Rising to the challenge? Inter-individual variation of the androgen response to social interactions in cichlid fish

The requirements of living in social groups, and forming and maintaining social relationships are hypothesized to be one of the major drivers behind the evolution of cognitive abilities. Most empirical studies investigating the relationships between sociality and cognition compare cognitive performance between species living in systems that differ in social complexity. In this review, we ask whether and how individuals benefit from cognitive skills in their social interactions. Cognitive abilities, such as perception, attention, learning, memory, and inhibitory control, aid in forming and maintaining social relationships. We investigate whether there is evidence that individual variation in these abilities influences individual variation in social relationships. We then consider the evolutionary consequences of the interaction between sociality and cognitive ability to address whether bi-directional relationships exist between the two, such that cognition can both shape and be shaped by social interactions and the social environment. In doing so, we suggest that social network analysis is emerging as a powerful tool that can be used to test for directional causal relationships between sociality and cognition. Overall, our review highlights the importance of investigating individual variation in cognition to understand how it shapes the patterns of social relationships. This article is part of the theme issue ‘Causes and consequences of individual differences in cognitive abilities’.

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A multidisciplinary study on social status and the relationship between inter-individual variation in hormone levels and agonistic behavior in a Neotropical cichlid fish

Hormones and Behavior ◽

10.1016/j.yhbeh.2015.01.008 ◽

2015 ◽

Vol 69 ◽

pp. 139-151 ◽

Cited By ~ 17

Author(s):

Martín R. Ramallo ◽

Agustina Birba ◽

Renato M. Honji ◽

Leonel Morandini ◽

Renata G. Moreira ◽

...

Keyword(s):

Social Status ◽

Individual Variation ◽

Agonistic Behavior ◽

Cichlid Fish ◽

Hormone Levels ◽

Multidisciplinary Study ◽

The Relationship

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Individual variation in male mating preferences for female coloration in a polymorphic cichlid fish

Behavioral Ecology ◽

10.1093/beheco/arm154 ◽

2008 ◽

Vol 19 (3) ◽

pp. 483-488 ◽

Cited By ~ 17

Author(s):

Michele E.R. Pierotti ◽

Mairi E. Knight ◽

Simone Immler ◽

Nicola J. Barson ◽

George F. Turner ◽

...

Keyword(s):

Individual Variation ◽

Cichlid Fish ◽

Male Mating ◽

Mating Preferences ◽

Female Coloration

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Genetic architecture of natural variation in cuticular hydrocarbon composition in Drosophila melanogaster

eLife ◽

10.7554/elife.09861 ◽

2015 ◽

Vol 4 ◽

Cited By ~ 61

Author(s):

Lauren M Dembeck ◽

Katalin Böröczky ◽

Wen Huang ◽

Coby Schal ◽

Robert R H Anholt ◽

...

Keyword(s):

Drosophila Melanogaster ◽

Social Interactions ◽

Individual Variation ◽

Genetic Architecture ◽

Natural Variation ◽

Genetic Basis ◽

Acid Metabolism ◽

Cuticular Hydrocarbon ◽

Principal Component ◽

Hydrocarbon Composition

Insect cuticular hydrocarbons (CHCs) prevent desiccation and serve as chemical signals that mediate social interactions. Drosophila melanogaster CHCs have been studied extensively, but the genetic basis for individual variation in CHC composition is largely unknown. We quantified variation in CHC profiles in the D. melanogaster Genetic Reference Panel (DGRP) and identified novel CHCs. We used principal component (PC) analysis to extract PCs that explain the majority of CHC variation and identified polymorphisms in or near 305 and 173 genes in females and males, respectively, associated with variation in these PCs. In addition, 17 DGRP lines contain the functional Desat2 allele characteristic of African and Caribbean D. melanogaster females (more 5,9-C27:2 and less 7,11-C27:2, female sex pheromone isomers). Disruption of expression of 24 candidate genes affected CHC composition in at least one sex. These genes are associated with fatty acid metabolism and represent mechanistic targets for individual variation in CHC composition.

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Hormonal anticipation of territorial challenges in cichlid fish

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.0900817106 ◽

2009 ◽

Vol 106 (37) ◽

pp. 15985-15989 ◽

Cited By ~ 28

Author(s):

Raquel A. Antunes ◽

Rui F. Oliveira

Keyword(s):

Conditioned Stimulus ◽

Social Interactions ◽

Test Trial ◽

Cichlid Fish ◽

Oreochromis Mossambicus ◽

Training Phase ◽

Social Challenges ◽

Social Challenge ◽

Aggressive Motivation ◽

Androgen Levels

In many territorial species androgens respond to social interactions. This response has been interpreted as a mechanism for adjusting aggressive motivation to a changing social environment. Therefore, it would be adaptive to anticipate social challenges and reacting to their clues with an anticipatory androgen response to adjust agonistic motivation to an imminent social challenge. Here we test the hypothesis of an anticipatory androgen response to territorial intrusions using classical conditioning to establish an association between a conditioned stimulus (CS = light) and an unconditioned stimulus (US = intruder male) in male cichlid fish (Oreochromis mossambicus). During the training phase conditioned males (CS−US paired presentations) showed a higher decrease in latency for agonistic response toward the intruder than unconditioned males (CS–US unpaired presentations). In the test trial, conditioned males showed an increase in androgen levels (i.e., testosterone and 11-ketotestosterone) relative to baseline, in response to the CS alone. This increase was similar to that of control males exposed to real intruders after CS, whereas unconditioned males showed a decrease in androgen levels in response to the CS. Furthermore, conditioned males were significantly more aggressive than unconditioned males during the post-CS period on test trial, even though the intruder male was not present during this period. These results reveal the occurrence of a conditioned androgen response that may give territorial males an advantage in mounting a defense to upcoming territorial intrusions, if the ability to readily elevate androgens does not co-vary with other traits that bear costs.

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Social interactions tune aggression and stress responsiveness in a territorial cichlid fish (Archocentrus nigrofasciatus)

Physiology & Behavior ◽

10.1016/j.physbeh.2006.04.002 ◽

2006 ◽

Vol 88 (4-5) ◽

pp. 353-363 ◽

Cited By ~ 82

Author(s):

R EARLEY ◽

J EDWARDS ◽

O ASEEM ◽

K FELTON ◽

L BLUMER ◽

...

Keyword(s):

Social Interactions ◽

Cichlid Fish ◽

Archocentrus Nigrofasciatus ◽

Stress Responsiveness

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Why do winners keep winning? Androgen mediation of winner but not loser effects in cichlid fish

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2009.0132 ◽

2009 ◽

Vol 276 (1665) ◽

pp. 2249-2256 ◽

Cited By ~ 144

Author(s):

Rui F. Oliveira ◽

Ana Silva ◽

Adelino V.M. Canário

Keyword(s):

Social Interactions ◽

Cyproterone Acetate ◽

Opposite Effect ◽

Cichlid Fish ◽

Oreochromis Mossambicus ◽

Social Experience ◽

Agonistic Interaction ◽

Mozambique Tilapia ◽

Androgen Levels

Animal conflicts are influenced by social experience such that a previous winning experience increases the probability of winning the next agonistic interaction, whereas a previous losing experience has the opposite effect. Since androgens respond to social interactions, increasing in winners and decreasing in losers, we hypothesized that socially induced transient changes in androgen levels could be a causal mediator of winner/loser effects. To test this hypothesis, we staged fights between dyads of size-matched males of the Mozambique tilapia ( Oreochromis mossambicus ). After the first contest, winners were treated with the anti-androgen cyproterone acetate and losers were supplemented with 11-ketotestosterone. Two hours after the end of the first fight, two contests were staged simultaneously between the winner of the first fight and a naive male and between the loser of first fight and another naive male. The majority (88%) of control winners also won the second interaction, whereas the majority of control losers (87%) lost their second fight, thus confirming the presence of winner/loser effects in this species. As predicted, the success of anti-androgen-treated winners in the second fight decreased significantly to chance levels (44%), but the success of androgenized losers (19%) did not show a significant increase. In summary, the treatment with anti-androgen blocks the winner effect, whereas androgen administration fails to reverse the loser effect, suggesting an involvement of androgens on the winner but not on the loser effect.

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Evidence of social niche construction: persistent and repeated social interactions generate stronger personalities in a social spider

Proceedings of The Royal Society B Biological Sciences ◽

10.1098/rspb.2013.3166 ◽

2014 ◽

Vol 281 (1783) ◽

pp. 20133166 ◽

Cited By ~ 65

Author(s):

Kate L. Laskowski ◽

Jonathan N. Pruitt

Keyword(s):

Individual Differences ◽

Social Interactions ◽

Social Environment ◽

Individual Variation ◽

Theoretical Models ◽

General Mechanism ◽

Social Spider ◽

Niche Specialization ◽

The Social ◽

Social Niche

While there are now a number of theoretical models predicting how consistent individual differences in behaviour may be generated and maintained, so far, there are few empirical tests. The social niche specialization hypothesis predicts that repeated social interactions among individuals may generate among-individual differences and reinforce within-individual consistency through positive feedback mechanisms. Here, we test this hypothesis using groups of the social spider Stegodyphus mimosarum that differ in their level of familiarity. In support of the social niche specialization hypothesis, individuals in groups of spiders that were more familiar with each other showed greater repeatable among-individual variation in behaviour. Additionally, individuals that were more familiar with each other exhibited lower within-individual variation in behaviour, providing one of the first examples of how the social environment can influence behavioural consistency. Our study demonstrates the potential for the social environment to generate and reinforce consistent individual differences in behaviour and provides a potentially general mechanism to explain this type of behavioural variation in animals with stable social groups.

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