Advertisement

Early ontogenic emergence of personality and its long-term persistence in a social spider

  • Bharat Parthasarathy
  • Chinmay Hemant Joshi
  • Sreethin Sreedharan Kalyadan
  • Hema SomanathanEmail author
Original Article

Abstract

Recent studies increasingly show that personality types in animals can vary with time. Personality types including boldness and aggression have been recently reported as important determinants of collective task performance, task specialisation and task proficiency in social spiders. These studies were performed in subadult and adult spiders and over the short term (3–15 days). Therefore, the ontogeny of these personality types and its persistence over timescales relevant to the lifespan of any social spider species remains unknown. In the social spider Stegodyphus sarasinorum, we investigated 1) if early instar juveniles exhibited consistent and repeatable personality types, 2) if personality types persisted over the long term in subadults and 3) if personality types are influenced by subadult body condition. Juveniles (3rd and 4th instars) showed consistent inter-individual differences and repeatability in boldness and aggression (across 21 days). Subadults showed consistency in boldness and aggression over a duration of 51 days, which covers a significant part of the subadult stage. However, repeatability of these traits declined over the long term. Moreover, boldness and aggression were not influenced by body condition (nutritional state) of subadults. Thus, we hypothesise that the early ontogeny of personality and its long-term persistence can influence behavioural propensities and task partitioning through later life stages in social spider colonies.

Significance statement

Personalities have been demonstrated in a number of animal species. In animal societies, individuals with different personality types are known to engage in different activities within the group, leading to overall efficiency. Personalities have recently been shown to exist in social spiders. For example, aggressive spiders have a greater tendency to hunt prey than less aggressive individuals. However, for most animals, it remains unknown whether personality types manifest in very young individuals. Here, we show for the first time in social spiders that juveniles have personalities just as in adults. We also show that personality types persist over significant portions of individuals’ life spans. These findings show that stable personality types can be important in collective tasks such as capturing prey.

Keywords

Ontogeny Personality Repeatability Social spiders Stegodyphus sarasinorum 

Notes

Authors’ contribution

BP and HS conceptualised the study and designed experiments; CHJ and SK and BP performed experiments; BP analysed data; BP and HS wrote and revised the manuscript.

Funding information

This study was financially supported by the Council for Industrial and Scientific Research (CSIR) India.

References

  1. Amir N, Whitehouse M, Lubin Y (2000) Food consumption rates and competition in a communally feeding social spider, Stegodyphus dumicola (Eresidae). J Arachnol 28:195–200CrossRefGoogle Scholar
  2. Avilés L (1997) Causes and consequences of cooperation and permanent-sociality in spiders. In: The evolution of social behavior in insects and arachnids. Cambridge University Press, Cambridge, pp 476–498CrossRefGoogle Scholar
  3. Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed models using lme4. J Stat Softw 67:1–48CrossRefGoogle Scholar
  4. Beleyur T, Bellur DU, Somanathan H (2015) Long-term behavioural consistency in prey capture but not in web maintenance in a social spider. Behav Ecol Sociobiol 69:1019–1028.  https://doi.org/10.1007/s00265-015-1915-z CrossRefGoogle Scholar
  5. Bell AM, Sih A (2007) Exposure to predation generates personality in threespined sticklebacks (Gasterosteus aculeatus). Ecol Lett 10:828–834.  https://doi.org/10.1111/j.1461-0248.2007.01081.x CrossRefPubMedGoogle Scholar
  6. Bell AM, Stamps JA (2004) Development of behavioural differences between individuals and populations of sticklebacks, Gasterosteus aculeatus. Anim Behav 68:1339–1348CrossRefGoogle Scholar
  7. Bell AM, Hankison SJ, Laskowski KL (2009) The repeatability of behaviour: a meta-analysis. Anim Behav 77:771–783.  https://doi.org/10.1016/j.anbehav.2008.12.022 CrossRefPubMedPubMedCentralGoogle Scholar
  8. Biro PA (2012) Do rapid assays predict repeatability in labile (behavioural) traits? Anim Behav 83:1295–1300.  https://doi.org/10.1016/j.anbehav.2012.01.036 CrossRefGoogle Scholar
  9. Briffa M, Weiss A (2010) Animal personality. Curr Biol 20:912–914.  https://doi.org/10.1016/j.cub.2010.09.019 CrossRefGoogle Scholar
  10. Christensen RHB (2018) Regression models for ordinal data. R Package Version 2018. 8–25Google Scholar
  11. Clark CW (1994) Antipredator behavior and the asset-protection principle. Behav Ecol 5:159–170CrossRefGoogle Scholar
  12. Dall SRX, Griffith SC (2014) An empiricist guide to animal personality variation in ecology and evolution. Front Ecol Evol 2:1–7.  https://doi.org/10.3389/fevo.2014.00003 CrossRefGoogle Scholar
  13. Dall SRX, Houston AI, McNamara JM (2004) The behavioural ecology of personality: consistent individual differences from an adaptive perspective. Ecol Lett 7:734–739.  https://doi.org/10.1111/j.1461-0248.2004.00618.x CrossRefGoogle Scholar
  14. David M, Auclair Y, Cézilly F (2012) Assessing short- and long-term repeatability and stability of personality in captive zebra finches using longitudinal data. Ethology 118:932–942.  https://doi.org/10.1111/j.1439-0310.2012.02085.x CrossRefGoogle Scholar
  15. de Villemereuil P, Morrissey MB, Nakagawa S, Schielzeth H (2018) Fixed effect variance and the estimation of repeatabilities and heritabilities: issues and solutions. J Evol Biol 31:621–632.  https://doi.org/10.1111/jeb.13232 CrossRefPubMedGoogle Scholar
  16. Dingemanse NJ, Kazem AJN, Reale D, Wright J (2010a) Behavioural reaction norms: animal personality meets individual plasticity. Trends Ecol Evol 25:81–89CrossRefGoogle Scholar
  17. Dingemanse NJ, Dochtermann N, Wright J (2010b) A method for exploring the structure of behavioural syndromes to allow formal comparison within and between data sets. Anim Behav 79:439–450.  https://doi.org/10.1016/j.anbehav.2009.11.024. CrossRefGoogle Scholar
  18. Dingemanse NJ, Bouwman KM, van de Pol M, van Overveld T, Patrick SC, Matthysen E, Quinn JL (2012) Variation in personality and behavioural plasticity across four populations of the great tit Parus major. J Anim Ecol 81:116–126.  https://doi.org/10.1111/j.1365-2656.2011.01877.x CrossRefPubMedGoogle Scholar
  19. Dochtermann NA, Schwab T, Sih A (2015) The contribution of additive genetic variation to personality variation: heritability of personality. Proc Biol Sci 282:20142201CrossRefGoogle Scholar
  20. Goodrich B, Gabry J, Ali I, Brilleman S (2018) rstanarm: Bayesian applied regression modelling via Stan. R Package Version 2.17.4. http://mc-stan.org/
  21. Gordon D (1996) The organization of work in social insect colonies. Nature 380:121–124CrossRefGoogle Scholar
  22. Grinsted L, Bacon JP (2014) Animal behaviour: task differentiation by personality in spider groups. Curr Biol 24:R749–R751.  https://doi.org/10.1016/j.cub.2014.07.008 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Grinsted L, Bilde T (2013) Effects of within-colony competition on body size asymmetries and reproductive skew in a social spider. J Evol Biol 26:553–561CrossRefGoogle Scholar
  24. Grinsted L, Pruitt JN, Settepani V, Bilde T (2013) Individual personalities shape task differentiation in a social spider. Proc Biol Sci 280:20131407.  https://doi.org/10.1098/rspb.2013.1407 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Gyuris E, Fero O, Barta Z (2012) Personality traits across ontogeny in firebugs Pyrrhocoris apterus. Anim Behav 84:103–109CrossRefGoogle Scholar
  26. Hadfield JD (2010) MCMC methods for multi-response generalized linear mixed models: the MCMCglmm R package. J Stat Softw 33:1–22CrossRefGoogle Scholar
  27. Herde A, Eccard J (2013) Consistency in boldness, activity and exploration at different stages of life. BMC Ecol 13:1–10.  https://doi.org/10.1186/1472-6785-13-49 CrossRefGoogle Scholar
  28. Holbrook CT, Wright CM, Pruitt JN (2014) Individual differences in personality and behavioural plasticity facilitate division of labour in social spider colonies. Anim Behav 97:177–183.  https://doi.org/10.1016/j.anbehav.2014.09.015 CrossRefGoogle Scholar
  29. Jacson C, Joseph K (1973) Life-history, bionomics and behaviour of the social spider Stegodyphus sarasinorum Karsch. Insect Soc 20:189–204CrossRefGoogle Scholar
  30. Jones TC, Akoury TS, Hauser CK, Neblett MF II, Linville BJ, Edge AA, Weber NO (2011) Octopamine and serotonin have opposite effects on antipredator behavior in the orb-weaving spider, Larinioides cornutus. J Comp Physiol 197:819–825.  https://doi.org/10.1007/s00359-011-0644-7 CrossRefGoogle Scholar
  31. Keiser CN, Pruitt JN (2014) Personality composition is more important than group size in determining collective foraging behaviour in the wild. Proc Biol Sci 281:20141424CrossRefGoogle Scholar
  32. Keiser CN, Jones DK, Modlmeier AP, Pruitt JN (2014) Exploring the effects of individual traits and within-colony variation on task differentiation and collective behavior in a desert social spider. Behav Ecol Sociobiol 68:839–850.  https://doi.org/10.1007/s00265-014-1696-9 CrossRefGoogle Scholar
  33. Keiser CN, Lichtenstein JLL, Wright CM, Chism GT, Pruitt JN (2018) Personalities and behavioural syndromes in insects and spiders. In: Cordoba-Aguilar A, Gonzalez-Tokman D, Gonzalez-Santoyo I (eds) Insect behavior: from mechanisms to ecological and evolutionary consequences. Oxford University Press, OxfordGoogle Scholar
  34. Kralj-Fiser S, Schuett W (2014) Studying personality variation in invertebrates: why bother? Anim Behav 91:41–25.  https://doi.org/10.1016/j.anbehav.2014.02.016 CrossRefGoogle Scholar
  35. Lichtenstein JLL, Dirienzo N, Knutson K, Kuo C, Zhao KC, Brittingham HA, Geary SE, Ministero S, Rice HK, David Z et al (2016) Prolonged food restriction decreases body condition and reduces repeatability in personality traits in web-building spiders. Behav Ecol Sociobiol 70:1793–1803.  https://doi.org/10.1007/s00265-016-2184-1 CrossRefGoogle Scholar
  36. Lubin Y, Bilde T (2007) The evolution of sociality in spiders. Adv Study Behav 37:83–145.  https://doi.org/10.1016/S0065-3454(07)37003-4 CrossRefGoogle Scholar
  37. Luedecke D (2018) sjPlot: data visualization for statistics in social science. R Package Version 2.6.2.  https://doi.org/10.5281/zenodo.1308157
  38. McElreath R, Luttbeg B, Fogarty SP, Brodin T, Sih A (2007) Evolution of animal personalities. Nature 450:E5–E5; discussion E6.  https://doi.org/10.1038/nature06326 CrossRefPubMedGoogle Scholar
  39. McNamara JM, Barta Z, Houston AI (2004) Variation in behaviour promotes cooperation in the prisoner’s dilemma game. Nature 428:745–748.  https://doi.org/10.1038/nature02432 CrossRefPubMedGoogle Scholar
  40. Modlmeier AP, Foitzik S (2011) Productivity increases with variation in aggression among group members in Temnothorax ants. Behav Ecol 22:1026–1032.  https://doi.org/10.1093/beheco/arr086 CrossRefGoogle Scholar
  41. Modlmeier AP, Liebmann JE, Foitzik S (2012) Diverse societies are more productive: a lesson from ants. Proc Biol Sci 279:2142–2150.  https://doi.org/10.1098/rspb.2011.2376 CrossRefPubMedPubMedCentralGoogle Scholar
  42. Nakagawa S, Schielzeth H (2010) Repeatability for Gaussian and non-Gaussian data: a practical guide for biologists. Biol Rev 85:935–956.  https://doi.org/10.1111/j.1469-185X.2010.00141.x. CrossRefGoogle Scholar
  43. Nakagawa S, Schielzeth H (2013) A general and simple method for obtaining R2 from generalized linear mixed-effects models. Methods Ecol Evol 4:133–142.  https://doi.org/10.1111/j.2041-210x.2012.00261.x CrossRefGoogle Scholar
  44. Niemelä PT, Vainikka A, Hedrick AV, Kortet R (2012) Integrating behaviour with life history: boldness of the field cricket, Gryllus integer, during ontogeny. Funct Ecol 26:450–456.  https://doi.org/10.1111/j.1365-2435.2011.01939.x CrossRefGoogle Scholar
  45. Nussey DH, Postma E, Gienapp P, Visser ME (2005) Selection on heritable phenotypic plasticity in a wild bird population. Science 310:304–306.  https://doi.org/10.1126/science.1117004. CrossRefPubMedGoogle Scholar
  46. Parthasarathy B, Somanathan H (2018) Body condition and food shapes group dispersal but not solitary dispersal in a social spider. Behav Ecol 29:619–627CrossRefGoogle Scholar
  47. Peig J, Green AJ (2009) New perspectives for estimating body condition from mass/length data: the scaled mass index as an alternative method. Oikos 118:1883–1891.  https://doi.org/10.1111/j.1600-0706.2009.17643.x CrossRefGoogle Scholar
  48. Petelle MB, McCoy DE, Alejandro V, Martin JGA, Blumstein DT (2013) Development of boldness and docility in yellow-bellied marmots. Anim Behav 86:1147–1154CrossRefGoogle Scholar
  49. Platnick N (2017) The world spider catalog, version 18.5. AM Mus Nat Hist. Available at http://research.amnh.org/entomology/spiders/catalog/index.html. Accessed 11 July 2017
  50. Price JB (2010) Neurochemical levels correlate with population level differences in social structure and individual behavior in the polyphenic spider, Anelosimus studiosus. Electron. Theses Diss. East Tennessee State Univ. Retrieved: Open Educational Resources (OER) Portal at https://dc.etsu.edu/etd/1760/
  51. Pruitt JN, Riechert SE (2011) How within-group behavioural variation and task efficiency enhance fitness in a social group. Proc Biol Sci 278:1209–1215.  https://doi.org/10.1098/rspb.2010.1700 CrossRefPubMedGoogle Scholar
  52. Pruitt J, Riechert SE, Jones TC (2008) Behavioural syndromes and their fitness consequences in a socially polymorphic spider, Anelosimus studiosus. Anim Behav 76:871–879.  https://doi.org/10.1016/j.anbehav.2008.05.009 CrossRefGoogle Scholar
  53. Pruitt JN, Demes KW, Dittrich-reed DR (2011) Temperature mediates shifts in individual aggressiveness, activity level, and social behavior in a spider. Ethology 117:318–325.  https://doi.org/10.1111/j.1439-0310.2011.01877.x CrossRefGoogle Scholar
  54. Pruitt JN, Grinsted L, Settepani V (2013) Linking levels of personality: personalities of the ‘average’ and ‘most extreme’ group members predict colony-level personality. Anim Behav 86:391–399.  https://doi.org/10.1016/j.anbehav.2013.05.030 CrossRefGoogle Scholar
  55. R Core Team (2018) A language and environment for statistical computing: R foundation for statistical computing, Vienna, AustriaGoogle Scholar
  56. Réale D, Reader SM, Sol D, McDougall PT, Dingemanse NJ (2007) Integrating animal temperament within ecology and evolution. Biol Rev 82:291–318.  https://doi.org/10.1111/j.1469-185X.2007.00010.x CrossRefPubMedPubMedCentralGoogle Scholar
  57. Riechert SE, Hedrick AV (1993) A test for correlations among fitness-linked behavioural traits in the spider Agelenopsis aperta (Araneae, Agelenidae). Anim Behav 46:669–675CrossRefGoogle Scholar
  58. Riechert SE, Johns PM (2003) Do female spiders select heavier males for the genes for behavioral aggressiveness they offer their offspring? Evolution 57:1367–1373CrossRefGoogle Scholar
  59. Salomon M, Mayntz D, Lubin Y (2008) Colony nutrition skews reproduction in a social spider. Behav Ecol 19:605–611CrossRefGoogle Scholar
  60. Schulte-Hostedde A, Hickling GJ, Millar JS, Hickling GJ (2001) Evaluating body condition in small mammals. Can J Zool 79:1021–1029.  https://doi.org/10.1139/cjz-79-6-1021 CrossRefGoogle Scholar
  61. Settepani V, Grinsted L, Bilde T (2013) Task specialization in two social spiders, Stegodyphus sarasinorum (Eresidae) and Anelosimus eximius (Theridiidae). J Evol Biol 26:51–62.  https://doi.org/10.1111/jeb.12024 CrossRefPubMedPubMedCentralGoogle Scholar
  62. Sih A, Bell AM (2008) Insights for behavioral ecology from behavoural syndromes. Adv Study Behav 38:227–281.  https://doi.org/10.1016/S0065-3454(08)00005-3 CrossRefPubMedPubMedCentralGoogle Scholar
  63. Sih A, Bell AM, Johnson CJ, Ziemba RE (2004a) Behavioural syndromes: an integrative overview. Q Rev Biol 79:241–277.  https://doi.org/10.1086/516403. CrossRefPubMedGoogle Scholar
  64. Sih A, Bell A, Johnson JC (2004b) Behavioral syndromes: an ecological and evolutionary overview. Trends Ecol Evol 19:372–378.  https://doi.org/10.1016/j.tree.2004.04.009. CrossRefGoogle Scholar
  65. Sih A, Mathot KJ, Moirón M, Montiglio PO, Wolf M, Dingemanse NJ (2015) Animal personality and state-behaviour feedbacks: a review and guide for empiricists. Trends Ecol Evol 30:50–60.  https://doi.org/10.1016/j.tree.2014.11.004 CrossRefGoogle Scholar
  66. Smith DR, Engel MS (1994) Population structure in an Indian cooperative spider, Stegodyphus sarasinorum, Karsch. J Arachnol 22:108–113Google Scholar
  67. Smith DR, Van Rijn S, Henschel J, Bilde T, Lubin Y (2009) Amplified fragment length polymorphism fingerprints support limited gene flow among social spider populations. Biol J Linn Soc 97:235–246CrossRefGoogle Scholar
  68. Stamps J, Groothuis TGG (2010) The development of animal personality: relevance, concepts and perspectives. Biol Rev 85:301–325.  https://doi.org/10.1111/j.1469-185X.2009.00103.x CrossRefGoogle Scholar
  69. van Oers K, de Jong G, van Noordwijk A, Drent P (2005) Contribution of genetics to the study of animal personalities: a review of case studies. Behaviour 142:1185–1206.  https://doi.org/10.1163/156853905774539364 CrossRefGoogle Scholar
  70. Whitehouse ME, Lubin Y (1999) Competitive foraging in the social spider Stegodyphus dumicola. Anim Behav 58:677–688.  https://doi.org/10.1006/anbe.1999.1168 CrossRefPubMedGoogle Scholar
  71. Wilson DS (1998) Adaptive individual differences within single populations. Philos Trans R Soc Lond B Biol Sci 353:199–205.  https://doi.org/10.1098/rstb.1998.0202 CrossRefPubMedCentralGoogle Scholar
  72. Wilson ADM, Krause J (2012) Personality and metamorphosis: is behavioral variation consistent across ontogenetic niche shifts? Behav Ecol 23:1316–1323.  https://doi.org/10.1093/beheco/ars123 CrossRefGoogle Scholar
  73. Wolf M, van Doorn GS, Leimar O, Weissing FJ (2007) Life-history trade-offs favour the evolution of animal personalities. Nature 447:581–584.  https://doi.org/10.1038/nature05835 CrossRefGoogle Scholar
  74. Wright CM, Holbrook CT, Pruitt JN (2014) Animal personality aligns task specialization and task proficiency in a spider society. Proc Natl Acad Sci U S A 111:9533–9537.  https://doi.org/10.1073/pnas.1400850111 CrossRefPubMedPubMedCentralGoogle Scholar
  75. Wright CM, Keiser CN, Pruitt J (2015) Personality and morphology shape task participation, collective foraging and escape behaviour in the social spider Stegodyphus dumicola. Anim Behav 105:47–54.  https://doi.org/10.1016/j.anbehav.2015.04.001 CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Germany, part of Springer Nature 2019

Authors and Affiliations

  1. 1.IISER TVM Centre for Research in Ecology and Evolution (ICREE), School of BiologyIndian Institute of Science Education and ResearchThiruvananthapuramIndia

Personalised recommendations