Metapopulation extinction caused by mutation accumulation

February 20, 2001
98 (5) 2928-2933

Abstract

Theory suggests that the risk of extinction by mutation accumulation can be comparable to that by environmental stochasticity for an isolated population smaller than a few thousand individuals. Here we show that metapopulation structure, habitat loss or fragmentation, and environmental stochasticity can be expected to greatly accelerate the accumulation of mildly deleterious mutations, lowering the genetic effective size to such a degree that even large metapopulations may be at risk of extinction. Because of mutation accumulation, viable metapopulations may need to be far larger and better connected than would be required under just stochastic demography.

Continue Reading

Acknowledgments

We thank C. Baer, J. Colbourne, J. Conery, J. F. Crow, R. Lande, M. O'Hely, I. Saccheri, and M. Sherrill for their valuable help with this research. Research funding was provided by a National Science Foundation Postdoctoral Research Fellowship in Biosciences Related to the Environment (DBI-9804267), with additional funding provided by the Oregon Department of Fish and Wildlife, the National Institutes of Health, and the Academy of Finland.

References

1
M Kimura, T Maruyama, J F Crow Genetics 48, 1303–1312 (1963).
2
J B S Haldane Am Nat 71, 337–349 (1937).
3
H J Muller Am J Hum Genet 2, 111–176 (1950).
4
B Wallace J Hered 78, 134–142 (1987).
5
M Lynch, W Gabriel Evolution (Lawrence, KS) 44, 1725–1737 (1990).
6
F A Hopf, R E Michod, M J Sanderson Theor Popul Biol 33, 243–265 (1988).
7
W Gabriel, M Lynch, R Bürger Evolution (Lawrence, KS) 47, 1744–1757 (1993).
8
R Lande Evolution (Lawrence, KS) 48, 1460–1469 (1994).
9
W Gabriel, R Bürger Conservation Genetics, eds V Loeschcke, J Tomiuk, S K Jain (Birkhäuser, Basel), pp. 69–84 (1994).
10
M Lynch, J Conery, R Bürger Am Nat 146, 489–518 (1995).
11
M Lynch, J Conery, R Bürger Evolution (Lawrence, KS) 49, 1067–1080 (1995).
12
R Lande Conserv Biol 9, 782–791 (1995).
13
R Lande Res Popul Ecol 40, 259–269 (1998).
14
S Wright Evolution and the Genetics of Populations; a Treatise (Univ. of Chicago Press, Chicago) 3, 485 (1977).
15
J F Crow Oxford Surveys in Evolutionary Biology, eds D Futuyma, J Antonovics (Oxford Univ. Press, Oxford, U.K.) 9, 3–42 (1993).
16
R Lande Am Nat 142, 911–927 (1993).
17
K Higgins Nat Resour Mod 12, 65–108 (1999).
18
M E Gilpin, M E Soulé Conservation Biology, ed M E Soulé (Sinauer, Sunderland, MA), pp. 19–34 (1986).
19
R Lande Science 241, 1455–1460 (1988).
20
M S Boyce Annu Rev Ecol Syst 23, 481–506 (1992).
21
G Caughley J Anim Ecol 63, 215–244 (1994).
22
R Frankham Annu Rev Genet 29, 305–327 (1995).
23
K Higgins, A Hastings, J N Sarvela, L W Botsford Science 276, 1431–1435 (1997).
24
J S Conery, M Lynch Bioinformatics 15, 85–86 (1999).
25
H Caswell, R M Nisbet, A M de Roos, S Tuljapurkar Structured-Population Models in Marine, Terrestrial and Freshwater Systems, eds S Tuljapurkar, H Caswell (Chapman & Hall, New York), pp. 3–17 (1997).
26
M Lynch, J Blanchard, D Houle, T Kibota, S Schultz, L Vassilieva, J Willis Evolution (Lawrence, KS) 53, 645–663 (1999).
27
J D Fry, P D Keightley, S L Heinsohn, S V Nuzhdin Proc Natl Acad Sci USA 96, 574–579 (1999).
28
A S Kondrashov Genetica (The Hague) 102/103, 183–197 (1998).
29
R Greenberg, J F Crow Genetics 45, 1153–1168 (1960).
30
J H Gillespie Population Genetics: A Concise Guide (Johns Hopkins Univ. Press, Baltimore, 1998).
31
K Higgins, A Hastings, L W Botsford Am Nat 149, 247–269 (1997).
32
D L Hartl, A G Clark Principles of Population Genetics (Sinauer, 3rd Ed., Sunderland, MA, 1997).
33
J F Crow, M Kimura An Introduction to Population Genetics Theory (Harper & Row, New York, 1970).
34
S Wright Genetics 16, 97–159 (1931).
35
B Efron, R J Tibshirani An Introduction to the Bootstrap (Chapman & Hall, New York, 1993).
36
L Nunney Evolution (Lawrence, KS) 47, 1329–1341 (1993).
37
L Nunney, D R Elam Conserv Biol 8, 175–184 (1994).
38
A Caballero Heredity 73, 657–679 (1994).
39
M C Whitlock, N H Barton Genetics 146, 427–441 (1997).
40
R Lande Am Nat 130, 624–635 (1987).

Information & Authors

Information

Published in

Go to Proceedings of the National Academy of Sciences
Go to Proceedings of the National Academy of Sciences
Proceedings of the National Academy of Sciences
Vol. 98 | No. 5
February 27, 2001
PubMed: 11226343

Classifications

Submission history

Received: July 31, 2000
Published online: February 20, 2001
Published in issue: February 27, 2001

Acknowledgments

We thank C. Baer, J. Colbourne, J. Conery, J. F. Crow, R. Lande, M. O'Hely, I. Saccheri, and M. Sherrill for their valuable help with this research. Research funding was provided by a National Science Foundation Postdoctoral Research Fellowship in Biosciences Related to the Environment (DBI-9804267), with additional funding provided by the Oregon Department of Fish and Wildlife, the National Institutes of Health, and the Academy of Finland.

Authors

Affiliations

Kevin Higgins*
Ecology and Evolution, Department of Biology, University of Oregon, Eugene, OR 97403
Michael Lynch
Ecology and Evolution, Department of Biology, University of Oregon, Eugene, OR 97403

Notes

*
To whom reprint requests should be addressed. E-mail: [email protected].
Edited by James F. Crow, University of Wisconsin-Madison, Madison, WI, and approved November 27, 2000

Metrics & Citations

Metrics

Note: The article usage is presented with a three- to four-day delay and will update daily once available. Due to ths delay, usage data will not appear immediately following publication. Citation information is sourced from Crossref Cited-by service.


Citation statements

Altmetrics

Citations

If you have the appropriate software installed, you can download article citation data to the citation manager of your choice. Simply select your manager software from the list below and click Download.

Cited by

    Loading...

    View Options

    View options

    PDF format

    Download this article as a PDF file

    DOWNLOAD PDF

    Get Access

    Login options

    Check if you have access through your login credentials or your institution to get full access on this article.

    Personal login Institutional Login

    Recommend to a librarian

    Recommend PNAS to a Librarian

    Purchase options

    Purchase this article to get full access to it.

    Single Article Purchase

    Metapopulation extinction caused by mutation accumulation
    Proceedings of the National Academy of Sciences
    • Vol. 98
    • No. 5
    • pp. 2113-2933

    Media

    Figures

    Tables

    Other

    Share

    Share

    Share article link

    Share on social media