Implications of absence of seawater-type mitochondria-rich cells and results of molecular analyses for derivation of the non-parasitic Ukrainian brook lamprey Eudontomyzon mariae
The Ukrainian brook lamprey Eudontomyzon mariae is the most widespread lamprey species in eastern Europe. Although E. mariae is generally considered a derivative of Eudontomyzon danfordi, an exclusively freshwater parasitic species, it has alternatively been suggested that it was recently derived from a now extinct anadromous Black Sea ancestor. Several non-parasitic lampreys and the landlocked sea lamprey, which have recently evolved from anadromous ancestors, still develop a seawater-type mitochondria-rich cell (SW-MRC) in their gills. In contrast, this cell type is not present in the gills of either Lampetra aepyptera, a non-parasitic lamprey of ancient origin, or the parasitic Ichthyomyzon unicuspis and I. castaneus that likewise have long evolutionary histories in fresh water. Eudontomyzon mariae from the Vistula River in the Baltic River basin does not possess SW-MRC, which is inconsistent with a recent origin from an anadromous ancestor. Mitochondrial DNA sequence data were thus used to infer the relationship between different populations of E. mariae and E. danfordi, and to reconstruct the transition from anadromy to freshwater residency. The results suggest that E. mariae evolved independently in the Baltic, Black, and Caspian Sea basins, and not recently from an anadromous ancestor. Although E. mariae in the Danube River may have arisen relatively recently from E. danfordi (differing by 0.7–1.1% in cytochrome b gene sequence), other E. mariae populations (including in the Vistula River) are genetically closer (0.6%) to the hypothetical ancestor of both E. mariae and E. danfordi. That ancestor was probably a freshwater resident, since SW-MRCs are not rapidly lost following confinement in fresh water.
KeywordsNon-parasitic lampreys Paired species Ukrainian brook lamprey Eudontomyzon mariae Gill epithelium Seawater-type mitochondria-rich cells Cytochrome b
The authors thank Claude B. Renaud for critically reading the manuscript. The excellent technical assistance of S. Fassbaender is gratefully acknowledged. A. Fox provided help with the network analyses. Financial support was provided by the Natural Sciences and Engineering Research Council of Canada, the Faculty of Science at the University of Manitoba, Murdoch University and the Polish Ministry for Science and Higher Education.
Compliance with ethical standards
The study was in accordance with the Polish law of animal welfare.
Conflict of interests
The authors declare no conflict of interest.
- Dawson HA, Quintella BR, Almeida PR, Treble AJ, Jolley JC (2015) The ecology of larval and metamorphosing lampreys. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 1. Springer, Dordrecht, pp 75–137Google Scholar
- Docker MF (2009) A review of the evolution of nonparasitism in lampreys and an update of the paired species concept. Am Fish Soc Symp 72:71–114Google Scholar
- Ferreira-Martins D, Coimbra J, Antunes C, Wilson JM (2016) Effects of salinity on upstream-migrating, spawning sea lamprey, Petromyzon marinus. Conserv Physiol 4: doi: 10.1093/conphys/cov064
- Freyhof J, Kottelat M (2008) Eudontomyzon sp. nov. ‘migratory’. The IUCN Red List of Threatened Species 2008: e.T135505A4134478. http://dx.doi.org/10.2305/IUCN.UK.2008.RLTS.T135505A4134478.en. Downloaded on 11 May 2016
- Hardisty MW (1986) Lampetra planeri (Bloch, 1784). In: Holčík J (ed) The freshwater fishes of Europe, vol.1, Part I Petromyzontiformes, vol 1. AULA-Verlag, Wiesbaden, pp 279–304Google Scholar
- Holčík J, Renaud CB (1986) Eudontomyzon mariae (Berg, 1931). In: Holčík J (ed) The freshwater fishes of Europe, vol.1, Part I Petromyzontiformes, vol 1. AULA-Verlag, Wiesbaden, pp 165–185Google Scholar
- Kottelat M, Bogutskaya NG, Freyhof J (2005) On the migratory Black Sea lamprey and the nomenclature of the ludoga, Peipsi and ripus whitefishes (Agnatha: Petromyzontidae; Teleostei: Coregonidae). Zoosyst Rossica 14:181–186Google Scholar
- Lang NJ, Roe KJ, Renaud CB, Gill HS, Potter IC, Freyhof J, Naseka AM, Cochran P, Espinosa Pérez H, Habit EM, Kuhajda BR, Neely DA, Reshetnikov YS, Salnikov VB, Stoumboudi MT, Mayden RL (2009) Novel relationships among lampreys (Petromyzontiformes) revealed by a taxonomically comprehensive molecular data set. Am Fish Soc Symp 72:41–55Google Scholar
- Levin B, Ermakov A, Ermakov O, Levina M, Sarycheva O, Sarychev V (2016) Ukrainian brook lamprey Eudontomyzon mariae (Berg): phylogenetic position, genetic diversity, distribution, and some data on biology. In: Orlov A, Beamish R (eds) Jawless fishes of the world, vol 1. Cambridge Scholars Publishing, Newcastle Upon Tyne, pp 58–82Google Scholar
- Li Y (2014) Phylogeny of the lamprey genus Lethenteron Creaser and Hubbs 1922 and closely related genera using the mitochondrial cytochrome b gene and nuclear gene introns. MSc thesis, Department of Biological Sciences, The University of Manitoba, Winnipeg, MBGoogle Scholar
- Manzon RG, Youson JH, Holmes JA (2015) Lamprey metamorphosis. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 1. Springer, Dordrecht, pp 139–214Google Scholar
- Morris R (1972) Osmoregulation. In: Hardisty MW, Potter IC (eds) The biology of Lampreys, vol 2. Academic Press, London, pp 192–239Google Scholar
- Potter IC, Gill HS, Renaud CB, Haoucher D (2015) The taxonomy, phylogeny and distribution of Lampreys. In: Docker MF (ed) Lampreys: biology, conservation and control, vol 1. Springer, Dordrecht, pp 35–74Google Scholar
- Renaud CB (1982) Revision of the lamprey genus Eudontomyzon Regan, 1911. MSc thesis, University of Ottawa, Ottawa, ONGoogle Scholar
- Renaud CB (2011) Lampreys of the world. An annotated and illustrated catalogue of lamprey species known to date. FAO Species Catalogue for Fishery Purposes. No. 5. Rome, FAO. 109 ppGoogle Scholar
- Rougemont Q, Roux C, Neuenschwander S, Goudet J, Launey S, Evanno G (2016) Reconstructing the demographic history of divergence between European river and brook lampreys using approximate Bayesian computations. PeerJ 4:e1910. doi: 10.7717/peerj.1910
- Rougemont Q, Gaigher P-A, Perrier C, Genthon C, Besnard A-L, Launey S, Evanno G (2017) Inferring the demographic history underlying parallel genomic divergence among pairs of parasitic and nonparasitic lamprey ecotypes. Mol Ecol 26:142-162Google Scholar