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No evidence for heritability of extra-pair mating behavior in a cooperatively breeding bird

Heredity (2025)Cite this article

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Abstract

While extra-pair mating prevails among socially monogamous birds, it does not occur in all individuals within a population. Then, what underlies this variability? A poorly explored mechanism is the genetic contribution to the behavioral trait, especially for cooperatively breeding species where promiscuity may potentially conflict with the acquisition of indirect benefits to altruistic helpers. We addressed the gap through a quantitative genetic approach with 8 years of data from an individually marked population of Tibetan ground tits (Pseudopodoces humilis). Extra-pair mating was observed in 33.2% of nests, and cooperative breeding occurred in 39.5% of nests. Animal models demonstrated no significant genetic component contributing to the variance in extra-pair mating both during a specific year and over an individual’s lifetime. Consequently, the heritabilities were not significantly different from zero. The lack of heritable variation in extra-pair mating can be accounted for by Fisher’s fundamental theorem of natural selection, which suggests that genotypes associated with this behavior facilitating reproductive success should have become widespread within the population. Furthermore, the fitness benefits derived from promiscuity were greater for breeders than those from receiving help; for helpers, the fitness benefits from extra-pair mating outweighed the indirect genetic benefits obtained from providing help. This may explain why extra-pair mating and cooperative breeding can coexist in the same population. Our findings imply that individual variation in performing extra-pair mating behavior is more likely to be influenced by environmental factors.

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Fig. 1: Comparisons of annual fitness benefits (mean + SE, sample sizes are provided above bars) between ground tit individuals with different social statuses.

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Data availability

Data used in this study are available in the Figshare Digital Repository (https://figshare.com/s/27576e52c169c120418e).

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Acknowledgements

We thank the past and present members of Ornithology Lab at Wuhan University for their field and laboratory work. We thank Dr. Daiping Wang for valuable suggestions on the earlier draft of this manuscript.

Funding

This work was supported by the National Natural Science Foundation of China (No. 31830085) and the Second Tibetan Plateau Scientific Expedition and Research Program (No. 2019QZKK0501).

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Authors and Affiliations

  1. Key Laboratory of Biodiversity and Environment on the Qinghai-Tibetan Plateau of the Ministry of Education, College of Life Sciences, Wuhan University, Wuhan, China

    Sai Wei, Zhibing Li & Xin Lu

  2. Department of Ecology, College of Life Sciences, Henan Normal University, Xinxiang, China

    Zhibing Li & Xin Lu

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  1. Sai Wei
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  2. Zhibing Li
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  3. Xin Lu
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Correspondence to Xin Lu.

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Ethics

Our study was approved by the Law of the People’s Republic of China on the Protection of Wildlife (reference 19881108) and Provisions of the Tibet Autonomous Region for the Protection of Wild Animals and Wild Plants (reference 20091001). The field protocol had no adverse effects on reproduction of the birds.

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Wei, S., Li, Z. & Lu, X. No evidence for heritability of extra-pair mating behavior in a cooperatively breeding bird. Heredity (2025). https://doi.org/10.1038/s41437-025-00796-4

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