Abstract
Most Antarctic notothenioids exhibit clear geographic structure at large scales of spatial separation, generally between populations off different Ocean sectors. At smaller distances, there is great variation in the extent of population structuring. The Antarctic Peninsula and the archipelago of the South Shetland Islands are separated by a narrow strait of deep water (1000 m). Despite the proximity of these two areas, the confluence of water masses of different origins establishes frontal systems and local gyres which may preclude migration between shelf populations. Among the most abundant fish species in the area, the painted notothen Lepidonotothen larseni and the gaudy notothen Lepidonotothen nudifrons are two of the most numerous and widely distributed. In the present study, the genetic and morphological population structure of these closely related species was evaluated between the Antarctic Peninsula and the South Shetland Islands. Nine meristic counts, 18 inter-landmark distances and a mitochondrial DNA marker (D-loop) were analyzed. Populations of L. nudifrons were significantly different based on both, morphogeometric and genetic analyses, while L. larseni showed no population differentiation. The results showed a moderate structuring not correlated with distance between L. nudifrons populations off the Antarctic Peninsula and the South Shetland Islands. These findings provide evidence that differences between the studied species may be linked to key life history events, such as timing and location of egg development, hatching times and dispersal period of larvae. The present data suggest that notothenioid population structuring at regional scale may be related to a combination of life history traits, oceanographic features and local adaptation.
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References
Agostini C, Patarnello T, Ashford JR, Torres JJ, Zane L, Papetti C (2015) Genetic differentiation in the ice dependent fish Pleuragramma antarctica along the Antarctic Peninsula. J Biogeogr 42:1103–1113. https://doi.org/10.1111/jbi.12497
Barrera-Oro E (2002) The role of fish in the Antarctic marine food web: differences between inshore and offshore waters in the southern Scotia Arc and west Antarctic Peninsula. Antarct Sci 14:293–309. https://doi.org/10.1017/S0954102002000111
Begg GA, Hare JA, Sheehan DD (1999) The role of life history parameters as indicators of stock structure. Fish Res 43:141–163. https://doi.org/10.1016/S0165-7836(99)00071-5
Blasina G, Molina JM, Lopez Cazorla A, Díaz de Astarloa J (2016) Relationship between ecomorphology and trophic segregation in four closely related sympatric fish species (Teleostei, Sciaenidae). Comptes Rendus Biol 339:498–506. https://doi.org/10.1016/j.crvi.2016.07.003
Blasina G, Lopez Cazorla A, Deli Antoni M, Bruno D, Delpiani M, Díaz de Astarloa J (2017) Ontogenetic changes in the feeding strategy of Lepidonotothen nudifrons (Pisces, Nototheniidae) off the South Shetland Islands and the Antarctic Peninsula. Polar Res 36:1331558. https://doi.org/10.1080/17518369.2017.1331558
Bushula T, Pakhomov EA, Kaehler S, Davis S, Kalin RM (2005) Diet and daily ration of two nototheniid fish on the shelf of the sub-Antarctic Prince Edward Islands. Polar Biol 28:585–593. https://doi.org/10.1007/s00300-005-0729-2
Cadrin SX (2000) Advances in morphometric identification of fishery stocks. Rev Fish Biol Fish 10:91–112. https://doi.org/10.1023/A:1008939104413
Clarke A, Johnston IA (1996) Evolution and adaptive radiation of Antarctic fishes. Trends Ecol Evol 11:212–218. https://doi.org/10.1016/0169-5347(96)10029-X
Curcio N, Tombari A, Capitanio F (2014) Otolith morphology and feeding ecology of an Antarctic nototheniid Lepidonotothen larseni. Antarct Sci 26(2):124–132. https://doi.org/10.1017/S0954102013000394
Damerau M, Salzburger W, Hanel R (2014) Population genetic structure of Lepidonotothen larseni revisited: cytb and microsatellites suggest limited connectivity in the Southern Ocean. Mar Ecol Prog Ser 517:251–263. https://doi.org/10.3354/meps11061
Damerau M, Matschiner M, Salzburger W, Hanel R (2012) 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. https://doi.org/10.1007/s00300-012-1155-x
DeWitt HH, Heemstra PC, Gon O (1990) Nototheniidae. In: Gon O, Heemstra PC (eds) Fishes of the Southern Ocean. J.L.B Smith Institute of Ichthyology, Grahamstown, pp 279–331
DeWoody JA, Avise JC (2000) Microsatellite variation in marine, freshwater, and anadromous fishes compared with other animals. J Fish Biol 56:461–473. https://doi.org/10.1111/j.1095-8649.2000.tb00748.x
Dornburg A, Federman S, Eytan RI, Near TJ (2016) Cryptic species diversity in sub-Antarctic islands: a case study of Lepidonotothen. Mol Phylogenet Evol 104:32–43. https://doi.org/10.1016/j.ympev.2016.07.013
Duhamel G, Ozouf-Costaz C, Cattaneo-Berrebi G, Berrebi P (1995) Interpopulation relationships in two species of Antarctic fish Notothenia rossii and Champsocephalus gunnari from the Kerguelen Islands: an allozyme study. Antarct Sci 7(4):351–356. https://doi.org/10.1017/S0954102095000496
Eastman JT (2005) The nature of the diversity of Antarctic fishes. Polar Biol 28:93–107. https://doi.org/10.1007/s00300-004-0667-4
Eastman JT, Eakin RR (2000) An updated species list for notothenioid fish (Perciformes; Notothenioidei), with comments on Antarctic species. J Appl Ichthyol 48:11–20
Excoffier L, Smouse PE, Quattro JM (1992) Analysis of molecular variance inferred from metric distances among DNA haplotypes: application to human mitochondrial DNA restriction data. Genetics 131:479–491
González-Castro M, Ibáñez-Aguirre AL, Heras S, Roldán MI, Cousseau MB (2012) Assessment of lineal versus landmark-based morphometry for discriminating species of Mugilidae (Actinopterygii). Zool Stud 51(8):1515–1528
González-Castro M, Ghasemzadeh J (2016) Morphology and morphometry based taxonomy of Mugillidae. In: Crosetti D, Blaber S (eds) Biology, ecology and culture of Grey Mullet (Mugillidae). CRC Press, Taylor and Francis Group, Boca Ratón, pp 1–21
González-Castro M, Rosso JJ, Mabragaña R, Díaz de Astarloa JM (2016) Surfing among species, populations and morphotypes: inferring boundaries between two species of new world silversides (Atherinopsidae). C R Biol 399(1):10–29. https://doi.org/10.1016/j.crvi.2015.11.004
Hartl D, Clark A (2007) Principles of population genetics, 4th edn. Sinauer Associates Inc, Massachusetts
Hauser L, Carvalho GR (2008) Paradigm shifts in marine fisheries genetics: ugly hypotheses slain by beautiful facts. Fish Fish 9:333–362. https://doi.org/10.1111/j.1467-2979.2008.00299.x
Hourigan TF, Radtke RL (1989) Reproduction of the Antarctic fish Nototheniops nudifrons. Mar Biol 100:277–283. https://doi.org/10.1007/BF00391969
Huneke WGC, Huhn O, Schröeder M (2016) Water masses in the Bransfield Strait and adjacent seas, austral summer 2013. Polar Biol 39:789–798. https://doi.org/10.1007/s00300-016-1936-8
Hureau JC (1994) The significance of fish in the marine Antarctic ecosystems. Polar Biol 14:307–313
Ihssen PE, Booke HE, Casselman JM, McGlade JM, Payne NR, Utter FM (1981) Stock identification: materials and methods. Can J Fish Aquat Sci 38:1838–1855. https://doi.org/10.1139/f81-230
Ivanova NV, deWaard JR, Hebert PDN (2006) An inexpensive, automation-friendly protocol for recovering high-quality DNA. Mol Ecol Notes 6:998–1002. https://doi.org/10.1111/j.1471-8286.2006.01428.x
Jones CD, Anderson E, Balushkin AV, Duhamel G, Eakin RR, Eastman JT, Kuhn KL, Lecointre G, Near TJ, North AW, Stein DL, Vacchi M, Detrich HW III (2008) Diversity, relative abundance, new locality records and population structure of Antarctic demersal fishes from the northern Scotia Arc islands and Bouvetøya. Polar Biol 31:1481–1497. https://doi.org/10.1007/s00300-008-0489-x
Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, Buxton S, Cooper A, Markowitz S, Duran C (2012) Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649. https://doi.org/10.1093/bioinformatics/bts199
Kellermann A (1990) Catalogue of early life stages of Antarctic notothenioid fishes. Ber Polarforsch 67:45–136
Kock KH (1992) Antarctic fish and fisheries. Cambridge University Press, Cambridge
Kock KH, Kellermann A (1991) Review. Reproduction in Antarctic notothenioid fish. Antarct Sci 3(2):125–150. https://doi.org/10.1017/S0954102091000172
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. https://doi.org/10.1080/10641260590953900
Konecki JT, Targett TE (1989) Eggs and larvae of Nototheniops larseni from the spongocoel of a hexactinellid sponge near Hugo Island, Antarctic Peninsula. Polar Biol 10:197–198
Kuhn KL, Gaffney PM (2006) Preliminary assessment of population structure in the mackerel icefish (Champsocephalus gunnari). Polar Biol 29:927–935. https://doi.org/10.1007/s00300-006-0134-5
La Mesa M, Eastman JT, Vacchi M (2004) The role of notothenioid fish in the food web of the Ross Sea shelf waters: a review. Polar Biol 27:321–338. https://doi.org/10.1007/s00300-004-0599-z
La Mesa M, La Mesa G, Catalano B, Jones CD (2016) Spatial distribution pattern and physical–biological interactions in the larval notothenioid fish assemblages from the Bransfield Strait and adjacent waters. Fish Oceanogr 25:624–636. https://doi.org/10.1111/fog.12178
La Mesa M, Riginella E, Catalano B, Jones CD, Mazzoldi C (2017) Maternal contribution to spawning and early life-history strategies of the genus Lepidonotothen (Nototheniidae, Perciformes) along the southern Scotia Arc. Polar Biol 40:1441–1450. https://doi.org/10.1007/s00300-016-2068-x
Librado P, Rozas J (2009) DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. Bioinformatics 25(11):1451–1452. https://doi.org/10.1093/bioinformatics/btp187
Lleonart J, Salat J, Torres GJ (2000) Removing allometric effects of body size in morphological analysis. J Theor Biol 205(1):85–93. https://doi.org/10.1006/jtbi.2000.2043
Llompart F, Delpiani M, Lattuca E, Delpiani G, Cruz-Jiménez A, Orlando P, Ceballos S, Díaz de Astarloa JM, Vanella F, Fernández D (2015) Spatial patterns of summer demersal fish assemblages around the Antarctic Peninsula and South Shetland Islands. Antarct Sci 27:109–117. https://doi.org/10.1017/S0954102014000352
Lombarte A, Lleonart J (1993) Otolith size changes related with body growth, habitat depth and temperature. Environ Biol Fishes 37(3):297–306. https://doi.org/10.1007/bf00004637
Marcil J, Swain DP, Hutchings JA (2006) Genetic and environmental components of phenotypic variation in body shape among populations of Atlantic cod (Gadus morhua L.). Biol J Linn Soc 88(3):351–365. https://doi.org/10.1111/j.1095-8312.2006.00656.x
Matschiner M, Hanel R, Salzburger W (2009) Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons. Mol Ecol 18:2574–2587. https://doi.org/10.1111/j.1365-294X.2009.04220.x
Miya T, Gon O, Mwale M, Poulin E (2016) Molecular systematics and taxonomic status of three latitudinally widespread nototheniid (Perciformes: Notothenioidei) fishes from the Southern Ocean. Zootaxa 4061(4):381–396. https://doi.org/10.11646/zootaxa.4061.4.4
Moore CS, Ruocchio MJ, Blakeslee AMH (2018) Distribution and population structure in the naked goby Gobiosoma bosc (Perciformes: Gobiidae) along a salinity gradient in two western Atlantic estuaries. PeerJ 6:e5380. https://doi.org/10.7717/peerj.5380
O'Reilly PT, Canino MF, Bailey KM, Bentzen P (2004) Inverse relationship between FST and microsatellite polymorphism in the marine fish, walleye pollock (Theragra chalcogramma): implications for resolving weak population structure. Mol Ecol 13:1799–1814. https://doi.org/10.1111/j.1365-294X.2004.02214.x
Papetti C, Susana E, La Mesa M, Kock KH, Patarnello T, Zane L (2007) Microsatellite analysis reveals genetic differentiation between year-classes in the icefish Chaenocephalus aceratus at South Shetlands and Elephant Island. Polar Biol 30:1605–1613. https://doi.org/10.1007/s00300-007-0325-8
Papetti C, Susana E, Patarnello T, Zane L (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. https://doi.org/10.3354/meps07831
Papetti C, Pujolar JM, Mezzavilla M, La Mesa M, Rock J, Zane L, Patarnello T (2012) Population genetic structure and gene flow patterns between populations of the Antarctic icefish Chionodraco rastrospinosus. J Biogeogr 39:1361–1372. https://doi.org/10.1111/j.1365-2699.2011.02682.x
Papetti C, Windisch HS, La Mesa M, Lucassen M, Marshall C, Lamare MD (2016) Non-Antarctic notothenioids: past phylogenetic history and contemporary phylogeographic implications in the face of environmental changes. Mar Genomics 25:1–9. https://doi.org/10.1016/j.margen.2015.11.007
Pineda J, Hare J, Sponaugle S (2007) Larval transport and dispersal in the coastal ocean and consequences for population connectivity. Oceanography 20(3):22–39
Purcell JFH, Cowen RK, Hughes CR, Williams DA (2006) Weak genetic structure indicates strong dispersal limits: a tale of two coral reef fish. Proc R Soc B 273:1483–1490. https://doi.org/10.1098/rspb.2006.3470
Quinn GP, Keough MJ (2002) Experimental design and data analysis for biologists. Cambridge University Press, Cambridge
Raymond M, Rousset F (1995) GENEPOP (version 1.2): population genetics software for exact tests and ecumenicism. J Hered 86:248–249
Riginos C, Douglas KE, Jin Y, Shanahan DF, Treml EA (2011) Effects of geography and life history traits on genetic differentiation in benthic marine fishes. Ecography 34:566–575. https://doi.org/10.1111/j.1600-0587.2010.06511.x
Rousset F (2008) Genepop'007: a complete reimplementation of the Genepop software for Windows and Linux. Mol Ecol Resour 8:103–106
Ruzicka JJ (1996) Comparison of the two alternative early life-history strategies of the Antarctic fishes Gobionotothen gibberifrons and Lepidonotothen larseni. Mar Ecol Prog Ser 133:29–41. https://doi.org/10.3354/meps133029
Sahade R, Lagger C, Torre L, Momo F, Monien P, Schloss I, Barnes DKA, Servetto N, Tarantelli S, Tatián M, Zamboni N, Abele D (2015) Climate change and glacier retreat drive shifts in an Antarctic benthic ecosystem. Sci Adv 1:e1500050. https://doi.org/10.1126/sciadv.1500050
Sanchez S, Dettaï A, Bonillo C, Ozouf-Costaz C, Detrich HW III, Lecointre G (2007) Molecular and morphological phylogenies of the Antarctic teleostean family Nototheniidae, with emphasis on the Trematominae. Polar Biol 30:155–166. https://doi.org/10.1007/s00300-006-0170-1
Sangra P, Gordo C, Hernández-Arencibia M, Marrero-Díaz A, Rodríguez-Santana A, Stegner A, Martínez-Marrero A, Pelegrí JL, Pichon T (2011) The Bransfield current system. Deep Sea Res Part I Oceanogr Res Pap 58:390–402. https://doi.org/10.1016/j.dsr.2011.01.011
Schneider S, Roessli D, Excoffier L (2000) Arlequin ver 2.0. A software for population genetic analysis. Genetics and Biometry Laboratory, University of Geneva, Geneva
Schunter C, Carreras-Carbonell J, MacPherson E, Tintore J, Vidal-Vijande E, Pascual A, Guidetti P, Pascual M (2011) Matching genetics with oceanography: directional gene flow in a Mediterranean fish species. Mol Ecol 20:5167–5181. https://doi.org/10.1111/j.1365-294X.2011.05355.x
Shanks AL (2009) Pelagic larval duration and dispersal distance revisited. Biol Bull 216:373–385. https://doi.org/10.1086/BBLv216n3p373
Sheskin DJ (2004) Handbook of parametric and nonparametric statistical procedures, 3rd edn. Chapman & Hall/CRC, Boca Raton
Shulman MJ, Bermingham E (1995) Early life histories, ocean currents, and the population genetics of Caribbean reef fishes. Evolution 49:897–910. https://doi.org/10.1111/j.1558-5646.1995.tb02325.x
Sosinski J (1985) Some data on taxonomy and biology of Antarctic icefish, Champsocephalus gunnari Lönnberg 1905. Acta Ichthyol Piscat 15:3–54
Strauss RE, Bookstein FL (1982) The truss: body form reconstruction in morphometrics. Syst Zool 31(2):113–135. https://doi.org/10.2307/2413032
Swain DP, Foote CJ (1999) Stocks and chameleons: the use of phenotypic variation in stock identification. Fish Res 43:113–128. https://doi.org/10.1016/S0165-7836(99)00069-7
Van de Putte AP, Janko K, Kasparova E, Maes GE, Rock J, Koubbi P, Volckaert FAM, Choleva L, Fraser KPP, Smykla J, Van Houdt JKJ, Marshall C (2012) Comparative phylogeography of three trematomid fishes reveals contrasting genetic structure patterns in benthic and pelagic species. Mar Genomics 8:23–34. https://doi.org/10.1016/j.margen.2012.05.002
Volckaert FA, Rock J, Van de Putte AP (2012) Connectivity and molecular ecology of Antarctic fishes. In: Prisco G, Verde C (eds) Adaptation and evolution in marine environments from pole to pole. Springer, Berlin, pp 75–96
Ward RD, Woodwark M, Skibinski DOF (1994) A comparison of genetic diversity levels in marine, freshwater, and anadromous fishes. J Fish Biol 44:213–232. https://doi.org/10.1111/j.1095-8649.1994.tb01200.x
White C, Selkoe KA, Watson J, Siegel DA, Zacherl DC, Toonen RJ (2010) Ocean currents help explain population genetic structure. Proc R Soc B 277:1685–1694. https://doi.org/10.1098/rspb.2009.2214
Young EF, Rock J, Meredith MP, Belchier M, Murphy EJ, Carvalho GR (2012) Physical and behavioral influences on larval fish retention: contrasting patterns in two Antarctic fishes. Mar Ecol Prog Ser 465:201–215. https://doi.org/10.3354/meps09908
Young EF, Belchier M, Hauser L, Horsburgh GJ, Meredith MP, Murphy EJ, Pascoal S, Rock J, Tysklind N, Carvalho GR (2015) Oceanography and life history predict contrasting genetic population structure in two Antarctic fish species. Evol Appl 8:486–509. https://doi.org/10.1111/eva.12259
Zane L, Marcato S, Bargelloni L, Bortolotto E, Papetti C, Simonato M, Varotto V, Patarnello T (2006) Demographic history and population structure of the Antarctic silverfish Pleuragramma antarcticum. Mol Ecol 15:499–511. https://doi.org/10.1111/j.1365-294X.2006.03105.x
Zar JH (1984) Biostatistical analysis, 2nd edn. Prentice Hall International Inc, Londres
Zhou M, Niller PP, Zhu Y, Dorland RD (2006) The western boundary current in the Bransfield Strait, Antarctica. Deep Sea Res Part I Oceanogr Res 53:1244–1252. https://doi.org/10.1016/j.dsr.2006.04.003
Zuur AF, Ieno EN, Smith GM (2007) Analyzing ecological data. Springer, New York
Acknowledgements
The authors thank Cristiane Kioko Shimabukuro Dias and Najila Nolie Catarine Dantas Cerqueira for their helpful assistance. This research was supported by Consejo Nacional de Investigaciones Científicas y Técnicas (Project-FONDO IBOL Grant No. 3657/15), Universidad Nacional de Mar del Plata (EXA Grant No. 767/16), the National Science and Technology Council of the Brazilian Federal Government (CNPq Grant No. 306054/2006-0 to CO) and São Paulo State Foundation (FAPESP Grant No. 2016/09204-6 to CO). Mariana Y. Deli Antoni and María C. Spath were supported by CONICET postdoctoral fellowships. Matías Delpiani was supported by an external CONICET CPA fellowship (12020160100004CO). Thanks to Dr. Mario La Mesa and anonymous reviewers who provided valuable suggestions for improving a previous version of the manuscript.
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Deli Antoni, M.Y., Delpiani, S.M., González-Castro, M. et al. Comparative populational study of Lepidonotothen larseni and L. nudifrons (Teleostei: Nototheniidae) from the Antarctic Peninsula and the South Shetland Islands, Antarctica. Polar Biol 42, 1537–1547 (2019). https://doi.org/10.1007/s00300-019-02540-1
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DOI: https://doi.org/10.1007/s00300-019-02540-1