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Molecular mechanisms and the conflict between courtship and aggression in three-spined sticklebacks.

ABSTRACT: In nature, animals often face conflicting demands. For example, breeding males must attract a mate but at the same time be ready to defend against rivals. The molecular mechanisms by which the brain resolves behavioural trade-offs are largely unknown. In this study, we compared the brain transcriptional responses of territorial male three-spined sticklebacks to a mating opportunity with a female and to a territorial challenge by a rival male. We focused on the diencephalon and the cerebellum, two regions of the brain implicated in courtship and aggression. There was a set of genes that were differentially expressed in response to both a courtship opportunity and a territorial challenge. Closer inspection of the direction of regulation revealed that genes that were downregulated in response to a courtship opportunity were upregulated in response to a territorial challenge and vice versa. Our study reveals some of the potential molecular mechanisms underlying behavioural trade-offs between sex and aggression, along with a possible solution to the conflict via social context-dependent gene regulation.

SUBMITTER: Sanogo YO

PROVIDER: S-EPMC5021609 | biostudies-literature | 2016 Sep

REPOSITORIES: biostudies-literature

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Molecular mechanisms and the conflict between courtship and aggression in three-spined sticklebacks.

Sanogo Yibayiri O YO Bell Alison M AM

Molecular ecology 20160826 17

In nature, animals often face conflicting demands. For example, breeding males must attract a mate but at the same time be ready to defend against rivals. The molecular mechanisms by which the brain resolves behavioural trade-offs are largely unknown. In this study, we compared the brain transcriptional responses of territorial male three-spined sticklebacks to a mating opportunity with a female and to a territorial challenge by a rival male. We focused on the diencephalon and the cerebellum, tw ...[more]

PMID: 27452346

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Project description:BACKGROUND: Comparative genomics approaches help to shed light on evolutionary processes that shape differentiation between lineages. The nine-spined stickleback (Pungitius pungitius) is a closely related species of the ecological 'supermodel' three-spined stickleback (Gasterosteus aculeatus). It is an emerging model system for evolutionary biology research but has garnered less attention and lacks extensive genomic resources. To expand on these resources and aid the study of sticklebacks in a phylogenetic framework, we characterized nine-spined stickleback transcriptomes from brain and liver using deep sequencing. RESULTS: We obtained nearly eight thousand assembled transcripts, of which 3,091 were assigned as putative one-to-one orthologs to genes found in the three-spined stickleback. These sequences were used for evaluating overall differentiation and substitution rates between nine- and three-spined sticklebacks, and to identify genes that are putatively evolving under positive selection. The synonymous substitution rate was estimated to be 7.1 × 10(-9) per site per year between the two species, and a total of 165 genes showed patterns of adaptive evolution in one or both species. A few nine-spined stickleback contigs lacked an obvious ortholog in three-spined sticklebacks but were found to match genes in other fish species, suggesting several gene losses within 13 million years since the divergence of the two stickleback species. We identified 47 SNPs in 25 different genes that differentiate pond and marine ecotypes. We also identified 468 microsatellites that could be further developed as genetic markers in nine-spined sticklebacks. CONCLUSION: With deep sequencing of nine-spined stickleback cDNA libraries, our study provides a significant increase in the number of gene sequences and microsatellite markers for this species, and identifies a number of genes showing patterns of adaptive evolution between nine- and three-spined sticklebacks. We also report several candidate genes that might be involved in differential adaptation between marine and freshwater nine-spined sticklebacks. This study provides a valuable resource for future studies aiming to identify candidate genes underlying ecological adaptation in this and other stickleback species.

Project description:Contact zones between divergent forms of the same species are often characterised by high levels of phenotypic diversity over small geographic distances. What processes are involved in generating such high phenotypic diversity? One possibility is that introgression and recombination between divergent forms in contact zones results in greater phenotypic and genetic polymorphism. Alternatively, strong reproductive isolation between forms may maintain distinct phenotypes, preventing homogenisation by gene flow. Contact zones between divergent freshwater-resident and anadromous stickleback (Gasterosteus aculeatus L.) forms are numerous and common throughout the species distribution, offering an opportunity to examine these contrasting hypotheses in greater detail. This study reports on an interesting new contact zone located in a tidally influenced lake catchment in western Ireland, characterised by high polymorphism for lateral plate phenotypes. Using neutral and QTL-linked microsatellite markers, we tested whether the high diversity observed in this contact zone arose as a result of introgression or reproductive isolation between divergent forms: we found strong support for the latter hypothesis. Three phenotypic and genetic clusters were identified, consistent with two divergent resident forms and a distinct anadromous completely plated population that migrates in and out of the system. Given the strong neutral differentiation detected between all three morphotypes (mean FST = 0.12), we hypothesised that divergent selection between forms maintains reproductive isolation. We found a correlation between neutral genetic and adaptive genetic differentiation that support this. While strong associations between QTL linked markers and phenotypes were also observed in this wild population, our results support the suggestion that such associations may be more complex in some Atlantic populations compared to those in the Pacific. These findings provide an important foundation for future work investigating the dynamics of gene flow and adaptive divergence in this newly discovered stickleback contact zone.

Dataset Information

Molecular mechanisms and the conflict between courtship and aggression in three-spined sticklebacks.

Publications

Molecular mechanisms and the conflict between courtship and aggression in three-spined sticklebacks.

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