Skip to main content
SpringerLink
Log in

Multiple mating and the evolution of social behavior in the hymenoptera

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

Summary

The data on the frequency of mating by queens of eusocial Hymenoptera are reviewed.

It is pointed out that the issue of sperm clumping is probably irrelevant to the evolution of eusociality.

The hypothesis is presented that multiple mating is an adaptation for maintaining large colonies. In ants there is a significant relation between the size of the colony and the frequency of mating.

The effect of multiple mating on the spread of a gene for worker behavior is explored. If a female mates twice, the effective number of matings is less than two except in the case of identical sperm contribution by the males.

Sperm bias is defined as the contribution of unequal amounts of sperm by the males that mate with a queen. Sperm bias can be produced as a sampling phenomenon, by inter-male competition for females and by sperm competition.

The relation between the ergonomic efficiency of the workers at the production of reproductives and the number of matings that is consistent with the evolution of eusociality is derived. If workers are only about 10% more efficient at producing reproductives within a eusocial colony than they are solitarily, then two matings by the queen will still produce a selective advantage to eusocial behavior.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alexander RD, Sherman PW (1977) Local mate competition and parental investment in social insects. Science 196:494–500

    Google Scholar 

  • Barrows EM (1975) Mating behavior in halictine bees (Hymen: Halictidae) III. Copulatory behavior and olfactory communication. Insectes Soc 22:307–331

    Google Scholar 

  • Barrows EM, Chabot MR, Michener CD, Snyder TP (1979) Foraging and mating behavior in Perdita texana. J Kans Entomol Soc 49:275–179

    Google Scholar 

  • Batra SWT (1966) Life cycle and behavior of the primitively social bee Lasioglossum zephyrum. Univ Kans Sci Bull 46:359–423

    Google Scholar 

  • Batra SWT (1978) Aggression, territoriality, mating and nest aggregation of some solitary bees. J Kans Entomol Soc 51:547–559

    Google Scholar 

  • Brian MV (1950) The stable winter population structure i species of Myrmica. J Anim Ecol 19:119–123

    Google Scholar 

  • Brian MV (1957) The growth and development of colonies of the ant Myrmica. Insectes Soc 4:177–190

    Google Scholar 

  • Brian MV (1965) Social insect populations Academic Press, London

    Google Scholar 

  • Brothers DJ (1972) Biology and immature stages of Pseudomethoca f. frigida with notes on other species (Hymenoptera: Mutillidae). Univ Kans Sci Bull 50:1–38

    Google Scholar 

  • Carpenter FW, Hermann HR (1979) Antiquity of sociality in insects. In: Hermann HR (ed) Social insects, vol 1. Academic Press, New York, pp 81–89

    Google Scholar 

  • Charnov EL (1978a) Sex ratio selection in eusocial hymenoptera. Am Nat 112:317–326

    Google Scholar 

  • Charnov EL (1978b) Evolution of eusocial behavior: offspring choice or parental parasitism? J Theor Biol 75:451–465

    Google Scholar 

  • Craig R, Crozier RH (1979) Relatedness in the polygynous ant Myrmecia pilosula. Evolution 33:335–341

    Google Scholar 

  • Crozier RH (1973) Apparent differential selection at an isozyme locus between queens and workers of the ant Aphaenogaster rudis. Genetics 73:313–318

    Google Scholar 

  • Crozier RH (1977) Genetic differentiation between populations of the ant Aphaenogaster rudis in the southeastern United States Genetica 47:17–36

    Google Scholar 

  • DaSilva DL, Zucchhi NR, Kerr WE (1972) Biological and behavioral aspects of reproduction in some species of Melipona (Hymenoptera, Apidae, Meliponinae). Anim Behav 20:123–132

    Google Scholar 

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

    Google Scholar 

  • Donisthorpe H St JK (1915) British ants. Brendon, Plymouth

    Google Scholar 

  • Forel A (1928) The social world of ants, vol II (Translated by Ogden CK). Putnam, New York

    Google Scholar 

  • Greene A, Akre RD, Landolt PJ (1978) Behavior of the yellow-jecket social parasite Dolichovespula arctica (Rohmer) Melanderia 29:1–28

    Google Scholar 

  • Halliday RB (1975) Electrophoretic variation of amylase in meat ants, Irdomyrmex purpureus, and its taxonomic significance. Aust J Zool 23:271–276

    Google Scholar 

  • Halliday RB (1979) Esterase variation at three loci in meat ants. J Hered 70:57–61

    Google Scholar 

  • Hamilton WD (1964) The genetical theory of social behavior. I, II. J Theor Biol 7:1–52

    Google Scholar 

  • Hamilton WD (1972) Altruism and related phenomena, mostly in social insects. Annu Rev Syst Ecol 3:193–232

    Google Scholar 

  • Headley AE (1949) A population study of the ant Aphaenogster fulva ssp. aquia Buckley (Hymenoptera, Formicidae). Ann Entomol Soc Am 42:265–272

    Google Scholar 

  • Hobbs GA (1967) Ecology of species of Bombus (Hymenoptera: Apidae) in southern Alberta. VI. Subgenus Pyrobombus. Can Entomol 99:1271–1292

    Google Scholar 

  • Hölldobler B (1976) The behavioral ecology of mating in harvester ants (Hymenoptera: Formicidae: Pogonomyrmex). Behav Ecol and Sociobiol 1:405–423

    Google Scholar 

  • Hung AC-F, Vinson SB (1976) Biochemical evidence for queen monogamy and sterile male diploidy in the fire ant, Solenopsis invicta. Isozyme Bull 4:55

    Google Scholar 

  • Ito M, Imamura S (1974) Observations on the nuptial flight and internidal relationship in a polydomous ant, Formica yessensis Forel. J Fac Sci Hokkaido Univ Ser VI Zool 19:681–694

    Google Scholar 

  • Kannowski PB (1963) The flight activities of formicine ants. Symp Genet Biol (Italica) 12:74–102

    Google Scholar 

  • Kannowski PB, Kannowski P (1957) The mating activities of the ant Myrmica americana Weber, Ohio J Sci 57:371

    Google Scholar 

  • Kemper H, Dohring E (1961) Zur Frage nach der Volksstärke und der Vermehrungspotenz bei den sozialen Faltenwespen Deutschlands. Z Angew Zool 48:163–197

    Google Scholar 

  • Kemper H, Dohring E (1967) Die Sozialen Faltenwespen Mitteleuropas. Parey, Berlin Hamburg

    Google Scholar 

  • Kerr W (1961) Acasalamento de rainhas com varios machos em duas especies da Tribu Attini (Hymenoptera, Formicidea). Rev Brasil Biol 21:45–48

    Google Scholar 

  • Kerr WE (1969) Some aspects of the evolution of social bees. Evol Biol 3:119–175

    Google Scholar 

  • Kerr W, Zucchi R, Nakadaira JT, Botolo JE (1962) Reproduction in the social bees. J NY Entomol Soc 70:265–76

    Google Scholar 

  • Lavigne R (1969) Bionomics and nest structure of Pogonomyrmex occidentalis (Hymenoptera: Formicidae). Ann Entomol Soc Am 62:1166–1175

    Google Scholar 

  • Lin N, Michener CD (1972) Evolution and selection in social insects. Q Rev Biol 47:131–159

    Google Scholar 

  • Lindauer M, Kerr W (1960) Communication between the workers of stingless bees. Bee World 41:29–41, 65–71

    Google Scholar 

  • MacDonald JF, Akre RD, Hill WB (1974) Comparative biology and behavior of Vespula atripilosa and V. pennsylvanica (Hymenoptera: Vespidae). Melanderia 18:1–66

    Google Scholar 

  • MacKay WP (1981) A comparison of the nest phenologies of three species of Pogonomyrmex harvester ants (Hymenoptera: Formicidae). Psyche 88:25–74

    Google Scholar 

  • Marchal P (1896) La reproduction et l'evolution des guepes sociales. Arch Zool Exp 4:1–100

    Google Scholar 

  • Marikovsky PI (1961) Material on sexual biology of the ant Formica rufa L. Insectes Soc 4:23–30

    Google Scholar 

  • Markin GP, Dillier JH, Collins HL (1973) Growth and development of colonies of the red imported fire ant, Solenopsis invicta. Ann Entomol Soc Am 66:803–808

    Google Scholar 

  • Metcalf RA (1980) Sex ratios, parent-offspring conflict and local competition for mates in the social wasps Polistes metricus and Polistes variatus. Am Nat 116:642–654

    Google Scholar 

  • Metcalf RA, Whitt GS (1977) Intra-nest relatedness in the social wasp Polistes metricus. Behav Ecol Sociobiol 2:339–351

    Google Scholar 

  • Michener CD (1974) The social behavior of the bees: a comparative study. Harvard/Belknap Press, Cambridge (Massachusetts)

    Google Scholar 

  • Michener CD, Lange RB (1958) Observations on the ethology of neotropical anthophorine bees. Univ Kans Sci Bull 39:69–96

    Google Scholar 

  • Nagel HG, Rettenmeyer CW (1973) Nuptial flights, reproductive behavior and colony founding of the western harvester ant, Pogonomyrmex occidentalis (Hymenoptera: Formicidae). J Kans Entomol Soc 46:82–101

    Google Scholar 

  • Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Monographs in population biology, vol 12. Princeton University Press, Princeton (New Jersey)

    Google Scholar 

  • Page RE (1982) Polyandry in Brachymyremex depilis emery (Hymenoptera: Formicidae). Pan Pac Entomol (in press)

  • Page RE, Metcalf RA (1982) Multiple mating, sperm utilization and social evolution. Am Nat 119:263–281

    Google Scholar 

  • Pamilo P, Rosengren R, Vepsalainen K, Varvio-Aho S-L, Pisarski B (1978) Population structure of Formica ants. I. Patterns of enzyme gene variation. Hereditas 89:233–248

    Google Scholar 

  • Pamilo P, Varvio-Aho S-L (1979) Genetic structure of nests in the ant Formica sanguinea. Behav Ecol Sociobiol 6:91–98

    Google Scholar 

  • Parker GA (1970) Sperm competition and its evolutionary consequences in the insects. Biol Rev 45:525–568

    Google Scholar 

  • Plateaux-Quenu C (1962) Biology of Halictus marginatus Brulle. J Apicult Res 1:44–51

    Google Scholar 

  • Pontin AJ (1978) The numbers and distribution of subterranean aphids and their exploitation by the ant Lasius flavus (Fabr.). Ecol Entomol 3:203–207

    Google Scholar 

  • Rettenmeyer CW (1963) Behavioral studies of army ants. Univ Kans Sci Bull 44:281–465

    Google Scholar 

  • Ribband CR (1953) The behavior and social life of honeybees. Bee Research Association, London

    Google Scholar 

  • Rogers L, Lavigne R, Miller JL (1972) Bioenergetics of the western harvester ant in the shortgrass plains ecosystem. Environ Entomol 1:763–8

    Google Scholar 

  • Scherba G (1961) Nest structure and reproduction in the mound-building ant Formica opaciventris Emery in Wyoming. J NY Entomol Soc 69:71–87

    Google Scholar 

  • Schnierla TC (1971) Army ants: a study in social organization. Topoff HR (ed). Freeman, San Francisco (California)

    Google Scholar 

  • Schulz-Langer E (1954) Beobachtungen zur Copulation gefangenegehaltener Wespen. Zool Anz 152:39–42

    Google Scholar 

  • Starr CK (1979) Origin and evolution of insect sociality: a review of modern theory. In: Hermann HR (ed) Social insects, vol I. Academic Press, New York, pp 35–79

    Google Scholar 

  • Stauffer HB (1979) A derivation for the Weibull distribution. J Ther Biol 81:55–63

    Google Scholar 

  • Taber S (1955) Sperm distribution in the spermathecae of multiplymated queen honeybees. J Econ Entomol 48:522–525

    Google Scholar 

  • Taber S IV, Wendel J (1958) Concerning the number of times queen bees mate. J Econ Entomol 51:786–789

    Google Scholar 

  • Talbot M (1943) Population studies of the ant, Prenolepis imparis Say. Ecology 24:31–44

    Google Scholar 

  • Talbot M (1945) A comparison of flights of four species of ants. Am Midl Nat 34:504–510

    Google Scholar 

  • Talbot M (1951) Populations and hibernating conditions of the ant Aphaenogaster (Attomyrma) rudis Emery (Hymenoptera: Formicidae). Ann Entomol Soc Am 44:302–307

    Google Scholar 

  • Talbot M (1959) Flight activities of two species of ants of the genus Formica. Am Midl Nat 61:124–132

    Google Scholar 

  • Talbot M (1971) Flights of the ant Formica dakotensis Emery. Psyche 78:169–179

    Google Scholar 

  • Talbot M (1972) Flights and swarms of the ant Formica obscuripes Forel. J Kans Entomol Soc 45:254–258

    Google Scholar 

  • Thomas CR (1960) The European Wasp (Vespula germanica Fab.) in New Zealand. Inf Ser Dept Sci Ind Res (New Zealand) 27:1–74

    Google Scholar 

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

    Google Scholar 

  • Ward PS (1978) Genetic variation, colony structure and social behavior in the Rhytidoponera impressa group, a species complex of ponerine ants. Ph D dissertation, University of Sydney (Australia)

  • Ward PS (1981) Ecology and life history of the Rhytidoponera impressa group (Hymenoptera: Formicidae) II. Colony origin, seasonal cycles and reproduction. Psyche 88:109–126

    Google Scholar 

  • Weber NA (1935) The biology of the thatching ant, Formica rufa obscuripes Forel, in North Dakota. Ecol Monogr 5:165–206

    Google Scholar 

  • Weber NA (1972) Gardening Ants: The Attines. American Philosophicl Society, Philadelphia (Pennsylvania)

    Google Scholar 

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

    Google Scholar 

  • Whitford WG, Bryant M (1979) Behavior of a predator and its prey: the horned lizard (Phrynosoma cornutum) and harvester ants (Pogonomyrmex spp.) Ecology 60:686–894

    Google Scholar 

  • Wildermuth VL, Davis EG (1931) The red harvester ant and how to subdue it. Farmer's Bull US Dept Agricult 1668:1–12

    Google Scholar 

  • Wilson EO (1957) The organization of a nuptial flight of the ant Pheidole sitarches Wheeler. Psyche 64:46–50

    Google Scholar 

  • Wilson EO (1971) The insect societies. Harvard/Belknap Press, Cambridge (Massachusetts)

    Google Scholar 

  • Woyke J (1973) Reproduction in Apis cerana. I. Mating behavior. J Apic Res 11:141–146

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Biology, University of Utah, 84112, Salt Lake City, Utah, USA

    Blaine J. Cole

Authors
  1. Blaine J. Cole
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

Cole, B.J. Multiple mating and the evolution of social behavior in the hymenoptera. Behav Ecol Sociobiol 12, 191–201 (1983). https://doi.org/10.1007/BF00290771

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00290771

Keywords

Search

Navigation