Reticulate evolution: Ancient introgression of the Adriatic brown trout mtDNA in softmouth trout Salmo obtusirostris (Teleostei: Salmonidae)

Biological Journal of the Linnean Society

Volumn 90, Issue 1, 2007, Pages 139-152

  Susnik S ^a   Weiss, S ^a   Odak, T ^b   Delling, B ^c   Treer, T ^b   Snoj, A ^d  

^a Inst Zool an Karl Franzens Univ   (Austria)

^b UNIVERSITY OF ZAGREB   (Croatia)

^c SWEDISH MUSEUM OF NATURAL HISTORY   (Sweden)

^d UNIVERSITY OF LJUBLJANA   (Slovenia)

Author keywords

Adriatic basin; Introgressive hybridization; Microsatellites; mtDNA capture

Indexed keywords

DIVERGENCE; GENETIC MARKER; INTROGRESSION; MITOCHONDRIAL DNA; MORPHOLOGY; SALMONID;

ADRIATIC COAST [CROATIA]; BOSNIA AND HERZEGOVINA; CROATIA; EURASIA; EUROPE; JADRO RIVER; NERETVA RIVER; SOUTHERN EUROPE;

SALMO OBTUSIROSTRIS; SALMO TRUTTA; SALMONIDAE; TELEOSTEI;

EID: 33846173918     PISSN: 00244066     EISSN: 10958312     Source Type: Journal    
DOI: 10.1111/j.1095-8312.2007.00717.x     Document Type: Article

References (67)

1. Allendorf FW, Leary RF, Spruell P, Wenburg JK. 2001. The problems with hybrids: setting conservation guidelines. Trends in Ecology and Evolution 16: 613-622.
2. Arnold ML. 1992. Natural hybridization as an evolutionary process. Annual Review of Ecology and Systematics 23: 237-261.
3. Baxter JS, Taylor EB, Devlin RH, Hagen J, McPhail JD. 1996. Evidence for natural hybridization between Dolly Varden (Salvelinus malma) and bull trout (Salvelinus confluentus) in a northcentral British Columbia watershed. Canadian Journal of Fisheries and Aquatic Sciences 54: 421-429.
4. Behnke RJ. 1965. A systematic study of the family Salmonidae with special reference to the genus Salmo. PhD Thesis, University of California.
5. Belkhir K, Borsa P, Chikhi L, Raufaste N, Bonhomme F. 1996-2004. GENETIX 4.04, logiciel sous Windows TM pour la genetique des populations. Montpellier: Laboratoire Genome, Populations, Interactions, Universite de Montpellier.
6. Bernatchez L. 2001. The evolutionary history of brown trout (Salmo trutta L.) inferred from phylogeographic, nestedclade, and mismatch analyses of mitochondrial DNA variation. Evolution 55: 351-379.
7. Bernatchez L, Danzmann RG. 1993. Congruence in control-region sequence and restriction-site variation in mitochondrial DNA of brook charr (Salvelinus fontinalis Mitchill). Molecular Biology and Evolution 10: 1002-1014.
8. Bernatchez L, Glemet H, Wilson CC, Danzmann RG. 1995. Introgression and fixation of Arctic char (Salvelinus alpinus) mitochondrial genome in an allopatric population of brook trout (Salvelinus fontinalis). Canadian Journal of Fisheries and Aquatic Sciences 52: 179-185.
9. Bowcock AM, Ruiz-Linares A, Tomfohrde J, Minch E, Kidd JR, Cavalli-Sforza LL. 1994. High resolution of human evolutionary trees with polymorphic microsatellites. Nature 31: 455-457.
10. Clement M, Posada D, Crandall KA. 2000. TCS: a computer program to estimate gene genealogies. Molecular Ecology 9: 1657-1659.
11. Conservation International. 2004. WWW document. Available at http://www.conservation.org/xp/CIWEB/home.
12. Cronin MA, Spearman WJ, Wilmot RL. 1993. Mitochondrial variation in Chinook (Oncorhynchus tsawytscha) and Chum salmon (O. keta) detected by restriction enzyme analysis of Polymerase Chain Reaction (PCR) products. Canadian Journal of Fisheries and Aquatic Sciences 50: 708-715.
13. Delling B. 2002. Morphological distinction of the marble trout, Salmo marmoratus, in comparison to marbled Salmo trutta from River Otra, Norway. Cybium 26: 283-300.
14. DeMarais BD, Dowling TE, Douglas ME, Minckley WL, Marsh PC. 1992. Origin of Gila seminuda (Teleostei: Cyprinidae) through introgressive hybridization: implications for evolution and conservation. Proceedings of the National Academy of Sciences of the United States of America 89: 2747-2751.
15. Dorofeyeva EA. 1999. Salmons and trouts of Eurasia: morphology, classification and relationships. Dissertation Thesis, St Petersburg State Universit.
16. Dowling TE, DeMarais BD. 1993. Evolutionary significance of introgressive hybridization in cyprinid fishes. Nature 362: 444-446.
17. Dowling TE, Secor C. 1997. The role of hybridization and introgression in the diversification of animals. Annual Review of Ecology and Systematics 28: 593-619.
18. Garcia-Paris M, Alcobendas M, Buclkey D, Wake DB. 2003. Dispersal of viviparity across contact zones in Iberian populations of fire salamanders (Salamandra) inferred from discordance of genetic and morphological traits. Evolution 57: 129-143.
19. Gephard S, Moran P, Garcia-Vazquez E. 2000. Evidence of successful natural reproduction between brown trout and mature male Atlantic salmon parr. Transactions of American Fisheries Society 129: 301-306.
20. Gomez A, Lunt DH. 2006. Current perspectives in phylogeography and the significance of South European refugia in the creation and maintenance of European biodiversity. In: Weiss S, Ferrand N, eds. Phylogeography of Southern European Refugia. Dordrecht: Kluwer Academic Publishers, 155-188.
21. Goudet J. 2001. FSTAT, version 2.9.3: a program to estimate and test gene diversities and fixation indices. Available at http://www.unil.ch/izea/softwares/fstat.html.
22. Hadžišče S. 1961. Zur Kenntnis des Salmothymus ohridanus (Steindachner) (Pisces, Salmonidae). Internationale Vereinigung für Theoretische und Angewandte Limnologie Verhandlungen 14: 785-791.
23. Heckel JJ. 1851. Bericht einer ichtyologischen Reise. II. Beiträge zu den Gattungen Salmo, Fario, Salar, Coregonus, Chondrostoma und Telestes. Wien: Sitzungsbarrichte der Akademie der Wissenschoften, 347-390.
24. Hubbs CL. 1955. Hybridization between fish species in nature. Systematic Zoology 4: 1-20.
25. Jansson H, Holmgren I, Wedin K, Andersson T. 1991. High frequency of natural hybrids between Atlantic salmon (Salmo salar L.) and brown trout (S. trutta) in a Swedish River. Journal of Fish Biology 39 (Suppl. A): 343-348.
26. Karaman S. 1927. Les salmonidés des Balkans. Bulletein de la Societé Scientifique de Skoplje 2: 253-268.
27. Kosorić Crossed D sign, Vuković T. 1969. Research of possibilities of hybridisation of Salmonidae species of the Neretva River confluence. Ichthyologia 1: 57-67.
28. Kottelat M. 1997. European freshwater fishes; An heuristic checklist of the freshwater fishes of Europe (exclusive of former USSR), with an introduction for non-systematists and comments on nomenclature and conservation. Biologia 52 (Suppl. 5): 1-271.
29. Kryštufek B, Reed JM. 2004. Pattern and process in Balkan biodiversity - an overview. In: Griffiths HI, Kryštufek B, Reed JM, eds. Balkan biodiversity pattern and process in the European hotspot. Dordrecht: Kluwer Academic Publishers, 203-217.
30. Lamb T, Avise JC. 1986. Directional introgression of mitochondrial DNA in a hybrid population of tree frogs: the influence of mating behavior. Proceedings of the National Academy of Sciences of the United States of America 83: 2526-2530.
31. Langella O. 2002. Populations, 1.2.28 (12/5/2002). Copyright 1999, Olivier Langella. Gif-sur-Yvette: CNRS UPR9034.
32. Ludwig A, Congiu L, Pitra C, Fickel J, Gessner J. Fontana F, Patarnello T, Zane L. 2003. Nonconcordant evolutionary history of maternal and paternal lineages in Adriatic sturgeon. Molecular Ecology 12: 3253-3264.
33. Marić D. 1995. Endemic fish species of Montenegro. Biological Conservation 72: 187-194.
34. McMeel OM, Hoey EM, Ferguson A. 2001. Partial nucleotide sequences, and routine typing by polymerase chain reaction-restriction fragment length polymorphism, of the brown trout (Salmo trutta) lactate dehydrogenase, LDH-C1* 90 and *100 alleles. Molecular Ecology 10: 29-34.
35. Mrakovčić M, Mišetić S. 1990. Status, distribution and conservation of the salmonid, Salmothymus obtusirostris (Heckel) and cyprinid, Aulopyge hugely (Heckel) in Yugoslavia. Journal of Fish Biology 37 (Suppl.): 241-242.
36. O'Reilly PT, Hamilton LC, McConnell SK, Wright JM. 1996. Rapid analysis of genetic variation in Atlantic salmon (Salmo salar) by PCR multiplexing of dinucleotide and tetranucleotide microsatellites. Canadian Journal of Fisheries and Aquatic Sciences 53: 2292-2298.
37. Ostberg CO, Slatton SL, Rodriguez RJ. 2004. Spatial partitioning and asymmetric hybridization among sympatric coastal steelhead trout (Oncorhynchus mykiss irideus), coastal cutthroat trout (O. clarki clarki) and interspecific hybrids. Molecular Ecology 13: 2773-2788.
38. Phillips RP, Matsuoka MP, Konon I, Reed KM. 2000. Phylogenetic analysis of mitochondrial and nuclear sequences supports inclusion of Acantholingua ohridana in the genus Salmo. Copeia 2: 546-550.
39. Poteaux C, Bonhomme F, Berrebi P. 1999. Microsatellite polymorphism and genetic impact of restocking in Mediterranean brown trout (Salmo trutta L.). Heredity 82: 645-653.
40. Presa P, Guyomard R. 1996. Conservation of microsatellites in three species of salmonids. Journal of Fish Biology 49: 1326-1329.
41. Redenbach Z, Taylor EB. 2002. Evidence for historical introgression along a contact zone between two species of char (Pisces: Salmonidae) in northwestern North America. Evolution 56: 1021-1035.
42. Rice WR. 1989. Analysing tables of statistical tests. Evolution 43: 223-225.
43. Rieseberg LH. 1997. Hybrid origins of plant species. Annual Review of Ecology and Systematics 28: 359-389.
44. Roca AL, Georgiodis N, O'Brien SJ. 2005. Cytonuclear genomic dissociation in African elephant species. Nature Genetics 37: 96-100.
45. Ruedi M, Smith MF, Patton JL. 1997. Phylogenetic evidence of mitochondrial introgression among pocket gophers in New Mexico (family Geomyidae). Molecular Ecology 6: 453-462.
46. Salzburger W, Baric S, Sturmbauer C. 2002. Speciation via introgressive hybridization in east African cichlids? Molecular Ecology 11: 619-625.
47. Sanford CPJ. 2000. Salmonid fish osteology and phylogeny (Teleostei: Salmonidei). Theses Zoologicae 33: 1-264.
48. Scribner KT, Gust JR, Fields RL. 1996. Isolation and characterization of novel microsatellite loci: cross-species amplification and population genetic applications. Canadian Journal of Fisheries and Aquatic Sciences 53: 833-841.
49. Scribner KT, Page KS, Bartron ML. 2001. Hybridization in freshwater fishes: a review of case studies and cytonuclear methods of biological inference. Reviews in Fish Biology and Fisheries 10: 293-323.
50. Seehausen O. 2004. Hybridization and adaptive radiation. Trends in Ecology and Evolution 19: 198-207.
51. Seehausen O, Alphen JJ, Witte F. 1997. Cichlid fish diversity threatened by eutrophication that curbs sexual selection. Science 277: 1808-1811.
52. Slettan A, Olsaker I, Lie O. 1996. Polymorphic Atlantic salmon, Salmo salar L., microsatellites at the SSOSL438, SSOSL439 and SSOSL444 loci. Animal Genetics 27: 57-58.
53. Smith PF, Konings A, Kornfield I. 2003. Hybrid origin of a cichlid population in Lake Malawi: implications for genetic variation and species diversity. Molecular Ecology 12: 2497-2504.
54. Snoj A, Jug T, Melkic E, Sušnik S, Jesentek D, Budihna N, Pohar J, Dovć P. 2000. Mitochondrial and microsatellite DNA analysis of marble trout in Slovenia. Journal of Freshwater Biology (Quaderni ETP) 29: 5-11.
55. Snoj A, Melkiè E, Sušnik S, Muhamedagiæ S, Dovè P. 2002. DNA phylogeny supports revised classification of Salmothymus obtusirostris. Biological Journal of the Linnean Society 77: 399-411.
56. Snoj A, Pohar J, Dovc P. 1997. The first microsatellite DNA marker BFRO001 for Marble trout. Journal of Animal Science 75: 1983.
57. Stearley RF, Smith GR. 1993. Phylogeny of the pacific trouts and salmons (Oncorhynchus) and genera of the family Salmonidae. Transections of the American Fisheries Society 122: 1-33.
58. Steindachner F. 1882. Ichthyologische Beiträge (XII). Wien: Sitzungsber Akademie Wiss, 61-82.
59. Sušnik S, Schöffman J, Snoj A. 2004. Phylogenetic position of Salmo (Platysalmo) platycephalus Behnke 1968 from South-Central Turkey, evidenced by genetic data. Journal of Fish Biology 64: 947-960.
60. Sušnik S, Snoj A, Pohar J, Dovc P. 1997. The microsatellite marker (BFRO 002) characteristic for different geographically remote brown trout, Salmo trutta L., populations. Animal Genetics 28: 372.
61. Svetovidov A. 1975. Comparative osteological study of the Balkan endemic genus Salmothymus in relation to its classification. Zoologicheskii Zhurn 54: 1174-1190.
62. Templeton AR. 2004. Using haplotype trees for phylogeographic and species inference in fish populations. Environmental Biology of Fishes 69: 7-20.
63. Templeton AR, Crandall KA, Sing CF. 1992. A cladistic analysis of phenotypic associations with haplotypes inferred from restriction endonuclease mapping and DNA sequence data. III. Cladogram estimation. Genetics 132: 619-633.
64. Thompson JD, Higgins DG, Gibson TJ. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22: 4637-4680.
65. Vuković T. 1982. Prirodni hibridi u otvorenim vodama. In: Habekovic D, ed. Slatkovodno ribarstvo. Zagreb: Jugoslovenska Medicinska Naklada, 166-168.
66. Weckstein JD, Zink RM, Blackwell-Rago C, Nelson DA. 2001. Anomalous variation in mitochondrial genomes of white-crowned (Zonotrichia leucophrys) and golden-crowned (Z. atricapilla) sparrows: pseudogenes, hybridization, or incomplete lineage sorting? Auk 118: 231-236.
67. Young WP, Ostberg CO, Keim P, Thorgaard GH. 2001. Genetic characterization of hybridization and introgression between anadromous rainbow trout (Oncorhynchus mykiss irideus) and coastal cutthroat trout (O. clarki clarki). Molecular Ecology 10: 921-930.