Abstract
Marbled murrelets (Brachyramphus marmoratus) are coastal seabirds that nest from California to the Aleutian Islands. They are declining and considered threatened in several regions. We compared variation in the mitochondrial control region, four nuclear introns and three microsatellite loci among194 murrelets from throughout their range except Washington and Oregon. Significant population genetic structure was found: nine private control region haplotypes and three private intron alleles occurred at high frequency in the Aleutians and California; global estimates of F ST or ΦST and most pairwise estimates involving the Aleutians and/or California were significant; and marked isolation-by-distance was found. Given the available samples, murrelets appear to comprise five genetic management units: (1) western Aleutian Islands, (2) central Aleutian Islands, (3) mainland Alaska and British Columbia, (4) northern California, and (5) central California.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Baker AJ, Marshall HD (1997). Mitochondrial control region sequences as tools for understanding evolution. In: Mindell DP (eds), Avian Molecular Evolution and Systematics. Academic, London, pp. 50–82
Byers JA (1999) Earth: Great circle distance calculator. Available at http://www.wcrl.ars.usda.gov/cec/java/la-long.htm
Chakraborty R (1990). Mitochondrial DNA polymorphism reveals hidden heterogeneity within some Asian populations. Am. J. Hum. Genet. 47: 87–94
Congdon BC, Piatt JF, Martin K, Friesen VL (2000). Rapid population expansion and peripheral isolation in marbled murrelets: Historical vs contemporary evolutionary processes. Evolution 54: 974–986
Crandall KA, Templeton AR (1993). Empirical tests of some predictions from coalescent theory with applications to intraspecific phylogeny reconstruction. Genetics 134: 959–969
Crandall KA, Bininda-Edmonds ORP, Mace GM, Wayne RK (2000). Considering evolutionary processes in conservation biology. Trends Ecol. Evol. 15: 290–295
Clement M, Posada D, Crandall D (2000). TCS: A computer program to estimate gene genealogies. Mol. Ecol. 9: 1657
COSEWIC (2003) Canadian Species at Risk, November 2003. Committee on the Status of Endangered Wildlife in Canada. 44pp.
Desjardins P, Morais R (1990). Sequence and organization of the chicken mitochondrial genome: A novel gene order in higher vertebrates. Mol. Biol. 212: 599–634
Ewens WJ (1972). The sampling theory of selective neutral alleles. Theor. Popul. Biol. 3: 87–112
Excoffier L, Smouse PE, Quattro JM (1992). Analysis of molecular variance inferred from metric distance among DNA haplotypes: Application to human mitochondrial DNA restriction data. Genetics 131: 479–491
Friesen VL, Baker AJ, Piatt JF (1996a). Evidence from cytochrome b sequences and allozymes for a ‘new’ species of alcid: The long-billed murrelet (Brachyramphus perdix). Condor 98: 681–690
FriesenVL, Montevecchi WA, Baker AJ, Barrett RT, Davidson WS (1996b). Population differentiation and evolution in the common guillemot Uria aalge. Mol. Ecol. 5: 793–805
Friesen VL, Congdon BC, Walsh HE, Birt TP (1997). Intron variation in marbled murrelets detected using analyses of single-stranded conformational polymorphisms. Mol. Ecol. 6: 1047–1058
Friesen VL, Congdon BC, Kidd MG, Birt TP (1999). PCR primers for the amplification of five nuclear introns in vertebrates. Mol. Ecol. 8: 2147–2149
Guo S, Thomson E (1992). Performing the exact test of Hardy–Weinberg proportion for multiple alleles. Biometrics 48: 361–372
Hayashi K (1991). PCR-SSCP: A simple and sensitive method for detection of mutations in the genomic DNA. PCR Meth. Applic. 1: 34–38
Ibarguchi G, Birt TP, Warheit KI, Boag PT, Friesen VL (2000). Microsatellite loci from common and thick-billed murres, Uria aalge and U. lomvia. Mol. Ecol. 9: 638–639
Kidd MG, Friesen VL (1998a). Sequence variation in the guillemot (Cepphus spp.) mitochondrial control region and its nuclear homolog. Mol. Biol. Evol. 15: 61–70
Kidd MG, Friesen VL (1998b). Analysis of mechanisms of microevolutionary change in Cepphus guillemots using patterns of control region variation. Evolution 52: 1158–1168
Kimura M (1980). A simple method for estimating evolutionary rate of base substitution through comparative studies of nucleotide sequences. J. Mol. Evol. 16: 111–120
Lesica P, Allendorf FW (1995). When are peripheral populations valuable for conservation?. Conserv. Biol. 9: 753–760
McShane C, Hamer T, Carter H, et al. (2004) Evaluation Report for the 5-Year Status Review for the Marbled Murrelet in Washington, Oregon, and California. Report to the U.S. Fish and Wildlife Service, Region 1. Portland, Oregon.
Miller SL, Meyer CB, Ralph CJ (2002). Land and seascape patterns associated with marbled murrelet abundance offshore. Waterbirds 25: 100–108
Moritz C (1994). Applications of mitochondrial DNA analysis in conservation: A critical review. Mol. Ecol. 3: 401–411
Moritz C (2002). Strategies to protect biological diversity and the evolutionary processes that sustain it. Syst. Biol. 51: 238–254
Moum T, Árnason A (2001). Genetic diversity and population history of two related seabird species based on mitochondrial DNA control region sequences. Mol. Ecol. 10: 2463–2478
Nei M (1987). Molecular Evolutionary Genetics. Columbia University Press, New York
Nelson K (1997) Marbled murrelet (Brachyramphus marmoratus). In: Birds of North America, No. 276 (eds. Poole A, Gill G). Academy of Natural Sciences, Philadelphia, and American Ornithologists’ Union, Washington.
Posada D, Crandall KA, Templeton AR (2000). GeoDis: A program for the cladistic nested analysis of the geographical distribution of genetic haplotypes. Mol. Ecol. 9: 487–488
Pritchard JK, Stephens M, Donnelly P (2000). Inference of population structure using multilocus genotype data. Genetics 155: 945–959
Pritchard JK, Wen W (2003) Documentation for Structure Software: Version 2. http://pritch.bsd.uchicago.edu.
Quinn TW, Wilson AC (1993). Sequence evolution in and around the mitochondrial control region in birds. J. Mol. Evol. 37: 417–425
Rice WR (1989). Analyzing tables of statistical tests. Evolution 43: 223–225
Schneider S, Roessli D, Excoffier L (2000) Arlequin, ver. 2.0: A software for population genetic data analysis. Genetics and Biometry Laboratory, University of Geneva, Switzerland
Slatkin M, Excoffier L (1996). Testing for linkage disequilibrium in genotypic data using the EM algorithm. Heredity 76: 377–383
Smouse PE, Long JC, Sokal RR (1986). Multiple regression and correlation extensions of the Mantel Test of matrix correspondence. Syst. Zool. 35: 627–632
Stanley HF, Casey S, Carnahan JM, Goodman S, Harwood J, Wayne RK (1992). Worldwide patterns of mitochondrial DNA differentiation in the harbour seal (Phoca vitulina). Mol. Biol. Evol. 13: 368–382
Templeton AR, Boerinkle E, Sing CF (1987). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping I Basic theory and an analysis of alcohol dehydrogenase activity in Drospohila. Genetics 117: 343–351
Templeton AR, Crandall KA, Sing CF (1992). A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619–633
Udvardy MDF (1963). Zoogeographical study of the Pacific Alcidae. In: Gressit JL (eds), Pacific Basin Biogeography: A Symposium. Bishop Museum Press, Honolulu, pp. 85–111
U.S. Fish and Wildlife Service (1992). Endangered and threatened wildlife and plants; determination of threatened status for the Washington, Oregon, and California population of the Marbled Murrelet. Fed. Reg. 57: 45328–45337
U.S. Fish and Wildlife Service (1997) Recovery plan for the threatened Marbled Murrelet (Brachyramphus marmoratus) in␣Washington, Oregon, and California. Portland, Oregon 203␣pp.
Veit, ML, Robertson RJ, Hamel PB, Friesen VL (2005) Population genetic structure and dispersal across a fragmented landscape in cerulean warblers (Dendroica cerulea). Conserv. Gen., 6, 159–174
Vucetich JA, Waite TA (2003). Spatial patterns of demography and genetic processes across the species range: Null hypotheses for landscape conservation genetics. Conserv. Gen. 4: 639–645
Watterson G (1978). The homozygosity test of neutrality. Genetics 88: 405–417
Wilson AC, Cann RL, Carr SM et al. (1985). Mitochondrial DNA and two perspectives on evolutionary genetics. Biol. J. Linn. Soc. 26: 375–400
Wright S (1931). Evolution in Mendelian populations. Genetics 16: 97–159
Acknowledgements
Samples used in this study were obtained through the assistance of E. Burkett, V. Byrd, H. Carter, F. Cooke, A. Derocher, T. Hofstra, G. Kaiser, M.␣Kassera, S. Kitaysky, K. Kuletz, K. Martin, Z. Peery, T. van Pelt, J. Pitocchelli, A. Pritchard, L.␣Roberts, D. Roseneau, H. Sakai, S. Speckman, W. Sydeman, J. Williams, and the Captain and Crew of the Tiglax. Help with data collection and interpretation was provided by C. Crossman, G. Ibarguchi, R. Kristensen, D. Michaud, V. Poland, and L.Veit. Funding was provided by the Exxon Valdez Oil Spill Trustee Council, Scotia Pacific Lumber, the U.S. National Park Service, the California Department of Fish and Game, the Natural Sciences and Engineering Research Council of Canada, and a Premier’s Research Excellence Award. The findings and conclusions presented by the authors are their own and do not necessarily reflect the views or position of the Exxon Valdez Oil Spill Trustee Council.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Friesen, V., Birt, T., Piatt, J. et al. Population genetic structure and conservation of marbled murrelets (Brachyramphus marmoratus). Conserv Genet 6, 607–614 (2005). https://doi.org/10.1007/s10592-005-9012-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10592-005-9012-x