Abstract
Cooperation between kin and cooperation between non-kin often appear functionally similar, but the evolutionary mechanisms that drive the emergence of these two forms of cooperation can be dramatically different. The mechanisms responsible for non-kin cooperation, in particular, are not well established in an empirical context. To truly understand the emergence of non-kin cooperation, the fitness outcomes of cooperation should be compared with the alternate strategy of solitary living in the same environment. Ant populations that contain a mix of queens who found nests alone (monogyny), and cooperative unrelated ant queens who found nests together and remain together through colony development (primary polygyny), provide a useful natural context to make such a comparison. To estimate the reproductive costs for primary polygyny relative to solitary nest founding, we measured alate (reproductive) production for colonies in a mixed population of polygynous and monogynous California harvester ant colonies over a 2-year period. Colony-level reproductive output was not substantially higher in polygynous colonies compared to those with single queens, and consequent per-queen reproductive gain was significantly lower. Given that polygynous queens in this population are unrelated, nest sharing thus generates a significant annual and potentially lifetime cost for cooperative queens. Comparative measures of colony dynamics, however, suggest that polygynous colonies have a larger or more active workforce than monogynous colonies. Additionally, polygynous colonies may be more conservative than monogynous colonies in resource allocation towards reproduction. These results collectively suggest that primary polygyny generates annual reproductive fitness costs. However, polygynous colonies likely also shift life history strategies in ways that emphasize long-term survival and colony growth over immediate reproduction. Over time, this shift may mitigate the annual fitness costs of cooperation.
Significance statement
When things get difficult, it pays to work together. In some ant species, unrelated queens form long-term cooperative associations that share resources and a workforce within a single nest. The fitness consequences and evolutionary drivers of non-kin cooperation in this and other systems are unclear. We compared the reproductive investment and colony dynamics of single-queen and multi-queen California harvester ant colonies in a shared environment to directly compare the fitness of cooperative and non-cooperative queens. Our data suggest that cooperation not only lowers annual per-queen reproduction, but also produces a more robust colony that may recoup annual fitness losses by extending colony longevity.
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All data generated or analyzed during this study are included in this published article [and its supplementary information files].
References
Allen RM, Buckley YM, Marshall DJ (2008) Offspring size plasticity in response to intraspecific competition: an adaptive maternal effect across life-history stages. The Am Nat 171:225–237
Avilés L (2002) Solving the freeloaders paradox: genetic associations and frequency-dependent selection in the evolution of cooperation among nonrelatives. Proc Natl Acad Sci 99:14268–14273
Axelrod R, Hamilton WD (1981) The evolution of cooperation. Science 211:1390–1396
Baddeley R, Turner R (2005) Spatstat: an R package for analyzing spatial point patterns. J Stat Softw 12:1–42
Bartz SH, Hölldobler B (1982) Colony founding in Myrmecocystus mimicus Wheeler (Hymenoptera: Formicidae) and the evolution of foundress associations. Behav Ecol Sociobiol 10:137–147
Boomsma JJ, Grafen A (1990) Intraspecific variation in ant sex ratios and the Trivers-Hare hypothesis. Evolution 44:1026–1034
Boomsma JJ, Grafen A (1991) Colony-level sex ratio selection in the eusocial Hymenoptera. J Evol Biol 4:383–407
Boulay R, Arnan X, Cerdá X, Retana J (2014) The ecological benefits of larger colony size may promote polygyny in ants. J Evol Biol 27:2856–2863
Brouwer L, Heg D, Taborsky M (2005) Experimental evidence for helper effects in a cooperatively breeding cichlid. Behav Ecol 16:667–673
Bshary R, Grutter AS (2005) Punishment and partner switching cause cooperative behaviour in a cleaning mutualism. Biol Lett 1:396–399
Cahan SH, Helms KR (2012) Relatedness does not explain geographic variation in queen cooperation in the seed-harvester ant Messor pergandei. Insectes Soc 59:579–585
Chan GL, Bourke AFG (1994) Split sex ratios in a multiple-queen ant population. Proc R Soc Lond B 258:261–266
Chapuisat M, Keller L (1999) Testing kin selection with sex allocation data in eusocial Hymenoptera. Heredity 82:473–478
Clark RM, Fewell JH (2014) Social dynamics drive selection in cooperative associations of ant queens. Behav Ecol 25:117–123
Clements KC, Stephens DW (1995) Testing models of non-kin cooperation: mutualism and the Prisoner’s Dilemma. Anim Behav 50:527–535
Clutton-Brock T (2002) Breeding together: kin selection and mutualism in cooperative vertebrates. Science 296:69–72
Clutton-Brock T (2009) Cooperation between non-kin in animal societies. Nature 462:51–57
Clutton-Brock TH, Parker GA (1995) Punishment in animal societies. Nature 373:209–216
Cole BJ, Wiernasz DC (2000) Colony size and reproduction in the western harvester ant, Pogonomyrmex occidentalis. Insectes Soc 47:249–255
Connor RC (1995) The benefits of mutualism: a conceptual framework. Biol Rev 70:427–457
Crozier RH, Pamilo P (1996) Evolution of social insect colonies: sex allocation and kin selection. Oxford University Press, Oxford, p 306p
Danforth BN (2002) Evolution of sociality in a primitively eusocial lineage of bees. Proc Natl Acad Sci 99:286–290
Davison PJ, Field J (2016) Social polymorphism in the sweat bee Lasioglossum (Evylaeus) calceatum. Insectes Soc 63:327–338
DeHeer CJ, Herbers JM (2004) Population genetics of the socially polymorphic ant Formica podzolica. Insectes Soc 51:309–316
Dugatkin L (2002) Animal cooperation among unrelated individuals. Naturwissenschaften 89:533–541
Dunn T, Richards MH (2003) When to bee social: interactions among environmental constraints, incentives, guarding, and relatedness in a facultatively social carpenter bee. Behav Ecol 14:417–424
Errbii M, Ernst UR, Lajmi A, Gadau J, Schrader L (2021) Genomic architecture and evolutionary dynamics of a social niche polymorphism in the California harvester ant, Pogonomyrmex californicus. bioRxiv
Evans JD (1995) Relatedness threshold for the production of female sexuals in colonies of a polygynous ant, Myrmica tahoensis, as revealed by microsatellite DNA analysis. Proc Natl Acad Sci 92:6514–6517
Foitzik S, Strätz M, Heinze J (2003) Ecology, life history and resource allocation in the ant, Leptothorax nylanderi. J Evol Biol 16:670–680
Fournier D, Keller L, Passera L, Aron S (2003) Colony sex ratios vary with breeding system but not relatedness asymmetry in the facultatively polygynous ant Pheidole pallidula. Evolution 57:1336–1342
Fox J, Weisberg S (2011) An {R} companion to applied regression, 2nd edn. Sage, Thousand Oaks CA
Frank SA (2013) Natural selection. VII. History and interpretation of kin selection theory. J Evol Biol 26:1151–1184
Gadau J, Gertsch PJ, Heinze J, Pamilo P, Hölldobler B (1998) Oligogyny by unrelated queens in the carpenter ant, Camponotus ligniperdus. Behav Ecol Sociobiol 44:23–33
Gordon DM, Wagner D (1997) Neighborhood density and reproductive potential in harvester ants. Oecologia 109:556–560
Hacker M, Kaib M, Bagine RKN, Epplen JT, Brandl R (2005) Unrelated queens coexist in colonies of the termite Macrotermes michaelseni. Mol Ecol 14:1527–1532
Hall JM, Mitchell TS, Thawley CJ, Stroud JT, Warner DA (2020) Adaptive seasonal shift towards investment in fewer, larger offspring: evidence from field and laboratory studies. J Anim Ecol 89:1242–1253
Hamilton WD (1964) The genetical evolution of social behaviour II. J Theor Biol 7:17–52
Haney BR (2017) Ecological drivers and reproductive consequences of queen cooperation in the California harvester ant Pogonomyrmex californicus. Dissertation,. Arizona State University
Haney BR, Fewell JH (2018) Ecological drivers and reproductive consequences of non-kin cooperation by ant queens. Oecologia 187:643–655
Harbo JR (1986) Effect of population size on brood production, worker survival and honey gain in colonies of honeybees. J Apic Res 25:22–29
Hartig F (2017) DHARMa: residual diagnostics for hierarchical (multi-level / mixed) regression models. R package version 0(1):5 http://florianhartig.github.io/DHARMa/. Accessed 13 Aug 2022
Heinze J, Trunzer B, Hölldobler B, Delabie JHC (2001) Reproductive skew and queen relatedness in an ant with primary polygyny. Insectes Soc 48:149–153
Helanterä H, Aehle O, Roux M, Heinze J, d’Ettorre P (2013) Family-based guilds in the ant Pachycondyla inversa. Biol Lett 9:20130125
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 25:3716–3730
Helms KR, Helms Cahan S (2012) Large-scale regional variation in cooperation and conflict among queens of the desert ant Messor pergandei. Anim Behav 84:499–507
Herbers JM (1986) Nest site limitation and facultative polygyny in the ant Leptothorax longispinosus. Behav Ecol Sociobiol 19:115–122. https://doi.org/10.1007/BF00299946
Hölldobler B, Grillenberger B, Gadau J (2011) Queen number and raiding behavior in the ant genus Myrmecocystus (Hymenoptera: Formicidae). Myrmecol News 15:53–61
Hughes WO, Oldroyd BP, Beekman M, Ratnieks FL (2008a) Ancestral monogamy shows kin selection is key to the evolution of eusociality. Science 320:1213–1216
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
Ingram KK (2002) Plasticity in queen number and social structure in the invasive Argentine ant (Linepithema humile). Evolution 56:2008–2016
Jeanne RL, Loope KJ, Bouwma AM, Nordheim EV, Smith ML (2022) Five decades of misunderstanding in the social Hymenoptera: a review and meta-analysis of Michener’s paradox. Biol Rev 97:1559–1611
Johnson RA (2004) Colony founding by pleometrosis in the semiclaustral seed-harvester ant Pogonomyrmex californicus (Hymenoptera: Formicidae). Anim Behav 68:1189–1200
Jones O, Wang J (2010) COLONY: a program for parentage and sibship inference from multilocus genotype data. Mol Ecol Resour 10:551–555
Kaspari M, Byrne MM (1995) Caste allocation in litter Pheidole: lessons from plant defense theory. Behav Ecol Sociobiol 37:255–263
Keller L, Reeve HK (1994) Genetic variability, queen number, and polyandry in social Hymenoptera. Evolution 48:694–704
Kingma SA, Hall ML, Arriero E, Peters A (2010) Multiple benefits of cooperative breeding in purple-crowned fairy-wrens: a consequence of fidelity? J Anim Ecol 79:757–768
Kingma SA, Santema P, Taborsky M, Komdeur J (2014) Group augmentation and the evolution of cooperation. Trends Ecol Evol 29:476–484
Koenig WD, Pitelka FA, Carmen WJ, Mumme RL, Stanback MT (1992) The evolution of delayed dispersal in cooperative breeders. Q Rev Biol 67:111–150
Kokko H, Johnstone RA, Clutton-Brock TH (2001) The evolution of cooperative breeding through group augmentation. Proc Royal Soc B 268:187–196
Krams I, Bērziņš A, Krama T, Wheatcroft D, Igaune K, Rantala MJ (2009) The increased risk of predation enhances cooperation. Proc Royal Soc B 277:513–518
Kukuk PF, Bitney C, Forbes SH (2005) Maintaining low intragroup relatedness: evolutionary stability of nonkin social groups. Anim Behav 70:1305–1311
Kümmerli R, Helms KR, Keller L (2005) Experimental manipulation of queen number affects colony sex ratio investment in the highly polygynous ant Formica exsecta. Proc Royal Soc B 272:1789–1794
Langsrud Ø (2003) ANOVA for unbalanced data: use type II instead of type III sums of squares. Stat Comput 13:163–167
Mattila HR, Seeley TD (2011) Does a polyandrous honeybee queen improve through patriline diversity the activity of her colony’s scouting foragers? Behav Ecol Sociobiol 65:799–811
McInnes DA, Tschinkel WR (1995) Queen dimorphism and reproductive strategies in the fire ant Solenopsis geminata (Hymenoptera: Formicidae). Behav Ecol Sociobiol 36:367–375
Mesterton-Gibbons M, Dugatkin LA (1992) Cooperation among unrelated individuals: evolutionary factors. Q Rev Biol 67:267–281
Michener CD (1964) Reproductive efficiency in relation to colony size in hymenopterous societies. Insectes Soc 11:317–341
Mintzer A (1987) Primary polygyny in the ant Atta texana: number and weight of females and colony foundation success in the laboratory. Insectes Soc 34:108–117
Möller LM, Beheregaray LB, Harcourt RG, Krützen M (2001) Alliance membership and kinship in wild male bottlenose dolphins (Tursiops aduncus) of southeastern Australia. Proc Royal Soc B 268:1941–1947
Ode P, Rissing S (2002) Resource abundance and sex allocation by queen and workers in the harvester ant, Messor pergandei. Behav Ecol Sociobiol 51:548–556
Oli MK (2003) Hamilton goes empirical: estimation of inclusive fitness from life-history data. Proc Royal Soc B 270:307–311
Ostwald M, Dahan RA, Shaffer Z, Fewell JH (2021) Fluid nest membership drives variable relatedness in groups of a facultatively social bee. Front Ecol Evol 893
Ostwald MM, Haney BR, Fewell JH (2022) Ecological drivers of non-kin cooperation in the Hymenoptera. Front Ecol Evol 10:19
Overson R, Fewell J, Gadau J (2016) Distribution and origin of intraspecific social variation in the California harvester ant Pogonomyrmex californicus. Insectes Soc 63:531–541
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 68:21–30
Palmer TM (2004) Wars of attrition: colony size determines competitive outcomes in a guild of African acacia ants. Anim Behav 68:993–1004
Pamilo P (1991) Evolution of colony characteristics in social insects I. Sex Allocation. Am Nat 137:83–107
Paxton RJ, Thorén PA, Tengö J, Estoup A, Pamilo P (1996) Mating structure and nestmate relatedness in a communal bee, Andrena jacobi (Hymenoptera, Andrenidae), using microsatellites. Mol Ecol 5:511–519
Prager SM (2014) Comparison of social and solitary nesting carpenter bees in sympatry reveals no advantage to social nesting. Biol J Linn Soc 113:998–1010
Pruett-Jones SG, Lewis MJ (1990) Sex ratio and habitat limitation promote delayed dispersal in superb fairy-wrens. Nature 348:541–542
Queller DC, Peters JM, Solís CR, Strassmann JE (1997) Control of reproduction in social insect colonies: individual and collective relatedness preferences in the paper wasp, Polistes annularis. Behav Ecol Sociobiol 40:3–16
Queller DC, Strassmann JE (1998) Kin selection and social insects. Bioscience 48:165–175
Queller DC, Zacchi F, Cervo R, Turillazzi S, Henshaw MT, Santorelli LA, Strassmann JE (2000) Unrelated helpers in a social insect. Nature 405:784–787
R Core Team (2013) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria
Raihani NJ, Thornton A, Bshary R (2012) Punishment and cooperation in nature. Trends Ecol Evol 27:288–295
Rehan SM, Berens AJ, Toth AL (2014) At the brink of eusociality: transcriptomic correlates of worker behaviour in a small carpenter bee. BMC Evol Biol 14:1–11
Reznick D, Callahan H, Llauredo R (1996) Maternal effects on offspring quality in poeciliid fishes. Am Zool 36:147–156
Rissing SW, Pollock GB (1991) An experimental analysis of pleometrotic advantage in the desert seed-harvester ant Messor pergandei (Hymenoptera; Formicidae). Insectes Soc 38:205–211
Seppä P, Queller DC, Strassmann JE (2002) Reproduction in foundress associations of the social wasp, Polistes carolina: conventions, competition, and skew. Behav Ecol 13:531–542
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 6:1–9
Shell WA, Rehan SM (2018) Behavioral and genetic mechanisms of social evolution: insights from incipiently and facultatively social bees. Apidologie 49:13–30
Smith AR, Wcislo WT, O’donnell S (2003) Assured fitness returns favor sociality in a mass-provisioning sweat bee, Megalopta genalis (Hymenoptera: Halictidae). Behav Ecol Sociobiol 54:14–21
Smith CR, Smith CD, Robertson HM, Helmkampf M, Zimin A, Yandell M et al (2011) Draft genome of the red harvester ant Pogonomyrmex barbatus. Proc Natl Acad Sci 108:5667–5672
Strassmann JE, Hughes CR, Turillazzi S, Solı́s CR, Queller DC (1994) Genetic relatedness and incipient eusociality in stenogastrine wasps. Anim Behav 48:813–821
Trunzer B, Heinze J, Hölldobler B (1998) Cooperative colony founding and experimental primary polygyny in the ponerine ant Pachycondyla villosa. Insectes Soc 45:267–276
Tschinkel WR (1999) Sociometry and sociogenesis of colony-level attributes of the Florida harvester ant (Hymenoptera: Formicidae). Ann Entomol Soc Am 92:80–89
Tschinkel WR, Howard DF (1983) Colony founding by pleometrosis in the fire ant, Solenopsis invicta. Behav Ecol Sociobiol 12:103–113
Van Horn RC, Engh AL, Scribner KT, Funk SM, Holekamp KE (2004) Behavioural structuring of relatedness in the spotted hyena (Crocuta crocuta) suggests direct fitness benefits of clan-level cooperation. Mol Ecol 13:449–458
Wcislo W, Fewell JH, Rubenstein DR, Abbot P (2017) Sociality in bees. In: Rubenstein DR, Abbot P (eds) Comparative social evolution. Cambridge University Press, pp 50–83
West SA, Griffin AS, Gardner A (2007) Evolutionary explanations for cooperation. Curr Biol 17:661–672
Wickham H (2009) ggplot2: elegant graphics for data analysis. Springer-Verlag, New York
Wiernasz DC, Cole BJ (2003) Queen size mediates queen survival and colony fitness in harvester ants. Evolution 57:2179–2183
Wiernasz DC, Hines J, Parker DG, Cole BJ (2008) Mating for variety increases foraging activity in the harvester ant, Pogonomyrmex occidentalis. Mol Ecol 17:1137–1144
Wiernasz DC, Sater AK, Abell AJ, Cole BJ (2001) Male size, sperm transfer, and colony fitness in the western harvester ant, Pogonomyrmex occidentals. Evolution 55:324–329
Acknowledgements
Special thanks to Bert Hölldobler, Rebecca Clark, and Ron Rutowski for advice and support. Thanks to field assistance from Luis Garcia, Fred Elick, Evan Farrar, and Anna Ortiz. Thanks to the California State Park system and to Cuyamaca Rancho State Park for facilitating collections and field work at Cuyamaca. Thanks to Jürgen Heinze and three anonymous reviewers for their helpful comments on this manuscript.
Funding
This research was partially funded by NSF Award IOS-1558127 to JHF, and by NSF IOS-1501655 to JHF and BRH. JG was funded by the German Research Foundation (DFG) as part of the SFB TRR 212 (NC3) – TP C04 project numbers 316099922 and 396780988.
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Haney, B.R., Gadau, J. & Fewell, J.H. Annual fitness costs may be balanced by a conservative life history strategy in groups of unrelated ant queens. Behav Ecol Sociobiol 77, 75 (2023). https://doi.org/10.1007/s00265-023-03347-1
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DOI: https://doi.org/10.1007/s00265-023-03347-1