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Reproductive skew, fighting costs and winner-loser effects in social dominance evolution.

ABSTRACT: Social hierarchies are often found in group-living animals and can be formed through pairwise aggressive interactions. The dominance rank can influence reproductive success (RS) with a skew towards high-ranking individuals. Using game theory, we investigate how the opportunity for differently ranked individuals to achieve RS influences the costs of hierarchy formation and the strength of winner and loser effects. In our model, individuals adjust their aggressive and submissive behaviour towards others through reinforcement learning. The learning is based on rewards and penalties, which depend on relative fighting ability. From individual-based simulations, we determine evolutionary equilibria of traits such as learning rates. We examine situations that differ in the extent of monopolisation of contested RS by dominants and in the proportion of total RS that is contested. The model implements two kinds of fighting costs: a decrease in effective fighting ability from damage (loss of condition) and a risk of mortality that increases with the total accumulated damage. Either of these costs can limit the amount of fighting. We find that individuals form stable dominance hierarchies, with a positive correlation between dominance position and fighting ability. The accumulated costs differ between dominance positions, with the highest costs paid by low or intermediately ranked individuals. Costs tend to be higher in high-skew situations. We identify a 'stay-in, opt-out' syndrome, comprising a range from weaker (stay-in) to stronger (opt-out) winner-loser effects. We interpret the opt-out phenotype to be favoured by selection on lower ranked individuals to opt out of contests over social dominance, because it is more pronounced when more of the total RS is uncontested. We discuss our results in relation to field and experimental observations and argue that there is a need for empirical investigation of the behaviour and reproductive success of lower ranked individuals.

SUBMITTER: Leimar O

PROVIDER: S-EPMC9315160 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:IntroductionMany animals use information acquired from recent experiences to modify their responses to new situations. Animals' decisions in contests also depend on their previous experience: after recent victories individuals tend to behave more aggressively and after defeats more submissively. Although these winner and/or loser effects have been reported for animals of different taxa, they have only recently been shown to be flexible traits, which can be influenced by extrinsic factors. In a mangrove killifish (Kryptolebias marmoratus), for instance, individuals which lost an earlier contest were more likely than others to alter contest decisions after a recent win/loss. This result suggests that individuals perceiving themselves to have worse fighting abilities are more inclined to adjust contest strategy based on new information. If this is the case, an individual's propensity to modify behaviour after a win/loss might also be modulated by intrinsic mechanisms related to its ability to fight. Stress and sex steroid hormones are often associated with an individual's contest behaviour and performance, so, in this study, we tested the hypothesis that an individual's propensity to change behaviour after wins or losses also depends on its hormonal state.ResultsOur results show that an individual's propensity to adjust contest decisions after wins and losses does depend on its hormonal state: individuals with lower levels of cortisol (F), testosterone (T) and 11-ketotestosterone (KT) are more receptive than others to the influence of recent contest experiences, especially losing experiences, and the influences last longer. Furthermore, although winning and losing experiences resulted in significant changes in behaviour, they did not bring about a significant change in the levels of F, T, KT or oestradiol (E2).ConclusionsThis study shows that an individual's receptivity to the influence of recent wins and losses is modulated by its internal state, as well as by extrinsic factors. Individuals with hormonal profiles corresponding to lower aggressiveness and a reduced likelihood of winning were more likely to alter contest decisions after a recent win/loss. The results also suggest that F, T, KT and E2 are not the primary physiological mechanisms mediating winner-loser effects in this fish.

Project description:Social plasticity is a pervasive feature of animal behavior. Animals adjust the expression of their social behavior to the daily changes in social life and to transitions between life-history stages, and the ability to change in these ways impacts their Darwinian fitness. This behavioral plasticity may be achieved either by rewiring or by biochemically switching nodes of the neural network underlying the social behavior in response to perceived social information. Independent of the proximate mechanisms, at the neuromolecular level social plasticity relies on the regulation of gene expression, such that different neurogenomic states emerge in response to different social stimuli and the switches between states are orchestrated by signaling pathways that interface the social environment and the genotype. Here, we test this hypothesis by characterizing the changes in the brain profile of gene expression in response to social odors in the Mozambique Tilapia, Oreochromis mossambicus. This species has a rich repertoire of social behaviors during which both visual and chemical information are conveyed to conspecifics. Specifically, dominant males increase their urination frequency during agonist encounters and during courtship to convey chemical information reflecting their dominance status. We recorded electro-olfactograms to test the extent to which the olfactory epithelium can discriminate between olfactory information from dominant and subordinate males as well as from pre- and post-spawning females. We then performed a genome-scale gene expression analysis of the olfactory bulb and the olfactory cortex homolog in order to identify the neuromolecular systems involved in processing these social stimuli. Our results show that different olfactory stimuli from conspecificsM-bM-^@M-^Y have a major impact in the brain transcriptome, with different chemical social cues eliciting specific patterns of gene expression in the brain. These results confirm the role of rapid changes in gene expression in the brain as a genomic mechanism underlying behavioural plasticity and reinforce the idea of an extensive transcriptional plasticity of cichlid genomes, especially in response to rapid changes in their social environment. Brain samples from 40 African cichlid males, Oreochromis mossambicus were collected after stimulation with different social olfactory stimuli. Samples were collected from 2 brain areas: BO and Dp after males were exposed to dominant (DOM) and subordinate (SUB) male urine and pre- (PRE) and post-ovulatory (POST) female scent. In OB 5 replicates were collected from males exposed to DOM and 6 to the other stimuli. For Dp 5 replicates were collected from males exposed to DOM and POST, 4 to SUB and 6 to PRE.

Project description:Social plasticity is a pervasive feature of animal behavior. Animals adjust the expression of their social behavior to the daily changes in social life and to transitions between life-history stages, and the ability to change in these ways impacts their Darwinian fitness. This behavioral plasticity may be achieved either by rewiring or by biochemically switching nodes of the neural network underlying the social behavior in response to perceived social information. Independent of the proximate mechanisms, at the neuromolecular level social plasticity relies on the regulation of gene expression, such that different neurogenomic states emerge in response to different social stimuli and the switches between states are orchestrated by signaling pathways that interface the social environment and the genotype. Here, we test this hypothesis by characterizing the changes in the brain profile of gene expression in response to social odors in the Mozambique Tilapia, Oreochromis mossambicus. This species has a rich repertoire of social behaviors during which both visual and chemical information are conveyed to conspecifics. Specifically, dominant males increase their urination frequency during agonist encounters and during courtship to convey chemical information reflecting their dominance status. We recorded electro-olfactograms to test the extent to which the olfactory epithelium can discriminate between olfactory information from dominant and subordinate males as well as from pre- and post-spawning females. We then performed a genome-scale gene expression analysis of the olfactory bulb and the olfactory cortex homolog in order to identify the neuromolecular systems involved in processing these social stimuli. Our results show that different olfactory stimuli from conspecifics’ have a major impact in the brain transcriptome, with different chemical social cues eliciting specific patterns of gene expression in the brain. These results confirm the role of rapid changes in gene expression in the brain as a genomic mechanism underlying behavioural plasticity and reinforce the idea of an extensive transcriptional plasticity of cichlid genomes, especially in response to rapid changes in their social environment.

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Reproductive skew, fighting costs and winner-loser effects in social dominance evolution.

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