Abstract
The northern spotted owl (Strix occidentalis caurina) is one of the most controversial threatened subspecies ever listed under the US Endangered Species Act. Despite protection of its remaining forest habitat, recent field studies show continued declines of northern spotted owls. One potential threat to northern spotted owls which has not yet been shown is loss of genetic variation from population bottlenecks. Bottlenecks can increase the probability of mating among related individuals, potentially causing inbreeding depression, and can decrease adaptive potential. Here we report evidence for recent bottlenecks in northern spotted owls using a large genetic dataset (352 individuals and 10 microsatellite loci). The signature of bottlenecks was strongest in the Washington Cascade Mountains, in agreement with field data. Our results provide independent evidence that northern spotted owls have recently declined, and suggest that loss of genetic variation is an emerging threat to the subspecies’ persistence. Reduced effective population size (N e) shown here in addition to field evidence for demographic decline highlights the increasing vulnerability of this bird to extinction.

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References
Allendorf FW, Luikart G (2007) Conservation and the genetics of populations. Blackwell, Oxford
Anthony RG, Forsman ED, Franklin AB, Anderson DR, Burnham KP, White GC, Schwarz CJ, Nichols JD, Hines JE, Olson GS, Ackers SH, Andrews LS, Biswell BL, Carlson PC, Diller LV, Dugger KM, Fehring KE, Fleming TL, Gerhardt RP, Gremel SA, Gutiérrez RJ, Happe PJ, Herter DR, Higley JM, Horn RB, Irwin LL, Loschl PJ, Reid JA, Sovern SG (2006) Status and trends in demography of northern spotted owls, 1985–2003. Wildl Monogr 163:1–47. doi:10.2193/0084-0173(2006)163[1:SATIDO]2.0.CO;2
Barrowclough GF, Groth JG, Mertz LA, Gutiérrez RJ (2005) Genetic structure, introgression, and a narrow hybrid zone between northern and California spotted owls (Strix occidentalis). Mol Ecol 14:1109–1120. doi:10.1111/j.1365-294X.2005.02465.x
Beebee T, Rowe G (2001) Application of genetic bottleneck testing to the investigation of amphibian declines: a case study with natterjack toads. Conserv Biol 15:266–270. doi:10.1046/j.1523-1739.2001.99438.x
Beerli P, Felsenstein J (2001) Maximum likelihood estimation of a migration matrix and effective population sizes in n subpopulations by using a coalescent approach. Proc Natl Acad Sci USA 98:4563–4568. doi:10.1073/pnas.081068098
Bürger R, Lynch M (1995) Evolution and extinction in a changing environment: a quantitative-genetic analysis. Evolution Int J Org Evolution 49:151–163. doi:10.2307/2410301
Busch JD, Waser PM, DeWoody A (2007) Recent demographic bottlenecks are not accompanied by a genetic signature in banner-tailed kangaroo rats (Dipodomys spectabilis). Mol Ecol 16:2450–2462. doi:10.1111/j.1365-294X.2007.03283.x
Cornuet JM, Luikart G (1996) Description and power analysis of two tests for detecting recent population bottlenecks from allele frequency data. Genetics 144:2001–2014
Crow JF, Kimura M (1970) An introduction to population genetics theory. Burgess Publishing, Minneapolis
Dark SJ, Gutiérrez RJ, Gould GI (1998) The barred owl (Strix varia) invasion in California. Auk 115:50–56
Di Rienzo A, Peterson AC, Garza JC, Valdes AM, Slatkin M, Freimer NB (1994) Mutational processes of simple-sequence repeat loci in human populations. Proc Natl Acad Sci USA 91:3166–3170. doi:10.1073/pnas.91.8.3166
Dieringer D, Schlötterer C (2003) Microsatellite analyser (MSA): a platform independent analysis tool for large microsatellite data sets. Mol Ecol Notes 3:167–169. doi:10.1046/j.1471-8286.2003.00351.x
El Mousadik A, Petit RJ (1996) High level of genetic differentiation for allelic richness among populations of the argan tree [Argania spinosa (L.) Skeels] endemic to Morocco. Theor Appl Genet 92:832–839. doi:10.1007/BF00221895
Fenger M, Buchanan J, Cade TC, Forsman ED, Haig SM, Martin K, Rapley WA (2007) Northern spotted owl population enhancement and recovery in British Columbia. Report to British Columbia Minister of Natural Resources
Funk WC, Mullins TD, Forsman ED, Haig SM (2007) Microsatellite loci for distinguishing spotted owls (Strix occidentalis), barred owls (Strix varia), and their hybrids. Mol Ecol Notes 7:284–286. doi:10.1111/j.1471-8286.2006.01581.x
Funk WC, Forsman ED, Mullins TD, Haig SM (2008) Introgression and dispersal among spotted owl (Strix occidentalis) subspecies. Evol Appl 1:161–171. doi:10.1111/j.1752-4571.2007.00002.x
Garza JC, Williamson EG (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318. doi:10.1046/j.1365-294x.2001.01190.x
Gaunt AS, Oring LW (1997) Guidelines to the use of wild birds in research. The Ornithological Council, Washington, DC
Goodnight KF, Queller DC (1999) Computer software for performing likelihood tests of pedigree relationship using genetic markers. Mol Ecol 8:1231–1234. doi:10.1046/j.1365-294x.1999.00664.x
Goossens B, Chikhi L, Ancrenaz M, Lackman-Ancrenaz I, Andau P, Bruford MW (2006) Genetic signature of anthropogenic population collapse in orang-utans. PLoS Biol 4:285–291. doi:10.1371/journal.pbio.0040025
Gutiérrez RJ, Franklin AB, Lahaye WS (1995) Spotted owl. In: Poole A, Gill F (eds) The birds of North America No. 179. Academy of Natural Sciences, Philadelphia, Pennsylvania, and American Ornithologists’ Union, Washington, DC, pp 1–28
Haig SM, Mullins TD, Forsman ED (2004a) Subspecific relationships and genetic structure in the spotted owl. Conserv Genet 5:683–705. doi:10.1007/s10592-004-1864-y
Haig SM, Mullins TD, Forsman ED, Trail PW, Wennerberg L (2004b) Genetic identification of spotted owls, barred owls, and their hybrids: legal implications of hybrid identity. Conserv Biol 18:1347–1357. doi:10.1111/j.1523-1739.2004.00206.x
Hsu Y-C, Severinghaus LL, Lin Y-S, Li S-H (2003) Isolation and characterization of microsatellite DNA markers from the Lanyu scops owl (Otus elegans botelensis). Mol Ecol Notes 3:595–597. doi:10.1046/j.1471-8286.2003.00523.x
Hsu Y-C, Li S-H, Lin Y-S, Severinghaus LL (2006) Microsatellite loci from Lanyu scops owl (Otus elegans botelensis) and their cross-species application in four species of Strigidae. Conserv Genet 7:161–165. doi:10.1007/s10592-005-5477-x
Kelly EG, Forsman ED (2004) Recent records of hybridization between barred owls (Strix varia) and northern spotted owls (S. occidentalis caurina). Auk 121:806–810. doi:10.1642/0004-8038(2004)121[0806:RROHBB]2.0.CO;2
Kelly EG, Forsman ED, Anthony RG (2003) Are barred owls displacing spotted owls? Condor 105:45–53. doi:10.1650/0010-5422(2003)105[45:ABODSO]2.0.CO;2
Lessa EP, Cook JA, Patton JL (2003) Genetic footprints of demographic expansion in North America, but not Amazonia, during the Late Quaternary. Proc Natl Acad Sci USA 100:10331–10334. doi:10.1073/pnas.1730921100
Luikart G, England PR, Tallmon D, Jordan S, Taberlet P (2003) The power and promise of population genomics: from genotyping to genome typing. Nat Rev Genet 4:1–15. doi:10.1038/nrg1226
Milá B, Girman DJ, Kimura M, Smith TB (2000) Genetic evidence for the effect of a postglacial population expansion on the phylogeography of a North American songbird. Proc R Soc Lond B Biol Sci 267:1033–1040. doi:10.1098/rspb.2000.1107
Narum SR (2006) Beyond Bonferroni: less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi:10.1007/s10592-005-9056-y
Noon BR, Blakesley JA (2006) Conservation of the northern spotted owl under the Northwest Forest Plan. Conserv Biol 20:288–296. doi:10.1111/j.1523-1739.2006.00387.x
Olson GS, Anthony RG, Forsman ED, Ackers SH, Loschl PJ, Reid JA, Dugger KM, Glenn EM, Ripple WJ (2005) Modeling of site occupancy dynamics for northern spotted owls, with emphasis on the effects of barred owls. J Wildl Manage 69:918–932. doi:10.2193/0022-541X(2005)069[0918:MOSODF]2.0.CO;2
Piry S, Luikart G, Cornuet J-M (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503. doi:10.1093/jhered/90.4.502
Proudfoot G, Honeycutt R, Douglas Slack R (2005) Development and characterization of microsatellite DNA primers for ferruginous pygmy-owls (Glaucidium brasilianum). Mol Ecol Notes 5:90–92. doi:10.1111/j.1471-8286.2004.00842.x
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Reichard TA (1974) Barred owl sightings in Washington. West Birds 5:138–140
Saccheri I, Kuussaari M, Kankare M, Vikman P, Fortelius W, Hanski I (1998) Inbreeding and extinction in a butterfly metapopulation. Nature 392:491–494. doi:10.1038/33136
Schwartz MK, Luikart G, Waples RS (2007) Genetic monitoring as a promising tool for conservation and management. Trends Ecol Evol 22:25–33. doi:10.1016/j.tree.2006.08.009
Shriver MD, Jin L, Chakraborty R, Boerwinkle E (1993) VNTR allele frequency-distributions under the stepwise mutation model—a computer simulation approach. Genetics 134:983–993
Soulé ME, Mills LS (1998) No need to isolate genetics. Science 282:1658–1659. doi:10.1126/science.282.5394.1658
Spear SF, Peterson CR, Matocq MD, Storfer A (2006) Molecular evidence for historical and recent population size reductions of tiger salamanders (Ambystoma tigrinum) in Yellowstone National Park. Conserv Genet 7:605–611. doi:10.1007/s10592-005-9095-4
Stokstad E (2005) Learning to adapt. Science 309:688–690. doi:10.1126/science.309.5735.688
Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595
Taylor AL, Forsman ED (1976) Recent range extensions of the barred owl in western North America, including the first records for Oregon. Condor 78:560–561. doi:10.2307/1367110
Thode AB, Maltbie M, Hansen LA, Green LD, Longmire LL (2002) Microsatellite markers for the Mexican spotted owl (Strix occidentalis lucida). Mol Ecol Notes 2:446–448. doi:10.1046/j.1471-8286.2002.00267.x
US Fish and Wildlife Service (1990) Endangered and threatened wildlife and plants: determination of threatened status of the northern spotted owl. Fed Regist 55:26114–26194
Weir BS, Cockerham CC (1984) Estimating F-statistics for the analysis of population structure. Evol Int J Org Evol 38:1358–1370. doi:10.2307/2408641
Whitlock MC (2005) Combining probability from independent tests: the weighted Z-method is superior to Fisher’s approach. J Evol Biol 18:1368–1373. doi:10.1111/j.1420-9101.2005.00917.x
Williamson-Natesan EG (2005) Comparison of methods for detecting bottlenecks from microsatellite loci. Conserv Genet 6:551–562. doi:10.1007/s10592-005-9009-5
Acknowledgments
We are indebted to the many people who helped with sample collection and logistics in the field, particularly P. Loschl, S. Ackers, R. Anthony, R. Claremont, D. Herter, S. Hopkins, J. Reid, and S. Sovern. We also thank M. Miller, F. Allendorf, D. Tallmon, G. Luikart, and two anonymous reviewers for comments on the manuscript. Funding was provided by the USGS Forest and Rangeland Ecosystem Science Center and the USDA Forest Service Pacific Northwest Research Station. Samples were collected under US Fish and Wildlife Service threatened species permit number TE026280-11 and Oregon State University Animal Care and Use permit number 3091.
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Funk, W.C., Forsman, E.D., Johnson, M. et al. Evidence for recent population bottlenecks in northern spotted owls (Strix occidentalis caurina). Conserv Genet 11, 1013–1021 (2010). https://doi.org/10.1007/s10592-009-9946-5
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DOI: https://doi.org/10.1007/s10592-009-9946-5


