Abstract
Genetic diversity might increase the performance of social groups by improving task efficiency or disease resistance, but direct experimental tests of these hypotheses are rare. We manipulated the level of genetic diversity in colonies of the Argentine ant Linepithema humile, and then recorded the short-term task efficiency of these experimental colonies. The efficiency of low and high genetic diversity colonies did not differ significantly for any of the following tasks: exploring a new territory, foraging, moving to a new nest site, or removing corpses. The tests were powerful enough to detect large effects, but may have failed to detect small differences. Indeed, observed effect sizes were generally small, except for the time to create a trail during nest emigration. In addition, genetic diversity had no statistically significant impact on the number of workers, males and females produced by the colony, but these tests had low power. Higher genetic diversity also did not result in lower variance in task efficiency and productivity. In contrast to genetic diversity, colony size was positively correlated with the efficiency at performing most tasks and with colony productivity. Altogether, these results suggest that genetic diversity does not strongly improve short-term task efficiency in L. humile, but that worker number is a key factor determining the success of this invasive species.
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References
Anderson C, Ratnieks FLW (1999) Task partitioning in insect societies. I. Effect of colony size on queueing delay and colony ergonomic efficiency. Am Nat 154:521–535
Baer B, Schmid-Hempel P (1999) Experimental variation in polyandry affects parasite loads and fitness in a bumble-bee. Nature 397:151–154
Baer B, Schmid-Hempel P (2001) Unexpected consequences of polyandry for parasitism and fitness in the bumblebee, Bombus terrestris. Evolution 55:1639–1643
Benois A (1973) Incidences des facteurs écologiques sur le cycle annuel et l’activité saisonnière de la fourmi d’Argentine Iridomyrmex humilis (Mayr) (Hymenoptera, Formicidae), dans la région d’Antibes. Insectes Soc 20:267–296
Beshers SN, Fewell JH (2001) Models of division of labor in social insects. Annu Rev Entomol 46:413–440
Boomsma JJ, Ratnieks FLW (1996) Paternity in eusocial Hymenoptera. Philos Trans R Soc Lond B 351:947–975
Bourke AFG, Franks NR (1995) Social evolution in ants. Princeton University Press, Princeton
Brown MJF, Schmid-Hempel P (2003) The evolution of female multiple mating in social hymenoptera. Evolution 57:2067–2081
Cahan SH, Keller L (2003) Complex hybrid origin of genetic caste determination in harvester ants. Nature 424:306–309
Cahan SH, Parker JD, Rissing SW, Johnson RA, Polony TS, Weiser MD, Smith DR (2002) Extreme genetic differences between queens and workers in hybridizing Pogonomyrmex harvester ants. Proc R Soc Lond B 269:1871–1877
Carlin NF, Reeve HK, Cover SP (1993) Kin discrimination and division of labour among matrilines in the polygynous carpenter ant, Camponotus planatus. In: Keller L (ed) Queen number and sociality in insects. Oxford University Press, Oxford, pp 362–401
Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72
Cohen J (1988) Statistical power analysis for the behavioral sciences. Erlbaum, Hillsdale, NJ
Cole BJ, Wiernasz DC (1999) The selective advantage of low relatedness. Science 285:891–893
Cole BJ, Wiernasz DC (2000) Colony size and reproduction in the western harvester ant, Pogonomyrmex occidentalis. Insectes Soc 47:249–255
Costa JT, Ross KG (2003) Fitness effects of group merging in a social insect. Proc R Soc Lond B 270:1697–1702
Crozier RH, Fjerdingstad EJ (2001) Polyandry in social Hymenoptera—disunity in diversity? Ann Zool Fenn 38:267–285
Crozier RH, Page RE (1985) On being the right size: male contributions and multiple mating in social Hymenoptera. Behav Ecol Sociobiol 18:105–115
Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, Oxford
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839
Erdfelder E, Faul F, Buchner A (1996) GPOWER: a general power analysis program. Behav Res Methods Instrum Comput 28:1–11
Fjerdingstad EJ, Gertsch PJ, Keller L (2003) The relationship between multiple mating by queens, within-colony genetic variability and fitness in the ant Lasius niger. J Evol Biol 16:844–853
Fraser VS, Kaufmann B, Oldroyd BP, Crozier RH (2000) Genetic influence on caste in the ant Camponotus consobrinus. Behav Ecol Sociobiol 47:188–194
Frumhoff PC, Baker J (1988) A genetic component to division of labour within honey bee colonies. Nature 333:358–361
Fuchs S, Schade V (1994) Lower performance in honeybee colonies of uniform paternity. Apidologie 25:155–168
Giraud T, Pedersen JS, Keller L (2002) Evolution of supercolonies: the Argentine ants of southern Europe. Proc Natl Acad Sci USA 99:6075–6079
Gordon DM (1995) The expandable network of ant exploration. Anim Behav 50:995–1007
Gordon DM, Mehdiabadi NJ (1999) Encounter rate and task allocation in harvester ants. Behav Ecol Sociobiol 45:370–377
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statisics. J Hered 86:485–486
Holway DA (1999) Competitive mechanisms underlying the displacement of native ants by the invasive Argentine ant. Ecology 80:238–251
Holway DA, Case TJ (2000) Mechanisms of dispersed central-place foraging in polydomous colonies of the Argentine ant. Anim Behav 59:433–441
Holway DA, Case TJ (2001) Effects of colony-level variation on competitive ability in the invasive Argentine ant. Anim Behav 61:1181–1192
Holway DA, Suarez AV, Case TJ (1998) Loss of intraspecific aggression in the success of a widespread invasive social insect. Science 282:949–952
Holway DA, Lach L, Suarez AV, Tsutsui ND, Case TJ (2002) The causes and consequences of ant invasions. Annu Rev Ecol Syst 33:181–233
Hughes WOH, Boomsma JJ (2004) Genetic diversity and disease resistance in leaf-cutting ant societies. Evolution 58:1251–1260
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
Human KG, Gordon DM (1996) Exploitation and interference competition between the invasive argentine ant, Linepithema humile, and native ant species. Oecologia 105:405–412
Human KG, Gordon DM (1999) Behavioral interactions of the invasive Argentine ant with native ant species. Insectes Soc 46:159–163
Ingram KK (2002) Flexibility in nest density and social structure in invasive populations of the Argentine ant, Linepithema humile. Oecologia 133:492–500
Jones JC, Myerscough MR, Graham S, Oldroyd BP (2004) Honey bee nest thermoregulation: diversity promotes stability. Science 305:402–404
Julian GE, Cahan S (1999) Undertaking specialization in the desert leaf-cutter ant Acromyrmex versicolor. Anim Behav 58:437–442
Julian GE, Fewell JH, Gadau J, Johnson RA, Larrabee D (2002) Genetic determination of the queen caste in an ant hybrid zone. Proc Natl Acad Sci USA 99:8157–8160
Keller L, Chapuisat M (1999) Cooperation among selfish individuals in insect societies. Bioscience 49:899–909
Keller L, Chapuisat M (2001) Eusociality and cooperation. Nature Encyclopedia of Life Sciences, http://www.els.net/. Nature, London
Keller L, Reeve HK (1994) Genetic variability, queen number, and polyandry in social hymenoptera. Evolution 48:694–704
Keller L, Cherix D, Ulloa-Chacón P (1989a) Description of a new artificial diet for rearing ant colonies as Iridomyrmex humilis, Monomorium pharaonis and Wasmannia auropunctata (Hymenoptera; Formicidae). Insectes Soc 36:348–352
Keller L, Passera L, Suzzoni JP (1989b) Queen execution in the Argentine ant Iridomyrmex humilis (Mayr). Physiol Entomol 14:157–163
Kraus B, Page RE (1998) Parasites, pathogens, and polyandry in social insects. Am Nat 151:383–391
Krieger MJB, Keller L (1999) Low polymorphism at 19 microsatellite loci in a French population of Argentine ants (Linepithema humile). Mol Ecol 8:1078–1080
Krieger MJB, Keller L (2000) Mating frequency and genetic structure of the Argentine ant Linepithema humile. Mol Ecol 9:119–126
Liersch S, Schmid-Hempel P (1998) Genetic variation within social insect colonies reduces parasite load. Proc R Soc Lond B 265:221–225
Neumann P, Moritz RFA (2000) Testing genetic variance hypotheses for the evolution of polyandry in the honeybee (Apis mellifera L.). Insectes Soc 47:271–279
Oldroyd BP, Rinderer TE, Harbo JR, Buco SM (1992) Effects of intracolonial genetic diversity on honeybee (Hymenoptera: Apidae) colony performances. Ann Entomol Soc Am 85:335–343
Oldroyd BP, Sylvester HA, Wongsiri S, Rinderer TS (1994) Task specialization in a wild bee, Apis florea (Hymenoptera: Apidae), revealed by RFLP banding. Behav Ecol Sociobiol 34:25–30
Oster GF, Wilson EO (1978) Caste and ecology in the social insects. Princeton University Press, Princeton
Page RE, Erber J (2002) Levels of behavioral organization and the evolution of division of labor. Naturwissenschaften 89:91–106
Page RE, Robinson GE, Fondrk MK, Nasr ME (1995) Effects of worker genotypic diversity on honey bee colony development and behavior (Apis mellifera L.). Behav Ecol Sociobiol 36:387–396
Palmer KA, Oldroyd BP (2003) Evidence for intra-colonial genetic variance in resistance to American foulbrood of honey bees (Apis mellifera): further support for the parasite/pathogen hypothesis for the evolution of polyandry. Naturwissenschaften 90:265–268
Passera L (1994) Characteristics of tramp species. In: Williams DF (ed) Exotic ants biology, impact, and control of introduced species. Westview, Boulder, Colo, pp 23–43
Passera L, Keller L (1987) Energy investment during the differentiation of sexuals and workers in the Argentine ant Iridomyrmex humilis (Mayr). Mitt Schweiz Entomol Ges 60:249–260
Passera L, Keller L, Suzzoni J-P (1988) Control of brood male production in the Argentine ant Iridomyrmex humilis (Mayr). Insectes Soc 35:19–33
Queller DC, Goodnight KF (1989) Estimating relatedness using genetic markers. Evolution 242:258–275
Queller DC, Strassmann JE (2002) The many selves of social insects. Science 296:311–313
Rice WR (1989) Analyzing tables of statistical tests. Evolution 43:223–225
Robinson GE (1992) Regulation of division of labor in insect societies. Annu Rev Entomol 37:637–665
Robinson GE, Page RE (1988) Genetic determination of guarding and undertaking in honey-bee colonies. Nature 333:356–358
Schmid-Hempel P, Crozier RH (1999) Polyandry versus polygyny versus parasites. Philos Trans R Soc Lond B 354:507–515
Sherman PW, Seeley TD, Reeve HK (1988) Parasites, pathogens, and polyandry in social Hymenoptera. Am Nat 131:602–610
Sherman PW, Seeley TD, Reeve HK (1998) Parasites, pathogens, and polyandry in honey bees. Am Nat 151:392–396
Starr CK (1984) Sperm competition, kinship, and sociality in the aculeate Hymenoptera. In: Smith RL (ed) Sperm competition and the evolution of animal mating systems. Academic, Orlando, Fla, pp 427–464
Stuart RJ, Page RE (1991) Genetic component to division of labor among workers of a leptothoracine ant. Naturwissenschaften 78:375–377
Suarez AV, Holway DA, Case TJ (2001) Patterns of spread in biological invasions dominated by long-distance jump dispersal: insights from Argentine ants. Proc Natl Acad Sci USA 98:1095–1100
Sundström L, Ratnieks FLW (1998) Sex ratio conflicts, mating frequency, and queen fitness in the ant Formica truncorum. Behav Ecol 9:116–121
Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc Lond B 270:99–103
Tsutsui ND, Case TJ (2001) Population genetics and colony structure of the argentine ant (Linepithema humile) in its native and introduced ranges. Evolution 55:976–985
Tsutsui ND, Suarez AV (2003) The colony structure and population biology of invasive ants. Conserv Biol 17:48–58
Vargo EL, Passera L (1991) Pheromonal and behavioral queen control over the production of gynes in the Argentine ant Iridomyrmex humilis (Mayr). Behav Ecol Sociobiol 28:161–169
Volny VP, Gordon DM (2002) Genetic basis for queen-worker dimorphism in a social insect. Proc Natl Acad Sci USA 99:6108–6111
Wiernasz DC, Perroni CL, Cole BJ (2004) Polyandry and fitness in the western harvester ant, Pogonomyrmex occidentalis. Mol Ecol 13:1601–1606
Acknowledgements
This research was supported by the Swiss National Science Foundation (grant 31-61934.00 to M.C. and several grants to L.K.). We thank Lotta Sundström and the anonymous reviewers for comments on the manuscript.
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Rosset, H., Keller, L. & Chapuisat, M. Experimental manipulation of colony genetic diversity had no effect on short-term task efficiency in the Argentine ant Linepithema humile. Behav Ecol Sociobiol 58, 87–98 (2005). https://doi.org/10.1007/s00265-004-0890-6
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DOI: https://doi.org/10.1007/s00265-004-0890-6