Abstract
Pacific herring (Clupea pallasii) is divided into three subspecies: two in northeast Europe and one in the north Pacific Ocean. Genetic studies have indicated that the populations in northeast Europe have derived from the northwest Pacific herring recently, or during the last 10–15 kyr, and that they are distinct from the population in the northeast Pacific. In addition, hybridization between the Pacific herring and the Atlantic herring has been documented. Otolith variation has been considered to be largely affected by environmental variation, but here we evaluate whether the genetic differentiation is reflected in otolith shape differences. A clear difference in otolith shape was observed between the genetically differentiated herring species Clupea harengus from the Atlantic and C. pallasii. The otolith shape of C. p. suworowi in the Barents Sea was different from the shape of C. pallasii in northern Norway and C. p. pallasii from the Pacific. Populations of C. p. pallasii, sampled east and west of the Alaska Peninsula, which belong to two genetically different clades of the C. p. pallasii in the Pacific Ocean, show a clear difference in otolith shape. C. p. suworowi and the local C. pallasii peripheral population in Balsfjord in northern Norway are more similar to the northwest Pacific herring (C. p. pallasii) than to the northeast Pacific herring (C. p. pallasii), both genetically and in otolith shape. The Balsfjord population, known to be influenced by introgression of mtDNA from the Atlantic herring, does not show any sign of admixture in otolith shape between the two species. A revised classification, considering the observed genetic and morphological evidence, should rather group the northwest Pacific herring in the Bering Sea together with the European populations of C. pallasii than with the northeast Pacific herring in the Gulf of Alaska.
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References
Anderson MJ, Willis TJ (2003) Canonical analysis of principal coordinates: a useful method of constrained ordination for ecology. Ecology 84:511–525. doi:10.1890/0012-9658(2003)084[0511:Caopca]2.0.Co;2
Bird JL, Eppler DT, Checkley DM (1986) Comparisons of herring otoliths using Fourier series shape analysis. Can J Fish Aquat Sci 43:1228–1234. doi:10.1139/F86-152
Burke N, Brophy D, King PA (2008a) Otolith shape analysis: its application for discriminating between stocks of Irish Sea and Celtic Sea herring (Clupea harengus) in the Irish Sea. ICES J Mar Sci 65:1670–1675. doi:10.1093/icesjms/fsn177
Burke N, Brophy D, King PA (2008b) Shape analysis of otolith annuli in Atlantic herring (Clupea harengus); a new method for tracking fish populations. Fish Res 91:133–143. doi:10.1016/j.fishres.2007.11.013
Carr SM, Kivlichan DS, Pepin P, Crutcher DC (1999) Molecular systematics of gadid fishes: implications for the biogeographic origins of Pacific species. Can J Zool 77:19–26
Castonguay M, Simard P, Gagnon P (1991) Usefulness of Fourier analysis of otolith shape for atlantic mackerel (Scomber scombrus) stock discrimination. Can J Fish Aquat Sci 48:296–302. doi:10.1139/f91-041
Christiansen J, Fevolden SE, Byrkjedal I (2005) The occurrence of Theragra finnmarchica Koefoed, 1956 (Teleostei, Gadidae), 1932–2004. J Fish Biol 66:1193–1197
Dray S, Dufour AB (2007) The ade4 package: implementing the duality diagram for ecologists. J Stat Softw 22:1–20
Eggers F, Slotte A, Libungan LA, Johannessen A, Kvamme C, Moland E, Olsen EM, Nash RDM (2014) Seasonal dynamics of Atlantic herring (Clupea harengus L.) populations spawning in the vicinity of marginal habitats. PLoS One 9(11):e111985. doi:10.1371/journal.pone.0111985
Jørstad K (2004) Evidence for two highly differentiated herring groups at Goose Bank in the Barents Sea and the genetic relationship to Pacific herring, Clupea pallasi. Environ Biol Fishes 69:211–221
Jørstad KE, Nævdal G (1981) Significance of population genetics on management of herring stocks. ICES CM1981/H: 64
Jørstad KE, Pedersen SA (1986) Discrimination of herring populations in a northern Norwegian fjord: genetic and biological aspects. ICES CM 1986/H: 63
Jørstad KE, Dahle C, Paulsen OI (1994) Genetic comparison between Pacific herring (Clupea pallasi) and a Norwegian fjord stock of Atlantic herring (Clupea harengus). Can J Fish Aquat Sci 51:233–239
Laakkonen HM, Lajus DL, Strelkov P, Vainola R (2013) Phylogeography of amphi-boreal fish: tracing the history of the Pacific herring Clupea pallasii in North-East European seas. BMC Evol Biol. doi:10.1186/1471-2148-13-67
Laakkonen HM, Strelkov P, Lajus DL, Väinölä R (2015) Introgressive hybridization between the Atlantic and Pacific herrings (Clupea harengus and C. pallasii) in the north of Europe. Mar Biol 162:39–54. doi:10.1007/s00227-014-2564-x
Libungan LA, Pálsson S (2015) ShapeR: an R package to study otolith shape variation among fish populations. PLoS One 10(3):e0121102. doi:10.1371/journal.pone.0121102
Libungan LA, Óskarsson GJ, Slotte A, Arge JA, Pálsson S (2015a) Otolith shape: a population marker for Atlantic herring Clupea harengus. J Fish Biol 86:1377–1395. doi:10.1111/jfb.12647
Libungan LA, Slotte A, Husebø Å, Godiksen JA, Pálsson S (2015b) Latitudinal gradient in otolith shape among local populations of Atlantic herring (Clupea harengus L.) in Norway. PLoS One 10:e0130847. doi:10.1371/journal.pone.0130847
Liu M, Lin LS, Gao TX, Yanagimoto T, Sakurai Y, Grant WS (2012) What maintains the Central North Pacific genetic discontinuity in Pacific herring? PLoS One 7(12):e50340. doi:10.1371/journal.pone.0050340
Lleonart J, Salat J, Torres GJ (2000) Removing allometric effects of body size in morphological analysis. J Theor Biol 205:85–93. doi:10.1006/jtbi.2000.2043
Messieh SN (1972) Use of otoliths in identifying herring stocks in the Southern Gulf of St. Lawrence and adjacent waters. J Fish Res Board Can 29:1113–1118. doi:10.1139/f72-166
Messieh SN, MacDougal C, Claytor R (1989) Separation of Atlantic herring (Clupea harengus) stocks in the Southern Gulf of St. Lawrence using digitized otolith morphometrics and discriminant function analysis. Can Tech Rep Fish Aquat Sci 1647:1–22
Mjanger H, Hestenes K, Svendsen BV, de Lange Wenneck T (2011) Håndbok for prøvetaking av fisk og krepsdyr. V. 3.16 (in Norwegian)
Nason G (2012) wavethresh: wavelets statistics and transforms, version 4.5. R package. http://CRAN.R-project.org/package=wavethresh
O’Connell M, Dillon MC, Wright JM, Bentzen P, Merkouris S, Seeb J (1998) Genetic structuring among Alaskan Pacific herring populations identified using microsatellite variation. J Fish Biol 53:150–163. doi:10.1111/j.1095-8649.1998.tb00117.x
Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’Hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H (2013) vegan: community ecology package, version 2.0-7. R package. http://CRAN.R-project.org/package=vegan
Pampoulie C, Slotte A, Óskarsson GJ, Helyar S, Jónsson Á, Ólafsdóttir G, Skírnisdóttir S, Libungan LA, Jacobsen JA, Joensen H, Nielsen HH, Sigurðsson SK, Daníelsdóttir AK (2015) Stock structure of Atlantic herring (Clupea harengus L.) in the Norwegian Sea and adjacent waters. Mar Ecol Prog Ser 522:219–230. doi:10.3354/meps11114
Præbel K, Knudsen R, Siwertsson A, Karhunen M, Kahilainen KK, Ovaskainen O, Østbye K, Peruzzi S, Fevolden SE, Amundsen PA (2013) Ecological speciation in postglacial European whitefish: rapid adaptive radiations into the littoral, pelagic, and profundal lake habitats. Ecol Evol 3:4970–4986
R Core Team (2015) R: a language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/
Reist JD (1985) An empirical-evaluation of several univariate methods that adjust for size variation in morphometric data. Can J Zool 63:1429–1439
Semenova AV, Andreeva AP, Karpov AK, Novikov GG (2009) An analysis of allozyme variation in herring Clupea pallasii from the White and Barents Seas. J Ichthyol 49:313–330. doi:10.1134/S0032945209040043
Semenova AV, Andreeva AP, Karpov AK, Stroganov AN, Rubtsova GA, Afanas’ev KI (2013) Analysis of microsatellite loci variations in herring (Clupea pallasii marisalbi) from the White Sea. Russ J Genet 49:652–666. doi:10.1134/S1022795413060100
Semenova AV, Stroganov AN, Afanasiev KI, Rubtsova GA (2015) Population structure and variability of Pacific herring (Clupea pallasii) in the White Sea, Barents and Kara Seas revealed by microsatellite DNA analyses. Polar Biol. doi:10.1007/s00300-015-1653-8
Svetovidov AN (1952) Seldevye (Clupeidae). In: Fauna SSSR. Ryby 2(1). Zoologicheskii Institut Akademiya Nauk SSSR, Moscow and Leningrad
Turan C (2000) Otolith shape and meristic analysis of herring (Clupea harengus) in the North-East Atlantic. Arch Fish Mar Res 48:283–295
Ursvik A, Breines R, Christiansen JS, Fevolden S-E, Coucheron DH, Johansen SD (2007) A mitogenomic approach to the taxonomy of pollocks: Theragra chalcogramma and T. finnmarchica represent one single species. BMC Evol Biol 7:86. doi:10.1186/1471-2148-7-86
Väinölä R (2003) Repeated trans-Arctic invasions in littoral bivalves: molecular zoogeography of the Macoma balthica complex. Mar Biol 143:935–946. doi:10.1007/s00227-003-1137-1
Vermeij GJ (1991) Anatomy of an invasion: the trans-Arctic interchange. Paleobiology 17:281–307
Vilhjálmsson H (1994) The Icelandic capelin stock. Capelin (Mallotus villosus Müller) in the Iceland–Greenland–Jan Mayen area. J Mar Res Inst 13:1–281
Warnes GR, Bolker B, Bonebakker L, Gentleman R, Liaw WHA, Lumley T, Maechler M, Magnusson A, Moeller S, Schwartz M, Venables B (2014) gplots: various R programming tools for plotting data. R package version 2.13.0. http://CRAN.R-project.org/package=gplots
Acknowledgments
Torstein Pedersen at the University of Tromsø is thanked for providing the samples from Balsfjord in Norway. Ole Ingar Paulsen at the Institute of Marine Research in Norway is thanked for allozyme analysis, splitting out Norwegian spring spawning herring (C. harengus) from Balsfjord herring (C. pallasii) in Balsfjord. This work was funded by the Assistant teacher’s grant of the University of Iceland.
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Libungan, L.A., Slotte, A., Otis, E.O. et al. Otolith variation in Pacific herring (Clupea pallasii) reflects mitogenomic variation rather than the subspecies classification. Polar Biol 39, 1571–1579 (2016). https://doi.org/10.1007/s00300-015-1882-x
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DOI: https://doi.org/10.1007/s00300-015-1882-x