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Cited by 95Neuroendocrine regulation and behaviorAnimal Behavior and ReproductionReproductive biology and impacts on aquatic species

An Essential Role of the Arginine Vasotocin System in Mate-Guarding Behaviors in Triadic Relationships of Medaka Fish (Oryzias latipes)

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Yokoi, Saori, Okuyama, Teruhiro, Kamei, Yasuhiro, Naruse, Kiyoshi, Taniguchi, Yoshihito, Ansai, Satoshi, Kinoshita, Masato, Young, Larry J. +3 more·2015·PLOS Genetics
DOI 10.1371/journal.pgen.1005009PMC PMC4342251
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Abstract

To increase individual male fitness, males of various species remain near a (potential) mating partner and repel their rivals (mate-guarding). Mate-guarding is assumed to be mediated by two different types of motivation: sexual motivation toward the opposite sex and competitive motivation toward the same sex. The genetic/molecular mechanisms underlying how mate presence affects male competitive motivation in a triadic relationship has remained largely unknown. Here we showed that male medaka fish prominently exhibit mate-guarding behavior. The presence of a female robustly triggers male-male competition for the female in a triadic relationship (2 males and 1 female). The male-male competition resulted in one male occupying a dominant position near the female while interfering with the other male's approach of the female. Paternity testing revealed that the dominant male had a significantly higher mating success rate than the other male in a triadic relationship. We next generated medaka mutants of arginine-vasotocin (avt) and its receptors (V1a1, V1a2) and revealed that two genes, avt and V1a2, are required for normal mate-guarding behavior. In addition, behavioral analysis of courtship behaviors in a dyadic relationship and aggressive behaviors within a male group revealed that avt mutant males displayed decreased sexual motivation but showed normal aggression. In contrast, heterozygote V1a2 mutant males displayed decreased aggression, but normal mate-guarding and courtship behavior. Thus, impaired mate-guarding in avt and V1a2 homozygote mutants may be due to the loss of sexual motivation toward the opposite sex, and not to the loss of competitive motivation toward rival males. The different behavioral phenotypes between avt, V1a2 heterozygote, and V1a2 homozygote mutants suggest that there are redundant systems to activate V1a2 and that endogenous ligands activating the receptor may differ according to the social context.

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  • In medaka fish, females preferentially mate with familiar males who successfully competed for proximity to the female the previous day.

    “In medaka fish, females preferentially mate with familiar males who successfully competed for proximity to the female the previous day (Yokoi et al. 2015, 2016).”

    From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Yokoi et al. 2015

    The Results section, “Positive correlation between dominance in mate-guarding and reproductive success” (page unavailable), reports that males dominant in a proximity-based guarding test before mating had higher reproductive success the next morning. It does not establish that females preferentially chose those males because they were familiar, rather than that dominant males gained greater access to mating. (LLM, conf=0.86)

    Experimental — accuracy not yet measured

  • Oxytocin mediates mating preferences in polygamous species.

    “Oxytocin also mediates mating preferences in polygamous species.”

    From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Yokoi et al. 2015

    The Discussion links arginine vasotocin (AVT), not oxytocin, to sexual motivation and mate-guarding in medaka. Its mention of oxytocin concerns receptor cross-talk and says further analysis of isotocin is needed. Searches for oxytocin, isotocin, and partner preference found no passage establishing that oxytocin mediates mating preferences in polygamous species. (LLM, conf=0.75)

    Experimental — accuracy not yet measured

  • In medaka fish, males typically mate indiscriminately and with no preference for familiarity.

    “By contrast, males typically mate indiscriminately and with no preference for familiarity.”

    From Oxytocin, Neural Plasticity, and Social Behavior (2021) · cites this paper as Yokoi et al. 2015

    The Introduction describes socially regulated female preference, while the Results examine male mate-guarding and reproductive success. Neither section establishes that males mate indiscriminately or lack a preference for familiar females; searches for familiarity and indiscriminate mating found no passage addressing those claims. (LLM, conf=0.74)

    Experimental — accuracy not yet measured

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Authors
Yokoi, S., Okuyama, T., Kamei, Y., Naruse, K., Taniguchi, Y., Ansai, S., Kinoshita, M., Young, L. J., Takemori, N., Kubo, T., & Takeuchi, H.
Affiliations
  • The University of Tokyo (JP)
  • National Institute for Basic Biology (JP)
  • Kyorin University (JP)
  • Kyoto University (JP)
  • Emory University (US)
  • Ehime University (JP)
Corresponding author
Takeuchi, Hideaki
ORCID
Venue
PLOS Genetics
Publisher
Public Library of Science (PLoS)
Published
2015-02-26
Volume
11
Issue
2
Pages
e1005009
ISSN
  • 1553-7390 (ISSN-L)
  • 1553-7404
DOI
10.1371/journal.pgen.1005009
PMC
PMC4342251
OpenAlex
W2067850204
Cited by
95
References
4
Citations by year
2026: 6 · 2025: 11 · 2024: 11 · 2023: 11 · 2022: 11 · 2021: 8 · 2020: 9 · 2019: 5 · 2018: 5 · 2017: 9 · 2016: 8 · 2015: 1
FWCI
12.58
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Genetics (publishedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Institutional Repositories DataBase (IRDB) (submittedVersion, other-oa)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
  • Figshare (submittedVersion, cc-by)
  • Kyoto University Research Information Repository (Kyoto University) (submittedVersion, cc-by)
Funders
  • Cell Science Research Foundation
  • Ministry of Education, Culture, Sports, Science and Technology (10-104)
  • Japan Society for the Promotion of Science (26290003, 23300115, 25640006, 12J05418, 13J01682)
  • National Institute for Basic Biology (10-104)
Topics
  • Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
  • Life Sciences › Agricultural and Biological Sciences › Ecology, Evolution, Behavior and Systematics › Animal Behavior and Reproduction
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Physiology › Reproductive biology and impacts on aquatic species
Keywords
mate guarding, arginine vasotocin, medaka, triadic relationships, male-male competition, sexual motivation, courtship behavior, aggression, paternity, social environment, neuropeptides
MeSH terms
Aggression, Animals, Copulation, Female, Male, Marriage, Motivation, Oryzias, Reproduction, Sexual Behavior, Animal, Vasotocin

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