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Type: Article
Published: 2023-06-09
Page range: 182-198
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Relative Genetic Homogeneity within a Phenotypically Diverse group: The Case of Lake Tana Labeobarbus (Cyprinidae) Species Flock, Ethiopia

Department of Biological Sciences and Chemistry; Southern University and Agricultural & Mechanical College; 801 Harding Blvd; Baton Rouge; LA 70807; USA
Biodiversity and Systematics; Department of Biological Sciences; The University of Alabama; Tuscaloosa; AL 35487-0345; USA
Department of Mathematics and Statistics; South Dakota State University; Box 2225; Brookings; SD
Pisces genetic differentiation hexaploid microsatellite loci spawning populations species delineation Torinii

Abstract

The Lake Tana Labeobarbus species flock represents one of the world’s most famous examples of lacustrine species radiations. Previous studies of this group have resulted in the description of at least 15 species based on their differences in functional morphology and definition of two clades (lacustrine and riverine spawning clades) based on life history traits. A total of 166 fish representing 14 Labeobarbus species were genotyped using 10 lineage-specific hexaploid microsatellite loci. Six of these loci were developed for this study based on DNA sequence contigs derived from a microsatellite-enriched genomic library of Labeobarbus intermedius from Lake Tana; the remaining four loci were obtained from a previous study. The genotypes of the 10 loci were analyzed to examine genetic diversity and population structure within Lake Tana Labeobarbus. Overall mean allelic richness (NA) was 17.6 alleles per locus and observed (Ho) and expected (He) heterozygosities were 0.84 ± 0.14 and 0.73 ± 0.09, respectively, across all Lake Tana Labeobarbus samples examined. Our analyses reveal that there is little genetic differentiation among species (FST = 0.020–0.099; only 10 of 91 species comparisons were significant), but moderate differentiation (FST = 0.11, p < 0.05) between lacustrine and riverine spawning populations. Relative to previous phylogenetic hypotheses, our phenetic analysis employing the R-based Analysis of Phylogenetics and Evolution (APE) program seems to perform marginally better in revealing lineages within Lake Tana Labeobarbus. Herein, our results are compared to a previous microsatellite-based study of the same populations.

 

References

  1. Albertson, R.C., Markert, J.A. Danley, P.D. & Kocher, T.D. (1999) Phylogeny of a rapidly evolving clade: the cichlid fishes of Lake Malawi, East Africa. Proceedings of the National Academy of Sciences of the USA, 96, 5107–5110. https://doi.org/10.1073/pnas.96.9.5107 DOI: https://doi.org/10.1073/pnas.96.9.5107
  2. Alekseyev, S.S., Dgebuadze, Y.Y., Mina, M.V. & Mironovsky, A.N. (1996) Small ‘large barbs’ spawning in tributaries of Lake Tana: what are they? Folia Zoologica, 45, 85–96.
  3. Amos, W., Hoffman, J.I., Frodsham, A., Zhang, L., Best, S. & Hill, A.V.S. (2007) Automated binning of microsatellite alleles: problems and solutions. Molecular Ecology Notes, 7, 10–14. https://doi.org/10.1111/j.1471-8286.2006.01560.x DOI: https://doi.org/10.1111/j.1471-8286.2006.01560.x
  4. Anteneh, W., Getahun, A., Dejen, E., Sibbing, F.A., Nagelkerke, L.A.J., de Graaf, M., Wudneh, T., Vijverberg, J. & Palstra, A.P. (2012) Spawning migrations of the endemic Labeobarbus (Cyprinidae, Teleostei) species of Lake Tana, Ethiopia: status and threats. Journal of Fish Biology, 81, 750–765. https://doi.org/10.1111/j.1095-8649.2012.03362.x DOI: https://doi.org/10.1111/j.1095-8649.2012.03362.x
  5. Banister, K.E. (1973) A revision of the large Barbus (Pisces, Cyprinidae) of East and Central Africa. Studies on African Cyprinidae. Bulletin of the British Museum of Natural History (Zoology), 26, 167–180. https://doi.org/10.5962/bhl.part.204 DOI: https://doi.org/10.5962/bhl.part.204
  6. Berrebi, P. & Valiushok, D. (1998) Genetic divergence among morphotypes of Lake Tana (Ethiopia) barbs. Biological Journal of Linnean Society, 64, 369–384. https://doi.org/10.1111/j.1095-8312.1998.tb00338.x DOI: https://doi.org/10.1111/j.1095-8312.1998.tb00338.x
  7. Beshera, K.A. & Harris, P.M. (2014) Mitochondrial DNA phylogeography of Labeobarbus intermedius (Cyprinidae; Pisces) from Ethiopia. Journal of Fish Biology, 85:228–245. https://doi.org/10.1111/jfb.12408 DOI: https://doi.org/10.1111/jfb.12408
  8. Bini, G. (1940) I Pesci de lago Tana. Missione di Studio al Lago Tana, 3, 138–246.
  9. Boulenger, G.A. (1902) Descriptions of new fishes from the collection made by Mr. E. Degen in Abyssinia. Annals and Magazine of Natural History, 10, 421–437. https://doi.org/10.1080/00222930208678700 DOI: https://doi.org/10.1080/00222930208678700
  10. Brown, K.M., Baltazar, G.A. & Hamilton, M.B. (2005) Reconciling nuclear microsatellite and mitochondrial marker estimates of population structure: breeding population structure of Chesapeake Bay striped bass (Morone saxatilis). Heredity, 94, 606–615. https://doi.org/10.1038/sj.hdy.6800668 DOI: https://doi.org/10.1038/sj.hdy.6800668
  11. Chenuil, A., Desmarais, E., Pouyaud, L. & Berrebi, P. (1997) Does polyploidy lead to fewer and shorter microsatellites in Barbus (Teleostei: Cyprinidae)? Molecular Ecology, 6, 169–178. https://doi.org/10.1046/j.1365-294x.1997.00170.x DOI: https://doi.org/10.1046/j.1365-294X.1997.00170.x
  12. Clark, L.V. & Jasieniuk, M. (2011) Polysat: An R package for polyploid microsatellite analysis. Molecular Ecology Resources, 11, 562–566. https://doi.org/10.1111/j.1755-0998.2011.02985.x DOI: https://doi.org/10.1111/j.1755-0998.2011.02985.x
  13. De Graaf, M., Dejen, E., Osse, W.J.M. & Sibbing, F.A. (2008) Adaptive radiation of Lake Tana’s Labeobarbus species-flock (Pisces, Cyprinidae). Marine and Freshwater Research, 59, 391–407. https://doi.org/10.1071/MF07123 DOI: https://doi.org/10.1071/MF07123
  14. De Graaf, M., Megens, H.J., Samallo, J. & Sibbing, F.A. (2010) Preliminary insight into the age and origin of the Labeobarbus species-flock from Lake Tana (Ethiopia) using the mtDNA cytochrome b gene. Molecular Phylogenetics and Evolution, 55, 488–500. https://doi.org/10.1016/j.ympev.2009.10.029 DOI: https://doi.org/10.1016/j.ympev.2009.10.029
  15. De Silva, H.N., Hall, A.J., Rikkerink, M.A., McNeilage, M.A. & Fraser, L.G. (2005) Estimation of allele frequencies in polyploids under certain patterns of inheritance. Heredity, 95, 327–334. https://doi.org/10.1038/sj.hdy.6800728 DOI: https://doi.org/10.1038/sj.hdy.6800728
  16. Dgebuadze, Y.Y. (1999) Observations on reproduction of Lake Tana barbs. Journal of Fish Biology, 54, 417–423. https://doi.org/10.1111/j.1095-8649.1999.tb00840.x DOI: https://doi.org/10.1111/j.1095-8649.1999.tb00840.x
  17. Dixon, B., Nagelkerke, L.A.J., Sibbing, F.A., Egberts, E. & Stet, R.J.M. (1996) Evolution of MHC class II βchain-encoding genes in the Lake Tana barbel species-flock (Barbus intermedius complex). Immunogenetics, 44, 419–431. https://doi.org/10.1007/s002510050148 https://doi.org/10.1007/BF02602803 DOI: https://doi.org/10.1007/s002510050148
  18. Drummond, A., Ashton, B., Cheung, M., Heled, J., Kearse, M., Moir, R., Stones-Havas, S., Thierer, T. & Wilson, A. (2009) Geneious v4.7. Available from: http://www.geneious.com/ (last accessed 02 Feburary 2022)
  19. Dufresne, F., Stift, M., Vergilino, R. & Mable, B.K. (2014) Recent progress and challenges in population genetics of polyploid organisms: an overview of current state–of–the–art molecular and statistical tools. Molecular Ecology, 23, 40–69. https://doi.org/10.1111/mec.12581 DOI: https://doi.org/10.1111/mec.12581
  20. Dzerzhinskii, F.N., Shkil, F.N., Abdissa, B., Zelalem, W. & Mina, M.V. (2007) Spawning of Large Barbus (Barbus intermedius Complex) in a Small River of the Lake Tana Basin (Ethiopia) and Relationships of Some Putative Species. Journal of Ichthyology, 47, 639–646. https://doi.org/10.1134/S0032945207080103 DOI: https://doi.org/10.1134/S0032945207080103
  21. Edwards, D.D., Vidrine, M.F. & Ernsting, B.R. (2010) Phylogenetic relationships among Unionicola (Acari: Unionicolidae) mussel–mites of North America based on mitochondrial cytochrome c oxidase I sequences. Zootaxa, 2537 (1), 47–50. https://doi.org/10.11646/zootaxa.2537.1.4 DOI: https://doi.org/10.11646/zootaxa.2537.1.4
  22. Evanno, G., Regnaut, S. & Goudet, J. (2005) Detecting the number of clusters of individuals using the software Structure: a simulation study. Molecular Ecology, 14, 2611–2620. https://doi.org/10.1111/j.1365-294X.2005.02553.x DOI: https://doi.org/10.1111/j.1365-294X.2005.02553.x
  23. Golubtsov, A.S. & Krysanov, E.Y. (1993) Karyological study of some cyprinid species from Ethiopia. The ploidy differences between large and small Barbus of Africa. Journal of Fish Biology, 42, 445–455. https://doi.org/10.1111/j.1095-8649.1993.tb00347.x DOI: https://doi.org/10.1111/j.1095-8649.1993.tb00347.x
  24. Guégan, J.-F, Rab, P., Machordom, A. & Doadrio, I. (1995) New evidence of hexaploidy in 'large' African Barbus with some considerations on the origin of hexaploidy. Journal of Fish Biology, 4, 192–198. https://doi.org/10.1111/j.1095-8649.1995.tb01888.x DOI: https://doi.org/10.1111/j.1095-8649.1995.tb01888.x
  25. Hamrick, J.L., Godt, M.J.W., Murawshi, D.A. & Loveless, M.D. (1991) Correlations between species traits and allozyme diversity: implications for conservation biology. In: Falk, D.A. & Holsinger, K.E. (Eds.), Genetics and conservation of rare plants. Oxford University Press, New York, pp. 75–86.
  26. Hillis, D.M., Mable, B.K., Larson, A., Davis, S.K. & Zimmer, E.A. (1996) Nucleic acids IV: sequencing and cloning. In: Hillis, D., Moritz, C. & Mable, B. (Eds.), Molecular Systematics. Sinauer Associates, Sunderland, MA.
  27. Jombart, T., Devillard, S. & Balloux, F. (2010) Discriminant analysis of principal components: a new method for the analysis of genetically structured populations. BMC Genetics, 11, 9. https://doi.org/10.1186/1471-2156-11-94 DOI: https://doi.org/10.1186/1471-2156-11-94
  28. Kruiswijk, C.P., Hermsen, T., Heerwaarden, J.V., Dixon, B., Savelkoul, H.F.J. & Stet, R.J.M. (2005) Major histocompatibility genes in Lake Tana African large barb species-flock; evidence for complete partitioning of class II B, but not class I, genes among different species. Immunogenetics, 56, 894–908. https://doi.org/10.1007/s00251-005-0767-5. Epub 2005 Feb 8
  29. Krysanov, E., Yu, E. & Golubtsov, A.S. (1996) Karyotypes of some Ethiopian Barbus and Varicorhinus from the Nile Basin including Lake Tana morphotypes. Folia Zoologica, 45 (1), 67–75.
  30. Levin, B.A., Casal-López, M., Simonov, E., Dgebuadze, Y.Y., Mugue, N.S., Tiunov, A.V., Doadrio, I. & Golubstov, A.S. (2019) Adaptive radiation of barbs of the genus Labeobarbus (Cyprinidae) in the East African river. Freshwater Biology, 64, 1721–1736. https://doi.org/10.1111/fwb.13364 DOI: https://doi.org/10.1111/fwb.13364
  31. Levin, B.A., Dgebuadze, Y.Y., Tefera, F., Tesfaye, G. & Golubstov, A.S. (2017) An evidence of past introgressive hybridization between Labeobarbus ethiopicus and Labeobarbus intermedius in the Ethiopian rift Valley, East Africa. Ethiopian Journal of Biological Sciences, 16 (Suppl.), 45-60.
  32. Levin, B.A., Komarova, A.S., Rozanova, O.L. & Golubtsov, A.S. (2021) Unexpected Diversity of Feeding Modes among Chisel–Mouthed Ethiopian Labeobarbus (Cyprinidae). Water, 13, 2345. https://doi.org/10.3390/w13172345 DOI: https://doi.org/10.3390/w13172345
  33. Levin, B.A., Simonov, E., Dgebuadze, Y.Y., Levina, M. & Golubstov, A.S. (2020) In the rivers: multiple adaptive radiations of cyprinid fishes (Labeobarbus) in Ethiopian highlands. Scientific Reports, 10, 7192. https://doi.org/10.1038/s41598-020-64350-4 DOI: https://doi.org/10.1038/s41598-020-64350-4
  34. Levin, B.A., Simonov, E., Franchini, P., Mugue, N., Golubtsov, A. & Meyer, A. (2021). Rapid adaptive radiation in a hillstream cyprinid fish in the East African White Nile River basin. Molecular Ecology, 30 (21), 5530–5550. https://doi.org/10.1111/mec.16130. DOI: https://doi.org/10.1111/mec.16130
  35. Levin, B., Simonov, E., Gabrielyan, B.K., Mayden, R.L., Rastorguev, S.M., Roubenyan, H.R., Sharko, F.S. & Nedoluzhko, A.V. (2022) Caucasian treasure: Genomics sheds light on the evolution of half-extinct Sevan trout, Salmo ischchan, species flock. Molecular Phylogenetics and Evolution, 167, 107346. https://doi.org/10.1016/j.ympev.2021.107346 DOI: https://doi.org/10.1016/j.ympev.2021.107346
  36. Mallet, J. (2005) Hybridization as an invasion of the genome. Trends in Ecology and Evolution, 20 (5), 229–239. https://doi.org/10.1016/j.tree.2005.02.010 DOI: https://doi.org/10.1016/j.tree.2005.02.010
  37. Mayer, C. (2006–2010) Phobos 3.3.11. Availabe from: http://www.rub.de/spezzoo/cm/cm_phobos.htm (Accessed 05 May 2014)
  38. Mayr, E. (1963) Animal species and evolution. Belknap Press, Cambridge, MA, 797 pp. https://doi.org/10.4159/harvard.9780674865327 DOI: https://doi.org/10.4159/harvard.9780674865327
  39. Meriams, P.G. & Tienderen, P.H.V. (2004) GENOTYPE and GENODIVE: two programs for the analysis of genetic diversity of asexual organisms. Molecular Ecology Notes, 4, 792–794. https://doi.org/10.1111/j.1471-8286.2004.00770.x DOI: https://doi.org/10.1111/j.1471-8286.2004.00770.x
  40. Moody, M.E., Muellert, L.D. & Soltis, D.E. (1993) Genetic Variation and Random Drift in Autotetraploid Population. Genetics, 154, 649–657. https://doi.org/10.1093/genetics/134.2.649 DOI: https://doi.org/10.1093/genetics/134.2.649
  41. Nagelkerke, L.A.J. & Sibbing, F.A. (1996) Reproductive segregation among the large barbs (Barbus intermedius complex) of Lake Tana, Ethiopia. An example of lacustrine speciation? Journal of Fish Biology, 49, 1244–1266. https://doi.org/10.1111/j.1095-8649.1996.tb01793.x DOI: https://doi.org/10.1111/j.1095-8649.1996.tb01793.x
  42. Nagelkerke, L.A.J. & Sibbing, F.A. (1997) A revision of the large barbs (Barbus spp., Cyprinidae, Teleostei) of Lake Tana, Ethiopia, with a description of seven new species. In: Nagelkerke, L.A.J (Ed.), The barbs of Lake Tana, Ethiopia: morphological diversity and its implications for taxonomy, trophic resource partitioning, and fisheries (Doctoral dissertation). Wageningen Agricultural University, Wageningen, pp. 105–171.
  43. Nagelkerke, L.A.J. & Sibbing, F.A. (2000) The large barbs (Barbus spp., Cyprinidae, Teleostei) of Lake Tana (Ethiopia), with a description of a new species, Barbus osseensis. Netherlands Journal of Zoology, 50, 179–214. https://doi.org/10.1163/156854200505946 DOI: https://doi.org/10.1163/156854200505946
  44. Nagelkerke, L.A.J., Sibbing, F.A., Boogaart, J.G.M., Lammens, E.H.R.R. & Osse, J.W.M. (1994) The barbs (Barbus spp.) of Lake Tana: a forgotten species flock? Environmental Biology of Fishes, 39, 1–22. https://doi.org/10.1007/BF00004751 DOI: https://doi.org/10.1007/BF00004751
  45. Nagelkerke, L.A.J., Leon-Kloosterziel, K.M., Megens, H.-J., de Graaf, M., Diekmann, O.E. & Sibbing, F.A. (2015) Shallow genetic divergence and species delineations in the endemic Labeobarbus species flock of Lake Tana, Ethiopia. Journal of Fish Biology, 87, 1191–208. https://doi.org/10.1111/jfb.12779 DOI: https://doi.org/10.1111/jfb.12779
  46. Naran, D., Skelton, P.H. & Villet, M.H. (2007) Karyology of three evolutionarily hexaploid southern African species of yellowfish, Labeobarbus Rüppel, 1836 (Cyprinidae). African Zoology, 42, 254–260. https://doi.org/10.3377/1562-020(2007)42[254:KOTEHS]2.0.CO;2 DOI: https://doi.org/10.3377/1562-7020(2007)42[254:KOTEHS]2.0.CO;2
  47. Nater, A., Burri, R., Kawakami, T., Smeds, L. & Ellegren, H. (2015) Resolving evolutionary relationships in closely related species with whole-genome sequencing data. Systematic Biology, 64 (6), 1017–2015. https://doi.org/10.1093/sysbio/syv045 DOI: https://doi.org/10.1093/sysbio/syv045
  48. Palstra, A. P., de Graaf, M., & Sibbing, F. A. (2004) Riverine spawning and reproductive segregation in a lacustrine cyprinid species flock, facilitated by homing? Animal Biology, 54, 393–415. https://doi.org/10.1163/1570756042729519 DOI: https://doi.org/10.1163/1570756042729519
  49. Paradis, E., Claude, J. & Strimmer, K. (2003) APE: Analyses of Phylogenetics and Evolution in R language. Bioinformatics, 20, 289–290. https://doi.org/10.1093/bioinformatics/btg412 DOI: https://doi.org/10.1093/bioinformatics/btg412
  50. Petren, K., Grant, P.R., Grant, B.R. & Keller, L.F. (2005) Comparative landscape genetics and the adaptive radiation of Darwin's finches: the role of peripheral isolation. Molecular Ecology, 14, 2943–2957. https://doi.org/10.1111/j.1365-294X.2005.02632.x DOI: https://doi.org/10.1111/j.1365-294X.2005.02632.x
  51. Prave, A.R., Bates, C.R., Donaldson, C.H., Toland, H., Condon, D.J., Mark, D. & Raub, T.D. (2016) Geology and geochronology of the Tana Basin, Ethiopia: LIP volcanism, super eruptions and Eocene–Oligocene environmental change. Earth Planet. Science Letters, 443, 1–8. https://doi.org/10.1016/j.epsl.2016.03.009 DOI: https://doi.org/10.1016/j.epsl.2016.03.009
  52. Pritchard, J. K., Stephens, M. & Donnely, P. (2000) Inference of population structure using multilocus genotype data. Genetics, 155, 945–959. https://doi.org/10.1093/genetics/155.2.945 DOI: https://doi.org/10.1093/genetics/155.2.945
  53. Riesch, R., Muschick, M., Lindtke, D., Villoutreix, R., Comeault, A.A., Farkas, T.E., Lucek, K., Hellen, E., Soria-Carrasco, V., Dennis, S.R., de Carvalho, C.F., Safran, R.J., Sandoval, C.P., Feder, J., Gries, R., Crespi, B.J., Gries, G., Gompert, Z. & Nosil, P. (2017) Transitions between phases of genomic differentiation during stick-insect speciation. Nature Ecology & Evolution, 1, 0082. https://doi.org/0.1038/s41559-017-0082 DOI: https://doi.org/10.1038/s41559-017-0082
  54. Rosenberg, N.A. (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes, 4, 137–138. https://doi.org/10.1046/j.1471-8286.2003.00566.x DOI: https://doi.org/10.1046/j.1471-8286.2003.00566.x
  55. Rüppell, W.P.E.S. (1836) Neuer Nachtrag von Beschreibungen und Abbildungen neuer Fische, im Nil entdeckt. Museum Senckenbergianum: Abhandlungen aus dem Gebiete der beschreibenden Naturgeschichte, van Mitgliedern der Senckenbergischen Naturforschenden Gesellschaft in Frankfurt, Main Frankfort, 2, 1–28.
  56. Salzburger, W. & Meyer, A. (2004) The species flock of east Africa cichlid fishes: recent advances in molecular phylogenetics and population genetics. Naturwissenschaften, 91, 277–290. https://doi.org/10.1007/s00114-004-0528-6 DOI: https://doi.org/10.1007/s00114-004-0528-6
  57. Scrucca, L., Fop, M., Murphy, T.B. & Raftery, A.E. (2016) mclust 5: clustering, classification and density estimation using Gaussian finite mixture models. The R Journal, 8 (1), 289–317. https://doi.org/10.32614/RJ-2016-021 DOI: https://doi.org/10.32614/RJ-2016-021
  58. Seehausen, O. (2004) Hybridization and adaptive radiation. Trends in Ecology and Evolution, 19, 198–207. https://doi.org/10.1016/j.tree.2004.01.003 DOI: https://doi.org/10.1016/j.tree.2004.01.003
  59. Shaffer, H.B. & Thomson, R.C. (2007) Delimiting Species in Recent Radiations. Systematic Biology, 56, 896–906. https://doi.org/10.1080/10635150701772563 DOI: https://doi.org/10.1080/10635150701772563
  60. Slatkin, M. (1994) Gene Flow and Population Structure. In: Real, L. Eds., Ecological Genetics, Princeton University Press, Princeton, 3–17.
  61. Soltis, P.S. & Soltis, D.E. (2000) The role of genetic and genomic attributes in the success of polyploids. PNAS, 97(13). 7051–7057. https://doi.org/10.1073/pnas.97.13.7051 DOI: https://doi.org/10.1073/pnas.97.13.7051
  62. Süsnik, S., Snoj, A., Wilson, I.F., Mrdak, D. & Weiss, S. (2007). Historical demography of brown trout (Salmo trutta) in the Adriatic drainage including the putative S. letnica endemic to Lake Ohrid. Molecular Phylogenetics and Evolution, 44, 63–76. https://doi.org/10.1016/j.ympev.2006.08.021 DOI: https://doi.org/10.1016/j.ympev.2006.08.021
  63. Vreven, E.J.W.M.N., Musschoot, T., Snoeks, J. & Schliewen, U.K. (2016) The African hexaploid Torini (Cypriniformes: Cyprinidae): review of a tumultuous history. Zoological Journal of Linnean Society, 177, 231–305. https://doi.org/10.1111/zoj.12366 DOI: https://doi.org/10.1111/zoj.12366
  64. Wang, Y.C., Liao, L. & Li, Z.Z. (2018) Genetic differentiation of Actinidia chinensis and analysis of gene flow barriers in the Qinling Mountains, the species’ northern distribution boundary. Genetic Resources and Crop Evolution, 65, 881–895. https://doi.org/10.1007/s10722-017-0578-1 DOI: https://doi.org/10.1007/s10722-017-0578-1
  65. Wang, Z., Hu, G., Li, Z., Zhong, C. & Yao, X. (2022) Characterizing Tetraploid populations of Actinidia chinensis for Kiwifruit genetic improvement. Plants, 11, 1154. https://doi.org/10.3390/plants11091154 DOI: https://doi.org/10.3390/plants11091154
  66. Wright, S. (1978) Evolutiom and the genetics of populations. Variability within and among natural populations (Vol. 4). University of Chicago Press, Chicago, IL, 590 pp.
  67. Zink, R.M. (1997) Phylogeographic studies of North American birds. In: Mindell, D.P. (Ed.), Avian Molecular Evolution and Systematics. Academic Press, San Diego, California, pp. 297–230. https://doi.org/10.1016/B978-012498315-1/50017-0 DOI: https://doi.org/10.1016/B978-012498315-1/50017-0
  68. Zink, R.M. & Barrowclough, G.F. (2008) Mitochondrial DNA under siege in avian phylogeography. Molecular Ecology, 17, 2107–2121. https://doi.org/10.1111/j.1365-294X.2008.03737.x DOI: https://doi.org/10.1111/j.1365-294X.2008.03737.x
  69. Zworykin, D., Budaev, S., Darkov, A., Dzerzhinskii, K., Lyovin, B. & Mina, M. (2006) Assessment of the role of chemoreception in the mate choice in barbs of the Barbus intermedius; complex from Lake Tana, Ethiopia. Journal of Ichthyology, 46, 661–667. https://doi.org/10.1134/S0032945206080133 DOI: https://doi.org/10.1134/S0032945206080133