Isotocin and sociality in the cooperatively breeding cichlid fish, Neolamprologus pulcher

in Behaviour
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The ultimate functions of sociality, or the tendency to associate with conspecifics and to live within a social group, are increasingly well understood. However, the proximate mechanisms that mediate this behaviour have received less attention. The oxytocin family of nonapeptide hormones (including isotocin in teleost fish) is thought to play an important role in regulating social behaviour across a wide range of taxa and social contexts. In the current study, we investigated the influence of exogenous administration of isotocin and an oxytocin receptor antagonist on sociality in a cooperatively breeding fish, Neolamprologus pulcher. In our first experiment, we found that a high (and a low) dose of peripherally administered exogenous isotocin decreased the time spent associating with conspecifics in N. pulcher, while an intermediate dose had no effect relative to control. In our second experiment, we found that a peripheral administration of an oxytocin receptor antagonist increased grouping preference in male N. pulcher. The results of both experiments suggest that IT may inhibit grouping behaviour in this species. These results contribute to a growing body of literature suggesting that the broad generalization that the oxytocin family of nonapeptides facilitate grouping behaviour is overly simplistic, and that specific behavioural effects depend the study species and testing conditions.

Isotocin and sociality in the cooperatively breeding cichlid fish, Neolamprologus pulcher

in Behaviour

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References

AgrilloC.DaddaM.BisazzaA. (2007). Quantity discrimination in female mosquitofish. — Anim. Cogn. 10: 63-70.

AlexanderR.D. (1974). The evolution of social behaviour. — Annu. Rev. Ecol. Syst. 5: 325-383.

BalshineS.LeachB.NeatF.ReidH.TaborskyM.WernerN. (2001). Correlates of group size in a cooperatively breeding cichlid fish (Neolamprologus pulcher). — Behav. Ecol. Sociobiol. 50: 134-140.

Balshine-EarnS.NeatF.C.ReidH.TaborskyM. (1998). Paying to stay or paying to breed? Field evidence for direct benefits of helping behaviour in a cooperatively breeding fish. — Behav. Ecol. 9: 432-438.

BernsteinJ.J.StreicherE. (1965). The blood-brain barrier of fish. — Exper. Neurol. 11: 464-473.

BraidaD.DonzelliA.MartucciR.CapurroV.BusnelliM.ChiniB.SalaM. (2012). Neurohypophyseal hormones manipulation modulate social and anxiety-related behaviour in zebrafish. — Psychopharmacology 220: 319-330.

ChurchlandP.S.WinkielmanP. (2012). Modulating social behaviour with oxytocin: how does it work? What does it mean?Horm. Behav. 61: 392-399.

CoteJ.FogartyS.WeinersmithK.BrodinT.SihA. (2010). Personality traits and dispersal tendency in the invasive mosquitofish (Gambusia affinis). — Proc. Roy. Soc. Lond. B: Biol. Sci. 277: 1571-1579.

DaddaM.PifferL.AgrilloC.BisazzaA. (2009). Spontaneous number representation in mosquitofish. — Cognition 112: 343-348.

DeyC.J.ReddonA.R.O’ConnorC.M.BalshineS. (2013). Network structure is related to social conflict in a cooperatively breeding fish. — Anim. Behav. 85: 395-402.

DonaldsonZ.R.YoungL.J. (2008). Oxytocin, vasopressin, and the neurogenetics of sociality. — Science 322: 900-904.

DugatkinL.A.SihA. (1995). Essay on contemporary issues in ethology: behavioural ecology and the study of partner choice. — Ethology 99: 265-277.

EarleyR.L.DugatkinL.A. (2010). Behaviour in groups. — In: Evolutionary behavioural ecology ( WestneatD.F.FoxC.W. eds). Oxford University PressOxford p.  285-307.

FilbyA.L.PaullG.C.HickmoreT.F.A.TylerC.R. (2010). Unravelling the neurophysiological basis of aggression in a fish model. — BMC Genomics 11: 498.

GodwinJ.ThompsonR. (2012). Nonapeptides and social behaviour in fishes. — Horm. Behav. 61: 230-238.

GoodsonJ.L. (2005). The vertebrate social behaviour network: evolutionary themes and variations. — Horm. Behav. 48: 11-22.

GoodsonJ.L. (2008). Nonapeptides and the evolutionary patterning of sociality. — Prog. Brain Res. 170: 3-15.

GoodsonJ.L. (2013). Deconstructing sociality, social evolution and relevant nonapeptide functions. — Psychoneuroendocrinology 38: 465-478.

GoodsonJ.L.BassA. (2000). Forebrain peptides modulate sexually polymorphic vocal circuitry. — Nature 403: 769-772.

GoodsonJ.L.KingsburyM.A. (2011). Nonapeptides and the evolution of social group sizes in birds. — Front. Neuroanat. 5: 13.

GoodsonJ.L.KingsburyM.A. (2013). What’s in a name? Homology-based nomenclature for vertebrate social behavior networks and the vertebrate nonapeptides. — Horm. Behav. 64: 103-112.

GoodsonJ.L.ThompsonR.R. (2010). Nonapeptide mechanisms of social cognition, behaviour and species-specific social systems. — Curr. Opin. Neurobiol. 20: 784-794.

GoodsonJ.L.SchrockS.E.KlattJ.D.KabelikD.KingsburyM.A. (2009). Mesotocin and nonapeptide receptors promote Estrildid flocking behaviour. — Science 325: 862-866.

GoodsonJ.L.KellyA.M.KingsburyM.A. (2012). Evolving nonapeptide mechanisms of gregariousness and social diversity in birds. — Horm. Behav. 61: 239-250.

HamiltonW.D. (1971). Geometry for the selfish herd. — J. Theor. Biol. 31: 295-311.

HegD.BrouwerL.BacharZ.TaborskyM. (2005). Large group size yields group stability in the cooperatively breeding cichlid Neolamprologus pulcher. — Behaviour 142: 1615-1641.

HoyleC.H. (1999). Neuropeptide families and their receptors: evolutionary perspectives. — Brain Res. 848: 1-25.

InselT.R.YoungL.J. (2001). The neurobiology of attachment. — Nature Rev. Neurosci. 2: 129-136.

JordanL.A.WongM.Y.L.BalshineS. (2010). The effects of familiarity and social hierarchy on group membership decisions in a social fish. — Biol. Lett. 6: 301-303.

KellyA.M.KingsburyM.A.HoffbuhrK.SchrockS.E.WaxmanB.KabelikD.ThompsonR.R.GoodsonJ.L. (2011). Vasotocin neurons and septal V1a-like receptors potently modulate songbird flocking and responses to novelty. — Horm. Behav. 60: 12-21.

KlattJ.D.GoodsonJ.L. (2012). Oxytocin-like receptors mediate pair bonding in a socially monogamous songbird. — Proc. Roy. Soc. Lond. B: Biol. Sci. 280: 20122396.

KoningsA. (1998). Tanganyika cichlids in their natural habitat. — Cichlid PressEl Paso, TX.

KrauseJ.RuxtonG.D. (2002). Living in groups. — Oxford University PressNew York, NY.

KrauseJ.RuxtonG.D. (2010). Important topics in group living. — In: Social behaviour: genes ecology and evolution ( SzekelyT.MooreA.J.KomdeurJ. eds). Cambridge University PressCambridge p.  203-225.

Le VinA.L.MableB.K.ArnoldK.E. (2010). Kin recognition via phenotype matching in a cooperatively breeding cichlid, Neolamprologus pulcher. — Anim. Behav. 79: 1109-1114.

LeeH.-J.MacbethA.H.PaganiJ.YoungW.S.3rd (2009). Oxytocin: the great facilitator of life. — Prog. Neurobiol. 88: 127-151.

LemaS.C.NevittG.A. (2004). Exogenous vasotocin alters aggression during agonistic exchanges in male Amargosa River pupfish (Cyprinodon nevadensis amargosae). — Horm. Behav. 46: 628-637.

LindeijerC.M. (2012). A neurobehavioural analysis of social behaviour and learning in fish and mammals. — PhD thesis Utrecht University Utrecht.

LiuJ.C.J.GuastellaA.J.DaddsM.R. (2012). Effects of oxytocin on human social approach measured using intimacy equilibriums. — Horm. Behav. 62: 585-591.

LiuY.WangZ.X. (2003). Nucleus accumbens oxytocin and dopamine interact to regulate pair bond formation in female prairie voles. — Neuroscience 121: 537-544.

LiuY.CurtisJ.T.WangZ. (2001). Vasopressin in the lateral septum regulates pair bond formation in male prairie voles (Microtus ochrogaster). — Behav. Neurosci. 115: 910-919.

LukasM.TothI.ReberS.O.SlatteryD.A.VeenemaA.H.NeumannI.D. (2011). The neuropeptide oxytocin facilitates pro-social behaviour and prevents social avoidance in rats and mice. — Neuropsychopharmacology 36: 2159-2168.

MacDonaldK.MacDonaldT.M. (2010). The peptide that binds: a systematic review of oxytocin and its prosocial effects in humans. — Harvard Rev. Psychiatr. 18: 1-21.

MaddenJ.R.Clutton-BrockT.H. (2011). Experimental peripheral administration of oxytocin elevates a suite of cooperative behaviours in a wild social mammal. — Proc. Roy. Soc. Lond. B: Biol. Sci. 278: 1189-1194.

MennigenJ.A.MartyniukC.J.CrumpK.XiongH.ZhaoE.PopeskuJ.AnismanH.CossinsA.R.XiaX.TrudeauV.L. (2008). Effects of fluoxetine on the reproductive axis of female goldfish (Carassius auratus). — Phys. Genom. 35: 273-282.

NorrisD.O. (2007). Vertebrate endocrinology4th edn.Elsevier Academic PressBurlington, MA.

O’ConnellL.A.HofmannH.A. (2012). Evolution of a vertebrate social decision-making network. — Science 336: 1154-1157.

O’ConnellL.A.MatthewsB.J.HofmannH.A. (2012). Isotocin regulates paternal care in a monogamous cichlid fish. — Horm. Behav. 61: 725-733.

OldfieldR.G.HofmannH.A. (2011). Neuropeptide regulation of social behaviour in a monogamous cichlid fish. — Phys. Behav. 102: 296-303.

OlsonR.D.KastinA.J.Montalbano-SmithD.OlsonG.A.CoyD.H.MichellG.F. (1978). Neuropeptides and the blood-brain barrier in goldfish. — Pharmacol. Biochem. Behav. 9: 521-524.

PedersenA.TomaszyckiM.L. (2012). Oxytocin antagonist treatments alter the formation of pair relationships in zebra finches of both sexes. — Horm. Behav. 62: 113-119.

PropperC.R.DixonT.B. (1997). Differential effects of arginine vasotocin and gonadotropin-releasing hormone on sexual behaviours in an anuran amphibian. — Horm. Behav. 32: 99-104.

ReddonA.R.O’ConnorC.M.Marsh-RolloS.E.BalshineS. (2012). Effects of isotocin on social responses in a cooperatively breeding fish. — Anim. Behav. 84: 753-760.

ReddonA.R.BalkD.BalshineS. (2011a). Sex differences in group-joining decisions in social fish. — Anim. Behav. 82: 229-234.

ReddonA.R.VoisinM.R.MenonN.Marsh-RolloS.E.WongM.Y.L.BalshineS. (2011b). Rules of engagement for resource contests in a social fish. — Anim. Behav. 82: 93-99.

RingR.H. (2011). A complicated picture of oxytocin action in the central nervous system revealed. — Biol. Psychol. 69: 818-819.

RingR.H.MalbergJ.E.PotestioL.PingJ.BoikessS.LuoB.SchechterL.E.RizzoS.RahmanZ.Rosenzweig-LipsonS. (2006). Anxiolytic-like activity of oxytocin in male mice: behavioural and autonomic evidence, therapeutic implications. — Psychopharmacology 185: 218-225.

RossH.E.ColeC.D.SmithY.NeumannI.D.LandgrafR.MurphyA.Z.YoungL.J. (2009a). Characterization of the oxytocin system regulating affiliative behaviour in female prairie voles. — Neuroscience 162: 892-903.

RossH.E.FreemanS.M.SpiegelL.L.RenX.TerwilligerE.F.YoungL.J. (2009b). Variation in oxytocin receptor density in the nucleus accumbens has differential effects on affiliative behaviours in monogamous and polygamous voles. — J. Neurosci. 29: 1312-1318.

RossH.E.YoungL.J. (2009). Oxytocin and the neural mechanisms regulating social cognition and affiliative behaviour. — Front. Neuroendocrinology 30: 534-547.

SantangeloN.BassA.H. (2006). New insights into neuropeptide modulation of aggression: field studies of arginine vasotocin in a territorial tropical damselfish. — Proc. Roy. Soc. Lond. B: Biol. Sci. 273: 3085-3092.

SemsarK.KandelF.L.M.GodwinJ. (2001). Manipulations of the AVT system shift social status and related courtship and aggressive behaviour in the bluehead wrasse. — Horm. Behav. 40: 21-31.

SmithA.S.ÅgmoA.BirnieA.K.FrenchJ.A. (2010). Manipulation of the oxytocin system alters social behaviour and attraction in pair-bonding primates, Callithrix penicillata. — Horm. Behav. 57: 255-262.

SoaresM.C.BsharyR.FusaniL.GoymannW.HauM.HirschenhauserK.OliveiraR.F. (2010). Hormonal mechanisms of cooperative behaviour. — Philos Trans. Roy. Soc. B 365: 2737-2750.

SopinkaN.M.FitzpatrickJ.L.DesjardinsJ.K.StiverK.A.Marsh-RolloS.E.BalshineS. (2009). Liver size reveals social status in the African cichlid Neolamprologus pulcher. — J. Fish Biol. 75: 1-16.

StiverK.A.DierkesP.TaborskyM.GibbsH.L.BalshineS. (2005). Relatedness and helping in fish: examining the theoretical predictions. — Proc. Roy. Soc. Lond. B: Biol. Sci. 272: 1593-1599.

StiverK.A.FitzpatrickJ.L.DesjardinsJ.K.BalshineS. (2006). Sex differences in rates of territory joining and inheritance in a cooperatively breeding cichlid fish. — Anim. Behav. 71: 449-456.

StiverK.A.DesjardinsJ.K.FitzpatrickJ.L.NeffB.QuinnJ.S.BalshineS. (2007). Evidence for size and sex-specific dispersal in a cooperatively breeding cichlid fish. — Mol. Ecol. 16: 2974-2984.

TaborskyM. (1984). Broodcare helpers in the cichlid fish Lamprologus brichardi: their costs and benefits. — Anim. Behav. 32: 1236-1252.

TaborskyM. (1985). Breeder-helper conflict in a cichlid fish with broodcare helpers: an experimental analysis. — Behaviour 95: 45-75.

TaborskyM.LimbergerD. (1981). Helpers in fish. — Behav. Ecol. Sociobiol. 8: 143-145.

ThompsonR.R.WaltonJ.C. (2004). Peptide effects on social behaviour: effects of vasotocin and isotocin on social approach behaviour in male goldfish (Carassius auratus). — Behav. Neurosci. 118: 620-626.

WilsonE.O. (1975). Sociobiology: the new synthesis. — Harvard University PressCambridge, MA.

WongM.BalshineS. (2011a). The evolution of cooperative breeding in the African cichlid fish, Neolamprologus pulcher. — Biol. Rev. 86: 511-530.

WongM.BalshineS. (2011b). Fight for your breeding right: hierarchy re-establishment predicts aggression in a social queue. — Biol. Lett. 7: 190-193.

ZöttlM.ChapuisL.FreiburghausM.TaborskyM. (2012). Strategic reduction of help before dispersal in a cooperative breeder. — Biol. Lett. 9: 20120878.

ZöttlM.FrommenJ.G.TaborskyM. (2013a). Group size adjustment to ecological demand in a cooperative breeder. — Proc. Roy. Soc. Lond. B: Biol. Sci. 280: 20122772.

ZöttlM.HegD.ChervetN.TaborskyM. (2013b). Kinship reduces alloparental care in cooperative cichlids where helpers pay-to-stay. — Nature Commun. 4: 1341-1349.

Figures

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    A schematic representation of the social choice apparatus as viewed from the front of the aquarium. The dashed lines delineate the preference zone for each stimulus chamber (10 cm). This figure is published in colour in the online edition of this journal, which can be accessed via http://booksandjournals.brillonline.com/content/journals/1568539x.

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    (A) Mean ± SE time focal fish spent associating with the large group minus the time spent associating with the lone fish during each of two observation periods when individuals were treated with one of three experimental doses of isotocin or a vehicle only control. There were significant effects (p<0.05) of isotocin dose and sex during the first observation. (B) Mean ± SE number of focal fish interactions (through the glass barrier) with the large group minus the number of such interactions with the lone fish during each of two observation periods. There was a significant effect (p<0.05) of sex during the first observation. N=10 fish per sex per treatment.

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    (A) Mean ± SE time focal fish spent associating with and (B) mean ± SE number of interactions (through the glass barrier) with the group of three conspecifics minus the time/interactions with the lone individual during each of four observation periods following treatment with one of three experimental doses of an oxytocin receptor antagonist or a vehicle-only control. There was no significant effect of sex or treatment on association time during any of the observation periods, but a significant effect (p<0.05) of treatment on number of interactions in males but not females during the first observation period, whereby males that received the high dose showed a greater number of interactions with the group of three fish. N=5 fish per sex per treatment.

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