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Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish.

ABSTRACT: Neuropeptides have widespread modulatory effects on behaviour and physiology and are associated with phenotypic transitions in a variety of animals. Arginine vasotocin (AVT) is implicated in mediating alternative male phenotypes in teleost fish, but the direction of the association differs among species, with either higher or lower AVT related to more territorial behaviour in different fishes. To clarify the complex relationship between AVT and alternative phenotype, we evaluated AVT expression in an African cichlid in which social status is associated with divergent behaviour and physiology. We compared AVT mRNA expression between territorial and non-territorial (NT) males in both whole brains and microdissected anterior preoptic areas using transcription profiling, and in individual preoptic nuclei using in situ hybridization. These complementary methods revealed that in the posterior preoptic area (gigantocellular nucleus), territorial males exhibit higher levels of AVT expression than NT males. Conversely, in the anterior preoptic area (parvocellular nucleus), AVT expression is lower in territorial males than NT males. We further correlated AVT expression with behavioural and physiological characteristics of social status to gain insight into the divergent functions of individual AVT nuclei. Overall, our findings highlight a complex association between AVT and social behaviour.

SUBMITTER: Greenwood AK

PROVIDER: S-EPMC2603226 | biostudies-literature | 2008 Oct

REPOSITORIES: biostudies-literature

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Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish.

Greenwood Anna K AK Wark Abigail R AR Fernald Russell D RD Hofmann Hans A HA

Proceedings. Biological sciences 20081001 1649

Neuropeptides have widespread modulatory effects on behaviour and physiology and are associated with phenotypic transitions in a variety of animals. Arginine vasotocin (AVT) is implicated in mediating alternative male phenotypes in teleost fish, but the direction of the association differs among species, with either higher or lower AVT related to more territorial behaviour in different fishes. To clarify the complex relationship between AVT and alternative phenotype, we evaluated AVT expression ...[more]

PMID: 18628117

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Project description:Animals constantly integrate external stimuli with their own internal physiological state to make appropriate behavioural decisions. Little is known, however, about where in the brain the salience of these signals is evaluated, or which neural and transcriptional mechanisms link this integration to adaptive behaviours. We used an African cichlid fish Astatotilapia burtoni to test the hypothesis that a new social opportunity activates the conserved 'social behaviour network' (SBN), a collection of brain nuclei known to regulate social behaviours across vertebrates. We measured mRNA levels of immediate early genes (IEGs) in microdissected brain regions as a proxy for neuronal activation, and discovered that IEGs were higher in all SBN nuclei in males that were given an opportunity to rise in social rank compared to control stable subordinate and dominant individuals. Furthermore, because the presence of sex-steroid receptors is one defining criteria of SBN nuclei, we also tested whether social opportunity or status influenced androgen and oestrogen receptor mRNA levels within these same regions. There were several rapid region-specific changes in receptor mRNA levels induced by social opportunity, most notably in oestrogen receptor subtypes in areas that regulate social aggression and reproduction, suggesting that oestrogenic signalling pathways play an important role in regulating male status. Several receptor mRNA changes occurred in regions with putative homologies to the mammalian septum and extended amygdala, two regions shared by SBN and reward circuits, suggesting an important role in the integration of social salience, stressors, hormonal state and adaptive behaviours. We also demonstrated increases in plasma sex- and stress-steroids at 30 min after a rise in social rank. This rapid endocrine and transcriptional response suggests that the SBN is involved in the integration of social inputs with internal hormonal state to facilitate the transition to dominant status, which ultimately leads to improved fitness for the previously reproductively-suppressed individual.

Project description:The African cichlid fish radiations are the most diverse extant animal radiations and provide a unique system to test predictions of speciation and adaptive radiation theory. The past few years have seen major advances in the phylogenetics, evolutionary biogeography and ecology of cichlid fish. Most of this work has concentrated on the most diverse radiations. Unfortunately, a large number of small radiations and 'non-radiations' have been overlooked, potentially limiting the contribution of the cichlid system to our understanding of speciation and adaptive radiation. I have reviewed the literature to identify 33 intralacustrine radiations and 76 failed radiations. For as many as possible I collected information on lake size, age and phylogenetic relationships. I use these data to address two questions: (i) whether the rate of speciation and the resulting species richness are related to temporal and spatial variation in ecological opportunity and (ii) whether the likelihood of undergoing adaptive radiation is similar for different African cichlid lineages. The former is a key prediction of the ecological theory of adaptive radiation that has been presumed true but remains untested for cichlid radiations. The second is based on the hypothesis that the propensity of cichlids to radiate is due to a key evolutionary innovation shared by all African cichlids. The evidence suggests that speciation rate declines through time as niches get filled up during adaptive radiation: young radiations and early stages of old radiations are characterized by high rates of speciation, whereas at least 0.5 Myr into a radiation speciation becomes a lot less frequent. The number of species in cichlid radiations increases with lake size, supporting the prediction that species diversity increases with habitat heterogeneity, but also with opportunity for isolation by distance. Finally, the data suggest that the propensity to radiate within lakes is a derived property that evolved during the evolutionary history of some African cichlids, and the appearance of which does not coincide with the appearance of proposed key innovations in morphology and life history.

Dataset Information

Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish.

Publications

Expression of arginine vasotocin in distinct preoptic regions is associated with dominant and subordinate behaviour in an African cichlid fish.

Similar Datasets

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