Cookies Policy

This site uses cookies. By continuing to browse the site you are agreeing to our use of cookies.

I accept this policy

Find out more here

Natural variation in brain gene expression profiles of aggressive and nonaggressive individual sticklebacks

No metrics data to plot.
The attempt to load metrics for this article has failed.
The attempt to plot a graph for these metrics has failed.
The full text of this article is not currently available.

Brill’s MyBook program is exclusively available on BrillOnline Books and Journals. Students and scholars affiliated with an institution that has purchased a Brill E-Book on the BrillOnline platform automatically have access to the MyBook option for the title(s) acquired by the Library. Brill MyBook is a print-on-demand paperback copy which is sold at a favorably uniform low price.

Access this article

+ Tax (if applicable)
Add to Favorites
You must be logged in to use this functionality

image of Behaviour

Within many species, some individuals are consistently more aggressive than others. We examine whether there are differences in brain gene expression between aggressive versus nonaggressive behavioural types of individuals within a natural population of male three-spined sticklebacks (Gasterosteus aculeatus). We compared gene expression profiles of aggressive male sticklebacks to nonaggressive males in four regions of the brain (brainstem, cerebellum, diencephalon and telencephalon). Relatively few genes were differentially expressed between behavioural types in telencephalon, cerebellum and diencephalon, but hundreds of genes were differentially expressed in brainstem, a brain area involved in detecting threats. Six genes that were differentially expressed in response to a territorial intrusion in a previous study were also differentially expressed between behavioural types in this study, implying primarily non-shared but some shared molecular mechanisms. Our findings offer new insights into the molecular causes and correlates of behavioural plasticity and individual variation in behaviour.

Affiliations: 1: aSchool of Integrative Biology, Program in Ecology, Evolution and Conservation, Program in Neuroscience, Carl R. Woese Institute for Genomic Biology, University of Illinois, Urbana Champaign, IL, USA ; 2: bIllinois Informatics Program, Carl R. Woese Institute for Genomic Biology, University of Illinois, Urbana Champaign, IL, USA ; 3: cGenomics Core, Lerner Research Institute, Cleveland Clinic Foundation, Cleveland, OH, USA

*Corresponding author’s e-mail address:
Loading data from figshare Loading data from figshare

Full text loading...


Data & Media loading...

1. Alaux C., Sinha S., Hasadsri L., Hunt G.J., Guzman-Novoa E., DeGrandi-Hoffman G., Uribe-Rubio J.L., Southey B.R., Rodriguez-Zas S., Robinson G.E. (2009). "Honey bee aggression supports a link between gene regulation and behavioral evolution". — Proc. Natl. Acad. Sci. USA Vol 106: 15400-15405.
2. Alexa A., Rahnenfuhrer J. (2010). topGO: topGO: enrichment analysis for gene ontology. R package version 2.22.0. — R Foundation for Statistical Computing Vienna.
3. Anholt R.R., Mackay T.F. (2012). "Genetics of aggression". — Annu. Rev. Genet. Vol 46: 145-164.
4. Arnold C., Taborsky B. (2010). "Social experience in early ontogeny has lasting effects on social skills in cooperatively breeding cichlids". — Anim. Behav. Vol 79: 621-630.
5. Aubin-Horth N., Deschenes M., Cloutier S. (2012). "Natural variation in the molecular stress network correlates with a behavioural syndrome". — Horm. Behav. Vol 61: 140-146.
6. Aubin-Horth N., Landry C.R., Letcher B.H., Hofmann H.A. (2005). "Alternative life histories shape brain gene expression profiles in males of the same population". — Proc. Roy. Soc. Lond. B: Biol. Sci. Vol 272: 1655-1662.
7. Aubin-Horth N., Renn S.C. (2009). "Genomic reaction norms: using integrative biology to understand molecular mechanisms of phenotypic plasticity". — Mol. Ecol. Vol 18: 3763-3780.
8. Bakker T.C.M. (1986). "Aggressiveness in sticklebacks (Gasterosteus aculeatus L.): a behaviour-genetic study". — Behaviour Vol 98: 1-144.
9. Bell A.M., Backstrom T., Huntingford F.A., Pottinger T.G., Winberg S. (2007). "Variable neuroendocrine responses to ecologically-relevant challenges in sticklebacks". — Physiol. Behav. Vol 91: 15-25.
10. Bell A.M., Robinson G.E. (2011). "Behavior and the dynamic genome". — Science Vol 332: 1161-1162.
11. Bentz A.B., Navara K.J., Siefferman L. (2013). "Phenotypic plasticity in response to breeding density in tree swallows: an adaptive maternal effect?" — Horm. Behav. Vol 64: 729-736.
12. Binder E.B., Bradley R.G., Liu W., Epstein M.P., Deveau T.C., Mercer K.B., Tang Y., Gillespie C.F., Heim C.M., Nemeroff C.B., Schwartz A.C., Cubells J.F., Ressler K.J. (2008). "Association of FKBP5 polymorphisms and childhood abuse with risk of posttraumatic stress disorder symptoms in adults". — J. Am. Med. Ass. Vol 299: 1291-1305.
13. Buitenhuis A.J., Kjaer J.B. (2008). "Long term selection for reduced or increased pecking behaviour in laying hens". — World Poultry Sci. J. Vol 64: 477-487.
14. Cardoso S.D., Teles M.C., Oliveira R.F. (2015). "Neurogenomic mechanisms of social plasticity". — J. Exp. Biol. Vol 218: 140-149.
15. Chandrasekaran S., Rittschof C.C., Djukovic D., Gu H., Raftery D., Price N.D., Robinson G.E. (2015). "Aggression is associated with aerobic glycolysis in the honey bee brain". — Genes Brain Behav. Vol 14: 158-166.
16. Curno O., Behnke J.M., McElligott A.G., Reader T., Barnard C. (2009). "Mothers produce less aggressive sons with altered immunity when there is a threat of disease during pregnancy". — Proc. Roy. Soc. Lond. B: Biol. Sci. Vol 276: 1047-1054.
17. Dierick H.A., Greenspan R.J. (2006). "Molecular analysis of flies selected for aggressive behavior". — Nature Genet. Vol 38: 1023-1031.
18. Edenbrow M., Croft D.P. (2013). "Environmental and genetic effects shape the development of personality traits in the mangrove killifish Kryptolebias marmoratus". — Oikos Vol 122: 667-681.
19. Edwards A.C., Ayroles J.F., Stone E.A., Carbone M.A., Lyman R.F., Mackay T.F. (2009). "A transcriptional network associated with natural variation in Drosophila aggressive behavior". — Genome Biol. Vol 10: R76.
20. Edwards A.C., Rollmann S.M., Morgan T.J., Mackay T.F. (2006). "Quantitative genomics of aggressive behavior in Drosophila melanogaster". — PLoS Genet. Vol 2: e154.
21. Feldker D.E., Datson N.A., Veenema A.H., Proutski V., Lathouwers D., De Kloet E.R., Vreugdenhil E. (2003). "GeneChip analysis of hippocampal gene expression profiles of short- and long-attack-latency mice: technical and biological implications". — J. Neurosci. Res. Vol 74: 701-716.
22. Filby A.L., Paull G.C., Hickmore T.F., Tyler C.R. (2010). "Unravelling the neurophysiological basis of aggression in a fish model". — BMC Genom. Vol 11: 498.
23. Fraser B.A., Janowitz I., Thairu M., Travis J., Hughes K.A. (2014). "Phenotypic and genomic plasticity of alternative male reproductive tactics in sailfin mollies". — Proc. Roy. Soc. Lond. B: Biol. Sci. Vol 281: 20132310.
24. Giancola P.R. (1995). "Evidence for dorsolateral and orbital prefrontal cortical involvement in the expression of aggressive behavior". — Aggr. Behav. Vol 21: 431-450.<431::AID-AB2480210604>3.0.CO;2-Q
25. Godwin J., Thompson R. (2012). "Nonapeptides and social behavior in fishes". — Horm. Behav. Vol 61: 230-238.
26. Goodson J.L., Adkins-Regan E. (1999). "Effect of intraseptal vasotocin and vasoactive intestinal polypeptide infusions on courtship song and aggression in the male zebra finch (Taeniopygia guttata)". — J. Neuroendocrinol. Vol 11: 19-25.
27. Goodson J.L., Kelly A.M., Kingsbury M.A., Thompson R.R. (2012). "An aggression-specific cell type in the anterior hypothalamus of finches". — Proc. Natl. Acad. Sci. USA Vol 109: 13847-13852.
28. Harris J.A. (1996). "Descending antinociceptive mechanisms in the brainstem: their role in the animal’s defensive system". — J. Physiol. Vol 90: 15-25.
29. Heyne H.O., Lautenschlager S., Nelson R., Besnier F., Rotival M., Cagan A., Kozhemyakina R., Plyusnina I.Z., Trut L., Carlborg O., Petretto E., Kruglyak L., Paabo S., Schoneberg T., Albert F.W. (2014). "Genetic influences on brain gene expression in rats selected for tameness and aggression". — Genetics Vol 198: 1277-1290.
30. Huffman L.S., Hinz F.I., Wojcik S., Aubin-Horth N., Hofmann H.A. (2015). "Arginine vasotocin regulates social ascent in the African cichlid fish, Astatotilapia burtoni". — Gen. Comp. Endocrinol. Vol 212: 106-213.
31. Huntingford F.A., Turner A.K., Downie L.M. (1987). Animal conflict. — Chapman & Hall/CRC, Boca Raton, FL.
32. Kanarik M., Alttoa A., Matrov D., Koiv K., Sharp T., Panksepp J., Harro J. (2011). "Brain responses to chronic social defeat stress: effects on regional oxidative metabolism as a function of a hedonic trait, and gene expression in susceptible and resilient rats". — Eur. Neuropsychopharmacol. Vol 21: 92-107.
33. Klengel T., Mehta D., Anacker C., Rex-Haffner M., Pruessner J.C., Pariante C.M., Pace T.W.W., Mercer K.B., Mayberg H.S., Bradley B., Nemeroff C.B., Holsboer F., Heim C.M., Ressler K.J., Rein T., Binder E.B. (2013). "Allele-specific FKBP5 DNA demethylation mediates gene-childhood trauma interactions". — Nature Neurosci. Vol 16: 33-41.
34. Kleszczynska A., Sokolowska E., Kulczykowska E. (2012). "Variation in brain arginine vasotocin (AVT) and isotocin (IT) levels with reproductive stage and social status in males of three-spined stickleback (Gasterosteus aculeatus)". — Gen. Comp. Endocrinol. Vol 175: 290-296.
35. Kroes R.A., Panksepp J., Burgdorf J., Otto N.J., Moskal J.R. (2006). "Modeling depression: social dominance-submission gene expression patterns in rat neocortex". — Neuroscience Vol 137: 37-49.
36. Kukekova A.V., Johnson J.L., Teiling C., Li L., Oskina I.N., Kharlamova A.V., Gulevich R.G., Padte R., Dubreuil M.M., Vladimirova A.V., Shepeleva D.V., Shikhevich S.G., Sun Q., Ponnala L., Temnykh S.V., Trut L.N., Acland G.M. (2011). "Sequence comparison of prefrontal cortical brain transcriptome from a tame and an aggressive silver fox (Vulpes vulpes)". — BMC Genom. Vol 12: 482.
37. Lema S.C., Sanders K.E., Walti K.A. (2015). "Arginine vasotocin, isotocin and nonapeptide receptor gene expression link to social status and aggression in sex-dependent patterns". — J. Neuroendocrinol. Vol 27: 142-157.
38. Liddell B.J., Brown K.J., Kemp A.H., Barton M.J., Das P., Peduto A., Gordon E., Williams L.M. (2005). "A direct brainstem-amygdala-cortical ‘alarm’ system for subliminal signals of fear". — NeuroImage Vol 24: 235-243.
39. Lin D., Boyle M.P., Dollar P., Lee H., Lein E.S., Perona P., Anderson D.J. (2011). "Functional identification of an aggression locus in the mouse hypothalamus". — Nature Vol 470: 221-226.
40. Miczek K.A., de Almeida R.M., Kravitz E.A., Rissman E.F., de Boer S.F., Raine A. (2007). "Neurobiology of escalated aggression and violence". — J. Neurosci. Vol 27: 11803-11806.
41. Misslin R. (2003). "The defense system of fear: behavior and neurocircuitry". — Clin. Neurophysiol. Vol 33: 55-66.
42. Muhie S., Gautam A., Meyerhoff J., Chakraborty N., Hammamieh R., Jett M. (2015). "Brain transcriptome profiles in mouse model simulating features of post-traumatic stress disorder". — Mol. Brain Vol 8: 14.
43. Mukai M., Replogle K., Drnevich J., Wang G., Wacker D., Band M., Clayton D.F., Wingfield J.C. (2009). "Seasonal differences of gene expression profiles in song sparrow (Melospiza melodia) hypothalamus in relation to territorial aggression". — PLoS ONE Vol 4: e8182.
44. Oldfield R.G., Harris R.M., Hofmann H.A. (2015). "Integrating resource defence theory with a neural nonapeptide pathway to explain territory-based mating systems". — Front. Zool. Vol 12: S16.
45. Oldfield R.G., Hofmann H.A. (2011). "Neuropeptide regulation of social behavior in a monogamous cichlid fish". — Physiol. Behav. Vol 102: 296-303.
46. Oliveira R.F., Simões J.M., Teles M.C., Oliveira C.R., Becker J.D., Lopes J.S. (2016). "Assessment of fight outcome is needed to activate socially driven transcriptional changes in the zebrafish brain". — Proc. Natl. Acad. Sci. USA Vol 113: E654-E661.
47. Provencal N., Booij L., Tremblay R.E. (2015). "The developmental origins of chronic physical aggression: biological pathways triggered by early life adversity". — J. Exp. Biol. Vol 218: 123-133.
48. Reale D., Reader S.M., Sol D., McDougall P.T., Dingemanse N.J. (2007). "Integrating animal temperament within ecology and evolution". — Biol. Rev. Vol 82: 291-318.
49. Redmond D.E. Jr., Huang Y.H. (1979). "Current concepts. II. New evidence for a locus coeruleus-norepinephrine connection with anxiety". — Life Sci. Vol 25: 2149-2162.
50. Renn S.C., Aubin-Horth N., Hofmann H.A. (2008). "Fish and chips: functional genomics of social plasticity in an African cichlid fish". — J. Exp. Biol. Vol 211: 3041-3056.
51. Rittschof C.C., Bukhari S.A., Sloofman L.G., Troy J.M., Caetano-Anolle D., Cash-Ahmed A., Kent M., Lu X.C., Sanogo Y.O., Weisner P.A., Zhang H.M., Bell A.M., Ma J., Sinha S., Robinson G.E., Stubbs L. (2014). "Neuromolecular responses to social challenge: common mechanisms across mouse, stickleback fish, and honey bee". — Proc. Natl. Acad. Sci. USA Vol 111: 17929-17934.
52. Sanogo Y.O., Band M., Blatti C., Sinha S., Bell A.M. (2012). "Transcriptional regulation of brain gene expression in response to a territorial intrusion". — Proc. Roy. Soc. Lond. B: Biol. Sci. Vol 279: 4929-4938.
53. Sanogo Y.O., Hankison S., Band M., Obregon A., Bell A.M. (2011). "Brain transcriptomic response of threespine sticklebacks to cues of a predator". — Brain Behav. Evol. Vol 77: 270-285.
54. Santangelo N., Bass A.H. (2010). "Individual behavioral and neuronal phenotypes for arginine vasotocin mediated courtship and aggression in a territorial teleost". — Brain Behav. Evol. Vol 75: 282-291.
55. Schumer M., Krishnakant K., Renn S.C. (2011). "Comparative gene expression profiles for highly similar aggressive phenotypes in male and female cichlid fishes (Julidochromis)". — J. Exp. Biol. Vol 214: 3269-3278.
56. Schunter C., Vollmer S.V., Macpherson E., Pascual M. (2014). "Transcriptome analyses and differential gene expression in a non-model fish species with alternative mating tactics". — BMC Genet. Vol 15: 167.
57. Shorter J., Couch C., Huang W., Carbone M.A., Peiffer J., Anholt R.R.H., Mackay T.F.C. (2015). "Genetic architecture of natural variation in Drosophila melanogaster aggressive behavior". — Proc. Natl. Acad. Sci. USA Vol 112: E3555-E3563.
58. Sluyter F., Bult A., Lynch C.B., Van Oortmerssen G.A., Koolhaas J.M. (1995). "A comparison between house mouse lines selected for attack latency or nest-building: evidence for a genetic basis of alternative behavioral strategies". — Behav. Genet. Vol 25: 247-252.
59. Smyth G.K. (2005). "Limma: linear models for microarray data". — In: Bioinformatics and computational biology solutions using R and bioconductor. Springer, New York, NY, p.  397-420.
60. Smyth G.K., Altman N.S. (2013). "Separate-channel analysis of two-channel microarrays: recovering inter-spot information". — BMC Bioinformat. Vol 14: 165.
61. Sneddon L., Schmidt R., Fang Y., Cossins A. (2011). "Molecular correlates of social dominance: a novel role for ependymin in aggression". — PLoS ONE Vol 6: e18181.
62. Stiver K.A., Harris R.M., Townsend J.P., Hofmann H.A., Alonzo S.H. (2015). "Neural gene expression profiles and androgen levels underlie alternative reproductive tactics in the ocellated wrasse, Symphodus ocellatus". — Ethology Vol 121: 152-167.
63. Supek F., Bošnjak M., Škunca N., Šmuc T. (2011). "REVIGO summarizes and visualizes long lists of gene ontology terms". — PLoS One Vol 6: e21800.
64. Takahashi A., Quadros I.M., de Almeida R.M., Miczek K.A. (2012). "Behavioral and pharmacogenetics of aggressive behavior". — Curr. Top. Behav. Neurosci. Vol 12: 73-138.
65. Tinbergen N. (1972). The animal in its world explorations of an ethologist. — Harvard University Press, Cambridge, MA.
66. Untergasser G., Martowicz A., Hermann M., Tochterle S., Meyer D. (2011). "Distinct expression patterns of Dickkopf genes during late embryonic development of Danio rerio". — Gene Expr. Patterns Vol 11: 491-500.
67. Wang L.M., Dankert H., Perona P., Anderson D.J. (2008). "A common genetic target for environmental and heritable influences on aggressiveness in Drosophila". — Proc. Natl. Acad. Sci. USA Vol 105: 5657-5663.
68. West-Eberhard M.J. (2003). Developmental plasticity and evolution. — Oxford University Press, Oxford.
69. Wootton R.J. (1984). A functional biology of sticklebacks. — University of California Press, Berkeley, CA.
70. Yokoi S., Okuyama T., Kamei Y., Naruse K., Taniguchi Y., Ansai S., Kinoshita M., Young L.J., Takemori N., Kubo T., Takeuchi H. (2015). "An essential role of the arginine vasotocin system in mate-guarding behaviors in triadic relationships of medaka fish (Oryzias latipes)". — PLoS Genet. Vol 11: e1005009.
71. Zannas A.S., Binder E.B. (2014). "Gene-environment interactions at the FKBP5 locus: sensitive periods, mechanisms and pleiotropism". — Genes Brain Behav. Vol 13: 25-37.
72. Zayed A., Robinson G.E. (2012). "Understanding the relationship between brain gene expression and social behavior: lessons from the honey bee". — Annu. Rev. Genet. Vol 46: 591-615.

Article metrics loading...



Can't access your account?
  • Tools

  • Add to Favorites
  • Printable version
  • Email this page
  • Subscribe to ToC alert
  • Get permissions
  • Recommend to your library

    You must fill out fields marked with: *

    Librarian details
    Your details
    Why are you recommending this title?
    Select reason:
    Behaviour — Recommend this title to your library
  • Export citations
  • Key

  • Full access
  • Open Access
  • Partial/No accessInformation