Differences in neural activity, but not behavior, across social contexts in guppies, Poecilia reticulata
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.
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.
KeywordsSocial 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.
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.
- 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. https://doi.org/10.1037/0735-7044.120.6.1326 CrossRefPubMedPubMedCentralGoogle Scholar
- 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. https://doi.org/10.1111/j.1460-9568.2009.06637.x CrossRefPubMedPubMedCentralGoogle Scholar
- Anken R, Rahmann H (1994) Brain atlas of the adult swordtail fish Xiphophorus helleri and of certain developmental stages. Fischer, StuttgartGoogle Scholar
- Bharati IS, Goodson JL (2006) Fos responses of dopamine neurons to sociosexual stimuli in male zebra finches. Neuroscience 143:661–670. https://doi.org/10.1016/j.neuroscience.2006.08.046 CrossRefPubMedPubMedCentralGoogle Scholar
- Davies NB, Krebs JR, West S (2012) An introduction to behavioural ecology, 4th edn. Wiley-Blackwell, OxfordGoogle Scholar
- 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. https://doi.org/10.1017/CBO9781107415324.004 CrossRefGoogle Scholar
- Houde AE (1997) Sex, color, and mate choice in guppies. Princeton University Press, PrincetonGoogle Scholar
- 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
- Northcutt RG (2008) Forebrain evolution in bony fishes. Brain Res Bull 75:191–205. https://doi.org/10.1016/j.brainresbull.2007.10.058 CrossRefPubMedGoogle Scholar
- 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
- 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. https://doi.org/10.1016/j.ygcen.2012.08.015 CrossRefPubMedGoogle Scholar
- 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. https://doi.org/10.1016/0031-9384(84)90167-7 CrossRefPubMedGoogle Scholar
- Vargas JP, López JC, Portavella M (2009) What are the functions of fish brain pallium? Brain Res Bull 79:436–440. https://doi.org/10.1016/j.brainresbull.2009.05.008 CrossRefPubMedGoogle Scholar