Drastic population fluctuations explain the rapid extinction of the passenger pigeon
- aDepartment of Life Science and
- dDepartment of Computer Science and Information Engineering, National Taiwan Normal University, Taipei 116, Taiwan;
- bDepartment of Ecology, Evolution, and Behavior, and Bell Museum, University of Minnesota, St. Paul, MN 55108;
- cInstitute of Statistical Science, Academia Sinica, Taipei 11529, Taiwan;
- eDepartment of Biology, National Museum of Natural Science, Taichung 404, Taiwan; and
- fDepartment of Life Sciences, National Chung Hsing University, Taichung 402, Taiwan
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Edited by Wen-Hsiung Li, University of Chicago, Chicago, IL, and approved May 27, 2014 (received for review January 24, 2014)

Significance
The number of passenger pigeons went from billions to zero in mere decades, in contrast to conventional wisdom that enormous population size provides a buffer against extinction. Our understanding of the passenger pigeon’s extinction, however, has been limited by a lack of knowledge of its long-term population history. Here we use both genomic and ecological analyses to show that the passenger pigeon was not always super abundant, but experienced dramatic population fluctuations, which could increase its vulnerability to human exploitation. Our study demonstrates that high-throughput–based ancient DNA analyses combined with ecological niche modeling can provide evidence allowing us to assess factors that led to the surprisingly rapid demise of the passenger pigeon.
Abstract
To assess the role of human disturbances in species’ extinction requires an understanding of the species population history before human impact. The passenger pigeon was once the most abundant bird in the world, with a population size estimated at 3–5 billion in the 1800s; its abrupt extinction in 1914 raises the question of how such an abundant bird could have been driven to extinction in mere decades. Although human exploitation is often blamed, the role of natural population dynamics in the passenger pigeon’s extinction remains unexplored. Applying high-throughput sequencing technologies to obtain sequences from most of the genome, we calculated that the passenger pigeon’s effective population size throughout the last million years was persistently about 1/10,000 of the 1800’s estimated number of individuals, a ratio 1,000-times lower than typically found. This result suggests that the passenger pigeon was not always super abundant but experienced dramatic population fluctuations, resembling those of an “outbreak” species. Ecological niche models supported inference of drastic changes in the extent of its breeding range over the last glacial–interglacial cycle. An estimate of acorn-based carrying capacity during the past 21,000 y showed great year-to-year variations. Based on our results, we hypothesize that ecological conditions that dramatically reduced population size under natural conditions could have interacted with human exploitation in causing the passenger pigeon’s rapid demise. Our study illustrates that even species as abundant as the passenger pigeon can be vulnerable to human threats if they are subject to dramatic population fluctuations, and provides a new perspective on the greatest human-caused extinction in recorded history.
Footnotes
↵1C.-M.H. and P.-J.L.S. contributed equally to this work.
- ↵2To whom correspondence may be addressed. E-mail: wshuang{at}mail.nmns.edu.tw or t43028{at}ntnu.edu.tw.
Author contributions: C.-M.H., P.-J.L.S., R.M.Z., and S.-H.L. designed research; C.-M.H., P.-J.L.S., R.M.Z., and S.-H.L. performed research; W.-S.H. and S.-H.L. contributed new reagents/analytic tools; C.-M.H., P.-J.L.S., W.-C.L., and T.-C.C. analyzed data; and C.-M.H., P.-J.L.S., R.M.Z., W.-S.H., and S.-H.L. wrote the paper.
The authors declare no conflict of interest.
This article is a PNAS Direct Submission.
Data deposition: The sequences reported in this paper have been deposited in the GenBank database (accession no. SRP042357).
See Commentary on page 10400.
This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10.1073/pnas.1401526111/-/DCSupplemental.
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