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Not too big, not too small: raids at moderately sized hosts lead to optimal outcomes for a slave-making ant

Abstract

Understanding the trajectory of host-parasite co-evolution requires knowledge of how hosts and parasites impact one another’s fitness, especially among the avian and insect social parasites. Host choice is an important first step in this process, but the principles guiding host choice are unresolved, especially for specialist parasites choosing among individual hosts with multiple traits. To determine how parasites weigh various host traits relative to others, we need to identify their costs and benefits. Here I use the slave-making ant, Temnothorax americanus, to investigate the payoffs from different host trait combinations. I measured the costs and benefits of raids at hosts that varied in their value (# brood), defensive power (# workers), or their ratios. Additionally, I investigated whether slave-maker fighting power influences which host trait combinations were optimal. Slave-makers performed best when hosts contained more brood but fewer workers. However, the ability to maximize this ratio is constrained by the correlation of brood and worker numbers in natural nests, making the optimal host moderately sized. Measures of costs reinforce this conclusion, since slave-maker mortality increased with the number of host workers. Additionally, I found that larger slave-maker colonies have higher payoffs at larger hosts, suggesting their optimal host trait profile differs from smaller colonies. This study shows that social parasites exercising force ought to balance a trade-off between host value and defensibility, rather than maximizing only value. Furthermore, the results highlight that host demography could play a larger role in insect social parasite arms races than previously appreciated.

Significance statement

A key to understanding the outcome of co-evolutionary arms races in social parasites is identifying the traits that contribute to the success of parasites and hosts. Host choice determines which traits experience selection, but the relative costs and benefits associated with different host traits, and how parasites ought to weigh them, remains unclear. I measure parasite success in relation to host and parasite demographic traits to distinguish the relative impacts of each using a slave-making ant. Maximizing host brood-to-worker ratio leads to higher payoffs, while the most populous hosts are impenetrable. These findings provide evidence that social parasites attacking by force seek a balance between a host’s value and defensibility, even if it means forgoing hosts with higher potential value. This in turn highlights colony demography and life history as important host traits under selection in co-evolutionary arms races in social insect parasites.

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Fig. 1
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Data availability

The datasets generated and analyzed during the current study will be available in the Dryad repository upon acceptance for publication.

References

  1. Alloway T (1979) Behaviour of two species of slave-making ants, Harpagoxenus americanus (Emery) and Leptothorax duloticus wesson (Hymenoptera: Formicidae). Anim Behav 27:202–210

  2. Alloway T, Del Rio Pesado MG (1983) Behvaior of the slave-making ant, Harpagoxenus americanus (Emery) and its host species under “seminatural” laboratory conditions. Psyche (Stuttg) 85:425–436

  3. Banks AJ, Martin TE (2001) Host and the risk of nest parasitism by brown-headed cowbirds. Behav Ecol 12:31–40. https://doi.org/10.1093/oxfordjournals.beheco.a000375

  4. Bates D, Maechler M, Bolker B, Walker S (2018) Package “lme4.” Linear Mixed Effect Models using “Eigen” S4. R package version 1.1-19. https://CRAN.R-project.org/package=lme4

  5. Bhatkar A, Whitcomb WH (1970) Artificial diet for rearing various species of ants. Florida Entomol 53:229–232

  6. Bize P, Jeanneret C, Klopfenstein A, Roulin A (2008) What makes a host profitable? Parasites balance host nutritive resources against immunity. Am Nat 171:107–118. https://doi.org/10.1086/523943

  7. Bolker BM, Brooks ME, Clark CJ, et al (2009) Generalized linear mixed models: a practical guide for ecology and evolution. Trends Ecol Evol 24:127–35. https://doi.org/10.1016/j.tree.2008.10.008

  8. Brandt M, Foitzik S (2004) Community context and specialization influence coevolution between a slavemaking ant and its hosts. Ecology 85:2997–3009

  9. Brandt M, Foitzik S, Fischer-blass B, Heinze J (2005) The coevolutionary dynamics of obligate ant social parasite systems – between prudence and antagonism. Biol Rev 80:251–267

  10. Brandt M, Heinze J, Schmitt T, Foitzik S (2006) Convergent evolution of the Dufour’s gland secretion as a propaganda substance in the slave-making ant genera Protomognathus and Harpagoxenus. Insect Soc 53:291–299. https://doi.org/10.1007/s00040-006-0871-z

  11. Burnham KP, Anderson DR, Huyvaert KP (2011) AIC model selection and multimodel inference in behavioral ecology: Some background, observations, and comparisons. Behav Ecol Sociobiol 65:23–35. https://doi.org/10.1007/s00265-010-1029-6

  12. Cervo R, Turillazzi S (1996) Host nest preference and nest choice in the cuckoo paper wasp Polistes sulcifer ( Hymenoptera : Vespidae ). J Insect Behav 9:297–306

  13. Christe P, Moller AP, de Lope F (1998) Immunocompetence and nestling survival in the house martin : the tasty chick hypothesis. Oikos 83:175–179

  14. Davies NB, Bourke AFG, de L. Brooke M (1989) Cuckoos and parasitic ants: interspecific brood parasitism as an evolutionary arms race. Trends Ecol Evol 4:274–278. https://doi.org/10.1016/0169-5347(89)90202-4

  15. Dawkins R, Krebs JR (1979) Arms races between and within species. Proc R Soc B 205:489–511

  16. Feeney WE, Welbergen JA, Langmore NE (2014) Advances in the study of coevolution between avian brood parasites and their hosts. Annu Rev Ecol Evol Syst 45:227–248. https://doi.org/10.1146/annurev-ecolsys-120213-091603

  17. Foitzik S, Fischer B, Heinze J (2003) Arms races between social parasites and their hosts: geographic patterns of manipulation and resistance. Behav Ecol 14:80–88. https://doi.org/10.1093/beheco/14.1.80

  18. Foitzik S, Achenbach A, Brandt M (2009) Locally adapted social parasite affects density, social structure, and life history of its ant hosts. Ecology 90:1195–1206

  19. Franks NR, Partridge LW (1993) Lanchester battles and the evolution of combat in ants. Anim Behav 45:197–199. https://doi.org/10.1006/anbe.1993.1021

  20. Grim T (2006) Cuckoo growth performance in parasitized and unused hosts: not only host size matters. Behav Ecol Sociobiol 60:716–723. https://doi.org/10.1007/s00265-006-0215-z

  21. Grim T, Samaš P, Moskát C et al (2011) Constraints on host choice: why do parasitic birds rarely exploit some common potential hosts? J Anim Ecol 80:508–518. https://doi.org/10.1111/j.1365-2656.2010.01798.x

  22. Grüter C, Jongepier E, Foitzik S (2018) Insect societies fight back: the evolution of defensive traits against social parasites. Philos Trans R Soc B Biol Sci 373:20170200. https://doi.org/10.1098/rstb.2017.0200

  23. Hölldobler B (1976) Tournaments and slavery in a desert ant. Science 192:912–914. https://doi.org/10.1126/science.192.4242.912

  24. Hölldobler B, Wilson EO (1990) The ants. Belknap Press, Cambridge

  25. Hunt J, Brooks R, Jennions MD (2005) Female mate choice as a condition-dependent life-history trait. Am Nat 166:79–92. https://doi.org/10.1086/430672

  26. Jongepier E, Kleeberg I, Job S, Foitzik S (2014) Collective defence portfolios of ant hosts shift with social parasite pressure. Proc Biol Sci 281:20140225. https://doi.org/10.1098/rspb.2014.0225

  27. Jongepier E, Kleeberg I, Foitzik S (2015) The ecological success of a social parasite increases with manipulation of collective host behaviour. J Evol Biol 28:2152–2162. https://doi.org/10.1111/jeb.12738

  28. Kilner RM, Langmore NE (2011) Cuckoos versus hosts in insects and birds: adaptations, counter-adaptations and outcomes. Biol Rev 838:836–852. https://doi.org/10.1111/j.1469-185X.2010.00173.x

  29. Kleeberg I, Pamminger T, Jongepier E et al (2014) Forewarned is forearmed: aggression and information use determine fitness costs of slave raids. Behav Ecol 25:1058–1063. https://doi.org/10.1093/beheco/aru084

  30. Kleeberg I, Jongepier E, Job S, Foitzik S (2015) Geographic variation in social parasite pressure predicts intraspecific but not interspecific aggressive responses in hosts of a slavemaking ant. Ethology 121:1–9. https://doi.org/10.1111/eth.12384

  31. Louder MIM, Schelsky WM, Albores AN, Hoover JP (2015) A generalist brood parasite modifies use of a host in response to reproductive success. Proc R Soc B Biol Sci 282:20151615. https://doi.org/10.1098/rspb.2015.1615

  32. Mcglynn TP (2000) Do Lanchester ’ s laws of combat describe competition in ants ? Behav Ecol 11:686–690

  33. Modlmeier AP, Liebmann JE, Foitzik S (2012) Diverse societies are more productive: a lesson from ants. Proc R Soc B 279:2142–2150. https://doi.org/10.1098/rspb.2011.2376

  34. Pamminger T, Scharf I, Pennings PS, Foitzik S (2011) Increased host aggression as an induced defense against slave-making ants. Behav Ecol 22:255–260. https://doi.org/10.1093/beheco/arq191

  35. Plowes NJR, Adams ES (2005) An empirical test of Lanchester ’ s square law : mortality during battles of the fire ant Solenopsis invicta. Proc R Soc B 272:1809–1814. https://doi.org/10.1098/rspb.2005.3162

  36. Pohl S, Foitzik S (2011) Slave-making ants prefer larger, better defended host colonies. Anim Behav 81:61–68. https://doi.org/10.1016/j.anbehav.2010.09.006

  37. Pohl S, Foitzik S (2013) Parasite scouting and host defence behaviours are influenced by colony size in the slave-making ant Protomognathus americanus. Insect Soc 60:293–301. https://doi.org/10.1007/s00040-013-0293-7

  38. Regnier FE, Wilson EO (1971) Chemical communication and “ propaganda ” in slave-maker ants. Science (80- ) 172:267–269

  39. Remeš V (2010) Explaining postnatal growth plasticity in a generalist brood parasite. Naturwissenschaften 97:331–335. https://doi.org/10.1007/s00114-009-0635-5

  40. Ripley B, Venables B, Bates DM, Hornik K, Gebhart A, Firth D (2018) Package “MASS”: Support Functions and Datasets for Venables and Ripley's MASS. R package version 7.3-511. http://www.stats.ox.ac.uk/pub/MASS4/

  41. Rosengren R, Pamilo P (1983) The evolution of polygyny and polydomy in mound-building Formica ants. Act Entomol Fenn 42:65–77

  42. Savolainen R, Deslippe RJ (1996) Facultative and obligate slavery in formicine ants : frequency of slavery, and proportion and size of slaves. Biol J Linn Soc 57:47–58

  43. Schmid-Hempel P (2003) Variation in immune defence as a question of evolutionary ecology. Proc R Soc B Biol Sci 270:357–366. https://doi.org/10.1098/rspb.2002.2265

  44. Schumann RD, Buschinger A (1995) Imprinting effects on host-selection behavior of slave-raiding Chalepoxenus muellerianus ( Finzi ) workers ( Hymenoptera : Formicidae ). Ethology 251:243–251

  45. Sheldon BC, Verhulst S (1996) Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends Ecol Evol 5347:1–5. https://doi.org/10.1016/0169-5347(96)10039-2

  46. Smith JA, Schwarz MP (2009) Decisions , decisions , decisions : the host colony choices of a social parasite. Ethology 27:385–389. https://doi.org/10.1007/s10164-008-0131-y

  47. Soler JJ, Soler M, Moller AP, Martinez JG (1995) Does the great spotted cuckoo choose magpie hosts according to their parenting ability ? Behav Ecol Sociobiol 36:201–206

  48. Soler JJ, Avilés JM, Martín-Gálvez D, de Neve L, Soler M (2014) Eavesdropping cuckoos: further insights on great spotted cuckoo preference by magpie nests and egg colour. Oecologia 175:105–115. https://doi.org/10.1007/s00442-014-2901-2

  49. Stephens DW, Krebs JR (1986) Foraging theory. Princeton University Press, Princeton

  50. Teuschl Y, Taborsky B, Taborsky M (1998) How do cuckoos find their hosts? The role of habitat imprinting. Anim Behav 56:1425–1433. https://doi.org/10.1006/anbe.1998.0931

  51. Theron A, Rognon A, Pages J-R (1998) Host choice by larval parasites : a study of Biomphalaria glabrata snails and Schistosoma mansoni miracidia related to host size. Parasitol Res 84:727–732

  52. Václav R, Valera F (2018) Host preference of a haematophagous avian ectoparasite: a micronutrient supplementation experiment to test an evolutionary trade-off. Biol J Linn Soc 125:171–183. https://doi.org/10.1093/BIOLINNEAN/BLY089

  53. Valera F, Hoi H, Darolova A, Kristofik J (2004) Size versus health as a cue for host choice : a test of the tasty chick hypothesis. Parasitology 129:59–68. https://doi.org/10.1017/S0031182004005232

  54. Wesson L (1939) Contributions to the natural history of Harpagoxenus americanus Emery (Hymenoptera: Formicidae). Trans Am Entomol Soc 65:97–122

  55. Whitehouse M, Jaffe K (1996) Ant wars: combat trategies, territory and nest defense in the leaf-cutting ant Atta laevigata. Anim Behav 51:1207–1217

  56. Wust M, Menzel F (2016) I smell where you walked - how chemical cues influence movement decisions in ants. Oikos 126:149–160. https://doi.org/10.1111/oik.03332

  57. Zamora-Muñoz C, Ruano F, Errard C et al (2003) Coevolution in the slave-parasite system Proformica longiseta-Rossomyrmex minuchae (Hymenoptera: Formicidae). Sociobiology 42:299–317

  58. Zuur A, Leno E, Walker NJ, Saveliev A (2009) GLM and GAM for Count Data. In: Mixed effects models and extensions in ecology with R. Springer, New York, pp 210–243

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Correspondence to Julie S. Miller.

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Miller, J.S. Not too big, not too small: raids at moderately sized hosts lead to optimal outcomes for a slave-making ant. Behav Ecol Sociobiol 74, 18 (2020). https://doi.org/10.1007/s00265-019-2797-2

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Keywords

  • Slave-making ants
  • Social parasite
  • Host
  • Choice
  • Colony size