An essential role of the arginine vasotocin system in mate-guarding behaviors in triadic relationships of medaka fish (Oryzias latipes)

Saori Yokoi, Teruhiro Okuyama, Yasuhiro Kamei, Kiyoshi Naruse, Yoshihito Taniguchi, Satoshi Ansai, Masato Kinoshita, Larry J. Young, Nobuaki Takemori, Takeo Kubo, Hideaki Takeuchi

Research output: Contribution to journalArticle

21 Citations (Scopus)

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.

Original languageEnglish
Pages (from-to)e1005009
JournalPLoS Genetics
Volume11
Issue number2
DOIs
Publication statusPublished - 2015
Externally publishedYes

Fingerprint

arginine vasotocin
Vasotocin
Oryzias
mate guarding
Oryzias latipes
Fishes
fish
Motivation
mutants
Courtship
aggression
Homozygote
courtship
Heterozygote
homozygosity
Aggression
gender
heterozygosity
receptors

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Molecular Biology
  • Genetics
  • Genetics(clinical)
  • Cancer Research

Cite this

An essential role of the arginine vasotocin system in mate-guarding behaviors in triadic relationships of medaka fish (Oryzias latipes). / Yokoi, Saori; Okuyama, Teruhiro; Kamei, Yasuhiro; Naruse, Kiyoshi; Taniguchi, Yoshihito; Ansai, Satoshi; Kinoshita, Masato; Young, Larry J.; Takemori, Nobuaki; Kubo, Takeo; Takeuchi, Hideaki.

In: PLoS Genetics, Vol. 11, No. 2, 2015, p. e1005009.

Research output: Contribution to journalArticle

Yokoi, S, Okuyama, T, Kamei, Y, Naruse, K, Taniguchi, Y, Ansai, S, Kinoshita, M, Young, LJ, Takemori, N, Kubo, T & Takeuchi, H 2015, 'An essential role of the arginine vasotocin system in mate-guarding behaviors in triadic relationships of medaka fish (Oryzias latipes)', PLoS Genetics, vol. 11, no. 2, pp. e1005009. https://doi.org/10.1371/journal.pgen.1005009
Yokoi, Saori ; Okuyama, Teruhiro ; Kamei, Yasuhiro ; Naruse, Kiyoshi ; Taniguchi, Yoshihito ; Ansai, Satoshi ; Kinoshita, Masato ; Young, Larry J. ; Takemori, Nobuaki ; Kubo, Takeo ; Takeuchi, Hideaki. / An essential role of the arginine vasotocin system in mate-guarding behaviors in triadic relationships of medaka fish (Oryzias latipes). In: PLoS Genetics. 2015 ; Vol. 11, No. 2. pp. e1005009.
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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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