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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
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  • Shou-Hsien Li,
  • Yang Liu,
  • Chia-Fen Yeh,
  • Yuchen Fu,
  • Carol K. L. Yeung,
  • Chun-cheng Lee,
  • Chi-Cheng Chiu,
  • Tung Hui Kuo,
  • FT Chan,
  • Yu-Chia Chen,
  • Wen-ya Ko,
  • Chen-te Yao
Shou-Hsien Li
National Taiwan Normal University
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Yang Liu
Sun Yat-sen University
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Chia-Fen Yeh
National Taiwan Normal University
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Carol K. L. Yeung
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Chun-cheng Lee
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Chi-Cheng Chiu
National Taiwan Normal University
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Tung Hui Kuo
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FT Chan
Endemic Species Research Institute
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Yu-Chia Chen
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Chen-te Yao
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Abstract

The long-term persistence of a population which has suffered a bottleneck partly depends on how historical demographic dynamics impacted its genetic diversity and the accumulation of deleterious mutations. Here we provide genomic evidence for the detrimental genetic effect of a recent population bottleneck in the endangered black-faced spoonbill (Platalea minor) even after its rapid population recovery. Our population genomic data suggest that the bird’s effective population size, Ne, had been relatively stable (7,500-9,000) since the end of the last glacial maximum; however, a recent brief yet severe bottleneck (Ne= 20) around the 1940s wiped out more than 99% of its historical Ne in roughly three generations. By comparing it with its sister species, the royal spoonbill (P. regia) whose conservation status is of lesser concern, we found that despite a more than 15-fold population recovery since 1988, genetic drift has led to higher levels of inbreeding (7.4 times more runs of homozygosity longer than 100 Kb) in the black-faced spoonbill than in the royal spoonbill genome. Although the two spoonbills have similar levels of genome-wide nucleotide diversity and heterozygosity, because of relaxed purifying selection, individual black-faced spoonbills carry 3% more nonsynonymous substitutions than royal spoonbills each of which is 7% more deleterious. Our results imply that the persistence of a threatened species cannot be inferred from a recovery in its population. They also highlight the necessity of continually using genomic indices to monitor its genetic health and employing all possible measures to assure its long-term persistence in the ever-changing environment.

Peer review status:IN REVISION

29 Jun 2021Submitted to Molecular Ecology
01 Jul 2021Assigned to Editor
01 Jul 2021Submission Checks Completed
12 Jul 2021Reviewer(s) Assigned
06 Aug 2021Review(s) Completed, Editorial Evaluation Pending
31 Aug 2021Editorial Decision: Revise Minor