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Inbreeding and demography interact to impact the recovery of a bottlenecked crested ibis population

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Abstract

Biodiversity loss driven by climate change and human activities poses a critical global challenge. Population restoration and reintroduction programs are essential for mitigating this threat to endangered species, yet their outcomes often remain unpredictable due to poorly understood success factors, such as the inevitable inbreeding during bottleneck events. The conservation programme of the crested ibis (Nipponia nippon) marks a successful example where the population rose from just seven individuals to over 9000 in the past four decades. By developing an individual-based model that simulates the restoration process and incorporates species-specific demography and inbreeding data, we conclude that this successful restoration is largely deterministic, as our results closely mirror empirical recovery time and population-level inbreeding coefficients. To establish general guidelines for reintroduction programs, we compare how inbreeding depression influences the recovery success of two reintroduction strategies involving small founder populations. Our simulations reveal that the ‘firework’ approach (one-source translocations) outperforms the ‘sequential’ (serial translocations) approach in restoration effectiveness. Furthermore, by expanding analyses over a broad demographic space, we demonstrate that the net effect of inbreeding varies with species-specific demography and highlight the importance of considering their interaction when interpreting conservation outcomes and designing future reintroduction programs.

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Data availability

All simulation outcomes and empirical data used for producing the results in this study have been deposited in the Zenodo repository: https://doi.org/10.5281/zenodo.18049101.

Code availability

All simulation and analysis codes supporting the findings of this study are accessible on Zenodo: https://doi.org/10.5281/zenodo.18049101.

References

  1. IUCN, The IUCN Red List of Threatened Species. Version 2024-2. 2024. Accessed on 01.10.2024. https://www.iucnredlist.org.

  2. Conference of the Parties to the Convention on Biological Diversity (COP15), Kunming–Montreal Global Biodiversity Framework. Decision 15/4 adopted 19 December 2022, UN, symbol CBD/COP/DEC/15/4 (2022).

  3. Kardos, M. et al. Inbreeding depression explains killer whale population dynamics. Nat. Ecol. Evol. 7, 675–686 (2023).

    Google Scholar 

  4. Jamieson, I. G. Founder effects, inbreeding, and loss of genetic diversity in four avian reintroduction programs. Conserv. Biol. 25, 115–123 (2011).

    Google Scholar 

  5. Hedrick, P. W. A. Garcia-Dorado, Understanding inbreeding depression, purging, and genetic rescue. Trends Ecol. Evol. 31, 940–952 (2016).

    Google Scholar 

  6. Bozzuto, C., Biebach, I., Muff, S., Ives, A. R. & Keller, L. F. Inbreeding reduces long-term growth of Alpine ibex populations. Nat. Ecol. Evol. 3, 1359–1364 (2019).

    Google Scholar 

  7. Griffith, B., Scott, J. M., Carpenter, J. W. & Reed, C. Translocation as a species conservation tool: status and strategy. Science 245, 477–480 (1989).

    Google Scholar 

  8. Sarrazin, F. & Barbault, R. Reintroduction: challenges and lessons for basic ecology. Trends Ecol. Evol. 11, 474–478 (1996).

    Google Scholar 

  9. Fischer, J. & Lindenmayer, D. B. Small patches can be valuable for biodiversity conservation: two case studies on birds in southeastern Australia. Biol. Conserv. 106, 129–136 (2002).

    Google Scholar 

  10. Ewen, J. G., Armstrong, D. P., Parker, K. A. & Seddon, P. J. Reintroduction Biology: Integrating Science and Management. (John Wiley & Sons, 2012).

  11. Jachowski, D.S., Millspaugh, J.J., Angermeier, P.L. & Slotow, R. Reintroduction of Fish and Wildlife Populations. (University of California Press, 2016).

  12. Grossen, C., Biebach, I., Angelone-Alasaad, S., Keller, L. F. & Croll, D. Population genomics analyses of European ibex species show lower diversity and higher inbreeding in reintroduced populations. Evol. Appl. 11, 123–139 (2018).

    Google Scholar 

  13. Schaub, M., Zink, R., Beissmann, H., Sarrazin, F. & Arlettaz, R. When to end releases in reintroduction programmes: demographic rates and population viability analysis of bearded vultures in the Alps. J. Appl. Ecol. 46, 92–100 (2009).

    Google Scholar 

  14. Ashbrook, K., Taylor, A., Jane, L., Carter, I. & Székely, T. Impacts of survival and reproductive success on the long-term population viability of reintroduced great bustards UK. Oryx 50, 583–592 (2016).

    Google Scholar 

  15. Burt, A. J. et al. The history, status and trends of the endangered Seychelles Magpie-robin Copsychus sechellarum. Bird. Conserv. Int. 26, 505–523 (2016).

    Google Scholar 

  16. Wakamiya, S. M. & Roy, C. L. Use of monitoring data and population viability analysis to inform reintroduction decisions: peregrine falcons in the Midwestern United States. Biol. Conserv. 142, 1767–1776 (2009).

    Google Scholar 

  17. Ewing, S. R., Nager, R. G., Nicoll, M. A. C., Aumjaud, A., Jones, C. G. & Keller, L. F. Inbreeding and loss of genetic variation in a reintroduced population of Mauritius kestrel. Conserv. Biol. 22, 395–404 (2008).

    Google Scholar 

  18. Armstrong, D. P. & Seddon, P. J. Directions in reintroduction biology. Trends Ecol. Evol. 23, 20–25 (2008).

    Google Scholar 

  19. Velando, A., Barros, Á & Moran, P. Heterozygosity–fitness correlations in a declining seabird population. Mol. Ecol. 24, 1007–1018 (2015).

    Google Scholar 

  20. Aisya, Z., White, D. J., Thavornkanlapachai, R., Friend, J. A., Rick, K. & Mitchell, N. J. Using PVA and captive breeding to balance trade-offs in the rescue of the island dibbler onto a new island ark. Sci. Rep. 12, 11913 (2022).

    Google Scholar 

  21. Sun, L., Zhou, T., Wan, Q.-H. & Fang, S.-G. Transcriptome comparison reveals key components of nuptial plumage coloration in crested ibis. Biomolecules 10, 905 (2020).

    Google Scholar 

  22. Soulé, M.E. & Wilcox, B.A. Conservation Biology. An Evolutionary-ecological Perspective. (University of California, San Diego, 1980).

  23. Taylor, H. R., Colbourne, R. M., Robertson, H. A., Nelson, N. J., Allendorf, F. W. & Ramstad, K. M. Cryptic inbreeding depression in a growing population of a long-lived species. Mol. Ecol. 26, 799–813 (2017).

    Google Scholar 

  24. Robinson, J. A. et al. The critically endangered vaquita is not doomed to extinction by inbreeding depression. Science 376, 635–639 (2022).

    Google Scholar 

  25. Brekke, P., Bennett, P. M., Wang, J., Pettorelli, N. & Ewen, J. G. Sensitive males: inbreeding depression in an endangered bird. Proc. R. Soc. B 277, 3677–3684 (2010).

    Google Scholar 

  26. Ahlinder, J., Giles, B. E. & García-Gil, M. R. Life stage-specific inbreeding depression in long-lived Pinaceae species depends on population connectivity. Sci. Rep. 11, 8834 (2021).

    Google Scholar 

  27. Huisman, J., Kruuk, L. E. B., Ellis, P. A., Clutton-Brock, T. & Pemberton, J. M. Inbreeding depression across the lifespan in a wild mammal population. Proc. Natl. Acad. Sci. USA 113, 3585–3590 (2016).

    Google Scholar 

  28. Hoeck, P. E. A., Wolak, M. E., Switzer, R. A., Kuehler, C. M. & Lieberman, A. A. Effects of inbreeding and parental incubation on captive breeding success in Hawaiian crows. Biol. Conserv. 184, 357–364 (2015).

    Google Scholar 

  29. Bichet, C. et al. Contrasting heterozygosity-fitness correlations across life in a long-lived seabird. Mol. Ecol. 28, 671–685 (2019).

    Google Scholar 

  30. Szulkin, M., Garant, D., McCleery, R. H. & Sheldon, B. C. Inbreeding depression along a life-history continuum in the great tit. J. Evol. Biol. 20, 1531–1543 (2007).

    Google Scholar 

  31. Kardos, M., Keller, L.F. & Funk, W.C. What can genome sequence data reveal about population viability? Mol. Ecol. 34, e17608 (2024).

  32. Li, S.-H., Liu, Y. et al. Not out of the woods yet: signatures of the prolonged negative genetic consequences of a population bottleneck in a rapidly re-expanding wader, the black-faced spoonbill Platalea minor. Mol. Ecol. 31, 529–545 (2022).

    Google Scholar 

  33. Harrisson, K. A. et al. Lifetime fitness costs of inbreeding and being inbred in a critically endangered bird. Curr. Biol. 29, 2711–2717 (2019).

    Google Scholar 

  34. Stock, S. E. et al. Uncovering inbreeding, small populations, and strong genetic isolation in an Australian threatened frog, Litoria littlejohni. Conserv. Genet. 24, 575–588 (2023).

    Google Scholar 

  35. Shi, D. The description of the decline of the crested ibis. J. Northwest Univ. 21, 25–30 (1991).

    Google Scholar 

  36. The State Council Information Office, People’s Republic of China, Global population of crested ibises exceeds 9000. http://english.scio.gov.cn/pressroom/2022-12/06/content_78553054.htm (2022).

  37. Ma, L. et al. Changes in the habitat preference of crested ibis Nipponia nippon) during a Period of Rapid Population Increase. Animals 11, 2626 (2021).

    Google Scholar 

  38. Kekkonen, J., Wikström, M. & Brommer, J. E. Heterozygosity in an isolated population of a large mammal founded by four individuals is predicted by an individual-based genetic model. PLoS ONE 7, e43482 (2012).

    Google Scholar 

  39. Slate, J., Kruuk, L. E. B., Marshall, T. C., Pemberton, J. M. & Clutton-Brock, T. H. Inbreeding depression influences lifetime breeding success in a wild population of red deer (Cervus elaphus). Proc. R. Soc. B 267, 1657–1662 (2000).

    Google Scholar 

  40. Zheng, J. Dataset: Inbreeding and demography interact to impact population recovery from bottlenecks. Zenodo. https://doi.org/10.5281/zenodo.15813368 (2025).

  41. Bell, D. A., Kovach, R. P., Robinson, Z. L., Whiteley, A. R. & Reed, T. The ecological causes and consequences of hard and soft selection. Ecol. Lett. 24, 1505–1521 (2021).

    Google Scholar 

  42. Green, R. E., Pienkowski, M. W. & Love, J. A. Long-term viability of the re-introduced population of the white-tailed eagle Haliaeetus albicilla in Scotland. J. Appl. Ecol. 33, 357–368 (1996).

    Google Scholar 

  43. Evans, R. J. et al. Growth and demography of a re-introduced population of White-tailed Eagles Haliaeetus albicilla. Ibis 151, 244–254 (2009).

    Google Scholar 

  44. Thevenon, S. & Couvet, D. The impact of inbreeding depression on population survival depending on demographic parameters. Anim. Conserv. 5, 53–60 (2002).

    Google Scholar 

  45. Lambert, D. M. et al. Serial population bottlenecks and genetic variation: translocated populations of the New Zealand saddleback (Philesturnus carunculatus rufusater). Conserv. Genet. 6, 1–14 (2005).

    Google Scholar 

  46. Parker, K. A., Anderson, M. J., Jenkins, P. F. & Brunton, D. H. The effects of translocation-induced isolation and fragmentation on the cultural evolution of bird song. Ecol. Lett. 15, 778–785 (2012).

    Google Scholar 

  47. Gautschi, B., Widmer, A., Joshi, J. & Koella, J. C. Increased frequency of scale anomalies and loss of genetic variation in serially bottlenecked populations of the dice snake, Natrix tessellata. Conserv. Genet. 3, 235–245 (2002).

    Google Scholar 

  48. Sutton, A. E. Leadership and management influences the outcome of wildlife reintroduction programs: findings from the Sea Eagle Recovery Project. PeerJ 3, e1012 (2015).

    Google Scholar 

  49. Sutherland, W. J. et al. Conserv. Lett. 3, 229–235 (2010).

    Google Scholar 

  50. Nabutanyi, P. & Wittmann, M. J. Models for eco-evolutionary extinction vortices under balancing selection. Am. Nat. 197, 336–350 (2021).

    Google Scholar 

  51. Li, X. et al. Understanding recovery is as important as understanding decline: The case of the crested ibis in China. Land 11, 1817 (2022).

    Google Scholar 

  52. Bozzuto, C., Hoeck, P. E. A., Bagheri, H. C. & Keller, L. F. Modelling different reintroduction strategies for the critically endangered Floreana mockingbird. Anim. Conserv. 20, 144–154 (2017).

    Google Scholar 

  53. Hernández, F., Janzen, T. & Lavretsky, P. simRestore: a decision-making tool for adaptive management of the native genetic status of wild populations. Mol. Ecol. Resour. 24, e13892 (2024).

    Google Scholar 

  54. Deredec, A. & Courchamp, F. Importance of the Allee effect for reintroductions. Ecoscience 14, 440–451 (2007).

    Google Scholar 

  55. Armstrong, D. P. & Wittmer, H. U. Incorporating Allee effects into reintroduction strategies. Ecol. Res. 26, 687–695 (2011).

    Google Scholar 

  56. Li, M. et al. Impact of Allee effects on the establishment of reintroduction populations of endangered species: The case of the Crested Ibis. Glob. Ecol. Conserv. 35, e02103 (2022).

    Google Scholar 

  57. BirdLife International, Nipponia nippon The IUCN Red List of Threatened Species, 2025-1, https://doi.org/10.2305/IUCN.UK.2018-2.RLTS.T22697548A132069229.en (2025).

  58. Liu, Y. Z. Rediscovery of crested ibis Nipponia nippon in Qinling Mountain. Chin. J. Zool. 27, 237 (1981).

    Google Scholar 

  59. Morrissey, M. B. & Wilson, A. J. Pedantics: an R package for pedigree-based genetic simulation and pedigree manipulation, characterization and viewing. Mol. Ecol. Resour. 10, 711–719 (2010).

    Google Scholar 

  60. Laake, J. R. Mark: an R interface for analysis of capture-recapture data with MARK. AFSC Processed Rep., Alaska Fish. Sci. Cent., NOAA, Natl. Mar. Fish. Serv., Seattle, WA (2013).

  61. R Core Team, R: A Language and Environment for Statistical Computing. (R Foundation for Statistical Computing, Vienna, Austria, 2024).

  62. Emik, L. O. & Terrill, C. E. Systematic procedures for calculating inbreeding coefficients. J. Hered. 40, 51–55 (1949).

    Google Scholar 

  63. Gill, F., Donsker, D. & Rasmussen, P. IOC World Bird List (v15.1). https://www.worldbirdnames.org/new/bow/ (2025).

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Acknowledgements

We acknowledge funding from the National Natural Science Foundation of China (32301290 to J.Z., 32570596 to D.W., 32125005 to X.Z.), the International Exchange and Talent Recruitment Programme of the Postdoctoral Management Committee (339478 to J.Z.), the Institute of Zoology, Chinese Academy of Sciences (2023IOZ0104 and 2024IOZ0107) and National Key Program of Research and Development, Ministry of Science and Technology of China (2023YFF1304800) to D.W., International Partnership Programme of Chinese Academy of Sciences for Grand Challenges (073GJHZ2023091GC), Joint Research Unit of Chinese Academy of Sciences (JRU CAS:152111ZYLH20250004) to X.Z., and the Swiss National Science Foundation (211549) to X-Y.L.R. We thank Dongzhai National Nature Reserve for providing us with the conservation data of the captive crested ibis and the research permit for this species. We thank the Centre for Information Technology of the University of Groningen for their support and for providing access to the Hábrók high-performance computing cluster. We also thank Stefano Canessa for insightful discussions.

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Authors and Affiliations

  1. Ministry of Education Key Laboratory for Biodiversity Sciences and Ecological Engineering, College of Life Sciences, Beijing Normal University, Beijing, China

    Jia Zheng & Zhengwang Zhang

  2. Institute of Ecology and Evolution, University of Bern, Bern, Switzerland

    Jia Zheng, Ella Rees-Baylis & Xiang-Yi Li Richter

  3. Groningen Institute for Evolutionary Life Sciences, University of Groningen, Groningen, The Netherlands

    Thijs Janzen

  4. State Key Laboratory of Animal Biodiversity Conservation and Integrated Pest Management, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

    Daiping Wang & Xiangjiang Zhan

  5. Key Laboratory of Animal Ecology and Conservation Biology, Institute of Zoology, Chinese Academy of Sciences, Beijing, China

    Daiping Wang & Xiangjiang Zhan

  6. Cardiff University – Institute of Zoology Joint Laboratory for Biocomplexity Research, Chinese Academy of Sciences, Beijing, China

    Daiping Wang & Xiangjiang Zhan

  7. Department of Biology, University of Konstanz, Konstanz, Germany

    Xiang-Yi Li Richter

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  1. Jia Zheng
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Contributions

J.Z. designed and implemented the model, produced the main results, and wrote the first draft of the manuscript; E.R-B. collected and analysed species demographic data; T. J. participated in model design and implementation; Z.Z., X.Z., D.W. initiated project conceptualisation, provided empirical data; X-Y.L.R. supervised model development and data visualisation. All authors contributed to the paper writing.

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Daiping Wang, Zhengwang Zhang or Xiangjiang Zhan.

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Nature Communications thanks George Olah, Lukas Keller and Marty Kardos for their contribution to the peer review of this work. A peer review file is available.”

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Zheng, J., Rees-Baylis, E., Janzen, T. et al. Inbreeding and demography interact to impact the recovery of a bottlenecked crested ibis population.
Nat Commun (2026). https://doi.org/10.1038/s41467-026-69278-3

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