Comparative phylogeography of vicariant species of the Daphnia longispina s.lat. complex (Crustacea: Cladocera) in North Eurasia
- Authors: Zuykova E.I.1,2, Sleptzova L.P.1, Bochkarev N.A.1,2, Zakharov E.S.3, Zakharova N.N.3, Kotov A.A.4
-
Affiliations:
- Institute of Systematics and Ecology of Animals of the Siberian Branch of Russian Academy of Sciences
- Saint Petersburg branch of the Federal State Budget Scientific Institution “Russian Federal Research Institute of Fisheries and oceanography”
- Federal State Autonomus Education Institute of Higher Education "M.K. Ammosov North-Eastern Federal University"
- A. N. Severtsov Institute of Ecology and Evolution of Russian Academy of Sciences
- Issue: Vol 17, No 5 (2024)
- Pages: 685-703
- Section: ВОДНАЯ ФЛОРА И ФАУНА
- URL: https://ruspoj.com/0320-9652/article/view/670036
- DOI: https://doi.org/10.31857/S0320965224050017
- EDN: https://elibrary.ru/XSQBFH
- ID: 670036
Cite item
Abstract
This study presents new data on population-genetic polymorphism, phylogeny and phylogeography of two vicariant species belonging to the Daphnia longispina s.lat. complex (Crustacea: Cladocera) in northern Eurasia, D. longispina s.str. and D. dentifera. Based on the variability of the fragments of non-coding 12S rRNA and the protein coding ND2 genes of mitochondrial DNA, the demographic processes that took place in populations of this vast region have been reconstructed. The previously suggested hypothesis about the different demographic history of the “Siberian” and “European” D. longispina s.str. clades has not been confirmed, since we first revealed a deep mitochondrial divergence within the “Siberian” clade. Moreover, a new divergent lineage of D. longispina s.str. in Siberia has been identified. Nevertheless, the phylogeographic patterns of D. longispina s.str. and D. dentifera in northern Eurasia confirm the earlier conclusion that repeated, combined effects on their populations of dispersion and vicariate events occurred in different phases of the Pleistocene.
Full Text

About the authors
E. I. Zuykova
Institute of Systematics and Ecology of Animals of the Siberian Branch of Russian Academy of Sciences; Saint Petersburg branch of the Federal State Budget Scientific Institution “Russian Federal Research Institute of Fisheries and oceanography”
Author for correspondence.
Email: zuykova1064@yandex.ru
Russian Federation, Novosibirsk; Saint Petersburg
L. P. Sleptzova
Institute of Systematics and Ecology of Animals of the Siberian Branch of Russian Academy of Sciences
Email: zuykova1064@yandex.ru
Russian Federation, Novosibirsk
N. A. Bochkarev
Institute of Systematics and Ecology of Animals of the Siberian Branch of Russian Academy of Sciences; Saint Petersburg branch of the Federal State Budget Scientific Institution “Russian Federal Research Institute of Fisheries and oceanography”
Email: zuykova1064@yandex.ru
Russian Federation, Novosibirsk; Saint Petersburg
E. S. Zakharov
Federal State Autonomus Education Institute of Higher Education "M.K. Ammosov North-Eastern Federal University"
Email: zuykova1064@yandex.ru
Russian Federation, Yakutsk
N. N. Zakharova
Federal State Autonomus Education Institute of Higher Education "M.K. Ammosov North-Eastern Federal University"
Email: zuykova1064@yandex.ru
Russian Federation, Yakutsk
A. A. Kotov
A. N. Severtsov Institute of Ecology and Evolution of Russian Academy of Sciences
Email: zuykova1064@yandex.ru
Russian Federation, Moscow
References
- Аржанников С.Г., Алексеев С.В., Глызин А.В. и др. 2000. Природная обстановка в Голоцене в западной части Тоджинской впадины на примере разреза Мерзлый Яр // Проблемы реконструкции климата и природной среды голоцена и плейстоцена Сибири. Новосибирск: Изд-во Ин-та археологии и этнографии СО РАН. Вып. 2. С. 18.
- Гречко В.В. 2013. Проблемы молекулярной филогенетики на примере отряда чешуйчатых рептилий (отряд Squamata): митохондриальные ДНК-маркеры // Мол. биол. Т. 47(1). С. 61.
- Картавцев Ю.Ф. 2013. Генетическая дивергенция видов и других таксонов. Географическое видообразование и генетическая парадигма неодарвинизма в действии // Успехи соврем. биол. Т. 133(5). С. 419.
- Adamowicz S.J., Petrusek A., Colbourne J.K. et al. 2009. The scale of divergence: a phylogenetic appraisal of intercontinental allopatric speciation in a passively dispersed freshwater zooplankton genus // Mol. Phyl. Evol. V. 50. P. 423.
- Avise J.C. 2000. Phylogeography. The history and formation of species. Cambridge: Harvard Univ. Press.
- Avise J.C., Arnold J., Ball R.M. et al. 1987. Intraspecific phylogeography: the mitochondrial DNA bridge between population genetics and systematics // Annual. Rev. Ecol. Syst. V. 18. P. 489.
- Bandelt H., Forster P., Röhl A. 1999. Median-joining networks for inferring intraspecific phylogenies // Mol. Biol. Evol. V. 16. P. 37.
- Belyaeva M., Taylor D.J. 2009. Cryptic species within the Chydorus sphaericus species complex (Crustacea: Cladocera) revealed by molecular markers and sexual stage morphology // Mol. Phyl. Evol. V. 50. P. 534.
- Benzie J.A.H. 2005. The genus Daphnia (including Daphniopsis) (Anomopoda: Daphniidae). Guides to the identification of the microinvertebrates of the continental waters of the world 21. Leiden: Ghent & Backhuys Publ.
- Crease T.J., Omilian A.R., Costanzo K.S. et al. 2012. Transcontinental phylogeography of the Daphnia pulex species complex // PLoS ONE. V. 7. № e46620. https://doi.org/10.1371/journal.pone.0046620
- Cornetti L., Fields P.D., Van Damme K. et al. 2019. A fossil-calibrated phylogenomic analysis of Daphnia and the Daphniidae // Mol. Phyl. Evol. V. 137. P. 250. https://doi.org/10.1016/j.ympev.2019.05.018
- Darriba D., Taboada G.L., Doallo R. et al. 2012. jModelTest 2: more models, new heuristics and parallel computing // Nature Meth. V. 9. № 772.
- De Gelas K., De Meester L. 2005. Phylogeography of Daphnia magna in Europe // Mol. Ecol. V. 1. P. 753. https://doi.org/10.1111/j.1365-294X.2004.02434.x
- De Meester L., Gómez A., Okamura B. et al. 2002. The Monopolization hypothesis and the dispersal-gene flow paradox in aquatic organisms // Acta Oecol. V. 23. P. 121.
- De Salle R., Freedman T., Prager E.M. et al. 1987. Tempo and mode of sequence evolution in mitochondrial DNA of Hawaiian Drosophila // J. Mol. Evol. V. 26. P. 157.
- Excoffier L. 2004. Patterns of DNA sequence diversity and genetic structure after a range expansion: lessons from the infinite-island model // Mol. Ecol. V. 3. P. 853.
- Excoffier L., Lischer H.E.L. 2010. Arlequin suite ver 3.5: A new series of programs to perform population genetics analyses under Linux and Windows // Mol. Ecol. Res. V. 10. P. 564.
- Figuerola J., Green A.J. 2002. Dispersal of aquatic organisms by water birds: a review of past research and priorities for future studies // Freshwater Biol. V. 47. P. 483. https://doi.org/10.1046/j.1365-2427.2002.00829.x
- Figuerola J., Green A.J., Michot T.C. 2005. Invertebrate eggs can fly: evidence of Waterfowl-mediated gene flow in aquatic invertebrates // Amer. Nat. V. 165. P. 274. https://doi.org/10.1086/427092
- Frey D.G. 1987. The non-cosmopolitanism of chydorid Cladocera: implications for biogeography and evolution // Crustacean Iss. V. 4. P. 237.
- Fu Y.X. 1997. Statistical tests of neutrality of mutations against population growth, hitchhiking and background selection // Genetics. V. 147. P. 915.
- Garrigan D., Lewontin R., Wakeley J. 2010. Measuring the sensitivity of single-locus “neutrality tests” using a direct perturbation approach // Mol. Biol. Evol. V. 27. P. 73. https://doi.org/10.1093/molbev/msp209
- Grant W.A.S., Bowen B.W. 1998. Shallow population histories in deep evolutionary lineages of marine fishes: Insights from sardines and anchovies and lessons for conservation // J. Heredity. V. 89. P. 415. https://doi.org/10.1093/jhered/89.5.415
- Grant W.S. 2015. Problems and cautions with sequence mismatch analysis and Bayesian Skyline Plots to infer historical demography // J. Heredity. V. 106. P. 333.
- Grosswald M.G., Kotlyakov V.M. 1989. Great preglacial drainage system Northern Asia and its importance for interregional correlations // Quaternary period. Paleography and lithology. Kishinev: Shtiinitsa. P. 5.
- Guindon S., Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood // System. Biol. V. 52. P. 696.
- Hall T.A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT // Nucl. Acids. Symp. Ser. V. 41. P. 95.
- Hamrová, E., Mergeay J., Petrusek A. 2011. Strong differences in the clonal variation of twoDaphnia species from mountain lakes affected by overwintering strategy // BMC Evol. Biol. V. 11. № 231. https://doi.org/10.1186/1471-2148-11-231
- Harpending H. 1994. Signature of ancient population growth in a low resolution mitochondrial DNA mismatch distribution // Hum. Biol. V. 66. P. 591.
- Havel J.E., Shurin J.B. 2004. Mechanisms, effects, and scales of dispersal in freshwater zooplankton // Limnol. Oceanogr. V. 49. P. 1229. https://doi.org/10.4319/lo.2004.49.4_part_2.1229
- Hebert P.D.N., Cywinska A., Ball S.L. et al. 2003. Biological identifications through DNA barcodes // Proc. Roy. Soc. B: Biol. Sci. V. 270. P. 313. https://doi.org/10.1098/rspb.2002.2218
- Hebert P.D.N., Wilson C.C. 1994. Provincialism in plankton: endemism and allopatric speciation in Australian Daphnia // Evolution. V. 48. P. 1333. https://doi.org/10.1111/j.1558-5646.1994.tb05317.x
- Hewitt G.M. 2000. The genetic legacy of the Quaternary ice ages // Nature. V. 405. P. 907.
- Ho S.Y.W., Phillips M.J., Cooper A. et al. 2005. Time dependency of molecular rate estimates and systematic overestimation of recent divergence times // Mol. Biol. Evol. V. 22. P. 1561. https://doi.org/10.1093/molbev/msi145
- Holsinger K.E. 2015. Lecture notes in population genetics. Department of Ecology and Evolutionary Biology. U-3043. University of Connecticut Storrs. https://doi.org/10.6084/M9.FIGSHARE.100687
- Huang X., Shi X., Kotov A.A. et al. 2014. Confirmation through genetic analysis of the existence of many local phyloclades of the genus Simocephalus (Crustacea, Cladocera) in China // PLoS ONE. V. 9. № e112808. https://doi.org/10.1371/journal.pone.0112808
- Ishida S., Taylor D.J. 2007. Quaternary diversification in a sexual Holarctic zooplankter, Daphnia galeata // Mol. Ecol. V. 16. P. 569. https://doi.org/10.1111/j.1365-294X.2006.03160.x
- Jeffery N.W., Elias-Gutierrez M., Adamowicz S.J. 2011. Species diversity and phylogeographical affinities of the Branchiopoda (Crustacea) of Churchill, Manitoba, Canada // PLoS ONE. V. 11. № e18364.
- Katoh K., Rozewicki J., Yamada K.D. 2019. MAFFT online service: multiple sequence alignment, interactive sequence choice and visualization // Brief. Bioinform. V. 20(4). P. 1160. https://doi.org/10.1093/bib/bbx108
- Karabanov D.P., Bekker E.I., Shiel R.J. et al. 2018. Invasion of a Holarctic planktonic cladoceran Daphnia galeata Sars (Crustacea: Cladocera) in the Lower Lakes of South Australia // Zootaxa. V. 4402. P. 136. https://doi.org/10.11646/zootaxa.4402.1.6
- Knowles L.L., Maddison W.P. 2002. Statistical phylogeography // Mol. Ecol. V. 11(12). P. 2623.
- Kotov A.A. Taylor D.J. 2019. Contrasting endemism in pond–dwelling cyclic parthenogens: the Daphnia curvirostris species group (Crustacea: Cladocera) /// Sci. Rep. V. 9. № 6812. https://doi.org/10.1038/s41598-019-43281-9
- Kotov A.A., Garibian P.G., Bekker E.I. et al. 2021. A new species group from the Daphnia curvirostris species complex (Cladocera: Anomopoda) from the eastern Palaearctic: taxonomy, phylogeny and phylogeography // Zool. J. Linn. Soc. V. 191. P. 772.
- Kumar S., Stecher G., Tamura K. 2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets // Mol. Biol. Evol. V. 33. P. 1870.
- Leigh J.W., Bryant D. 2015. PopART: Full-feature software for haplotype network construction // Methods Ecol. Evol. V. 6. P. 1110.
- Librado P., Rozas J. 2009. DnaSP v5: A software for comprehensive analysis of DNA polymorphism data // Bioinformatics. V. 25. P. 1451.
- Louette G., De Meester L. 2005. High dispersal capacity of cladoceran zooplankton in newly founded communities // Ecology. V. 86. P. 353.
- Lynch M. 2010. Evolution of the mutation rate // Trends Genet. V. 26. P. 345. https://doi.org/10.1016/j.tig.2010.05.003
- Ma X., Petrusek A., Wolinska J. et al. 2014. Diversity of the Daphnia longispina species complex in Chinese lakes: a DNA taxonomy approach // J. Plank. Res. V. 37. P. 56. https://doi.org/10.1093/plankt/fbu091
- Minh B.Q., Nguyen M.A.T., von Haeseler A. 2013. Ultrafast approximation for phylogenetic bootstrap // Mol. Biol. Evol. V. 30. P. 1188. https://doi.org/10.1093/molbev/mst024
- Nei M., Kumar S. 2000. Molecular Evolution and Phylogenetics. N.Y.: Oxford Univ. Press. P. 333.
- Nguyen L.-T., Schmidt H.A., von Haeseler A. et al. 2015. IQ-TREE: A fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies // Mol. Biol. Evol. V. 32. P. 268. https://doi.org/10.1093/molbev/msu300
- Penton E.H., Crease T.J. 2004. Evolution of the transposable element Pokey in the ribosomal DNA of species in the subgenus Daphnia (Crustacea: Cladocera) // Mol. Biol. Evol. V. 21. P. 1727.
- Petrusek A., Thielsch A., Schwenk K. 2012. Mitochondrial sequence variation suggests extensive cryptic diversity within the Western Palearctic Daphnia longispina complex // Limnol., Oceanogr. V. 57. P. 1838.
- Rambaut A., Drummond A.J., Xie D. et al. 2018. Posterior summarisation in Bayesian phylogenetics using Tracer 1.7 // Syst. Biol. V. 67. P. 901. https://doi.org/10.1093/sysbio/syy032
- Ray N., Currat M., Excoffier L. 2003. Intra-deme molecular diversity in spatially expanding populations // Mol. Biol. Evol. V. 20. P. 76.
- Rogers A.R., Harpending H. 1992. Population growth makes waves in the distribution of pairwise genetic differences // Mol. Biol. Evol. V. 9. P. 552.
- Rogers A.R., Fraley A.E., Bamshad M.J. et al. 1996. Mitochondrial mismatch analysis is insensitive to mutational process // Mol. Biol. Evol. V. 17. P. 895. https://doi.org/10.1093/molbev/13.7.895
- Ronquist F., Huelsenbeck J.P. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models // Bioinformatics. V. 19. P. 1572.
- Rosenberg N.A., Nordborg M. 2002. Genealogical trees, coalescent theory and the analysis of genetic polymorphisms // Nat. Rev. Genet. V. 3. P. 380. https://doi.org/10.1038/nrg795
- Saitou N., Nei M. 1987. The neighbor-joining method: a new method for reconstructing phylogenetic trees // Mol. Biol. Evol. V. 4. P. 6.
- Schenekar T. Weiss S. 2011. High rate of calculation errors in mismatch distribution analysis results in numerous false inferences of biological importance // Heredity. V. 107. P. 511. https://doi.org/10.1038/hdy.2011.48
- Schneider S., Excoffier L. 1999. Estimation of past demographic parameters from the distribution of pairwise differences when the mutation rates vary among sites: application to human mitochondrial DNA // Genetics. V. 152. P. 1079.
- Slatkin M., Hudson R. 1991. Pairwise comparisons of mitochondrial DNA sequences in stable and exponentially growing populations // Genetics. V. 129. P. 555.
- Tajima F. 1989. Statistical methods for testing the neutral mutation hypothesis by DNA polymorphism // Genetics. V. 123. P. 585.
- Taylor D.J., Hebert P.D., Colbourne J.K. 1996. Phylogenetics and evolution of the Daphnia longispina group (Crustacea) based on 12S rDNA sequence and allozyme variation // Mol. Phyl. Evol. V. 5. P. 495.
- Taylor D.J., Finston T.L., Hebert P.D.N. 1998. Biogeography of a widespread freshwater crustacean: pseudocongruence and cryptic endemism in the North American Daphnia laevis complex // Evolution. V. 52. P. 1648.
- Templeton A.R. 1998. Nested clade analysis of phylogeographic data: testing hypotheses about gene flow and population history // Mol. Ecol. V. 7. P. 381.
- Thielsch A., Brede N., Petrusek A. et al. 2009. Contribution of cyclic parthenogenesis and colonization history to population structure in Daphnia // Mol. Ecol. V. 18. V. 1616.
- Trifinopoulos J., Nguyen L.T., von Haeseler A. et al. 2016. W-IQ-TREE: a fast online phylogenetic tool for maximum likelihood analysis // Nucleic Acids Res. V. 44. P. 232. https://doi.org/10.1093/nar/gkw256
- Van de Meutter F., Stoks R. et al. 2008. Size-selective dispersal of Daphnia resting eggs by backswimmers (Notonecta maculata) // Biol. Lett. V. 4. P. 494. https://doi.org/10.1098/rsbl.2008.0323
- Ventura M., Petrusek A., Miró A. et al. 2014. Local and regional founder effects in lake zooplankton persist after thousands of years despite high dispersal potential // Mol. Ecol. V. 23. P. 1014. https://doi.org/10.1111/mec.12656
- Vysotskiy E.M. 2001. Geomorphology of the basin of Teletskoe Lake // Physical and geological environment of Lake Teletskoe. Tervuren: Musee Royal de I Afrigue Centrale Tervuren. P. 164.
- Zuykova E.I., Bochkarev N.A., Katokhin A.V. 2013a. Molecular-genetic diagnosis and phylogeny of Daphnia species in water bodies of the Chany Lake basin // Rus. J. Genetics. V. 49. P. 206.
- Zuykova E.I., Bochkarev N.A., Katokhin A.V. 2013b. Identification of the Daphnia species (Crustacea: Cladocera) in the lakes of the Ob and Yenisei River basins: morphological and molecular phylogenetic approaches // Hydrobiologia. V. 715. P. 135.
- Zuykova E.I., Simonov E.P., Bochkarev N.A. 2017. Comparative morphological and genetic analysis of populations and species of the genus Daphnia O.F. Müller, 1785 (Crustacea; Daphniidae) from Lake Glubokoe and Lake Chany // Biol. Bull. V. 44. P. 277. https://doi.org/10.1134/S106235901703013X
- Zuykova E.I., Simonov E.P., Bochkarev N.A. et al. 2018a. Contrasting phylogeographic patterns in closely related species of Daphnia longispina group (Crustacea: Cladocera) with focus on north-eastern Eurasia // PLoS ONE. V. 13. № 11. № e0207347.
- Zuykova E.I., Simonov E.P., Bochkarev N.A. et al. 2018b. Resolution of the Daphnia umbra problem (Crustacea: Cladocera) using an integrated taxonomic approach // Zool. J. Linn. Soc. V. 184. P. 969.
- Zuykova E.I., Bochkarev N.A., Talor D.J. et al. 2019. Unexpected endemism in the Daphnia longispina complex (Crustacea: Cladocera) in Southern Siberia // PLoS ONE. V. 14. № e0221527.
- Zuykova E.I., Bochkarev N.A., Kotov A.A. 2021. Specific and genetic structure of the Daphnia longispina s. l. complex (Cladocera, Daphniidae) in water bodies of Southern Siberia // Biol. Bull. V. 48. P. 880.
- Zuykova E.I., Sleptzova L.P., Bochkarev N.A. et al. 2022. Mitochondrial lineage diversity and phylogeography of Daphnia (Daphnia) (Crustacea: Cladocera) in North-East Russia // Water. V. 14. № 1946. https://doi.org/10.3390/w14121946
Supplementary files
