker bees’. Agr J Union S Afr 1:720-728

    Google Scholar 

  • Oster GF, Wilson EO (1978) Caste and Ecology in the Social Insects. Princeton University Press, Princeton

    Google Scholar 

  • Page RE Jr (1986) Sperm utilization in social insects. Annu Rev Entomol 31:297-320

    Google Scholar 

  • Page RE Jr, Amdam GV (2007) The making of a social insect: developmental architectures of social design. Bioessays 29:334-343

    PubMed  CAS  Google Scholar 

  • Page RE Jr, Mitchell SD (1998) Self-organization and the evolution of division of labor. Apidologie 29:171-190

    Google Scholar 

  • Page RE Jr, Robinson GE, Fondrk MK (1989) Genetic specialists, kin recognition and nepotism. Nature 338:576-579

    Google Scholar 

  • Page RE Jr, Erber J, Fondrk MK (1998) The effect of genotype on response thresholds to sucrose and foraging behavior of honey bees (Apis mellifera L.). J Comp Physiol A 182:489-500

    PubMed  Google Scholar 

  • Palmer KA, Oldroyd BP (2000) Evolution of multiple mating in the genus Apis. Apidologie 31:235-248

    Google Scholar 

  • Ratnieks FLW (1988) Reproductive harmony via mutual policing by workers in eusocial Hymenoptera. Am Nat 132:217-236

    Google Scholar 

  • Ratnieks FLW, Boomsma JJ (1995) Facultative sex allocation by workers and the evolution of polyandry by queens in social Hymenoptera. Am Nat 145:969-993

    Google Scholar 

  • Ratnieks FLW, Boomsma JJ (1997) On the robustness of split sex ratio predictions in social Hymenoptera. J Theor Biol 185:423-439

    Google Scholar 

  • Rheindt FE, Strehl CP, Gadau J (2005) A genetic component in the determination of worker polymorphism in the Florida harvester ant Pogonomyrmex badius. Insectes Soc 52:163-168

    Google Scholar 

  • Robinson GE, Page RE Jr (1989) Genetic determination of nectar foraging, pollen foraging, and nest-site scouting in honey bee colonies. Behav Ecol Sociobiol 24:317-323

    Google Scholar 

  • Robinson GE, Page RE Jr (1995) Genotypic constraints on plasticity for corpse removal in honey bee colonies. Anim Behav 49:867-876

    Google Scholar 

  • Ross KG, Vargo EL, Keller L (1996) Simple genetic basis for important social traits in the fire ant Solenopsis invicta. Evolution 50:2387-2399

    Google Scholar 

  • Ruttner H (1980) Haltung der Königinnen während der Paarungszeit. In: Ruttner F (ed) Königinnenzucht. Apimondia, Bukarest, pp 225-267

    Google Scholar 

  • Ruttner F, Koeniger G (1971) Die Füllung der Spermatheka der Bienenkönigin. Z Vgl Physiol 72:411-422

    Google Scholar 

  • Scheiner R, Page RE Jr, Erber J (2001) The effects of genotype, foraging role, and sucrose responsiveness on the tactile learning performance of honey bees (Apis mellifera L.). Neurobiol Learn Mem 76:138-150

    PubMed  CAS  Google Scholar 

  • Schlüns H, Koeniger G, Koeniger N, Moritz RFA (2004) Sperm utilization pattern in the honeybee (Apis mellifera). Behav Ecol Sociobiol 56:458-463

    Google Scholar 

  • Schlüns H, Moritz RFA, Neumann P, Kryger P, Koeniger G (2005) Multiple nuptial flights, sperm transfer and the evolution of extreme polyandry in honeybee queens. Anim Behav 70:125-131

    Google Scholar 

  • Schmid-Hempel P (1994) Infection and colony variability in social insects. Philos Trans R Soc Lond B 346:313-321

    Google Scholar 

  • Schmid-Hempel P, Crozier RH (1999) Polyandry versus polygyny versus parasites. Philos Trans R Soc Lond B 354:507-515

    Google Scholar 

  • Schwander T, Keller L (2008) Genetic compatibility affects queen and worker caste determination. Science 322:552

    PubMed  CAS  Google Scholar 

  • Simon UE, Moritz RFA, Crewe RM (2005) Reproductive dominance among honeybee workers in experimental groups of Apis mellifera capensis. Apidologie 36:413-419

    Google Scholar 

  • Snyder LE (1993) Non-random behavioral interactions among genetic subgroups in a polygynous ant. Anim Behav 46:431-439

    Google Scholar 

  • Starr CK (1985) Sperm competition, kinship and sociality in the aculeate Hymenoptera. In: Smith RL (ed) Sperm Competition and the Evolution of Animal Mating Systems. Academic Press, New York, pp 428-464

    Google Scholar 

  • Stuart RJ, Page RE Jr (1991) Genetic component to division of labor among workers of a leptothoracine ant. Naturwissenschaften 78:375-377

    Google Scholar 

  • Tarpy DR, Page RE Jr (2000) No behavioral control over mating frequency in queen honey bees (Apis mellifera L.): implications for the evolution of extreme polyandry. Am Nat 155:820-827

    PubMed  Google Scholar 

  • Trivers RL, Hare H (1976) Haplodiploidy and theevolution of the social insects. Science 191:249-263

    PubMed  CAS  Google Scholar 

  • Vahed K (1998) The function of nuptial feeding in insects: review of empirical studies. Biol Rev 73:43-78

    Google Scholar 

  • van Wilgenburg E, Driessen G, Beukeboom L (2006) Single locus complementary sex determination in Hymenoptera: an ‘unintelligent’ design? Front Zool 3:1

    PubMed  Google Scholar 

  • Wang Y, Amdam GV, Rueppell O, Wallrichs MA, Fondrk MK, Kaftanoglu O, Page RE Jr (2009) PDK1 and HR46 gene homologs tie social behavior to ovary signals. PloS ONE 4:e4899, doi:10.1371/journal.pone.0004899

    Google Scholar 

  • Wattanachaiyingcharoen W, Oldroyd BP, Wongsiri S, Palmer K, Paar R (2003) A scientific note on the mating frequency of Apis dorsata. Apidologie 34:85-86

    Google Scholar 

  • Wenseleers T, Ratnieks FLW (2006) Comparative analysis of worker reproduction and policing in eusocial Hymenoptera supports relatedness theory. Am Nat 168:E163-E179

    PubMed  Google Scholar 

  • West-Eberhard MJ (1987) Flexible strategy and social evolution. In: Ito Y, Brown JL, Kikkawa J (eds) Animal Societies, Theories and Facts. Japan Scientific Societies, Tokyo, pp 35-51

    Google Scholar 

  • West-Eberhard MJ (1996) Wasp societies as microcosms for the study of development and evolution. In: Turillazzi S, West-Eberhard MJ (eds) Natural History and Evolution of Paper Wasps. Oxford University, New York, pp 290-317

    Google Scholar 

  • Woyke J (1964) Causes of repeated mating flights by queen honeybees. J Apic Res 3:17-23

    Google Scholar 

  • Woyke J (1965) Genetic proof of the origin of diploid drones from fertilised eggs of the honeybee. J Apic Res 4:7-11

    Google Scholar 

  • Yue C, Schröder M, Gisder S, Genersch E (2007) Vertical-transmission routes for deformed wing virus of honeybees (Apis mellifera). J Gen Virol 88:2329-2336

    PubMed  CAS  Google Scholar 

  • Zeh JA, Zeh DW (1996) The evolution of polyandry. I. Intragenomic conflict and genetic incompatibility. Proc R Soc Lond B 263:1711-1717

    Google Scholar 

  • Zeh JA, Zeh DW (1997) The evolution of polyandry. II. Post-copulatory defences against genetic incompatibility. Proc R Soc Lond B 264:69-75

    Google Scholar 

  • Zeh JA, Zeh DW (2001) Reproductive mode and the genetic benefits of polyandry. Anim Behav 61:1051-1063

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2010 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Kraus, F., Moritz, R. (2010). Extreme polyandry in social Hymenoptera: evolutionary causes and consequences for colony organisation. In: Kappeler, P. (eds) Animal Behaviour: Evolution and Mechanisms. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-642-02624-9_14

Download citation

Publish with us

Policies and ethics