Abstract
As southern species undergo northward range expansions, reports of hybridization between temperate and arctic taxa are increasing, which may have important implications for the evolution, conservation, and management of arctic species. The extent of hybridization between temperate common murres (Uria aalge) and arctic thick-billed murres (U. lomvia), seabirds in the family Alcidae, has been the subject of debate. In a previous survey of variation in mitochondrial DNA (mtDNA) in common and thick-billed murres sampled from throughout the North Pacific and low Arctic, 12 of 327 common murres (~4%) were found to possess DNA sequences characteristic of thick-billed murres. In the present study, we surveyed variation in three nuclear introns in 230 common murres and 56 thick-billed murres and report that these putative hybrids carry various combinations of intron alleles from common and thick-billed murres. Analysis using the program STRUCTURE indicated that nine of these individuals possessed high proportions of thick-billed murre intron alleles, two possessed alleles in F1 and F2 proportions, and one individual possessed predominantly common murre intron alleles. We propose that the asymmetric mtDNA introgression we observed is most likely the result of mate choice at mixed colonies based on differences in male mating behaviours. Our results highlight that hybridization between thick-billed and common murres is more prevalent than previously thought, which may have important implications for the conservation and management of arctic-dwelling thick-billed murres as common murres expand northward.
Similar content being viewed by others
References
Ainley DG, Nettleship DN, Carter HR, Storey AE (2002) Common Murre (Uria aalge). In: Poole A, Gill F (eds) The birds of North America, no. 666. Philadelphia, PA
Allendorf FW, Leary RF, Spruell P, Wenburg JK (2001) The problems with hybrids: setting conservation guidelines. Trends Ecol Evol 16:613–622
Anderson E (1949) Introgressive hybridization. Wiley, New York
Arnold ML (1997) Natural hybridization and evolution. Oxford University Press, New York
Avise JC, Saunders NC (1984) Hybridization and introgression among species of sunfish (Lepomis): analysis by mitochondrial DNA and allozyme markers. Genetics 108:237–255
Avise JC, Neigel JE, Arnold J (1984) Demographic influences on mitochondrial DNA lineage survivorship in animals populations. J Mol Evol 20:99–105
Baker A, Marshall HD (1997) Mitochondrial control region sequences as tools for understanding evolution. In: Mindell DP (ed) Avian molecular evolution and systematics. Academic Press, New York, pp 51–82
Ballard JWO, Whitlock MC (2004) The ncomplete natural history of mitochondria. Mol Ecol 13:729–744
Barilani M, Sfougaris A, Giannakopoulos A, Mucci N, Tabarroni C, Randi E (2007) Detecting introgressive hybridization in rock partridge populations (Alectoris graeca) in Greece through Bayesian admixture analyses of multilocus genotypes. Conserv Genet 8:343–354
Barton NH (2001) The role of hybridization in evolution. Mol Ecol 10:551–568
Birt T, Friesen VL, Damus M (2007) Population genetic structure in the thick-billed murre throughout its range. Report to the Minister of the Environment, Canada
Bryson RW, Nieto-Montes De Oca A, Jaeger JR, Riddle BR (2010) Elucidation of cryptic diversity in a widespread nearctic treefrog reveals episodes of mitochondrial gene capture as frogs diversified across a dynamic landscape. Evolution 64:2315–2330
Burek KA, Gulland FDM (2008) Effects of climate change on arctic marine mammal health. Ecol Appl 18:S126–S134
Butlin RK, Neems RM (1994) Hybrid zones and sexual selection. Science 265:122
Byrd GV, Murphy EC, Kaiser GW, Kondratyev AY, Shibaev YV (1993) Status and ecology of offshore fish-feeding alcids (murres and puffins) in the North Pacific. In: Vermeer K, Briggs KT, Morgan KH, Siegel-Causey D (eds) The status, ecology and conservation of marine birds of the north Pacific. Canadian Wildlife Service, Ottawa, pp 76–186
Cairns DK, DeYoung B (1981) Back-crossing of a common murre (Uria aalge) and a common murre-thick-billed murre hybrid (U aalge x U lomvia). Auk 98:847
Carter HR, Wilson UW, Lowe RW, Rodway MS, Manual DD, Takekawa JE, Lee JL (2002) Population trends of the common murre (Uria aalge californica). In: Manuwal DA, Carter HR, Zimmerman TS, Orthmeyer DL (eds) Biology and conservation of the common murre in California, Oregon, Washington, and British Columbia, vol 1. U. S. Geological Survey, Washington, pp 35–71
Clement M, Posada D, Crandall KA (2000) TCS: a computer program to estimate gene genealogies. Mol Ecol 9:1657–1659
Coyne JA, Orr HA (2004) Speciation. Sinauer Associates, Massachusetts
D’Eon RG, Seymour NR, Boer AH (1994) Black duck–mallard behavioural interactions in relation to hybridization. Can J Zool 72:1517–1521
Deffontane V, Libois R, Kotlik P, Sommer R, Nieberding C, Paradis E, Searle JB, Michaux JR (2005) Beyond the Mediterranean peninsulas: evidence of central European glacial refugia for a temperate forest mammal species, the bank vole (Clethrionomys glareolus). Mol Ecol 14:1727–1739
Friesen VL, Barrett RT, Montevecchi WA, Davidson WS (1993) Molecular identification of a backcross between a female common murre × thick-billed murre hybrid and a male common murre. Can J Zool 71:1474–1477
Friesen VL, Montevecchi WA, Baker AJ, Barrett RT, Davidson WS (1996) Population differentiation and evolution in the common Guillemot Uria aalge. Mol Ecol 5:793–805
Gaston AJ, Hipfner JM (2000) Thick-billed Murre (Uria lomvia). In: Poole A, Gill F (eds) The birds of North America. Philadelphia, PA
Gaston AJ, Jones IL (1998) The auks: Alcidae. Oxford University Press, Oxford
Gaston AJ, Hipfner JM, Campbell D (2002) Heat and mosquitoes cause breeding failures and adult mortality in an Arctic-nesting seabird. Ibis 144:185–191
Gaston AJ, Woo K, Hipfner JM (2003) Trends in forage fish populations in Northern Hudson Bay since 1981 from diet of nestling thick-billed murres Uria lomvia. Arctic 56:227–233
Gaston AJ, Gilchrist HG, Hipfner JM (2005) Climate change, ice conditions and reproduction in an Arctic nesting marine bird: Brunnich’s Guillemot (Uria lomvia L.). J Anim Ecol 74:832–841
Good JM, Demboski JR, Nagorsen DW, Sullivan J (2003) Phylogeography and introgressive hybridization: chipmunks (genus Tamais) in the northern Rocky Mountains. Evolution 57:1900–1916
Grant PR, Grant BR (1992) Hybridization of bird species. Science 256:193–197
Haldane JBS (1922) Sex ratio and unisexual sterility in hybrid animals. Genetics 12:101–109
Hall TA (1999) BioEdit: a user friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acid Symp Ser 41:95–98
Harrigan RJ, Mazza ME, Sorenson MD (2008) Computation vs. cloning: evaluation of two methods for haplotype determination. Mol Ecol Res 8:1239–1248
Harris MP, Wanless S, Barton TR (1996) Site use and fidelity in the common Guillemot Uria aalge. Ibis 138:399–404
Harrison RG (1993) Hybrid zones and the evolutionary process. Oxford University Press, New York
Hipfner JM, Greenwood JL (2008) Breeding biology of the common murre at Triangle Island, British Columbia, Canada 2002–2007. Northwestern Nat 89:76–84
Hudson PJ (1985) Population parameters for the Atlantic Alcidae. In: Nettleship DN, Birkhead TR (eds) The Atlantic Alcidae: the evolution, distribution and biology of the auks inhabiting the Atlantic Ocean and adjacent water areas. Academic Press, London, pp 233–261
Hunter CM, Caswell H, Runge MC, Regehr EV, Amstrup SC, Stirling I (2010) Climate change threatens polar bear populations: a stochastic demographic analysis. Ecology 91:2883–2897
Irwin DE, Rubtsov AS, Panv EN (2009) Mitochondrial introgression and replacement between yellowhammers (Emberiza citronella) and pine buntings (Emberiza leucocephalus) (Aves: Passeriformes). Biol J Linn Soc 98:422–438
Jiggins CD, Mallet J (2000) Bimodal hybrid zones and speciation. Trends Ecol Evol 15:250–255
Johnson SR, Ward JG (1985) Observations of thick-billed murres (Uria lomvia) and other seabirds at Cape parry, Amundsen Gulf, N. W. T. Arctic 38:112–115
Kelly B, Whiteley A, Tallmon D (2010) The Arctic melting pot. Nature 468:891
Kimura M (1980) A simple model for estimating evolutionary rate of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120
Kondratyev AY, Litvinenko NM, Shibaev YV, Vyatkin PS, Kondratyeva LF (2000) The breeding seabirds of the Russian Far East. In: Kondratyev AY, Litvinenko NM, Kaiser GW (eds) Seabirds of the Russian Far East. Candian Wildlife Service, Ottawa, pp 37–81
Melo-Ferreira J, Boursot P, Suchentrunk F, Ferrand N, Alves PC (2005) Invasions from the cold past: extensive introgression of mountain hare (Lepus timidus) mitochondrial DNA into three other hare species in northern Iberia. Mol Ecol 14:2459–2464
Morris-Pocock JA, Taylor SA, Birt TP, Damus M, Piatt FF, Warheit KI, Friesen VL (2008) Population genetic structure in Atlantic and Pacific Ocean common murres: natural replicate tests of post-Pleistocene evolution. Mol Ecol 17:4859–4873
Moum T, Johansen S, Erikstad KE, Piatt JH (1994) Phylogeny and evolution of the auks (subfamily Alcinae) based on mitochondrial DNA sequences. Proc Natl Acad Sci USA 91:7912–7916
Patirana A (1998) A conservation genetic study of common murres (Uria aalge) in the Exxon Valdex spill area through comparison of mitochondrial control region and cytochrome b sequences. Dissertation, Queen’s University
Piatt JF, Lensink CJ, Butler W, Kendziorek M, Nysewander DR (1990) Immediate impact of the ‘Exxon Valdez’ oil spill on marine birds. Auk 107:387–397
Plötner J, Uzzell T, Beerli P, Splosky C, Ohst T, Litvinchuk SN, Guex G-D, Reyer H-U, Hotz H (2008) Winespread unidirectional transfer of mitochondrial DNA: a case in western Palaearctic water frogs. J Evol Biol 21:668–681
Post E, Forchhammer MC (2008) Climate change reduces the reproductive success of an Arctic herbivore through trophic mismatch. Phil Trans R Soc B 12:2367–2373
Price T (2008) Speciation in birds. Roberts and Company, Colorado
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Randler C (2002) Avian hybridization and mixed pairing. Anim Behav 63:674–685
Rohwer S, Bermingham E, Wood C (2001) Plumage and mitochondrial DNA haplotype variation across a moving hybrid zone. Evolution 55:405–422
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual, 3rd edn. Cold Spring Harbor Laboratory Press, New York
Seehausen O (2004) Hybridization and adaptive radiation. Trends Ecol Evol 19:198–207
Servedio MR, Lande R (2006) Population genetic models of male and mutual mate choice. Evolution 60:674–685
Sluys R (1983) Evidence for hybrid murre reconsidered. Auk 100:236–237
Southern HN, Carrick R, Potter WG (1965) The natural history of a population of guillemots (Uria aalge). J Anim Ecol 34:649–665
Spring L (1971) A comparison of functional and morphological adaptations in the common murre (Uria aalge) and thick-billed murre (Uria lomvia). Condor 73:1–27
Steiner UK, Gaston AJ (2005) Reproductive consequences of natal dispersal in a highly philopatric seabird. Behav Ecol 16:634–639
Stephens M, Donnelly P (2003) A comparison of Bayesian methods for haplotype reconstruction from population genotype data. Am J Hum Genet 73:1162–1169
Stephens M, Smith NJ, Donnelly P (2001) A new statistical method for haplotype reconstruction from population data. Am J Hum Genet 68:978–989
Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599
Tegelström H, Gelter HP (1990) Haldanes rule and sex-biased gene flow between two hybridization flycatcher species (Ficedula albicolis and F. hypoleuca, Aves: Muscicapidae). Evolution 44:2012–2021
Tschanz B, Wehrlin J (1968) Kreuzung zwischen trottellumme und dickschnabellumme. Fauna (oslo) 21:53–55
United States Fish and Wildlife Service (2009) North Pacific seabird colony database, computer database and colony status record archives. http://alaska.fws.gov/mbsp/mbm/northpacificseabirds/colonies/ Accessed 29 October 2007
Weckstein JD, Zink RM, Blackwell-Rago RC, Nelson DA (2001) Anomalous variation in mitochondrial genomes of white-crowned (Zonotrichia leucophrys) and golden-crowned (Z. atricapilla) sparrows: pseudogenes, hybridization, or incomplete lineage sorting? Auk 118:231–236
Wiese FK, Robertson GJ, Gaston AJ (2004) Impacts of chronic marine oil pollution and the murre hunt in Newfoundland on thick-billed murre Uria lomvia populations in the eastern Canadian Arctic. Biol Conserv 116:205–216
Wilhelm SI, Walsh CJ, Stenhouse IJ, Storey AE (2001) A possible common guillemot (Uria aalge) X razorbill (Alca torda) hybrid. Atl Seabirds 3:85–88
Wirtz P (1999) Mother species–father species: unidirectional hybridization in animals with female choice. Anim Behav 58:1–12
Acknowledgments
We would like to thank Y.Artukhin, D.A. Banin, J. Broughton, G.V. Byrd, P.J. Gross, Y. Krasnov, R. Lanctot, R. Lowe, S. Newman, N. Nikolaeva, J. Parrish, J.F. Piatt, J. Pitocchelli, S. Rohwer, D.G. Roseneau, D. Causey, T. Van Pelt, H. Walsh, K. Warheit, the Burke Museum, the captain and crew of M/V Tiglax, and Alaskan Maritime National Wildlife Refuge for assistance with logistics, sample collection, and preparation. We would also like to thank S. Leung for preliminary laboratory work. G. Ibarguchi generously shared an unpublished finding of a potential hybrid murre. Thanks also to Jan T Lifjeld, Mark Hipfner, J.F. Piatt, and four anonymous reviewers for their helpful comments on the manuscript. Funding was provided by Exxon Valdez Oil Spill Trustee Council, Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant (V.L.F.), and an NSERC Postgraduate Scholarship (S.A.T.). 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
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Taylor, S.A., Patirana, A., Birt, T. et al. Cryptic introgression between murre sister species (Uria spp.) in the Pacific low Arctic: frequency, cause, and implications. Polar Biol 35, 931–940 (2012). https://doi.org/10.1007/s00300-011-1141-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00300-011-1141-8