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Journal of Ethology

, Volume 35, Issue 1, pp 137–144 | Cite as

Sex differences in intrasexual aggression among sex-role-reversed, cooperatively breeding cichlid fish Julidochromis regani

  • Munehiko H. ItoEmail author
  • Motoomi Yamaguchi
  • Nobuyuki Kutsukake
Article

Abstract

In sex-role-reversed species, females compete for resources (e.g., mates) more intensively than do males. However, it remains unclear whether these species exhibit sex differences in the intensity of aggressive behavior in the context of within-sex contests. Cichlid fish in the genus Julidochromis exhibit intraspecific variation in mating systems, ranging from monogamy to cooperative polyandry with sex-role reversal. In the study reported here, we observed aggressive interactions among three same-sex individuals in Julidochromis regani in the laboratory and tested whether inter-female aggression was more intense than inter-male aggression. Although difference in body size strongly determined the direction of aggression in fish, aggression by a smaller-sized individuals toward larger ones was occasionally observed. This type of aggression was common between individuals of a similar body size (≤5 mm) and occurred more frequently among females than males. In contrast, differences in body size and sex did not affect the frequency of aggression by larger-sized individuals against smaller ones. Bidirectional aggression (i.e., mouth fighting) occurred frequently when two individuals had similar body size, and there was no difference in its frequency between sexes. However, temporal analysis showed that females performed bidirectional aggression more persistently than males. These sex differences in the intensity of intrasexual aggression could be the behavioral mechanisms underpinning cooperative polyandry.

Keywords

Aggression Sex difference Sex-role reversal Cooperative breeding Cichlid fish Julidochromi

Notes

Acknowledgements

We thank members of the Evolutionary and Behavioral Ecology Group in SOKENDAI for their discussions and valuable comments. We also thank Dr. Satoshi Awata for providing information on wild J. regani and Ken Nagata for programming advice.

References

  1. Andersson MB (1994) Sexual selection. Princeton University Press, PrincetonGoogle Scholar
  2. Arnott G, Elwood RW (2009) Assessment of fighting ability in animal contests. Anim Behav 77:991–1004CrossRefGoogle Scholar
  3. Awata S, Kohda M (2004) Parental roles and the amount of care in a bi-parental substrate brooding cichlid: the effect of size differences within pairs. Behaviour 141:1135–1149CrossRefGoogle Scholar
  4. Awata S, Munehara H, Kohda M (2005) Social system and reproduction of helpers in a cooperatively breeding cichlid fish (Julidochromis ornatus) in Lake Tanganyika: field observations and parentage analyses. Behav Ecol Sociobiol 58:506–516CrossRefGoogle Scholar
  5. Awata S, Takeuchi H, Kohda M (2006) The effect of body size on mating system and parental roles in a biparental cichlid fish (Julidochromis transcriptus): a preliminary laboratory experiment. J Ethol 24:125–132CrossRefGoogle Scholar
  6. Axelrod HR (1996) The most complete colored lexicon of cichlids: every known cichlid illustrated in color, 2nd edn. T.F.H Publications, NeptuneGoogle Scholar
  7. Barlow GW, Lee JS (2005) Sex-reversed dominance and aggression in the cichlid fish Julidochromis marlieri. Ann Zool Fenn 42:1–7Google Scholar
  8. Bollmer JL, Sanchez T, Cannon MD, Sanchez D, Cannon B, Bednarz JC, Tjitte de Vries M, Struve Susana, Parker PG (2003) Variation in morphology and mating system among island populations of Galápagos hawks. Condor 105:428–438CrossRefGoogle Scholar
  9. Bruintjes R, Heg-Bachar Z, Heg D (2013) Subordinate removal affects parental investment, but not offspring survival in a cooperative cichlid. Funct Ecol 27:730–738CrossRefGoogle Scholar
  10. Cant MA, Johnstone RA (2000) Power struggles, dominance testing, and reproductive skew. Am Nat 155:406–417CrossRefPubMedGoogle Scholar
  11. Clutton-Brock T (2007) Sexual selection in males and females. Science 318:1882–1885CrossRefPubMedGoogle Scholar
  12. Clutton-Brock TH, Parker GA (1995) Sexual coercion in animal societies. Anim Behav 49:1345–1365CrossRefGoogle Scholar
  13. Clutton-Brock TH, Hodge SJ, Spong G, Russell AF, Jordan NR, Bennett NC, Sharpe LL, Manser MB (2006) Intrasexual competition and sexual selection in cooperative mammals. Nature 444:1065–1068CrossRefPubMedGoogle Scholar
  14. Davies NB (1992) Dunnock behaviour and social evolution. Oxford University Press, OxfordGoogle Scholar
  15. Dey CJ, Reddon AR, O’Connor CM, Balshine S (2013) Network structure is related to social conflict in a cooperatively breeding fish. Anim Behav 85:395–402CrossRefGoogle Scholar
  16. Draud M, Lynch PA (2002) Asymmetric contests for breeding sites between monogamous pairs of convict cichlids (Archocentrus nigrofasciatum, Cichlidae): pair experience pays. Behaviour 139:861–873CrossRefGoogle Scholar
  17. Emlen ST, Wrege PH (2004) Size dimorphism, intrasexual competition, and sexual selection in Wattled jacana (Jacana jacana), a sex-role-reversed shorebird in Panama. Auk 121:391–403Google Scholar
  18. Emlen ST, Demong NJ, Emlen DJ (1989) Experimental induction of infanticide in female wattled jacanas. Auk 106:1–7CrossRefGoogle Scholar
  19. Faaborg J, Patterson CB (1981) The characteristics and occurrence of cooperative polyandry. Ibis 123:477–484CrossRefGoogle Scholar
  20. Heg D, Bachar Z (2006) Cooperative breeding in the Lake Tanganyika cichlid Julidochromis ornatus. Environ Biol Fishes 76:265–281CrossRefGoogle Scholar
  21. Hotta T, Takeyama T, Jordan LA, Kohda M (2014) Duration of memory of dominance relationships in a group living cichlid. Naturwissenschaften 101:745–751CrossRefPubMedGoogle Scholar
  22. Kokko H, Jennions MD (2008) Parental investment, sexual selection and sex ratios. J Evol Biol 21:919–948CrossRefPubMedGoogle Scholar
  23. Kutsukake N, Clutton-Brock TH (2006) Aggression and submission reflect reproductive conflict between females in cooperatively breeding meerkats Suricata suricatta. Behav Ecol Sociobiol 59:541–548CrossRefGoogle Scholar
  24. Neat FC, Huntingford FA, Beveridge MM (1998) Fighting and assessment in male cichlid fish: the effects of asymmetries in gonadal state and body size. Anim Behav 55:883–891CrossRefPubMedGoogle Scholar
  25. Owens IP, Hartley IR (1998) Sexual dimorphism in birds: why are there so many different forms of dimorphism? Proc R Soc Lond B 265:397–407CrossRefGoogle Scholar
  26. Owens IP, Burke T, Thompson DB (1994) Extraordinary sex roles in the Eurasian dotterel: female mating arenas, female-female competition, and female mate choice. Am Nat 144:76–100CrossRefGoogle Scholar
  27. Reddon AR, Voisin MR, Menon N, Marsh-Rollo SE, Wong MY, Balshine S (2011) Rules of engagement for resource contests in a social fish. Anim Behav 82:93–99CrossRefGoogle Scholar
  28. Reeve HK, Ratnieks FLW (1993) Queen–queen conflicts in polygynous societies: mutual tolerance and reproductive skew. In: Keller L (ed) Queen number and sociality in insects. Oxford University Press, Oxford, pp 45–85Google Scholar
  29. Rubenstein DR, Lovette IJ (2009) Reproductive skew and selection on female ornamentation in social species. Nature 462:786–789CrossRefPubMedGoogle Scholar
  30. Schumer M, Krishnakant K, Renn SC (2011) Comparative gene expression profiles for highly similar aggressive phenotypes in male and female cichlid fishes (Julidochromis). J Exp Biol 214:3269–3278CrossRefPubMedPubMedCentralGoogle Scholar
  31. Shuster S, Wade MJ (2003) Mating systems and strategies. Princeton University Press, PrincetonGoogle Scholar
  32. Sturmbauer C, Verheyen E, Meyer A (1994) Mitochondrial phylogeny of the Lamprologini, the major substrate spawning lineage of cichild fishes from Lake Tanganyika in eastern Africa. Mol Biol Evol 11:691–703PubMedGoogle Scholar
  33. Sturmbauer C, Salzburger W, Duftner N, Schelly R, Koblmüller S (2010) Evolutionary history of the Lake Tanganyika cichlid tribe Lamprologini (Teleostei: Perciformes) derived from mitochondrial and nuclear DNA data. Mol Phylogenet Evol 57:266–284CrossRefPubMedPubMedCentralGoogle Scholar
  34. Sunobe T (2000) Social structure, nest guarding and interspecific relationships of the cichild fish (Julidochromis marlieri) in Lake Tanganyika. Afr Stud Monogr 21:83–89Google Scholar
  35. Tashiro F (2011) Taxonomic revision of the Lamprologine fishes of the genera Julidochromis and Chalinochromis from Lake Tanganyika in East Africa (Perciformes: Cichlidae). PhD thesis. Hokkaido University, SapporoGoogle Scholar
  36. Tobias JA, Montgomerie R, Lyon BE (2012) The evolution of female ornaments and weaponry: social selection, sexual selection and ecological competition. Phil Trans R Soc B 367:2274–2293CrossRefPubMedPubMedCentralGoogle Scholar
  37. Trivers RL (1972) Parental investment and sexual selection. In: Campbell B (ed) Sexual selection and the descent of man. Aldinc, Chicago, pp 136–179Google Scholar
  38. Werner NY, Balshine S, Leach B, Lotem A (2003) Helping opportunities and space segregation in cooperatively breeding cichlids. Behav Ecol 14:749–756CrossRefGoogle Scholar
  39. Wood KJ, Zero VH, Jones A, Renn SC (2014) Social reversal of sex-biased aggression and dominance in a biparental cichlid fish (Julidochromis marlieri). Ethology 120:540–550CrossRefGoogle Scholar
  40. Yamagishi S, Kohda M (1996) Is the cichlid fish Julidochromis marlieri polyandrous? Ichthyol Res 43:469–471CrossRefGoogle Scholar
  41. Young AJ, Carlson AA, Monfort SL, Russell AF, Bennett NC, Clutton-Brock T (2006) Stress and the suppression of subordinate reproduction in cooperatively breeding meerkats. Proc Natl Acad Sci USA 103:12005–12010CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Japan Ethological Society and Springer Japan 2016

Authors and Affiliations

  • Munehiko H. Ito
    • 1
    Email author
  • Motoomi Yamaguchi
    • 1
  • Nobuyuki Kutsukake
    • 1
  1. 1.Department of Evolutionary Studies of Biosystems, School of Advanced SciencesSOKENDAI (The Graduate University for Advanced Studies)Hayama-machi, MiuragunJapan

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