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The Crested Auklet, Aethia cristatella (Alcidae, Charadriiformes), does not vary geographically in genetics, morphology or vocalizations

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Abstract

The study of population differentiation is essential for understanding species evolution and ecology. Despite a large amount of published works in this area of study, the prediction of population structure in a number of animal species and, particularly, in seabirds remains difficult. The Crested Auklet (Aethia cristatella) is a small, planktivorous seabird species that breeds in colonies on islands and along the coastline of the North Pacific. Despite their vast breeding area and huge population numbers, the phenotypic features of adult birds from different colonies and genetic population variability have not been studied yet. Here we conducted a combined study of population differentiation in the Crested Auklet, using both phenotypic and genetic features. Data were collected at nine points across the species’ distribution range from 1988 to 2012. We analyzed population variability of the mitochondrial control region fragment, microsatellites, two types of vocalizations (barks and trumpet calls), morphometric and ornamentation measurements. However, we did not detect any obvious cues to different populations, either in genetic, morphometric or acoustic variables. Crested Auklets from different geographic areas do not express any genetic differences. We surmise that the absence of population separation in Crested Auklet can be explained by an important ecological characteristic of the species: these birds are pelagic during non-breeding season; therefore, young birds likely migrate far away from their natal colonies during their first year of life and do not often return to breed at their native colony.

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References

  • Abbott CL, Millikin RL, Hipfner MJ, Hatch S, Ito M, Watanuki Y, Burg TM (2014) Genetic structure of Rhinoceros Auklets, Cerorhinca monocerata, breeding in British Columbia, Alaska, and Japan. Mar Biol 161:275–283. doi:10.1007/s00227-013-2333-2

    Article  Google Scholar 

  • Alström P, Olsson U, Rasmussen PC, Yao C, Ericson PGP, Sundberg P (2007) Morphological, vocal and genetic divergence in the Cettia acanthizoides complex (Aves: Cettiidae). Zool J Linn Soc 149:437–452. doi:10.1111/j.1096-3642.2007.00250.x

    Google Scholar 

  • Andreev AV, Yu GE, Zubakin VA, Kharitonov SP (2010) The number of seabirds on Talan Island: the 20-year trend assessment. Bull NESC FEB RAS 2:30–42 (in Russian)

    Google Scholar 

  • Andreev AV, Kharitonov SP, Sleptsov YuA (2012) Seabirds of Saint Jonah’s Island (the Sea of Okhotsk). Zoologicheskii Zhurnal 91(7):843–855 (in Russian)

    Google Scholar 

  • Appleby BM, Redpath SM (1997) Indicators of male quality in the hoots of Tawny Owls (Strix aluco). J Raptor Res 31(1):65–70

    Google Scholar 

  • Artukhin YuB (1999) Cadaster of seabirds colonies of the Commander Islands. Biol Conserv Birds Kamchatk 1:25–35 (in Russian)

    Google Scholar 

  • Artukhin YuB, Burkanov VN, Nikulin VS (2010) Accidental by-catch of marine birds and mammals in the salmon gillnet fishery in the northwestern Pacific Ocean. Skorost’ Tsveta, Moscow (in Russian)

    Google Scholar 

  • Bandelt HJ, Forster P, Rohl A (1999) Median-joining networks for inferring intraspecific phylogenies. Mol Biol Evol 16(1):37–48

    Article  CAS  Google Scholar 

  • Birt TP, Mackinnon D, Piatt JF, Friesen VL (2011) Genetic differentiation of the Kittlitz’s Murrelet Brachyramphus brevirostris in the Aleutian Islands and Gulf of Alaska. Marine Ornithol 39:45–51

    Google Scholar 

  • Birt-Friesen VL, Montevecchi WA, Gaston AJ, Davidson WS (1992) Genetic structure of Thick-billed Murre (Uria lomvia) populations examined using direct sequence analysis of amplified DNA. Evolution 46(1):267–272

    Article  CAS  Google Scholar 

  • Bohonak AJ (1999) Dispersal, gene flow, and population structure. Q Rev Biol 74(1):21–45

    Article  CAS  Google Scholar 

  • Bretagnolle V (1989) Calls of Wilson’s storm petrel: functions, individual and sexual recognitions, and geographic variation. Behaviour 111:98–112

    Article  Google Scholar 

  • Burg TM, Croxall JP (2001) Global relationships amongst Black-browed and Grey-headed Albatrosses: analysis of population structure using mitochondrial DNA and microsatellites. Mol Ecol 10:2647–2660

    Article  CAS  Google Scholar 

  • Burney CW, Brumfield RT (2009) Ecology predicts levels of genetic differentiation in Neotropical birds. Am Nat 174(3):358–368. doi:10.1086/603613

    Article  Google Scholar 

  • Byrd GV, Williams JC (1993) Whiskered Auklet (Aethia pygmaea). In: Poole A, Gill F (eds) The birds of North America No 76. Philadelphia: The Academy of Natural Sciences. The American Ornithologists’ Union, Washington, D.C.

  • Cerit H, Avanus K (2007) Sex identification in avian species using DNA typing methods. World Poult Sci J 63:91–99. doi:10.1017/S0043933907001316

    Article  Google Scholar 

  • Chakraborty R (1990) Mitochondrial DNA polymorphism reveals hidden heterogeneity within some Asian populations. Am J Hum Genet 47:87–94

    CAS  Google Scholar 

  • Dawson DA, Hunter FM, Pandhal J, Buckland R, Parham A, Jones IL, Bradshow M, Jehle R, Burke T (2005) Assessment of 17 new Whiskered Auklet (Aethia pygmaea) microsatellite loci in 42 seabirds identifies 5-15 polymorphic markers for each of nine Alcinae species. Mol Ecol Notes 5:289–297. doi:10.1111/j.1471-8286.2005.00906.x

    Article  CAS  Google Scholar 

  • Dearborn DC, Anders AD, Schreiber EA, Adams RMM, Mueller UG (2003) Inter-island movements and population differentiation in a pelagic seabird. Mol Ecol 12:2835–2843. doi:10.1046/j.1365-294X.2003.01931.x

    Article  CAS  Google Scholar 

  • Denlinger LM (2006) Crested Auklet (Aethia cristatella). In Alaska Seabird Information Series. U.S. Fish and Wildlife Service, Migratory Bird Management 79–80

  • Ewens WJ (1972) The sampling theory of selectively neutral alleles. Theor Popul Biol 3:87–112

    Article  CAS  Google Scholar 

  • Excoffier L, Lischer HEL (2010) Arlequin suite ver 3.5: a new series of programs to perform population genetics analyses under Linux and Windows. Mol Ecol Resources 1:564–567. http://cmpg.unibe.ch/software/arlequin3

  • Feinstein B (1959) Geographic variation in the Whiskered Auklet. Auk 76(1):60–67

    Article  Google Scholar 

  • Fraser GS, Jones IL, Hunter FM, Cowen L (2004) Mate switching patterns in Crested Auklets (Aethia cristatella): the role of breeding success and ornamentation. Bird Behav 16:7–12

    Google Scholar 

  • Friesen VL, Montevecchi WA, Gaston AJ, Barrett RT, Davidson WS (1996a) Molecular evidence for kin groups in the absence of large-scale genetic differentiation in a migratory bird. Evolution 50(2):924–930

    Article  Google Scholar 

  • Friesen VL, Piatt JF, Baker AJ (1996b) Evidence from cytochrome b sequences and allozymes for a’new’ species of alcid: the Long-billed Murrelet (Brachyramphus perdix). Condor 98:681–690

    Article  Google Scholar 

  • Friesen VL, Birt TP, Piatt JF, Golightly RT, Newman SH, Hébert PN, Congdon BC, Gissing G (2005) Population genetic structure and conservation of Marbled Murrelets (Brachyramphus marmoratus). Conserv Gen 6:607–614. doi:10.1007/s10592-005-9012-x

    Article  Google Scholar 

  • Friesen VL, González JA, Cruz-Delgado F (2006) Population genetic structure and conservation of the Galapagos Petrel (Pterodroma phaeopygia). Conserv Gen 7:105–115. doi:10.1007/s10592-005-8704-6

    Article  Google Scholar 

  • Friesen VL, Burg TM, McCoy KD (2007) Mechanisms of population differentiation in seabirds. Mol Ecol 16:1765–1785. doi:10.1111/j.1365-294X.2006.03197.x

    Article  CAS  Google Scholar 

  • Gaston AJ, Jones IL (1998) The Auks. Oxford University Pres, Oxford

    Google Scholar 

  • Genovart M, Oro D, Bonhomme F (2003) Genetic and morphological differentiation between the two largest breeding colonies of Audouin’s Gull Larus audouinii. Ibis 145:448–456. doi:10.1046/j.1474-919X.2003.00187.x

    Article  Google Scholar 

  • Gibson DD, Byrd GV (2007) Birds of the Aleutian Islands, Alaska. Series in Ornithology, No.1. Nuttall Ornithological Club and American Ornithologists’ Union

  • Hardouin LA, Reby YD, Bavoux C, Burneleau G, Bretagnolle V (2007) Communication of male quality in owl hoots. Am Nat 169:552–562

    Article  Google Scholar 

  • Ibarguchi G, Gaston AJ, Friesen VL (2011) Philopatry, morphological divergence, and kin groups: structuring in Thick-billed Murres Uria lomvia within a colony in Arctic Canada. J Avian Biol 42:134–150. doi:10.1111/j.1600-048X.2010.05023.x

    Article  Google Scholar 

  • Jones IL (1993a) Crested Auklet (Aethia cristatella). In: Poole A. and Gill F. (eds). The birds of North America, No 70. Philadelphia: The Academy of Natural Sciences. The American Ornithologists’ Union, Washington, D.C.

  • Jones IL (1993b) Sexual differences in bill shape and external measurements of Crested Auklets. Wilson Bull 105(3):525–529

    Google Scholar 

  • Jones IL, Hunter FM (1999) Experimental evidence for mutual inter- and intrasexual selection favouring a Crested Auklet ornament. Anim Behav 57:521–528

    Article  Google Scholar 

  • Jones IL, Hunter FM, Fraser G (2000) Patterns in variation of ornaments of Crested Auklets Aethia cristatella. J Avian Biol 31:119–127

    Article  Google Scholar 

  • Jones IL, Hunter FM, Robertson GJ, Fraser G (2004) Natural variation in the sexually selected feather ornaments of Crested Auklets (Aethia cristatella) does not predict future survival. Behav Ecol 15(2):332–337. doi:10.1093/beheco/arh018

    Article  Google Scholar 

  • Kalinowski ST, Taper ML, Marshall TC (2007) Revising how the computer program CERVUS accommodates genotyping error increases success in paternity assignment. Mol Ecol 16:1099–1106. doi:10.1111/j.1365-294x.2007.03089.x

    Article  Google Scholar 

  • Kidd MG, Friesen VL (1998) Sequence variation in the guillemot (Alcidae: Cepphus) mitochondrial control region and its nuclear homolog. Mol Biol Evol 15(1):61–70

    Article  CAS  Google Scholar 

  • Klenova AV, Shienok AN (2012) Findings of rare auk species on Mednyi Island (Commander Islands) during summer 2012. Conservation of Biodiversity of Kamchatka and Coastal Waters. In: Torkanov AM, Cherniagina OA, Bugaev VF (eds). Kamchatpress, Petropavlovsk-Kamchatsky, Russia, pp 238–242 (in Russian)

  • Klenova AV, Zubakin VA, Zubakina EV (2011) Vocal and optical indicators of individual quality in a social seabird, the Crested Auklet (Aethia cristatella). Ethology 117:356–365. doi:10.1111/j.1439-0310.2011.01880.x

    Article  Google Scholar 

  • Klenova AV, Zubakin VA, Zubakina EV (2012a) Inter- and intra-season stability of vocal individual signatures in a social seabird, the Crested Auklet. Acta Ethol 15:141–152. doi:10.1007/s10211-011-0120-y

    Article  Google Scholar 

  • Klenova AV, Zubakin VA, Zubakina EV, Kolesnikova YA (2012b) Indicators of individuality and sex in advertising calls of two closely related auklet species (Charadriiformes, Alcidae): Crested Auklet and Parakeet Auklet (Aethia cristatella, Cyclorhynchus psittacula). Zoologicheskii Zhurnal 91(7):869–880 (in Russian)

    Google Scholar 

  • Klenova AV, Konyukhov NB, Andreev AV, Kharitonov SP, Zubakin VA, Shienok AN (2013) Between-population variability in body size and acoustic communication of Whiskered Auklet (Aethia pygmaea). In: Pacific Seabird Group 40th Annual Meeting, Portland 37

  • Konyukhov NB, Zubakin VA (1994) Paradoxes of the Whiskered Auklet (Aethia pygmaea) II. Return of juveniles to a colony. Beringian Seab Bull Magadan 2:60–63

    Google Scholar 

  • Louis VLS, Barlow JC (1987) Comparisons between morphometric and genetic differentiation among populations of the Eurasian Tree Sparrow (Passer montanus). Wilson Bull 99(4):628–641

    Google Scholar 

  • Mager JNIII, Walcott C, Piper WH (2007) Male Common Loons, Gavia immer, communicate body mass and condition through dominant frequencies of territorial yodels. Anim Behav 73:683–690. doi:10.1016/j.anbehav.2006.10.009

    Article  Google Scholar 

  • Meyers RA, Stakebake EF (2005) Anatomy and histochemistry of spread-wing posture in birds. 3. Immunochemistry of flight muscles and the “shoulder lock” in Albatrosses. J Morphol 263:12–29. doi:10.1002/jmor.10284

    Article  Google Scholar 

  • Miyazaki M, Waas JR (2003) Acoustic properties of male advertisement and their impact on female responsiveness in Little Penguins Eudyptula minor. J Avian Biol 34:229–232. doi:10.1034/j.1600-048X.2003.03099.x

    Article  Google Scholar 

  • Moum T, Arnason E (2001) Genetic diversity and population history of two related seabird species based on mitochondrial DNA control region sequences. Mol Ecol 10:2463–2478. doi:10.1046/j.0962-1083.2001.01375.x

    Article  CAS  Google Scholar 

  • Moum T, Erikstad KE, Bjorklid E (1991) Restriction fragment analysis of mitochondrial DNA in Common Murres, Uria aalge, from four Norwegian seabird colonies. Can J Zool 69:1577–1584

    Article  CAS  Google Scholar 

  • Narum SR (2006) Beyond Bonferroni: Less conservative analyses for conservation genetics. Conserv Genet 7:783–787. doi:10.1007/s10592-005-9056-y

    Article  CAS  Google Scholar 

  • Nei M (1987) Molecular evolutionary genetics. Columbia University Press, New-York

    Google Scholar 

  • Nettleship DN (1996) Family Alcidae. In: Del Hoyo J, Elliot A, Sargatal J (eds) Handbook of the birds of the world 3. Lynx Edicions, Barcelona, pp 678–724

    Google Scholar 

  • Patirana A, Hatch SA, Friesen VL (2002) Population differentiation in the red-legged kittiwake (Rissa brevirostris) as revealed by mitochondrial DNA. Conserv Genet 3:335–340. doi:10.1023/A:1019935726807

    Article  CAS  Google Scholar 

  • Pearce RL, Wood JJ, Artukhin Y, Birt TP (2002) Mitochondrial DNA suggests high gene flow in Ancient Murrelets. The Condor 104:84–91. doi:10.1650/0010-5422(2002)104[0084:MDSHGF]2.0.CO;2

    Article  Google Scholar 

  • Pennycuick CJ (1982) The flight of Petrels and Albatrosses (Procellariiformes), observed in South Georgia and its vicinity. Philos Trans R Soc Lond B Biol Sci 300(1098):75–106. doi:10.1098/rstb.1982.0158

    Article  Google Scholar 

  • Posada D, Crandall KA (1998) MODELTEST: testing the model of DNA substitution. Bioinformatics 14(9):817–818

    Article  CAS  Google Scholar 

  • Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959

    CAS  Google Scholar 

  • Quinn JP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge

    Book  Google Scholar 

  • Robinson JL, Jones IL (2013) Year-round spatial and temporal distribution of a small, diving seabird, the Crested Auklet (Aethia cristatella), originating from a breeding site at Buldir island, Aleutian Islands. In: Pacific Seabird Group 40th Annual Meeting. Portland, p 61

  • Seneviratne SS, Jones IL, Miller EH (2009) Vocal repertoires of auklets (Alcidae: Aethini): structural organization and categorization. Wilson J Ornithol 121(3):568–584. doi:10.1676/08-008.1

    Article  Google Scholar 

  • Shuntov VP (1965) Seasonal aspects in the distribution of seabirds in open waters of the Sea of Japan. Zoologicheskii Zhurnal 44(3):411–422

    Google Scholar 

  • Smith AL, Friesen VL (2007) Differentiation of sympatric populations of the Band-rumped Storm-petrel in the Galapagos Islands: an examination of genetics, morphology, and vocalizations. Mol Ecol 16:1593–1603. doi:10.1111/j.1365-294X.2006.03154.x

    Article  CAS  Google Scholar 

  • Smith AL, Monteiro L, Hasegawa O, Friesen VL (2007) Global phylogeography of the Band-rumped Storm-petrel (Oceanodroma castro; Procellariiformes: Hydrobatidae). Mol Phylogenet Evol 43:755–773. doi:10.1016/j.ympev.2007.02.012

    Article  Google Scholar 

  • Soha JA, Nelson DA, Parker PG (2004) Genetic analysis of song dialect populations in Puget Sound White-crowned Sparrows. Behav Ecol 15(4):636–646. doi:10.1093/beheco/arh055

    Article  Google Scholar 

  • Steeves TE, Anderson DJ, Friesen VL (2005) A role for nonphysical barriers to gene flow in the diversification of a highly vagile seabird, the Masked Booby (Sula dactylatra). Mol Ecol 14:3877–3887. doi:10.1111/j.1365-294X.2005.02713.x

    Article  CAS  Google Scholar 

  • Tajima F (1989) Statistical method for testing the neutral mutation hypothesis by DNA polymorphism. Genetics 123:585–595

    CAS  Google Scholar 

  • Tajima F (1993) Measurement of DNA polymorphism. In: Takahata N, Clark AG (eds) Mechanisms of molecular evolution. Introduction to molecular paleopopulation biology. Japan Scientific Societies Press, Tokyo, pp 37–59

    Google Scholar 

  • Taylor SA, Friesen VL (2012) Use of molecular genetics for understanding seabird evolution, ecology and conservation. Mar Ecol Prog Ser 451:285–304. doi:10.3354/meps09694

    Article  Google Scholar 

  • Vásquez-Carrillo C, Friesen V, Hall L, Peery MZ (2014) Variation in MHC class II B genes in marbled murrelets: implications for delineating conservation units. Anim Conservation 17:244–255. doi:10.1111/acv.12089

    Article  Google Scholar 

  • Wallace SJ, Wolf SG, Bradley RW, Harvey AL, Friesen VL (2015) The influence of biogeographical barriers on the population genetic structure and gene flow in a coastal Pacific seabird. J Biogeogr 42:390–400. doi:10.1111/jbi.12404

    Article  Google Scholar 

  • Walsh HE, Jones IL, Friesen VL (2005) A test of founder effect speciation using multiple loci in the auklets (Aethia spp.). Genetics 171:1885–1894. doi:10.1534/genetics.105.043380

    Article  CAS  Google Scholar 

  • Watterson G (1978) The homozygosity test of neutrality. Genetics 88:405–417

    CAS  Google Scholar 

  • Wojczulanis-Jakubas K, Jakubas D, Welcker J, Harding AMA, Karnovsky NJ, Kidawa D, Steen H, Stempniewicz L, Camphuysen CJ (2011) Body size variation of a high-Arctic seabird: the Dovekie (Alle alle). Polar Biol 34(6):847–854. doi:10.1007/s00300-010-0941-6

    Article  Google Scholar 

  • Wojczulanis-Jakubas K, Kilikowska A, Harding AMA, Jakubas D, Karnovsky NJ, Steen H, Strøm H, Welcker J, Gavrilo M, Lifjeld JT, Johnsen A (2014) Weak population genetic differentiation in the most numerous Arctic seabird, the Little Auk. Polar Biol 37:621–630. doi:10.1007/s00300-014-1462-5

    Article  Google Scholar 

  • Wright TF, Rodriguez AM, Fleischer RC (2005) Vocal dialects, sex-biased dispersal, and microsatellite population structure in the parrot Amazona auropalliata. Mol Ecol 14:1197–1205. doi:10.1111/j.1365-294X.2005.02466.x

    Article  CAS  Google Scholar 

  • Zubakin VA (1990) Some aspects of breeding biology and social behavior of Crested Auklet (Aethia cristatella). In: Kondratyev AYA (ed) Studies of colonial seabirds in USSR (information bulletin). Institute of Biological Problems of the North, Magadan, pp 9–13 (in Russian)

    Google Scholar 

  • Zubakin VA, Konyukhov NB (2001) Breeding biology of the Whiskered Auklet (Aethia pygmaea): postbreeding season. Biol Bull 28(1):31–39

    Article  Google Scholar 

  • Zubakin VA, Volodin IA, Klenova AV, Zubakina EV, Volodina EV, Lapshina EN (2010) Behavior of the Crested Auklet (Aethia cristatella, Charadriiformes, Alcidae) in breeding season: visual and acoustic displays. Biol Bull 37(8):823–835 (in Russian)

    Article  Google Scholar 

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Acknowledgments

We thank Vladimir Burkanov, Mikhail Goltsman, Alexander Shienok and staff of Komandorsky Nature Reserve, especially Evgeniy Mamaev and Anastasia Kuznecova, for providing opportunity for work on Medny Island and logistic support. Vladimir Burkanov also provided logistical support for collecting the samples at the salmon gillnet fishery. We also thank Alexander Andreev, Elena Golubova, Elena Zubakina, for providing opportunity for work and for help with data gathering on Talan island. We are very grateful to Mr. Toshiji Fukuda, the animal photographer, for hiring a ship to get to the Saint-Jonah Island, and also to Vladimir Medvedev, the animal photographer, for help during the Saint-Jonah Island voyage. We also thank US Fish and Wildlife Service for providing the opportunity for work on Buldir, Little Diomede and St. Lawrence islands, and our American colleagues David Irons, Adrian Gall, Lisa Sheffield, Ian Rose and Jeffrey Williams for help with data gathering on these islands. We also thank Marina Kholodova for help with genetic DNA analysis. We also thank anonymous reviewers, prof. Edward H. Miller and Thomas I. Van Pelt for manuscript reading, multiple constructive comments and correction of written English. During our work, we adhered to the “Guidelines for the treatment of animals in behavioral research and teaching” (Anim. Behav. 65: 249–255) and to the laws of Russian Federation, the country where the research was conducted. This study was funded by the Grant of President RF (grant MK-1781-2012.4) and by the Russian Foundation for Basic Research (grant 14-04-01138a). None of our funders had any influence on the content of the submitted or published manuscript. None of our funders require approval of the final manuscript to be published.

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Pshenichnikova, O.S., Klenova, A.V., Sorokin, P.A. et al. The Crested Auklet, Aethia cristatella (Alcidae, Charadriiformes), does not vary geographically in genetics, morphology or vocalizations. Mar Biol 162, 1329–1342 (2015). https://doi.org/10.1007/s00227-015-2672-2

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