Skip to main content

Advertisement

Log in

Recent diversification in an ancient lineage of Notothenioid fishes (Bovichtus: Notothenioidei)

  • Original Paper
  • Published:
Polar Biology Aims and scope Submit manuscript

Abstract

Notothenioids are among the most intensively studied lineages of marine fishes. However, notothenioid research is predominately focused on the approximately 100 species of Antarctic cryonotothenioids. Far less attention is devoted to the non-Antarctic lineages Bovichtidae, Pseudaphritis urvillii, and Eleginops maclovinus, all of which originated prior to the diversification of cryonotothenioid species. Here we utilize DNA sequence data from mitochondrial and nuclear genes, as well as meristic trait morphology to investigate the evolutionary history of Bovichtidae. Bovichtus is the only polytypic lineage of early diverging non-Antarctic notothenioids providing a unique opportunity to contextualize the diversification dynamics of cryonotothenioids with their non-Antarctic relatives. We find strong evidence that species of Bovichtus represent a recent evolutionary radiation with divergence times similar to those estimated among the most closely related species of cryonotothenioids. The divergence in traditional meristic trait morphology among species of Bovichtus is consistent with their phylogenetic relationships. The phylogeny of Bovichtus implies the wide geographic distribution of species in the clade is likely the result of West Wind drift-driven dispersal. The phylogeny and divergence time estimates results reject a hypothesis that species persistence in Bovichtus reflects long periods of evolutionary stasis. Instead, we hypothesize that patterns of extinction and diversification in Bovichtus closely mirror those observed in their Antarctic relatives.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Andrew TG, Hecht T, Heemstra PC, Lutjeharms JRE (1995) Fishes of the Tristan da Cunha group and Gough Island, South Atlantic Ocean. Ichthyol Bull JLB Smith Inst Ichthol 63:1–43

    Google Scholar 

  • Balushkin AV (2000) Morphology, classification, and evolution of notothenioid fishes of the Southern Ocean (Notothenioidei, Perciformes). J Ichthyol 40:S74–S109

    Google Scholar 

  • Balushkin AV (2016) Systematics of the Antarctic thornfishes of the genus Bovichtus (Bovichtidae) of the seamounts of the New Zealand Basin. J Ichthyol 56:631–638. https://doi.org/10.1134/S0032945216050015

    Article  Google Scholar 

  • Bargelloni L, Marcato S, Zane L, Patarnello T (2000) Mitochondrial phylogeny of notothenioids: a molecular approach to Antarctic fish evolution and biogeography. Syst Biol 49:114–129

    Article  CAS  PubMed  Google Scholar 

  • 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. Antarctic Sci 14:293–309

    Article  Google Scholar 

  • Bauret L, Gaudeul M, Sundue MA, Parris BS, Ranker TA, Rakotondrainibe F, Hennequin S, Ranaivo J, Selosse MA, Rouhan G (2017) Madagascar sheds new light on the molecular systematics and biogeography of grammitid ferns: New unexpected lineages and numerous long-distance dispersal events. Mol Phylogenet Evol 111:1–17

    Article  PubMed  Google Scholar 

  • Berendzen PB, Olson WM, Barron SM (2009) The utility of molecular hypotheses for uncovering morphological diversity in the Notropis rubellus species complex (Cypriniformes: Cyprinidae). Copeia 2009:661–673

    Article  Google Scholar 

  • Bouckaert R, Heled J, Kuhnert D, Vaughan T, Wu CH, Xie D, Suchard MA, Rambaut A, Drummond AJ (2014) BEAST 2: a software platform for Bayesian evolutionary analysis. PloS Comput Biol 10

  • Bravo R, Lloris D, Pequeño G, Rucabado J (1999) Revisión de las distintas especies del género Bovichtus (Perciformes, Bovichtidae) citadas para el cono sur americano y península Antártica. Rev Biol Mar Oceanogr 34:123–137

    Google Scholar 

  • Carlton JT, Chapman JW, Geller JB, Miller JA, Carlton DA, McCuller MI, Treneman NC, Steves BP, Ruiz GM (2017) Tsunami-driven rafting: transoceanic species dispersal and implications for marine biogeography. Science 357:1402–1405

    Article  CAS  PubMed  Google Scholar 

  • Cheng C-HC, Detrich HW (2007) Molecular ecophysiology of Antarctic notothenioid fishes. Philos Trans R Soc B 362:2215–2232

    Article  CAS  Google Scholar 

  • Clarke A, Johnston IA (1996) Evolution and adaptive radiation of Antarctic fishes. Trends Ecol Evol 11:212–218

    Article  CAS  PubMed  Google Scholar 

  • Collins MA, Brickle P, Brown J, Belchier M (2010) The Patagonian Toothfish: biology, ecology and fishery. Advances in marine biology, vol 58, pp 227–300

  • 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

    Article  Google Scholar 

  • DeWitt HH (1971) Costal and deep-water benthic fishes of the Antarctic. In: Bushnell VC (ed) Antarctic map folio series. American Geographical Society, New York, pp 1–10

    Google Scholar 

  • Dornburg A, Moore J, Beaulieu JM, Eytan RI, Near TJ (2015) The impact of shifts in marine biodiversity hotspots on patterns of range evolution: evidence from the Holocentridae (squirrelfishes and soldierfishes). Evolution 69:146–161

    Article  PubMed  Google Scholar 

  • Dornburg A, Eytan RI, Federman S, Pennington JN, Stewart AL, Jones CD, Near TJ (2016a) Molecular data support the existence of two species of the Antarctic fish genus Cryodraco (Channichthyidae). Polar Biol 39:1369–1379. https://doi.org/10.1007/s00300-015-1859-9

    Article  Google Scholar 

  • Dornburg A, Federman S, Eytan RI, Near TJ (2016b) 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

    Article  PubMed  Google Scholar 

  • Dornburg A, Federman S, Lamb AD, Jones CD, Near TJ (2017) Cradles and museums of Antarctic teleost biodiversity. Nat Ecol Evol 1:1379–1384. https://doi.org/10.1038/s41559-017-0239-y

    Article  PubMed  Google Scholar 

  • Eastman JT (1985a) The evolution of neutrally buoyant notothenioid fishes: their specializations and potential interactions in the Antarctic marine food web. In: Siegfried WR, Condy PR, Laws RM (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, pp 430–436

    Chapter  Google Scholar 

  • Eastman JT (1985b) Pleuragramma antarcticum (Pisces, Nototheniidae) as food items for other fishes in McMurdo Sound, Antarctica. Polar Biol 4:155–160

    Article  Google Scholar 

  • Eastman JT (1993) Antarctic fish biology: evolution in a unique environment. Academic Press, San Diego

    Google Scholar 

  • Federman S, Dornburg A, Downie A, Richard AF, Daly DC, Donoghue MJ (2015) The biogeographic origin of a radiation of trees in Madagascar: implications for the assembly of a tropical forest biome. BMC Evol Biol 15:216

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fell HB (1962) West-Wind-drift dispersal of echinoderms in the Southern Hemisphere. Nature 193:759. https://doi.org/10.1038/193759a0

    Article  Google Scholar 

  • Fraser CI, Nikula R, Waters JM (2011) Oceanic rafting by a coastal community. Proc R Soc B 278:649–655

    Article  PubMed  Google Scholar 

  • Gillespie RG, Baldwin BG, Waters JM, Fraser CI, Nikula R, Roderick GK (2012) Long-distance dispersal: a framework for hypothesis testing. Trends Ecol Evol 27:47–56

    Article  PubMed  Google Scholar 

  • Hardy GS (1988) A revision of Bovichtus Cuvier, 1831 (Pisces: Bovichthyidae) from Australasia, with description of a new deepwater species from the New Zealand Subantarctic. J Nat Hist 22:1639–1655

    Article  Google Scholar 

  • Hou ZG, Li SQ (2018) Tethyan changes shaped aquatic diversification. Biol Rev 93:874–896

    Article  PubMed  Google Scholar 

  • Hüne M, González-Wevar C, Poulin E, Mansilla A, Fernández DA, Barrera-Oro E (2015) Low level of genetic divergence between Harpagifer fish species (Perciformes: Notothenioidei) suggests a Quaternary colonization of Patagonia from the Antarctic Peninsula. Polar Biol 38:607–617. https://doi.org/10.1007/s00300-014-1623-6

    Article  Google Scholar 

  • Hureau JC, Tomo AP (1977) Bovichtus elongatus n.sp., poisson Bovichthyidae, famille nouvelle pour l'Antarctique. Cybium 3:67–74

    Google Scholar 

  • Kingsford MJ, Schiel DR, Battershill CN (1989) Distribution and abundance of fish in a rocky reef environment at the subantarctic Auckland Islands, New Zealand. Polar Biol 9:179–186. https://doi.org/10.1007/BF00297173

    Article  Google Scholar 

  • Kocher TD, Conroy JA, McKaye KR, Stauffer JR, Lockwood SF (1995) Evolution of NADH dehydrogenase subunit 2 in east African cichlid fish. Mol Phylogenet Evol 4:420–432

    Article  CAS  PubMed  Google Scholar 

  • Kock K-H (1985) Krill consumption by Antarctic notothenioid fishes. In: Siegfried WR, Condy PR, Laws RW (eds) Antarctic nutrient cycles and food webs. Springer, Berlin, pp 437–444

    Chapter  Google Scholar 

  • Kock KH (1992) Antarctic fish and fisheries. Cambridge University Press, Cambridge

    Google Scholar 

  • Kozal LC, Simmons JW, Mollish JM, MacGuigan DJ, Benavides E, Keck BP, Near TJ (2017) Phylogenetic and morphological diversity of the Etheostoma zonistium species complex with the description of a new species endemic to the Cumberland Plateau of Alabama. Bull Peabody Mus Nat Hist 58:263–286. https://doi.org/10.3374/014.058.0202

    Article  Google Scholar 

  • 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

    Article  Google Scholar 

  • La Mesa M, Caputo V, Eastman JT (2010) Some reproductive traits of the Tristan klipfish, Bovichtus diacanthus (Carmichael 1819) (Notothenioidei: Bovichtidae) from Tristan da Cunha (South Atlantic). Polar Biol 33:337–346

    Article  Google Scholar 

  • Last PR, Balushkin AV, Hutchins JB (2002) Halaphritis platycephala (Notothenioidei: Bovichtidae): a new genus and species of temperate icefish from Southeastern Australia. Copeia 2002:433–440

    Article  Google Scholar 

  • Li CH, Ortí G, Zhang G, Lu GQ (2007) A practical approach to phylogenomics: the phylogeny of ray-finned fish (Actinopterygii) as a case study. BMC Evol Biol 7:44

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lopez JA, Chen WJ, Ortí G (2004) Esociform phylogeny. Copeia 2004:449–464

    Article  Google Scholar 

  • Luiz OJ, Allen AP, Robertson DR, Floeter SR, Madin JS (2015) Seafarers or castaways: ecological traits associated with rafting dispersal in tropical reef fishes. J Biogeogr 42:2323–2333

    Article  Google Scholar 

  • Matschiner M, Hanel R, Salzburger W (2009) Gene flow by larval dispersal in the Antarctic notothenioid fish Gobionotothen gibberifrons. Mol Ecol 18:2574–2587

    Article  CAS  PubMed  Google Scholar 

  • McDowall RM (1978) Generalized tracks and dispersal in biogeography. Syst Zool 27:88–104

    Article  Google Scholar 

  • Miller RG (1987) Origins and pathways possible for the fishes of the Antarctic Ocean. In: Kullander SO, Fernholm B (eds) Proceedings of the Fifth Congress of European Ichthyologists. Swedish National Museum, Stockholm, pp 373–380

  • Nagalingum NS, Marshall CR, Quental TB, Rai HS, Little DP, Mathews S (2011) Recent synchronous radiation of a living fossil. Science 334:796–799

    Article  CAS  PubMed  Google Scholar 

  • Near TJ (2004) Estimating divergence times of notothenioid fishes using a fossil-calibrated molecular clock. Antarctic Sci 16:37–44

    Article  Google Scholar 

  • Near TJ (2009) Notothenioid fishes (Notothenioidei). In: Hedges SB, Kumar S (eds) The timetree of life. Oxford University Press, New York, pp 339–343

    Google Scholar 

  • Near TJ, Dornburg A, Kuhn KL, Eastman JT, Pennington JN, Patarnello T, Zane L, Fernandez DA, Jones CD (2012) Ancient climate change, antifreeze, and the evolutionary diversification of Antarctic fishes. Proc Nat Acad Sci USA 109:3434–3439. https://doi.org/10.1073/pnas.1115169109

    Article  PubMed  Google Scholar 

  • Near TJ, Dornburg A, Tokita M, Suzuki D, Brandley MC, Friedman M (2014) Boom and bust: ancient and recent diversification in bichirs (Polypteridae: Actinopterygii), a relictual lineage of ray-finned fishes. Evolution 68:1014–1026. https://doi.org/10.1111/evo.12323

    Article  PubMed  Google Scholar 

  • Near TJ, Dornburg A, Harrington RC, Oliveira C, Pietsch TW, Thacker CE, Satoh TP, Katayama E, Wainwright PC, Eastman JT, Beaulieu JM (2015) Identification of the notothenioid sister lineage illuminates the biogeographic history of an Antarctic adaptive radiation. BMC Evol Biol 15:109. https://doi.org/10.1186/s12862-015-0362-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Near TJ, Simmons JW, Mollish J-M, Correa MA, Benavides E, Harrington RC, Keck BP (2017) A new species of logperch endemic to Tennessee (Percidae: Etheostomatinae: Percina). Bull Peabody Mus Nat Hist 58:287–309. https://doi.org/10.3374/014.058.0203

    Article  Google Scholar 

  • Near TJ, MacGuigan DJ, Parker E, Struthers CD, Jones CD, Dornburg A (2018) Phylogenetic analysis of Antarctic notothenioids illuminates the utility of RADseq for resolving Cenozoic adaptive radiations. Mol Phylogenet Evol 129:268–279. https://doi.org/10.1016/j.ympev.2018.09.001

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  PubMed  Google Scholar 

  • Pequeño G, Farías D, Thiel M, Hinojosa I (2004) Peces asociados con la deriva de macroalgas en Aysén, Chile. Rev Biol Mar Oceanogr 39:93–99

    Article  Google Scholar 

  • Pequeño G, Inzunza AJ (1987) Variabilidad intraespecifica y status sistematico del "torito" Bovichthys chilensis Regan 1913 (Osteichthyes, Bovichthyidae) en Valdivia, Chile. Bol Soc Biol Concepción 58:127–139

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Regan CT (1913) The Antarctic fishes of the Scottish National Antarctic expedition. Trans R Soc Edinburgh 49:229–292

    Article  Google Scholar 

  • Reynolds RG, Niemiller ML, Hedges SB, Dornburg A, Puente-Rolon AR, Revell LJ (2013) Molecular phylogeny and historical biogeography of West Indian boid snakes (Chilabothrus). Mol Phylogenet Evol 68:461–470

    Article  PubMed  Google Scholar 

  • Ronquist F, Teslenko M, van der Mark P, Ayres DL, Darling A, Hohna S, Larget B, Liu L, Suchard MA, Huelsenbeck JP (2012) MrBayes 3.2: efficient Bayesian phylogenetic inference and model choice across a large model space. Syst Biol 61:539–542

    Article  PubMed  PubMed Central  Google Scholar 

  • Sauvage H-E (1879) Mémoire sur la faune ichthyologique d l'île St Paul. Arch Zool Exper Gen 8:1–46

    Google Scholar 

  • Stadler T (2011) Inferring speciation and extinction processes from extant species data. Proc Nat Acad Sci USA 108:16145–16146

    Article  CAS  PubMed  Google Scholar 

  • Stankovic A, Spalik K, Kamler E, Borsuk P, Weglenski P (2002) Recent origin of sub-Antarctic notothenioids. Polar Biol 25:203–205

    Google Scholar 

  • Sutton CA, Bruce BD (1988) Bovichtidae: thornfishes. In: Neira FJ, Miskiewicz AG, Trnski T (eds) Lavae of temperate Australian fishes Laboratory guide for larval fish identification. University of Western Australia Press, Nedlands, pp 338–343

    Google Scholar 

  • Waters JM (2008) Driven by the West Wind Drift? A synthesis of southern temperate marine biogeography, with new directions for dispersalism. J Biogeogr 35:417–427

    Article  Google Scholar 

Download references

Acknowledgements

G. Watkins-Colwell provided outstanding assistance with all aspects arising from the use of specimens housed in museum collections. A. Lamb provided assistance with various aspects in the preparation of this manuscript. All images were obtained through creative commons licenses. Alastair Graham (CSIRO) provided valuable tissue specimens. Financial support was provided by the Bingham Oceanographic fund maintained and managed at the Peabody Museum of Natural History, Yale University.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Thomas J. Near.

Ethics declarations

Conflicts of interest

The authors of this paper have no conflicts of interest.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Near, T.J., Ghezelayagh, A., Ojeda, F.P. et al. Recent diversification in an ancient lineage of Notothenioid fishes (Bovichtus: Notothenioidei). Polar Biol 42, 943–952 (2019). https://doi.org/10.1007/s00300-019-02489-1

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00300-019-02489-1

Keywords

Navigation