Abstract
The Antarctic fish fauna is characterized by high endemism and low species diversity with one perciform suborder, the Notothenioidei, dominating the whole species assemblage on the shelves and slopes. Notothenioids diversified in situ through adaptive radiation and show a variety of life history strategies as adults ranging from benthic to pelagic modes. Their larval development is unusually long, lasting from a few months to more than a year, and generally includes a pelagic larval stage. Therefore, the advection of eggs and larvae with ocean currents is a key factor modulating population connectivity. Here, we compare the genetic population structures and gene flow of seven ecologically distinct notothenioid species of the southern Scotia Arc based on nuclear microsatellites and mitochondrial DNA sequences (D-loop/cytochrome b). The seven species belong to the families Nototheniidae (Gobionotothen gibberifrons, Lepidonotothen squamifrons, Trematomus eulepidotus, T. newnesi) and Channichthyidae (Chaenocephalus aceratus, Champsocephalus gunnari, Chionodraco rastrospinosus). Our results show low-population differentiation and high gene flow for all investigated species independent of their adult life history strategies. In addition, gene flow is primarily in congruence with the prevailing ocean current system, highlighting the role of larval dispersal in population structuring of notothenioids.
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References
Andriashev AP (1987) A general review of the Antarctic bottom fish fauna. In: Kullander SO, Fernholm B (eds) Proceedings, fifth congress of European ichthyologists, Stockholm 1985. Swedish Museum of Natural History, Stockholm, pp 357–372
Appleyard S, Ward R, Williams R (2002) Population structure of the Patagonian toothfish around Heard, McDonald and Macquarie Islands. Antarct Sci 14:364–373
Barnes DKA, Conlan KE (2007) Disturbance, colonization and development of Antarctic benthic communities. Phil Trans R Soc B 362:11–38
Bay LK, Crozier RH, Caley MJ (2006) The relationship between population genetic structure and pelagic larval duration in coral reef fishes on the Great Barrier Reef. Mar Biol 149:1247–1256
Belkhir K, Borsa P, Chikhi et al (2001) Genetix 402, logiciel sous Windows TM pour la génétique des populations
Briggs J (2003) Marine centres of origin as evolutionary engines. J Biogeogr 30:1–18
Casaux R, Mazzotta A, Barrera-Oro ER (1990) Seasonal aspects of the biology and diet of nearshore nototheniid fish at Potter Cove, South Shetland Islands, Antarctica. Polar Biol 11:63–72
Chapuis M, Estoup A (2007) Microsatellite null alleles and estimation of population differentiation. Mol Biol Evol 24:621–631
Cheng CC (1998) Origin and mechanism of evolution of anti-freeze glycoproteins in polar fishes. In: Di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica. A biological overview. Springer, Milan, pp 311–328
Clarke A, Johnston I (1996) Evolution and adaptive radiation of Antarctic fish. Trends Ecol Evol 11:212–218
Cowen R, Sponaugle S (2009) Larval dispersal and marine population connectivity. Annu Rev Mar Sci 1:443–466
Daniels R (1982) Feeding ecology of some fishes of the Antarctic Peninsula. Fish Bull US 80:575–588
Dayton P, Mordida B, Bacon F (1994) Polar marine communities. Am Zool 34:90–99
Derome N, Chen W, Dettai A et al (2002) Phylogeny of Antarctic dragonfishes (Bathydraconidae, Notothenioidei, Teleostei) and related families based on their anatomy and two mitochondrial genes. Mol Phylogenet Evol 24:139–152
Detrich H, Jones C, Kim S et al (2005) Nesting behavior of the icefish Chaenocephalus aceratus at Bouvetøya Island, Southern Ocean. Polar Biol 28:828–832
DeWitt HH, Heemstra PC, Gon O (1990) Nototheniidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 279–380
Duhamel G (1981) Caracteristiques biologiques des principales especes de poissons du plateau continental des Iles Kerguelen. Cybium 5:19–32
Duhamel G, Ozouf-Costaz C (1985) Age, growth and reproductive biology of Notothenia squamifrons Gunther, 1880 from the Indian sector of the Southern Ocean. Polar Biol 4:143–153
Eastman JT (1991) Evolution and diversification of antarctic notothenioid fishes. Am Zool 31:93–109
Eastman JT (1993) Antarctic fish biology: evolution in a unique environment. Academic Press, San Diego
Eastman JT (2000) Antarctic notothenioid fishes as subjects for research in evolutionary biology. Antarct Sci 12:276–287
Eastman JT (2005) The nature of the diversity of Antarctic fishes. Polar Biol 28:93–107
Eastman JT, McCune A (2000) Fishes on the Antarctic continental shelf: evolution of a marine species flock. J Fish Biol 57(Suppl A):84–102
Ekau W (1989) Egg development of Trematomus eulepidotus Regan, 1914 (Nototheniidae, Pisces) from the Weddell Sea, Antarctica. Cybium 13:213–219
Ekau W (1990) Demersal fish fauna of the Weddell Sea, Antarctica. Antarct Sci 2:129–137
Ekau W (1991) Reproduction in high Antarctic fishes (Notothenioidei). Meeresforsch 33:159–167
Evanno G, Regnaut S, Goudet J (2005) Detecting the number of clusters of individuals using the software structure: a simulation study. Mol Ecol 14:2611–2620
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 Resour 10:564–567
Fanta E, Meyer AA, Grötzner SR, Luvizotto MF (1994) Comparative study on feeding strategy and activity patterns of two Antarctic fish: Trematomus newnesi Boulenger, 1902 and Gobionotothen gibberifrons (Lonnberg, 1905) (Pisces, Nototheniidae) under different light conditions. Antarct Rec 38:13–29
Garza J, Williamson E (2001) Detection of reduction in population size using data from microsatellite loci. Mol Ecol 10:305–318
Glaubitz JC (2004) Convert: a user-friendly program to reformat diploid genotypic data for commonly used population genetic software packages. Mol Ecol Notes 4:309–310
Goudet J (1995) FSTAT (Version 1.2): a computer program to calculate F-statistics. J Hered 86:485–486
Goudet J (2001) FSTAT, a program to estimate and test gene diversities and fixation indices, version 2.9.3. http://www2.unil.ch/popgen/softwares/fstat.htm
Hej J, Nielsen R (2007) Integration within the Felsenstein equation for improved Markov chain Monte Carlo methods in population genetics. Proc Natl Acad Sci USA 104:2785–2790
Heywood KJ, Garabato A, Stevens D (2002) High mixing rates in the abyssal Southern Ocean. Nature 415:1011–1014
Hureau JC (1985) Channichthyidae. In: Fischer W, Hureau JC (eds) FAO species identification sheets for fishery purposes. Southern Ocean (Fishing areas 48, 58 and 88), vol 2. FAO, Rome, pp 261–277
Iwami T, Kock KH (1990) Channichthyidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. JLB Smith Institute of Ichthyology, Grahamstown, pp 381–399
Jones CD, Kock KH (2006) Standing stock, spatial distribution, and biological features of demersal finfish from the 2006 US AMLR bottom trawl survey of the northern Antarctic Peninsula and Joinville-D’Urville Islands (Subarea 48.1). WG-FSA-06/14. CCAMLR, Hobart
Kellermann AK (1986) Zur Biologie der Jugendstadien der Notothenioidei (Pisces) an der Antarktischen Halbinsel. Ber Polarforsch 31:1–155
Kellermann AK (1989) The larval fish community in the zone of seasonal pack-ice cover and its seasonal and interannual variability. Arch Fisch Wiss 39(Beih 1):81–109
Kock KH (1981) Fischereibiologische Untersuchungen an drei antarktischen Fischarten: Champsocephalus gunnari Lönnberg, 1905, Chaenocephalus aceratus (Lönnberg, 1906) und Pseudochaenichthys georgianus Norman, 1937 (Notothenioidei, Channichthyidae). Mitt Inst Seefisch Hambg 32:1–226
Kock KH (1989) Reproduction in fish around Elephant Island. Arch Fisch Wiss 39(Beih 1):171–210
Kock KH (1992) Antarctic fish and fisheries. Cambridge University Press, Cambridge
Kock KH (2005a) Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, part I. Polar Biol 28:862–895
Kock KH (2005b) Antarctic icefishes (Channichthyidae): a unique family of fishes. A review, part II. Polar Biol 28:897–909
Kock KH, Everson I (1997) Biology and ecology of mackerel icefish, Champsocephalus gunnari: an Antarctic fish lacking hemoglobin. Comp Biochem Physiol A 118:1067–1077
Kock KH, Jones CD (2005) Fish stocks in the southern Scotia Arc region—a review and prospects for future research. Rev Fish Sci 13:75–108
Kock KH, Kellermann AK (1991) Reproduction in Antarctic notothenioid fish. Antarct Sci 3:125–150
Kock KH, Möller H (1977) On the occurrence of the parasite copepod Eubrachiella antarctica on some Antarctic fish. Arch Fisch Wiss 28:149–156
Kock KH, Jones CD, Wilhelms S (2001) Biological characteristics of Antarctic fish stocks in the southern Scotia Arc region. Ccamlr Sci 7:1–41
Kuhn KL, Gaffney PM (2006) Preliminary assessment of population structure in the mackerel icefish (Champsocephalus gunnari). Polar Biol 29:927–935
Kuhn KL, Gaffney PM (2008) Population subdivision in the Antarctic toothfish (Dissostichus mawsoni) revealed by mitochondrial and nuclear single nucleotide polymorphisms (SNPs). Antarct Sci 20:327–338
La Mesa M, Ashford J (2008a) Age and growth of ocellated icefish, Chionodraco rastrospinosus DeWitt and Hureau, 1979, from the South Shetland Islands. Polar Biol 31:1333–1342
La Mesa M, Ashford J (2008b) Age and early life history of juvenile scotia sea icefish, Chaenocephalus aceratus, from Elephant and the South Shetland Islands. Polar Biol 31:221–228
La Mesa M, Vacchi M, Sertorio T (2000) Feeding plasticity of Trematomus newnesi (Pisces, Nototheniidae) in Terra Nova Bay, Ross Sea, in relation to environmental conditions. Polar Biol 23:38–45
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinforma 25:1451–1452
Lisovenko LA, Sil’yanova ZS (1979) The fecundity of some species of the family Nototheniidae in the Atlantic sector of the Southern Ocean. J Ichthyol 19:79–85
Lisovenko LA, Sil’yanova ZS (1980) The reproduction and fecundity of fish of the family Chaenichthyidae. In: An ecological and biological description of some species of Antarctic Fishes. Trudy All-Union Institute for Fisheries Research and Oceanography, Moscow, pp 38–52
Lisovenko LA, Zakharov GP (1988) On fecundity of the striped pike glassfish, Champsocephalus gunnari, in the region of South Georgia Island. J Ichthyol 27:131–134
Loeb VJ, Kellermann AK, Koubbi P et al (1993) Antarctic larval fish assemblages: a review. Bull Mar Sci 53:416–449
Lumpkin R, Pazos M (2007) Measuring surface currents with surface velocity program drifters: the instrument, the data, and some recent results. In: Mariano A et al (eds) Lagrangian analysis and prediction of coastal and ocean dynamics. Cambridge University Press, Cambridge, pp 39–67
Matschiner M, Salzburger W (2009) TANDEM: integrating automated allele binning into genetics and genomics workflows. Bioinforma 25:1982–1983
Matschiner M, Hanel R, Salzburger W (2009) Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons. Mol Ecol 18:2574–2587
Matschiner M, Hanel R, Salzburger W (2010) Phylogeography and speciation processes in marine fishes and fishes from large freshwater lakes. In: Rutgers DS (ed) Phylogeography. Concepts, intraspecific patterns and speciation processes. Nova Science Publishers, New York, pp 1–29
Matschiner M, Hanel R, Salzburger W (2011) On the origin and trigger of the notothenioid adaptive radiation. PLoS one 6:e18911
Mills L, Allendorf F (1996) The one-migrant-per-generation rule in conservation and management. Conserv Biol 10:1509–1518
North AW (2001) Early life history strategies of notothenioids at South Georgia. J Fish Biol 58:496–505
North AW (2005) Mackerel icefish size and age differences and long-term change at South Georgia and Shag Rocks. J Fish Biol 67:1666–1685
Papetti C, Zane LL, Patarnello T (2006) Isolation and characterization of microsatellite loci in the icefish Chionodraco rastrospinosus (Perciformes, Notothenioidea, Channichthyidae). Mol Ecol Notes 6:207–209
Papetti C, Susana E, Patarnello T, Zane LL (2009) Spatial and temporal boundaries to gene flow between Chaenocephalus aceratus populations at South Orkney and South Shetlands. Mar Ecol Prog Ser 376:269–281
Parker R, Paige K, De Vries A (2002) Genetic variation among populations of the Antarctic toothfish: evolutionary insights and implications for conservation. Polar Biol 25:256–261
Permitin Y (1973) Fecundity and reproductive biology of icefish (Chaenichthyidae), fish of the family Muarenolepidae and dragonfish (Bathydraconidae) of the Scotia Sea (Antarctica). J Ichthyol 13:204–215
Permitin Y, Sil’yanova Z (1971) New data on the reproductive biology and fecundity of fishes of the genus Notothenia Rich. in the Scotia Sea (Antarctica). J Ichthyol 11:693–705
Piry S, Luikart G, Cornuet J (1999) BOTTLENECK: a computer program for detecting recent reductions in the effective population size using allele frequency data. J Hered 90:502–503
Posada D (2008) jModelTest: phylogenetic model averaging. Mol Biol Evol 25:1253–1256
Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155:945–959
Radtke R, Targett T, Kellermann AK et al (1989) Antarctic fish growth: profile of Trematomus newnesi. Mar Ecol Prog Ser 57:103–117
Raymond M, Rousset F (1995) Genepop (Version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Rogers AD, Morley S, Fitzcharles E et al (2006) Genetic structure of Patagonian toothfish (Dissostichus eleginoides) populations on the Patagonian Shelf and Atlantic and western Indian Ocean Sectors of the Southern Ocean. Mar Biol 149:915–924
Rutschmann S, Matschiner M, Damerau M et al (2011) Parallel ecological diversification in Antarctic notothenioid fishes as evidence for adaptive radiation. Mol Ecol 20:4707–4721
Ryman N, Palm S (2006) POWSIM: a computer program for assessing statistical power when testing for genetic differentiation. Mol Ecol Notes 6:600–602
Salzburger W (2009) The interaction of sexually and naturally selected traits in the adaptive radiations of cichlid fishes. Mol Ecol 18:169–185
Salzburger W, Ewing GB, von Haeseler A (2011) The performance of phylogenetic algorithms in estimating haplotype genealogies. Mol Ecol 20:1952–1963
Schneppenheim R, Kock KH, Duhamel G, Janssen G (1994) On the taxonomy of the Lepidonotothen squamifrons group (Pisces, Perciformes, Notothenioidei). Arch Fish Mar Res 42:137–148
Seehausen O (2006) African cichlid fish: a model system in adaptive radiation research. Proc R Soc B 273:1987–1998
Selkoe K, Toonen R (2006) Microsatellites for ecologists: a practical guide to using and evaluating microsatellite markers. Ecol Lett 9:615–629
Shaw P, Arkhipkin A, Al-Khairulla H (2004) Genetic structuring of Patagonian toothfish populations in the Southwest Atlantic Ocean: the effect of the Antarctic Polar Front and deep-water troughs as barriers to genetic exchange. Mol Ecol 13:3293–3303
Shust KV (1987) Distribution and important biological aspects of abundant Antarctic notothenioid species. In: Skarlato OA, Alekseev AP, Liubimova TG (eds) Biological resources of the Arctic and Antarctic. Nauka, Moscow, pp 296–320
Siegel V (1980a) Quantitative investigations on parasites of Antarctic channichtyid and nototheniid fishes. Meeresforsch 28:146–156
Siegel V (1980b) Parasite tags for some Antarctic channichthyid fish. Arch Fisch Wiss 31:97–103
Ślósarczyk W (1987) Contribution to the early life history of Channichthyidae from the Bransfield Strait and South Georgia (Antarctica). In: Kullander SO, Fernholm B (eds) Proceedings, fifth congress of European ichthyologists, Stockholm 1985. Swedish Museum of Natural History, Stockholm, pp 427–433
Smith PJ, Gaffney PM (2005) Low genetic diversity in the Antarctic toothfish (Dissostichus mawsoni) observed with mitochondrial and intron DNA markers. Ccamlr Science 12:43–51
Smith P, McVeagh M (2000) Allozyme and microsatellite DNA markers of toothfish population structure in the Southern Ocean. J Fish Biol 57:72–83
Susana E, Papetti C, Barbisan F et al (2007) Isolation and characterization of eight microsatellite loci in the icefish Chaenocephalus aceratus (Perciformes, Notothenioidei, Channichthyidae). Mol Ecol Notes 7:791–793
Swofford DL (2003) PAUP*. Phylogenetic analysis using parsimony (*and other methods). ed. 4.04a. Sinauer Associates, Sunderland, Massachusetts
Taylor M, Hellberg ME (2003) Genetic evidence for local retention of pelagic larvae in a Caribbean reef fish. Science 299:107–109
Tiedtke JE, Kock K (1989) Structure and composition of the demersal fish fauna around Elephant Island. Arch Fisch Wiss 39(Beih 1):143–169
Van Houdt JKJ, Hellemans B, Van De Putte AP et al (2006) Isolation and multiplex analysis of six polymorphic microsatellites in the Antarctic notothenioid fish, Trematomus newnesi. Mol Ecol Notes 6:157–159
Van Oosterhout C, Hutchinson W, Wills D, Shipley P (2004) Micro-Checker: software for identifying and correcting genotyping errors in microsatellite data. Mol Ecol Notes 4:535–538
White M (1998) Development, dispersal and recruitment: a paradox for survival among Antarctic fish. In: Di Prisco G, Pisano E, Clarke A (eds) Fishes of Antarctica. A biological overview. Springer, Milan, pp 53–62
Whitworth T, Nowlin WD, Orsi A et al (1994) Weddell Sea shelf water in the Bransfield Strait and Weddell-Scotia confluence. Deep-Sea Res I 41:629–641
Zane L, Marcato S, Bargelloni L et al (2006) Demographic history and population structure of the Antarctic silverfish Pleuragramma antarcticum. Mol Ecol 15:4499–4511
Acknowledgments
We are grateful to Christopher D. Jones from NOAA (National Oceanic and Atmospheric Administration) and all scientists and crew members who helped with sampling and species identification during the US AMLR (United States Antarctic Marine Living Resources Program) 2009 finfish survey aboard RV Yuzhmorgeologiya. We further thank Karl-Hermann Kock from the Institute of Sea Fisheries (Hamburg) for sharing his invaluable knowledge about notothenioids and their ecology as well as all lab members who gave a helping hand, especially Brigitte Aeschbach and Sereina Rutschmann (Basel). We also thank two anonymous referees for their helpful suggestions on the manuscript. The study was funded by grant HA 4328/4 from the Deutsche Forschungsgemeinschaft (DFG-Priority Programme 1158) to RH and WS, and by a PhD scholarship of the VolkswagenStiftung to MM.
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Damerau, M., Matschiner, M., Salzburger, W. et al. Comparative population genetics of seven notothenioid fish species reveals high levels of gene flow along ocean currents in the southern Scotia Arc, Antarctica. Polar Biol 35, 1073–1086 (2012). https://doi.org/10.1007/s00300-012-1155-x
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DOI: https://doi.org/10.1007/s00300-012-1155-x