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Monogamy and protandry caused by exclusion of the same sex and random pairing in anemonefishes: a simulation model and aquarium experiments

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Abstract

The size-advantage model predicts that the evolution of protandry (male-to-female sex change) is favored in random mating (lack of female mate choice and/or monopolization of multiple females by large males). All anemonefishes (Amphiprion spp.) are protandrous, yet they have a monogamous mating system. Fricke and Fricke (Nature 266:830–832, 1977) identified two factors that favor the evolution of protandry and monogamy in anemonefishes: (1) random pairing without mate choice, and (2) monogamy caused by a limitation of resources and the inability of homosexual individuals to coexist in a host. To investigate this hypothesis, we developed a mathematical model based on the dynamics among individuals and conducted simulations. The results were consistent with the size-advantage model predicting protandry. Next, we conducted aquarium experiments using A. ocellaris to test the second assumption above, whether males and females are competing each other for mates and spawning sites, respectively. The results support the prediction for males but not for females. Females may compete not for each spawning site but for the entire space covering the sea anemone, suggesting that they cannot coexist in a single host. These findings suggest that intrasexual competition results in monogamy and that, even in pairs that are maintained for a long time, protandry can evolve if random pair formation occurs.

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Acknowledgements

We are grateful to S Tsumura for his valuable advice on rearing A. ocellaris. We also thank S Tomatsu, S Endo, Y Yokokawa, M Sasaki, K Ogiso, and all other members of the Laboratory of Fish Behavioral Ecology for their assistance throughout this study. Thanks are also due to the anonymous reviewers for their valuable advices.

Funding

This work was supported by a JSPS KAKENHI Grant (no. 16K07507) to TS from the Japan Society for the Promotion of Science.

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Author notes

  1. Tetsuo Kuwamura

    Present address: Institute for Research in Social Science, Advanced Collaborative Research Organization of Chukyo University, Yagoto-honmachi, Nagoya, 466-8666, Japan

Authors and Affiliations

  1. Laboratory of Fish Behavioral Ecology, Tateyama Station, Field Science Center, Tokyo University of Marine Science and Technology, Banda, Tateyama, 294-0308, Japan

    Tomoki Sunobe & Chenhao Shi

  2. Department of Marine Biosciences, Tokyo University of Marine Science and Technology, Konan, Minato-ku, 108-8477, Japan

    Shigehide Iwata

  3. Faculty of Liberal Arts and Sciences, Chukyo University, Yagoto-honmachi, Nagoya, 466-8666, Japan

    Tetsuo Kuwamura

Authors
  1. Tomoki Sunobe
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  2. Shigehide Iwata
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  3. Chenhao Shi
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  4. Tetsuo Kuwamura
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Contributions

TK and TS designed the study. SI created a simulation based on the dynamics of individuals. CS and TS collected the data. TS, TK, and SI prepared the manuscript.

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Correspondence to Tomoki Sunobe.

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The authors declare that they have no conflict of interest.

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The experimental protocol in this study was approved by Tokyo University of Marine Science and Technology where the research was conducted, and all procedures were carried out in accordance with approved guidelines.

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Sunobe, T., Iwata, S., Shi, C. et al. Monogamy and protandry caused by exclusion of the same sex and random pairing in anemonefishes: a simulation model and aquarium experiments. J Ethol 40, 265–272 (2022). https://doi.org/10.1007/s10164-022-00759-w

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  • DOI: https://doi.org/10.1007/s10164-022-00759-w

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