Differences in neural activity, but not behavior, across social contexts in guppies, Poecilia reticulata

  • Eva K. FischerEmail author
  • Sarah E. Westrick
  • Lauren Hartsough
  • Kim L. Hoke
Original Article


Animals are continually faced with the challenge of producing context-appropriate social behaviors. In many instances, appropriate behaviors differ by social situation. However, in some instances, the same behaviors are employed across different social contexts, albeit in response to distinct stimuli and with distinct purposes. We took advantage of behavioral similarities across mating and aggression contexts in guppies, Poecilia reticulata, to understand how patterns of neural activity differ across social contexts when behaviors are nonetheless shared. While there is growing interest in understanding behavioral mechanisms in guppies, resources are sparse. As part of this study, we developed a neuroanatomical atlas of the guppy brain as a research community resource. Using this atlas, we found that neural activity in the preoptic area reflected social context, whereas individual differences in behavioral motivation paralleled activity in the posterior tuberculum and ventral telencephalon (teleost homologs of the mammalian ventral tegmental area and lateral septum, respectively). Our findings suggest independent coding of social salience versus behavioral motivation when behavioral repertoires are shared across social contexts.

Significance statement

Choosing behaviors appropriate to the current social situation is of central importance to animals. Interactions with different social partners (e.g., mates, competitors, or offspring) generally require distinct behavioral repertories. However, in some cases, similar behaviors are used across social contexts. The neural mechanisms underlying social behavior are particularly intriguing in these situations, where the same behaviors are produced in response to distinct social stimuli and for distinct purposes. We took advantage of behavioral similarities across mating and aggression interactions in Trinidadian guppies to explore how social information is reflected in the brain when fish perform a common set of behaviors across contexts. We found that activity in distinct brain regions reflects social context versus behavioral motivation, suggesting a means by which social inputs and behavioral outputs can be coded independently of one another.


Social behavior Neural activation Preoptic area Teleost Poecilia reticulata Guppy 



We thank the members of the Guppy Lab for help with fish care, Lauren A. O’Connell for consultation on the guppy brain atlas, and two anonymous reviewers for comments on previous versions of the manuscript. We gratefully acknowledge support from the National Science Foundation (NSF IOS-1354755 to KLH).


This study was funded by the National Science Foundation (NSF IOS-1354755 to KLH).

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest.

Ethical approval

All applicable international, national, and/or institutional guidelines for the care and use of animals were followed. All procedures involving animals were in accordance with the ethical standards of Colorado State University Animal Care and Use Committee (Approval #12-3818A), who approved all animal husbandry, experimental methods, and tissue collection procedures.

Supplementary material

265_2018_2548_MOESM1_ESM.pdf (21.8 mb)
ESM S1 Neuroanatomical atlas of the guppy brain (PDF 22278 kb)
265_2018_2548_MOESM2_ESM.xlsx (68 kb)
ESM S2 Raw data for behavior and pS6 cell counts (XLSX 67 kb)


  1. Alger SJ, Riters LV (2006) Lesions to the medial preoptic nucleus differentially affect singing and nest box-directed behaviors within and outside of the breeding season in European starlings (Sturnus vulgaris). Behav Neurosci 120:1326–1336. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Alger SJ, Maasch SN, Riters LV (2009) Lesions to the medial preoptic nucleus affect immediate early gene immunolabeling in brain regions involved in song control and social behavior in male European starlings. Eur J Neurosci 29:970–982. CrossRefPubMedPubMedCentralGoogle Scholar
  3. Almeida O, Gozdowska M, Kulczykowska E, Oliveira RF (2012) Brain levels of arginine-vasotocin and isotocin in dominant and subordinate males of a cichlid fish. Horm Behav 61:212–217. CrossRefPubMedGoogle Scholar
  4. Anken R, Rahmann H (1994) Brain atlas of the adult swordtail fish Xiphophorus helleri and of certain developmental stages. Fischer, StuttgartGoogle Scholar
  5. Bharati IS, Goodson JL (2006) Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches. Neuroscience 143:661–670. CrossRefPubMedPubMedCentralGoogle Scholar
  6. Bielsky IF, Hu SB, Ren X, Terwilliger EF, Young LJ (2005) The V1a vasopressin receptor is necessary and sufficient for normal social recognition: a gene replacement study. Neuron 47:503–513. CrossRefPubMedGoogle Scholar
  7. Botham MS, Hayward RK, Morrell LJ, Croft D, Ward J, Ramnarine I, Krause J (2008) Risk-sensitive antipredator behavior in the Trinidadian gupy, Poecilia reticulata. Ecology 89:3174–3185. CrossRefGoogle Scholar
  8. Bruce KE, White WG (1995) Agonistic relationships and sexual behaviour patterns in male guppies, Poecilia reticulata. Anim Behav 50:1009–1021. CrossRefGoogle Scholar
  9. Burmeister SS, Mangiamele LA, Lebonville CL (2008) Acoustic modulation of immediate early gene expression in the auditory midbrain of female túngara frogs. Brain Res 1190:105–114. CrossRefPubMedGoogle Scholar
  10. Burns JG, Price AC, Thomson JD, Hughes KA, Rodd FH (2016) Environmental and genetic effects on exploratory behavior of high- and low-predation guppies (Poecilia reticulata). Behav Ecol Sociobiol 70:1187–1196. CrossRefGoogle Scholar
  11. Cabrera-Álvarez MJ, Swaney WT, Reader SM (2017) Forebrain activation during social exposure in wild-type guppies. Physiol Behav 182:107–113. CrossRefPubMedGoogle Scholar
  12. Catchpole CK (2008) Bird song: biological themes and variations, 2nd edn. Cambridge University Press, CambridgeCrossRefGoogle Scholar
  13. Chapman BB, Morrell LJ, Krause J (2009) Plasticity in male courtship behaviour as a function of light intensity in guppies. Behav Ecol Sociobiol 63:1757–1763. CrossRefGoogle Scholar
  14. Croft DP, Arrowsmith BJ, Bielby J, White E, Couzin ID, Magurran AE, Ramnarine I, Krause J (2003) Mechanisms underlying shoal composition in the Trinidadian guppy, Poecilia reticulata. Oikos 100:429–438. CrossRefGoogle Scholar
  15. Dantzer R, Koob GF, Bluthé RM, Le Moal M (1988) Septal vasopressin modulates social memory in male rats. Brain Res 457:143–147. CrossRefPubMedGoogle Scholar
  16. Davies NB, Krebs JR, West S (2012) An introduction to behavioural ecology, 4th edn. Wiley-Blackwell, OxfordGoogle Scholar
  17. Demski LS (1973) Feeding and aggressive behavior evoked by hypothalamic stimulation in a cichlid fish. Comp Biochem Physiol A Physiol 44:685–692. CrossRefGoogle Scholar
  18. Demski LS, Knigge KM (1971) The telencephalon and hypothalamus of the bluegill and reproductive behavior with representative frontal sections. J Comp Neurol 143:1–16CrossRefPubMedGoogle Scholar
  19. Farr JA (1976) Social facilitation of male sexual behavior, intrasexual competition, and sexual selection in the guppy, Poecilia reticulata (Pisces: Poeciliidae). Evolution 30:707–717CrossRefPubMedGoogle Scholar
  20. Farr JA (1980) Social behaviour patterns as determinants of reproductive success in the guppy, Poecilia reticulata Peters (Pisces: Poeciliidae): an experimental study of the effects of intermale competition, female choice, and sexual selection. Behaviour 74:38–91. CrossRefGoogle Scholar
  21. Farr JA, Herrnkind WF (1974) A quantitative analysis of social interaction of the guppy, Poecilia reticulata (Pisces:Poeciliida ) as a function of population density. Anim Behav 22:582–591. CrossRefGoogle Scholar
  22. Field KL, Waite TA (2004) Absence of female conspecifics induces homosexual behaviour in male guppies. Anim Behav 68:1381–1389. CrossRefGoogle Scholar
  23. Fischer EK, Ghalambor CK, Hoke KL (2016) Plasticity and evolution in correlated suites of traits. J Evol Biol 29:991–1002. CrossRefPubMedGoogle Scholar
  24. Foran CM, Bass AH (1999) Preoptic GnRH and AVT: axes for sexual plasticity in teleost fish. Gen Comp Endocrinol 116:141–152. CrossRefPubMedGoogle Scholar
  25. Godwin J, Thompson R (2012) Nonapeptides and social behavior in fishes. Horm Behav 61:230–238. CrossRefPubMedGoogle Scholar
  26. Gorlick DL (1976) Dominance hierarchies and factors influencing dominance in the guppy Poecilia reticulata (Peters). Anim Behav 24:336–346. CrossRefGoogle Scholar
  27. Greenwood AK, Wark AR, Fernald RD, Hofmann HA (2008) Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish. Proc R Soc Lond B 275:2393–2402. CrossRefGoogle Scholar
  28. Griffiths SW, Magurran AE (1998) Sex and schooling behaviour in the Trinidadian guppy. Anim Behav 56:689–693. CrossRefPubMedGoogle Scholar
  29. Hara E, Kubikova L, Hessler NA, Jarvis ED (2007) Role of the midbrain dopaminergic system in modulation of vocal brain activation by social context. Eur J Neurosci 25:3406–3416. CrossRefPubMedPubMedCentralGoogle Scholar
  30. Hebets EA, Barron AB, Balakrishnan CN, Hauber ME, Mason PH, Hoke KL (2016) A systems approach to animal communication. Proc R Soc B 283:20152889. CrossRefPubMedGoogle Scholar
  31. Heimovics SA, Riters LV (2005) Immediate early gene activity in song control nuclei and brain areas regulating motivation relates positively to singing behavior during, but not outside of, a breeding context. J Neurobiol 65:207–224. CrossRefPubMedGoogle Scholar
  32. Heintz MM, Brander SM, White JW (2015) Endocrine disrupting compounds alter risk-taking behavior in guppies (Poecilia reticulata). Ethology 121:480–491. CrossRefGoogle Scholar
  33. Houde AE (1988) The effects of female choice and male-male competition on the mating success of male guppies. Anim Behav 36:888–896. CrossRefGoogle Scholar
  34. Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, PrincetonGoogle Scholar
  35. Huang YC, Hessler NA (2008) Social modulation during songbird courtship potentiates midbrain dopaminergic neurons. PLoS One 3:e3281. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Huizinga M, Ghalambor CK, Reznick DN (2009) The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies, Poecilia reticulata. J Evol Biol 22:1860–1866. CrossRefPubMedGoogle Scholar
  37. Jirotkul M (1999) Population density influences male–male competition in guppies. Anim Behav 58:1169–1175CrossRefPubMedGoogle Scholar
  38. Knight ZA, Tan K, Birsoy K, Schmidt S, Garrison JL, Wysocki RW, Emiliano A, Ekstrand MI, Friedman JM (2012) Molecular profiling of activated neurons by phosphorylated ribosome capture. Cell 151:1126–1137. CrossRefPubMedGoogle Scholar
  39. Kodric-Brown A (1992) Male dominance can enhance mating success in guppies. Anim Behav 44:165–167. CrossRefGoogle Scholar
  40. Kolluru GR, Grether GF (2005) The effects of resource availability on alternative mating tactics in guppies (Poecilia reticulata). Behav Ecol 16:294–300. CrossRefGoogle Scholar
  41. Kotrschal A, Rogell B, Maklakov AA, Kolm N (2012) Sex-specific plasticity in brain morphology depends on social environment of the guppy, Poecilia reticulata. Behav Ecol Sociobiol 66:1485–1492. CrossRefGoogle Scholar
  42. Koyama Y, Satou M, Oka Y, Ueda K (1984) Involvment of the telencephalic hemispheres and the preoptic area in sexual behavior of the male goldfish, Carasius aurata: a brain-lesion study. Behav Neural Biol 40:70–86CrossRefPubMedGoogle Scholar
  43. Landgraf R, Gerstberger R, Montkowski A, Probst JC, Wotjak CT, Holsboer F, Engelmann M (1995) V1 vasopressin receptor antisense oligodeoxynucleotide into septum reduces vasopressin binding, social discrimination abilities, and anxiety-related behavior in rats. J Neurosci 15:4250–4258CrossRefPubMedGoogle Scholar
  44. Larson ET, O’Malley DM, Melloni RH (2006) Aggression and vasotocin are associated with dominant-subordinate relationships in zebrafish. Behav Brain Res 167:94–102. CrossRefPubMedGoogle Scholar
  45. Liebsch G, Wotjak CT, Landgraf R, Engelmann M (1996) Septal vasopressin modulates anxiety-related behaviour in rats. Neurosci Lett 217:101–104. CrossRefPubMedGoogle Scholar
  46. Lucon-Xiccato T, Dadda M, Bisazza A (2016) Sex differences in discrimination of shoal size in the guppy (Poecilia reticulata). Ethology 122:481–491. CrossRefGoogle Scholar
  47. Macey MJ, Pickford GE, Peter RE (1974) Forebrain localization of the spawning reflex response to exogenous neurohypophysial hormones in the killifish, Fundulus heteroclitus. J Exp Zool 190:269–279. CrossRefPubMedGoogle Scholar
  48. Maeda H, Mogenson GJ (1981) Electrophysiological responses of neurons of the ventral tegmental area to electrical stimulation of amygdala and lateral septum. Neuroscience 6:367–376. CrossRefPubMedGoogle Scholar
  49. Magurran AE (1998) Population differentiation without speciation. Philos Trans R Soc B 353:275–286. CrossRefGoogle Scholar
  50. Magurran AE (2005) Evolutionary ecology: the Trinidadian guppy. Oxford University Press, OxfordCrossRefGoogle Scholar
  51. Magurran AE, Seghers BH, Carvalho GR, Shaw PW (1992) Behavioural consequences of an artificial introduction of guppies (Poecilia reticulata) in N. Trinidad : evidence for the evolution of anti-predator behaviour in the wild. Proc R Soc Lond B 248:117–122CrossRefGoogle Scholar
  52. Malsbury CW (1971) Facilitation of male rat copulatory behavior by electrical stimulation of the medial preoptic area. Physiol Behav 7:797–805. CrossRefPubMedGoogle Scholar
  53. Maney DL, Ball GF (2003) Fos-like immunoreactivity in catecholaminergic brain nuclei after territorial behavior in free-living song sparrows. J Neurobiol 56:163–170. CrossRefPubMedGoogle Scholar
  54. Mariette MM, Zajitschek SRK, Garcia CM, Brooks RC (2010) The effects of familiarity and group size on mating preferences in the guppy, Poecilia reticulata. J Evol Biol 23:1772–1782. CrossRefPubMedGoogle Scholar
  55. Meibach RC, Siegel A (1977) Efferent connections of the septal area in the rat: an analysis utilizing retrograde and anterograde transport methods. Brain Res 119:1–20. CrossRefPubMedGoogle Scholar
  56. Munchrath LA, Hofmann HA (2010) Distribution of sex steroid hormone receptors in the brain of an african cichlid fish, Astatotilapia burtoni. J Comp Neurol 518:3302–3326. CrossRefPubMedGoogle Scholar
  57. Northcutt RG (2008) Forebrain evolution in bony fishes. Brain Res Bull 75:191–205. CrossRefPubMedGoogle Scholar
  58. Nuffer R, Alburn SM (2010) The significance of male display during male-male interactions in guppies (Poecilia reticulata). Honors Thesis, Cal Poly State University, San Luis Obispo, CAGoogle Scholar
  59. O’Connell LA, Hofmann HA (2011a) Genes, hormones, and circuits: an integrative approach to study the evolution of social behavior. Front Neuroendocrinol 32:320–335. CrossRefPubMedGoogle Scholar
  60. O’Connell LA, Hofmann HA (2011b) The vertebrate mesolimbic reward system and social behavior network: a comparative synthesis. J Comp Neurol 519:3599–3639. CrossRefPubMedGoogle Scholar
  61. O’Connell LA, Matthews BJ, Hofmann HA (2012) Isotocin regulates paternal care in a monogamous cichlid fish. Horm Behav 61:725–733. CrossRefPubMedGoogle Scholar
  62. Portfors CV (2007) Types and functions of ultrasonic vocalizations in laboratory rats and mice. J Am Assoc Lab Anim Sci 46:28–34PubMedGoogle Scholar
  63. Price AC, Rodd FH (2006) The effect of social environment on male–male competition in guppies (Poecilia reticulata). Ethology 112:22–32. CrossRefGoogle Scholar
  64. Ramallo MR, Grober M, Canepa MM, Morandini L, Pandolfi M (2012) Arginine-vasotocin expression and participation in reproduction and social behavior in males of the cichlid fish Cichlasoma dimerus. Gen Comp Endocrinol 179:221–231. CrossRefPubMedGoogle Scholar
  65. Ramirez MJ, Salas C, Portavella M (1988) Offense and defense after lateral septal lesions in Columba Livia. Int J Neurosci 41:241–250. CrossRefPubMedGoogle Scholar
  66. Rink E, Wullimann MF (2001) The teleostean (zebrafish) dopaminergic system ascending to the subpallium (striatum) is located in the basal diencephalon (posterior tuberculum). Brain Res 889:316–330. CrossRefPubMedGoogle Scholar
  67. Rink E, Wullimann MF (2004) Connections of the ventral telencephalon (subpallium) in the zebrafish (Danio rerio). Brain Res 1011:206–220. CrossRefPubMedGoogle Scholar
  68. Riters LV (2012) The role of motivation and reward neural systems in vocal communication in songbirds. Front Neuroendocrinol 33:194–209. CrossRefPubMedPubMedCentralGoogle Scholar
  69. Riters L, Ball G (1999) Lesions to the medial preoptic area affect singing in the male European starling (Sturnus vulgaris). Horm Behav 36:276–286. CrossRefPubMedGoogle Scholar
  70. Satou M, Oka Y, Kusunoki M, Matsushima T, Kato M, Rujita I, Ueda K (1984) Telencephalic and preoptic areas integrate sexual behavior in hime salmon (landlocked red salmon, Oncorhynchus nerka): results of electrical brain stimulation experiments. Physiol Behav 33:441–447. CrossRefPubMedGoogle Scholar
  71. Schindelin J, Arganda-Carreras I, Frise E et al (2012) Fiji: an open-source platform for biological-image analysis. Nat Methods 9:676–682. CrossRefPubMedGoogle Scholar
  72. Semsar K, Kandel FLM, Godwin J (2001) Manipulations of the AVT system shift social status and related courtship and aggressive behavior in the bluehead wrasse. Horm Behav 40:21–31. CrossRefPubMedGoogle Scholar
  73. Slimp JC, Hart BL, Goy RW (1978) Heterosexual, autosexual and social behavior of adult male rhesus monkeys with medial preoptic-anterior hypothalamic lesions. Brain Res 142:105–122. CrossRefPubMedGoogle Scholar
  74. Staiger J, Nürnberger F (1989) Pattern of afferents to the lateral septum in the guinea pig. Cell Tissue Res 257:471–490CrossRefPubMedGoogle Scholar
  75. Swanson L, Cowan W (1979) The connections of the septal region in the rat. J Comp Neurol 186:621–656. CrossRefPubMedGoogle Scholar
  76. Teles MC, Almeida O, Lopes JS, Oliveira RF (2015) Social interactions elicit rapid shifts in functional connectivity in the social decision-making network of zebrafish. Proc R Soc B 282:20151099. CrossRefPubMedGoogle Scholar
  77. Vargas JP, López JC, Portavella M (2009) What are the functions of fish brain pallium? Brain Res Bull 79:436–440. CrossRefPubMedGoogle Scholar
  78. Velho TAF, Pinaud R, Rodrigues PV, Mello CV (2005) Co-induction of activity-dependent genes in songbirds. Eur J Neurosci 22:1667–1678. CrossRefPubMedGoogle Scholar
  79. Wang Z, Hulihan TJ, Insel TR (1997) Sexual and social experience is associated with different patterns of behavior and neural activation in male prairie voles. Brain Res 767:321–332. CrossRefPubMedGoogle Scholar
  80. Wells K (2007) The ecology and behavior of amphibians. University of Chicago Press, ChicagoCrossRefGoogle Scholar
  81. Wong CJH (2000) Electrical stimulation of the preoptic area in Eigenmannia: evoked interruptions in the electric organ discharge. J Comp Physiol A 186:81–93. CrossRefPubMedGoogle Scholar
  82. Wullimann MF, Rupp B, Reichert H (1996) Neuroanatomy of the zebrafish brain: a topological atlas. Birkhäuser Verlag, BaselCrossRefGoogle Scholar
  83. Yanagihara S, Hessler NA (2006) Modulation of singing-related activity in the songbird ventral tegmental area by social context. Eur J Neurosci 24:3619–3627. CrossRefPubMedGoogle Scholar

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© Springer-Verlag GmbH Germany, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Stanford UniversityStanfordUSA
  2. 2.University of MichiganAnn ArborUSA
  3. 3.Vanderbilt UniversityNashvilleUSA
  4. 4.Colorado State UniversityFort CollinsUSA

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