Abstract
Cooperative breeding systems, where individuals other than parents assist in raising offspring, have been documented in insects, fish, birds, and mammals. Still, the factors driving the evolution of such complex systems are not fully understood. Here, we report a new example of cooperative breeding in the obligate shell-brooding cichlid fish Neolamprologus meeli from Lake Tanganyika. Field observations revealed that dominant males were either monogamous or polygynous, with each mating with one to four dominant females. Dominant females maintain nests containing one to ten empty gastropod shells used as breeding substrates and shelters. Up to four immature subordinates of either sex lived in these nests. They assisted with territory defense and nest maintenance, the frequency of which was not different from that of the dominants. Parentage analyses showed that most subordinates were the offspring of at least one of the breeders, suggesting that juveniles delay dispersal and help in raising their relatives. The relatedness of subordinates to the breeders declined with increasing body size and was significantly higher to female than to male breeders. These patterns could be caused by extra-pair paternity, between-group dispersal of helpers, or sex differences in breeder turnover. Male helpers were larger than female helpers, and six out of eight dispersed individuals were females, suggesting female-biased dispersal. Because N. meeli is phylogenetically distinct from other cooperatively breeding cichlids, these results contribute to a better understanding of cooperative breeding in fishes and to understanding of the evolution of complex social systems in general.
Significance statement
Cooperatively breeding cichlid fishes of Lake Tanganyika are an excellent model for studying the evolution of social complexity because cooperative breeding evolved at least 5–6 times independently in a small phylogenetic group. Here, we provide a new example of cooperative breeding in the cichlid Neolamprologus meeli. Field observations revealed that these fish were either monogamous or polygynous. Subordinates remained in the breeders’ nests and helped with territory defense and nest maintenance. Subordinates of both sexes were unlikely to participate in reproduction because of their immature gonads. Parentage analyses showed that most helpers and juveniles were offspring of the dominant breeders, suggesting that N. meeli has a kin-structured cooperative breeding system. As N. meeli is phylogenetically distinct from all other cooperatively breeding cichlids, these results pose a hitherto undescribed independent evolutionary event, leading to a highly complex social system.
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Data availability
The dataset generated during the current study is available as supplementary material.
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Acknowledgements
We would like to thank the members of the Maneno Tanganyika Research Team, especially the late Hirokazu Tanaka, who provided constructive feedback during the preliminary field survey of the study, and the staff of the Department of Fisheries, Republic of Zambia, especially Harris Phili, Mbamwai Mbewe, Taylor Banda, and Bumango Musando, for their field support. We thank the anonymous reviewers for their comments on an earlier version of this manuscript and members of the Animal Sociology Laboratory, Osaka City University, for their support throughout the study.
Funding
This study was financially supported by the Japan Society for the Promotion of Science (JSPS) KAKENHI (Grant numbers 20J13379 [to TS], 21K06346 [to SS], 16H05773 and 19H03306 [to MK], and 20KK0168 [to SA]).
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TS, SS, and MK designed the study. TS and SS collected the data. TS, SS, and SA conducted the analyses. TS and SA performed the genetic analyses. TS, SS, and SA wrote the manuscript with significant contributions from JGF. All authors contributed critically to the drafts and approved the manuscript for publication.
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All experimental protocols were approved by the Animal Care and Use Committee of Osaka City University for Advanced Studies, Japan. Our field observations and sampling in Lake Tanganyika as well as the transportation of specimens for DNA analysis were conducted with permission from the Zambian Ministry of Agriculture, Livestock, and Fisheries, and complied with the current laws in Zambia.
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Saeki, T., Satoh, S., Frommen, J.G. et al. Kin-structured cooperatively breeding groups due to limited dispersal in the obligate shell-brooding cichlid Neolamprologus meeli. Behav Ecol Sociobiol 76, 89 (2022). https://doi.org/10.1007/s00265-022-03201-w
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DOI: https://doi.org/10.1007/s00265-022-03201-w