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Ecological drivers and reproductive consequences of non-kin cooperation by ant queens

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Abstract

The fitness consequences of joining a group are highly dependent on ecological context, especially for non-kin. To assess the relationships between cooperation and environment, we examined variation in colony reproductive success for a harvester ant species that nests either solitarily or with multiple, unrelated queens, a social strategy known as primary polygyny. We measured the reproductive investment of colonies of solitary versus social nesting types at two sites, one with primarily single-queen colonies, and the other with a majority of polygynous nests. Our results were consistent with the hypothesis that cooperative nesting by unrelated ant queens is likely a selection response to difficult environments, rather than a strategy to maximize reproduction under favorable conditions. Fewer colonies at the primarily polygynous site reproduced than at the site with primarily single queen nests, and those that did had lower reproductive investment, as measured by number and total mass of reproductives. Assessment of ecological conditions also support the harsh environment hypothesis. Colony density in the multi-queen population was higher, and nearest neighbor distances were lower for non-reproducing than reproducing colonies. To more directly test the hypothesis that colony reproduction was ecologically constrained, we experimentally supplemented food resources for a subset of colonies at the primary polygyny site. Supplemented colonies increased reproductive investment levels to equal that of colonies at the single-queen population, further indicating that environmental pressures are severe where primary polygyny is dominant, and may drive the evolution of non-kin cooperation in this context.

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References

  • Adams ES, Tschinkel WR (1995a) Density-dependent competition in fire ants: effects on colony survivorship and size variation. J Anim Ecol 64(3):315–324

    Article  Google Scholar 

  • Adams ES, Tschinkel WR (1995b) Effects of foundress number on brood raids and queen survival in the fire ant Solenopsis invicta. Behav Ecol Sociobiol 37(4):233–242

    Article  Google Scholar 

  • Avilés L (2002) Solving the freeloaders paradox: genetic associations and frequency-dependent selection in the evolution of cooperation among nonrelatives. Proc Natl Acad Sci 99(22):14268–14273

    Article  PubMed  PubMed Central  Google Scholar 

  • Baddeley R, Turner R (2005) Spatstat: an R package for analyzing spatial point patterns. J Stat Softw 12(6):1–42

    Article  Google Scholar 

  • Bennett B (1987) Ecological differences between monogynous and polygynous sibling ant species (Hymenoptera: Formicidae). Sociobiology 13:249–270

    Google Scholar 

  • Bernasconi G, Strassmann JE (1999) Cooperation among unrelated individuals: the ant foundress case. Trends Ecol Evol 14(12):477–482

    Article  PubMed  CAS  Google Scholar 

  • Bilde T, Coates KS, Birkhofer K, Bird T, Maklakov AA, Lubin Y, Aviles L (2007) Survival benefits select for group living in a social spider despite reproductive costs. J Evol Biol 20(6):2412–2426

    Article  PubMed  CAS  Google Scholar 

  • Bourke AFG, Heinze J (1994) The ecology of communal breeding: the case of multiple-queen leptothoracine ants. Philos Trans R Soc Lond B 345(1314):359–372

    Article  Google Scholar 

  • Brandl R, Hacker M, Bagine RKN, Kaib M (2004) Yearly variation in polygyny in the termite Macrotermes michaelseni (Sjöstedt). Insectes Soc 51(3):294–298

    Article  Google Scholar 

  • Cahan S (2001) Ecological variation across a transition in colony-founding behavior in the ant Messor pergandei. Oecologia 129(4):629–635

    Article  PubMed  Google Scholar 

  • Cahan SH, Helms KR (2012) Relatedness does not explain geographic variation in queen cooperation in the seed-harvester ant Messor pergandei. Insectes Soc 59(4):579–585

    Article  Google Scholar 

  • Cameron EZ, Setsaas TH, Linklater WL (2009) Social bonds between unrelated females increase reproductive success in feral horses. Proc Natl Acad Sci 106(33):13850–13853

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Clark RM, Fewell JH (2014) Social dynamics drive selection in cooperative associations of ant queens. Behav Ecol 25(1):117–123

    Article  Google Scholar 

  • Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296(5565):69–72

    Article  PubMed  CAS  Google Scholar 

  • Clutton-Brock T (2009) Cooperation between non-kin in animal societies. Nature 462(7269):51–57

    Article  PubMed  CAS  Google Scholar 

  • Clutton-Brock TH, Guinness FE, Albon SD (1982) Red deer: behavior and ecology of two sexes, 1st edn. University of Chicago Press, Chicago

    Google Scholar 

  • Clutton-Brock TH, Brotherton PNM, O’Riain MJ, Griffin AS, Gaynor D, Sharpe L, Kansky R, Manser MB, McIlrath GM (2000) Individual contributions to babysitting in a cooperative mongoose, Suricata suricatta. Proc R Soc Lond B 267(1440):301–305

    Article  CAS  Google Scholar 

  • Cole BJ, Wiernasz DC (2000) Colony size and reproduction in the western harvester ant, Pogonomyrmex occidentalis. Insectes Soc 47(3):249–255

    Article  Google Scholar 

  • Connor RC (2010) Cooperation beyond the dyad: on simple models and a complex society. Philos Trans R Soc B 365(1553):2687–2697

    Article  Google Scholar 

  • Core Team R (2013) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna

    Google Scholar 

  • DeHeer CJ, Herbers JM (2004) Population genetics of the socially polymorphic ant Formica podzolica. Insectes Soc 51(4):309–316

    Article  Google Scholar 

  • Deslippe RJ, Savolainen R (1995) Colony foundation and polygyny in the ant Formica podzolica. Behav Ecol Sociobiol 37(1):1–6

    Article  Google Scholar 

  • Dugatkin L (2002) Animal cooperation among unrelated individuals. Naturwissenschaften 89(12):533–541

    PubMed  CAS  Google Scholar 

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

    Google Scholar 

  • Giesel JT (1976) Reproductive strategies as adaptations to life in temporally heterogeneous environments. Annu Rev Ecol Syst 7(1):57–79

    Article  Google Scholar 

  • Gordon DM, Wagner D (1997) Neighborhood density and reproductive potential in harvester ants. Oecologia 109(4):556–560

    Article  PubMed  Google Scholar 

  • Gordon DM, Guetz A, Greene MJ, Holmes S (2011) Colony variation in the collective regulation of foraging by harvester ants. Behav Ecol 22(2):429–435

    Article  PubMed  PubMed Central  Google Scholar 

  • Hacker M, Kaib M, Bagine RKN, Epplen JT, Brandl R (2005) Unrelated queens coexist in colonies of the termite Macrotermes michaelseni. Mol Ecol 14(5):1527–1532

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • Haney BR (2017) Ecological drivers and reproductive consequences of Queen Cooperation in the California Harvester Ant Pogonomyrmex Californicus. PhD dissertation, School of Life Science, Arizona State University, Tempe, Arizona, USA

  • Heinze J, Trunzer B, Hölldobler B, Delabie JHC (2001) Reproductive skew and queen relatedness in an ant with primary polygyny. Insectes Soc 48(2):149–153

    Article  Google Scholar 

  • Helanterä H, Aehle O, Roux M, Heinze J, d’Ettorre P (2013) Family-based guilds in the ant Pachycondyla inversa. Biol Let 9(3):20130125

    Article  Google Scholar 

  • Helmkampf M, Mikheyev AS, Kang Y, Fewell J, Gadau J (2016) Gene expression and variation in social aggression by queens of the harvester ant Pogonomyrmex californicus. Mol Ecol 25(15):3716–3730

    Article  PubMed  Google Scholar 

  • Helms KR, Cahan SH (2012) Large-scale regional variation in cooperation and conflict among queens of the desert ant Messor pergandei. Anim Behav 84(3):499–507

    Article  Google Scholar 

  • Hölldobler B (1976) Recruitment behavior, home range orientation and territoriality in harvester ants, Pogonomyrmex. Behav Ecol Sociobiol 1(1):3–44

    Article  Google Scholar 

  • Hölldobler B, Wilson EO (1990) The ants, 1st edn. Harvard University Press, Boston

    Book  Google Scholar 

  • Hölldobler B, Grillenberger B, Gadau J (2011) Queen number and raiding behavior in the ant genus Myrmecocystus (Hymenoptera: Formicidae). Myrmecological News 15:53–61

    Google Scholar 

  • Johnson RA (2002) Semi-claustral colony founding in the seed-harvester ant Pogonomyrmex californicus: a comparative analysis of colony founding strategies. Oecologia 132(1):60–67

    Article  PubMed  Google Scholar 

  • Johnson RA (2004) Colony founding by pleometrosis in the semiclaustral seed-harvester ant Pogonomyrmex californicus (Hymenoptera: Formicidae). Anim Behav 68(5):1189–1200

    Article  Google Scholar 

  • Keller L, Ross KG (1993) Phenotypic plasticity and “cultural transmission” of alternative social organizations in the fire ant Solenopsis invicta. Behav Ecol Sociobiol 33(2):121–129

    Article  Google Scholar 

  • Kolmer K, Heinze J (2000) Rank orders and division of labour among unrelated cofounding ant queens. Proc R Soc Lond B 267(1454):1729–1734

    Article  CAS  Google Scholar 

  • Krams I, Krama T, Berzins A, Rantala MJ (2010) The risk of predation favors cooperation among breeding prey. Commun Integr Biol 3(3):243–244

    Article  PubMed  PubMed Central  Google Scholar 

  • Kwapich CL, Tschinkel WR (2013) Demography, demand, death, and the seasonal allocation of labor in the Florida harvester ant (Pogonomyrmex badius). Behav Ecol Sociobiol 67(12):2011–2027

    Article  Google Scholar 

  • Leadbeater E, Carruthers JM, Green JP, Rosser NS, Field J (2011) Nest inheritance is the missing source of direct fitness in a primitively eusocial insect. Science 333(6044):874–876

    Article  PubMed  CAS  Google Scholar 

  • Lehmann L, Keller L (2006) The evolution of cooperation and altruism—a general framework and a classification of models. J Evol Biol 19(5):1365–1376

    Article  PubMed  CAS  Google Scholar 

  • Macom TE, Porter SD (1996) Comparison of polygyne and monogyne red imported fire ant (Hymenoptera: Formicidae) population densities. Ann Entomol Soc Am 89(4):535–543

    Article  Google Scholar 

  • Marshall JA (2011) Group selection and kin selection: formally equivalent approaches. Trends Ecol Evol 26(7):325–332

    Article  PubMed  Google Scholar 

  • McGraw JB, Caswell H (1996) Estimation of individual fitness from life-history data. Am Nat 147(1):47–64

    Article  Google Scholar 

  • McInnes DA, Tschinkel WR (1995) Queen dimorphism and reproductive strategies in the fire ant Solenopsis geminata (Hymenoptera: Formicidae). Behav Ecol Sociobiol 36(6):367–375

    Article  Google Scholar 

  • Mesterton-Gibbons M, Dugatkin LA (1992) Cooperation among unrelated individuals: evolutionary factors. Q Rev Biol 67(3):267–281

    Article  Google Scholar 

  • Mintzer A (1987) Primary polygyny in the Atta texana: Number and weight of females and colony foundation success in the laboratory. Insectes Soc 34(2):108–117

    Article  Google Scholar 

  • Mosser A, Packer C (2009) Group territoriality and the benefits of sociality in the African lion, Panthera leo. Anim Behav 78(2):359–370

    Article  Google Scholar 

  • Myllymäki M, Grabarnik P, Seijo H, Stoyan D (2015) Deviation test construction and power comparison for marked spatial point patterns. Spat Stat 11:19–34

    Article  Google Scholar 

  • Nonacs P, Kapheim KM (2007) Social heterosis and the maintenance of genetic diversity. J Evol Biol 20(6):2253–2265

    Article  PubMed  CAS  Google Scholar 

  • Nowak MA (2006) Five rules for the evolution of cooperation. Science 314(5805):1560–1563

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Nur N (1984) The consequences of brood size for breeding blue tits I. Adult survival, weight change and the cost of reproduction. J Anim Ecol 53(2):479–496

    Article  Google Scholar 

  • Ode PJ, Rissing SW (2002) Resource abundance and sex allocation by queen and workers in the harvester ant, Messor pergandei. Behav Ecol Sociobiol 51(6):548–556

    Article  Google Scholar 

  • Offenberg J, Peng R, Nielsen MG (2012) Development rate and brood production in haplo- and pleometrotic colonies of Oecophylla smaragdina. Insectes Soc 59(3):307–311

    Article  Google Scholar 

  • Okasha S (2006) Evolution and the levels of selection, 1st edn. Oxford University Press, Oxford

    Book  Google Scholar 

  • Okasha S (2016) The relation between kin and multilevel selection: an approach using causal graphs. Br J Philos Sci 67(2):435–470

    Article  Google Scholar 

  • Oldroyd BP, Fewell JH (2007) Genetic diversity promotes homeostasis in insect colonies. Trends Ecol Evol 22(8):408–413

    Article  PubMed  Google Scholar 

  • Overson R, Gadau J, Clark RM, Pratt SC, Fewell JH (2014) Behavioral transitions with the evolution of cooperative nest founding by harvester ant queens. Behav Ecol Sociobiol 68(1):21–30

    Article  Google Scholar 

  • Overson R, Fewell J, Gadau J (2016) Distribution and origin on intraspecific social variation in the California harvester ant Pogonomyrmex californicus. Insect Sociaux 63:531–541

    Article  Google Scholar 

  • Partridge L, Farquhar M (1981) Sexual activity reduces lifespan of male fruitflies. Nature 294(58):580–582

    Article  Google Scholar 

  • Queller DC (2011) Expanded social fitness and Hamilton’s rule for kin, kith, and kind. Proc Natl Acad Sci 108:10792–10799

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Rehan SM, Richards MH, Adams M, Schwarz MP (2014) The costs and benefits of sociality in a facultatively social bee. Anim Behav 97:77–85

    Article  Google Scholar 

  • Riehl C (2013) Evolutionary routes to non-kin cooperative breeding in birds. Proc R Soc Lond B 280(1772):20132245

    Article  Google Scholar 

  • Ripley BD (1976) The second-order analysis of stationary point processes. J Appl Probab 13(2):255–266

    Article  Google Scholar 

  • Rissing SW, Pollock GB (1991) An experimental analysis of pleometrotic advantage in the desert seed-harvester ant Messor pergandei (Hymenoptera; Formicidae). Insectes Soc 38(2):205–211

    Article  Google Scholar 

  • Rissing SW, Johnson RA, Pollock GB (1986) Natal nest distribution and peometrosis in the desert leaf-cutter ant Acromyrmex versicolor(pergande) (Hymenoptera: Formicidae). Psyche 93:177–186

    Article  Google Scholar 

  • Rosenberg MS, Anderson CD (2011) PASSaGE: pattern analysis, spatial statistics and geographic exegesis. Version 2. Methods Ecol Evol 2(3):229–232

    Article  Google Scholar 

  • Rüppell O, Heinze J (1999) Alternative reproductive tactics in females: the case of size polymorphism in winged ant queens. Insectes Soc 46(1):6–17

    Article  Google Scholar 

  • Rüppell O, Heinze J, Hölldobler B (2001) Alternative reproductive tactics in the queen-size-dimorphic ant Leptothorax rugatulus (Emery) and their consequences for genetic population structure. Behav Ecol Sociobiol 50(2):189–197

    Article  Google Scholar 

  • Rutte C, Taborsky M (2008) The influence of social experience on cooperative behaviour of rats (Rattus norvegicus): direct vs generalized reciprocity. Behav Ecol Sociobiol 62(4):499–505

    Article  Google Scholar 

  • Schaffer WM (1974) Selection for optimal life histories: the effects of age structure. Ecology 55(2):291–303

    Article  Google Scholar 

  • Shaffer Z, Sasaki T, Haney B, Janssen M, Pratt SC, Fewell JH (2016) The foundress’s dilemma: group selection for cooperation among queens of the harvester ant, Pogonomyrmex californicus. Sci Rep 6:29828

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Silk JB, Beehner JC, Bergman TJ, Crockford C, Engh AL, Moscovice LR, Witting RM, Seyfarth RM, Cheney DL (2010) Strong and consistent social bonds enhance the longevity of female baboons. Curr Biol 20(15):1359–1361

    Article  PubMed  CAS  Google Scholar 

  • Smith CR, Tschinkel WR (2006) The sociometry and sociogenesis of reproduction in the Florida harvester ant, Pogonomyrmex badius. J Insect Sci 6:32

    Article  PubMed Central  Google Scholar 

  • Snell TW, King CE (1977) Lifespan and fecundity patterns in rotifers: the cost of reproduction. Evolution 31(4):882–890

    Article  PubMed  Google Scholar 

  • Tarpy DR (2003) Genetic diversity within honeybee colonies prevents severe infections and promotes colony growth. Proc R Soc Lond B 270(1510):99–103

    Article  Google Scholar 

  • Trivers RL, Hare H (1976) Haploidploidy and the evolution of the social insect. Science 191(4224):249–263

    Article  PubMed  CAS  Google Scholar 

  • Trunzer B, Heinze J, Hölldobler B (1998) Cooperative colony founding and experimental primary polygyny in the ponerine ant Pachycondyla villosa. Insectes Soc 45(3):267–276

    Article  Google Scholar 

  • Tschinkel WR (1999) Sociometry and sociogenesis of colony-level attributes of the Florida harvester ant (Hymenoptera: Formicidae). Ann Entomol Soc Am 92(1):80–89

    Article  Google Scholar 

  • Tschinkel WR (2006) The fire ants. Harvard University Press

  • Van Cleve J, Akcay E (2014) Pathways to social evolution: reciprocity, relatedness, and synergy. Evolution 68(8):2245–2258

    PubMed  Google Scholar 

  • West SA, Griffin AS, Gardner A (2007) Evolutionary explanations for cooperation. Curr Biol 17(16):661–672

    Article  Google Scholar 

  • Wiernasz DC, Cole BJ (1995) Spatial distribution of Pogonomyrmex occidentalis: recruitment, mortality and overdispersion. J Anim Ecol 63(4):519–527

    Article  Google Scholar 

  • Wiernasz DC, Cole BJ (2003) Queen size mediates queen survival and colony fitness in Harvester Ants. Evolution 57(9):2179–2183

    Article  PubMed  Google Scholar 

  • Wiernasz DC, Perroni CL, Cole BJ (2004) Polyandry and fitness in the western harvester ant, Pogonomyrmex occidentalis. Mol Ecol 13(6):1601–1606

    Article  PubMed  CAS  Google Scholar 

  • Wiernasz DC, Hines J, Parker DG, Cole BJ (2008) Mating for variety increases foraging activity in the harvester ant, Pogonomyrmex occidentalis. Mol Ecol 17(4):1137–1144

    Article  PubMed  Google Scholar 

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Acknowledgements

This work was supported in part by NSF Awards 1558127 and 1501655 to JHF and BRH. Additional support to BRH was provided by The International Union for the Study of Social Insects Tschinkel Ant Natural History Research Grant, The Animal Behavior Society Student Research Grant, The Sigma Xi Grant in Aid or Research. Arizona State University also gave support to JHF and BRH. The authors thank Juergen Gadau, Martin Helmkampf, Ioulia Bespalova, Nathan Smith, Luis Garcia, Evan Farrar, Annie Ortiz, Daniel Restrepo, and Samuel Zirbel for their assistance in the project. Special thanks to the San Diego County Parks Department, the folks at the Pine Valley County Park for their support, and the Lake Henshaw Resort for use of their land.

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    Brian R. Haney & Jennifer H. Fewell

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  1. Brian R. Haney
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BRH and JHF conceived and designed the experiments. BRH performed the experiments. BRH and JHF analyzed the data and write the manuscript.

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Correspondence to Brian R. Haney.

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Haney, B.R., Fewell, J.H. Ecological drivers and reproductive consequences of non-kin cooperation by ant queens. Oecologia 187, 643–655 (2018). https://doi.org/10.1007/s00442-018-4148-9

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