Mate-guarding behavior enhances male reproductive success via familiarization with mating partners in medaka fish
Open accessAbstract
BACKGROUND: Male-male competition and female mating preference are major mechanisms of sexual selection, which influences individual fitness. How male-male competition affects female preference, however, remains poorly understood. Under laboratory conditions, medaka (Oryzias latipes) males compete to position themselves between a rival male and the female (mate-guarding) in triadic relationships (male, male, and female). In addition, females prefer to mate with visually familiar males. In the present study, to examine whether mate-guarding affects female preference via visual familiarization, we established a novel behavioral test to simultaneously quantify visual familiarization of focal males with females and mate-guarding against rival males. In addition, we investigated the effect of familiarization on male reproductive success in triadic relationships. RESULTS: Three fish (female, male, male) were placed separately in a transparent three-chamber tank, which allowed the male in the center (near male) to maintain closer proximity to the female than the other male (far male). Placement of the wild-type male in the center blocked visual familiarization of the far male by the female via mate-guarding. In contrast, placement of an arginine-vasotocin receptor mutant male, which exhibits mate-guarding deficits, in the center, allowing for maintaining close proximity to the female, did not block familiarization of the far male by the female. We also demonstrated that the reproductive success of males was significantly decreased by depriving females visual familiarization with the males. CONCLUSIONS: Our findings indicated that, at least in triadic relationships, dominance in mate-guarding, not simply close proximity, allows males to gain familiarity with the female over their rivals, which may enhance female preference for the dominant male. These findings focusing on the triadic relationships of medaka may contribute to our understanding of the adaptive significance of persistent mate-guarding, as well as female preference for familiar mates.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
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. 2016
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. 2016
The Background and Results discuss female mating preference in medaka and experiments involving the arginine-vasotocin receptor V1a2, not oxytocin. A search for oxytocin found no passage in our copy saying that it mediates mating preferences in polygamous species. (LLM, conf=0.76)
Experimental — accuracy not yet measuredIn 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. 2016
The Background (page unavailable) says medaka females prefer visually familiar males and that medaka do not maintain monogamous relationships. Neither establishes whether males mate indiscriminately or prefer familiar females. A search for male mate choice and familiarity found no passage addressing those points. (LLM, conf=0.74)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
No references could be resolved yet.
Research works printed but not linked: 37
- [1]Hunt J Breuker CJ Sadowski JA Moore AJ Male-male competition, female mate choice and their interaction: determining total sexual selection J Evol Biol. 2009 22 13 26 10.1111/j.1420-9101.2008.01633.x 19120810 · DOI
- [2]Paull GC Filby AL Giddins HG Coe TS Hamilton PB Tyler CR Dominance hierarchies in zebrafish (Danio rerio) and their relationship with reproductive success Zebrafish. 2010 7 109 17 10.1089/zeb.2009.0618 20192850 · DOI
- [3]Botero CA Rossman RJ Caro LM Stenzier LM Lovette IJ De Kort SR Syllable Type Consistency is Related to Age, Social Status, and Reproductive Success in the Tropical Mockingbird Anim Behav. 2009 77 701 706 10.1016/j.anbehav.2008.11.020 20161558 PMC2805192 · DOI
- [4]Rodriguez-Llanes JM Verbeke G Finlayson C Reproductive benefits of high social status in male macaques (Macaca) Anim Behav. 2009 78 643 649 10.1016/j.anbehav.2009.06.012 · DOI
- [5]Andersson M Female choice selects for extreme tail length in a widowbird Nature. 1982 299 818 820 10.1038/299818a0 · DOI
- [6]Kodric-Brown A Nicoletto PF Female choice in the guppy (Poecilia reticulate): the interaction between male color and display Behav Ecol Sociobiol. 2001 50 346 351 10.1007/s002650100374 · DOI
- [7]Wagner WEJ Reiser MG The importance of calling song and courtship song in females mate choice in the variable field cricket Anim Behav. 2000 59 1219 26 10.1006/anbe.1999.1428 10877901 · DOI
- [8]Birkhead TR Mate guarding in the magpie Pica pica Anim Behav. 1979 27 866 874 10.1016/0003-3472(79)90024-1 · DOI
- [9]Calbacho-Rosa L Córdoba-Aguilar A Peretti AV Occurrence and duration of post-copulatory mate guarding in a spider with last sperm precedence Behavior. 2010 147 1267 1283 10.1163/000579510X514544 · DOI
- [10]Miki M Costs of mate guarding and opportunistic mating among wild male Japanese macaques Int J Primatol 2003 24 1057 1075 10.1023/A:1026228312706 · DOI
- [11]Parker GA Sperm competition and its evolutionary consequence in the insects Biol Rev. 1970 45 525 567 10.1111/j.1469-185X.1970.tb01176.x · DOI · Paper page
- [12]Robinson SK Benefits, costs, and determinants of dominance in a polygynous oriole Anim Behav. 1986 341 241 255 10.1016/0003-3472(86)90029-1 · DOI
- [13]Schubert M Schradin C Toedel HG Pillay N Ribble DO Male mate guarding in a socially monogamous mammal, the round-eared sengi: on costs and trade-offs Behav Ecol Sociobiol. 2009 64 257 264 10.1007/s00265-009-0842-2 · DOI
- [14]Yokoi S Okuyama T Kamei Y Naruse K Taniguchi Y Ansai S An essential role of the arginine vasotocin system in mate-guarding behaviors in triadic relationships of medaka fish (Oryzias latipes) PLoS Genet. 2015 11 e1005009 10.1371/journal.pgen.1005009 25719383 PMC4342251 · DOI · Paper page
- [15]Fukamachi S Kinoshita M Aizawa K Oda S Meyer A Mitani H Dual control by a single gene of secondary sexual characters and mating preferences in medaka BMC Biol. 2009 7 64 10.1186/1741-7007-7-64 19788724 PMC2761876 · DOI
- [16]Kobayashi M Yoritsune T Suzuki S Shimizu A Koido A Kawaguchi Y Reproductive behavior of wild medaka in an outdoor pond Nippon Suisan Gakkaishi. 2012 78 922 933 10.2331/suisan.78.922 · DOI
- [18]Parker GA Courtship persistence and female-guarding as male time investment strategies Behavior. 1974 48 157 184 10.1163/156853974X00327 · DOI
- [19]Okuyama T Yokoi S Abe H Isoe Y Suehiro Y Imada H A neural mechanism underlying mating preference for familiar individuals in medaka fish Science. 2014 343 91 94 10.1126/science.1244724 24385628 · DOI
- [20]Hughes KA Du L Rodd FH Reznick DN Familiarity leads to female mate preference for novel males in the guppy, Poecilia reticulata Anim Behav 1999 58 907 916 10.1006/anbe.1999.1225 10512664 · DOI
- [21]Penn D Potts W MHC-disassortative mating preferences reversed by cross-fostering Proc Biol Sci. 1998 265 1299 1306 10.1098/rspb.1998.0433 9718737 PMC1689202 · DOI
- [22]Cheetham SA Thom MD Beynon RJ Hurst JL The effect of familiarity on mate choice 2008 New York Springer
- [23]Senar JC Mateos-Gonzalez F Urive F Arroyo L Familiarity adds to attractiveness in matters of siskin mate choice Proc Biol Sci. 2013 280 20132361 10.1098/rspb.2013.2361 24174112 PMC3826233 · DOI
- [24]Shapiro LE Austin D Ward SE Dewsbury DA Familiarity and female mate choice in 2 species of voles (Microtus-Ochrogaster and Microtus-Montanus) Anim Behav. 1986 34 90 97 10.1016/0003-3472(86)90010-2 · DOI
- [25]Ansai S Sakuma T Yamamoto T Ariga H Uemura N Takahashi R Efficient targeted mutagenesis in medaka using custom-designed transcription activator-like effector nucleases Genetics. 2013 193 739 749 10.1534/genetics.112.147645 23288935 PMC3583995 · DOI
- [26]Ansai S Inohaya K Yoshiura Y Schartl M Uemura N Takahashi R Design, evaluation, and screening methods for efficient targeted mutagenesis with transcription activator-like effector nucleases in medaka Dev Growth Differ. 2014 56 98 107 10.1111/dgd.12104 24286287 · DOI
- [27]Engelhardt A Heistermann M Hodges JK Nürnberg P Niemitz C Determinants of male reproductive success in wild long-tailed macaques (Macaca fascicularis)-male monopolisation, female mate choice or post-copulatory mechanisms? Behav Ecol Sociobiol. 2006 59 740 752 10.1007/s00265-005-0104-x · DOI
- [28]Wong BB Candolin U How is female mate choice affected by male competition? Biol Rev Camb Philos Soc. 2005 80 559 571 10.1017/S1464793105006809 16221329 · DOI
- [30]Mateos C Carranza J Effects of male dominance and courtship display on female choice in the ring-necked pheasant Behav Ecol Sociobiol. 1999 45 235 244 10.1007/s002650050558 · DOI
- [31]Nilsson SÖ Nilsson GE Free choice by female sticklebacks: lack of preference for male dominance traits Can J Zool. 2000 78 1251 1258 10.1139/z00-051 · DOI
- [32]Rich TJ Hurst JL Scent marks as reliable signals of the competitive ability of mates Anim Behav. 1998 56 727 735 10.1006/anbe.1998.0803 9784223 · DOI
- [33]Moore AJ Genetic evidence for the “good genes” process of sexual selection Behav Ecol Sociobiol. 1994 35 235 241 10.1007/BF00170703 · DOI
- [34]Barber I Hoare D Krause J Effects of parasites on fish behavior: a review and evolutionary perspective Rev Fish Biol Fish. 2000 10 131 165 10.1023/A:1016658224470 · DOI
- [35]Birkhead TR Martínez JG Burke T Froman DP Sperm mobility determines the outcome of sperm competition in the domestic fowl Proc Biol Sci. 1999 266 1759 1764 10.1098/rspb.1999.0843 10577160 PMC1690205 · DOI
- [37]Stoltz JA Neff BD Sperm competition in a fish with external fertilization: the contribution of sperm number, speed and length J Evol Biol. 2006 19 1873 81 10.1111/j.1420-9101.2006.01165.x 17040384 · DOI
- [38]Lim MM Wang Z Olazabal DE Ren X Terwilliger EF Young LJ Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene Nature. 2004 429 754 757 10.1038/nature02539 15201909 · DOI · Paper page
- [39]McGraw LA Young LJ The prairie vole: an emerging model organism for understanding the social brain Trends Neurosci. 2010 33 103 109 10.1016/j.tins.2009.11.006 20005580 PMC2822034 · DOI · Paper page
- [40]Imada H Hoki M Suehiro Y Okuyama T Kurabayashi D Shimada A Coordinated and cohesive movement of two small conspecific fish induced by eliciting a simultaneous optomotor response PLoS One 2010 5 e11248 10.1371/journal.pone.0011248 20582314 PMC2889830 · DOI
Cited by
Sorted by citations
Oxytocin, Neural Plasticity, and Social Behavior
Froemke, R. C., & Young, L. J. (2021) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-102320-102847 · Cited by 487 · see citing works
“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).”
BackgroundSelf-citationSocial memory engram in the hippocampus
Okuyama, T. (2018) · Neuroscience Research · doi:10.1016/j.neures.2017.05.007 · Cited by 95 · see citing works
Self-citationSexually dimorphic role of oxytocin in medaka mate choice
Yokoi, S., Naruse, K., Kamei, Y., Ansai, S., Kinoshita, M., Mito, M., Iwasaki, S., Inoue, S., Okuyama, T., Nakagawa, S., et al. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1921446117 · Cited by 62 · see citing works
Self-citation
- Authors
- Yokoi, S., Ansai, S., Kinoshita, M., Naruse, K., Kamei, Y., Young, L. J., Okuyama, T., & Takeuchi, H.
- Affiliations
- National Institute for Basic Biology (JP)
- Kyoto University (JP)
- Emory University (US)
- Massachusetts Institute of Technology (US)
- Okayama University (JP)
- Corresponding author
- Takeuchi, Hideaki
- ORCID
- Venue
- Frontiers in Zoology
- Published
- 2016-06-02
- Volume
- 13
- Issue
- 1
- Pages
- 21-21
- ISSN
- 1742-9994 (ISSN-L)
- PMC
- PMC4890520
- OpenAlex
- W2403507071
- Cited by
- 49
- References
- 0
- Citations by year
- 2026: 8 · 2025: 9 · 2024: 4 · 2023: 6 · 2022: 5 · 2021: 4 · 2020: 6 · 2019: 3 · 2018: 1 · 2017: 3
- FWCI
- 2.56
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Licence
- cc-by
- Locations
- Frontiers in Zoology (publishedVersion, cc-by)
- Europe PMC (PubMed Central) (publishedVersion, cc-by)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- Funders
- JSPS KAKENHI (26290003, 26115508)
- Grant-in-Aid for JSPS Fellows
- Brain Science Foundation
- Yamada Science Foundation
- Topics
- 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
- Social Sciences › Psychology › Social Psychology › Neuroendocrine regulation and behavior
- Keywords
- mate guarding, medaka, female mate preference, male-male competition, sexual selection, male reproductive success, triadic relationships, male dominance
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review