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Homologous Series by Chromosome Number and the Genome Rearrangements in the Phylogeny of Salmonoidei Yu

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Homologous Series by Chromosome Number and the Genome Rearrangements in the Phylogeny of Salmonoidei Yu Russian Journal of Genetics, Vol. 38, No. 10, 2002, pp. 1115–1120. Translated from Genetika, Vol. 38, No. 10, 2002, pp. 1317–1323. Original Russian Text Copyright © 2002 by Zelinsky, Makhrov. THEORETICAL PAPERS AND REVIEWS Homologous Series by Chromosome Number and the Genome Rearrangements in the Phylogeny of Salmonoidei Yu. P. Zelinsky1 and A. A. Makhrov2 1 Department of Zoology, Tolstoy Tula State Pedagogical University, Tula, 300026 Russia 2 Vavilov Institute of General Genetics, Russian Academy of Sciences, Moscow, 119991 Russia; e-mail: [email protected] Received February 19, 2002 Abstract—Published data on chromosome numbers of Salmonoidei are summarized. The existence of homol- ogous variation of chromosome number in different phyletic lines of this suborder is substantiated. It is sug- gested that the origin of homologous series is related to major genome rearrangements (simultaneous fusion of several chromosomes). STRUCTURE AND ORIGIN mon ancestor of Salmonoidei had 112 chromosomes OF THE GROUP and 144 to 156 chromosome arms [13]. The reports karyological diversity in animals [1], in particular, in vertebrates [2] including fish [3], are cur- KARYOTYPES rently available. The ample evidence accumulated in lit- OF THE EXTANT SALMONOIDEI erature provides the possibility to elucidate the regulari- ties of karyotype evolution in individual fish taxa. In this To date, karyotypes have been studied in several work, we summarized the published data on the karyo- dozens of Salmonoidei species (Fig. 1). As it is impos- types of the members of the suborder Salmonoidei. sible to provide all references to original works within According to the classification [4] that we follow in the limits of this review, we used the data from pub- this work, this suborder includes the families Salmo- lished reviews [3, 13, 16–18, 28–30]. nidae, Coregonidae, and Thymallidae. Salmonoidei are In representatives of the family Thymallidae, karyo- distinguished from other representatives of the order types are closest to the ancestral karyotype. They have Salmoniformes by a number of traits (see [5] for about 100 chromosomes and a considerable number of review). However, the most important specific feature chromosome arms. During the evolution of Salmonidae of Salmonoidei is their polyploid origin. and Coregonidae, chromosome number significantly Svardson [6] proposed that the species that are cur- decreased by chromosome fusion [14]. Salmonidae and rently included in the order Salmoniformes constitute a Coregonidae are characterized by karyotypes with a polyploid series with the basic chromosome number diploid chromosome number near 80 or 60 (Fig. 1). of 10. He distinguished groups with a diploid chromo- Thus, current data confirm the existence of the groups some number of 58 to 60 (hexaploids), 80 to 84 (octap- revealed by Svardson (Fig. 2). In particular, these loids), and 102 (decaploids). Later, it was revealed that groups are distinguished in a recent review [17]. the Atlantic salmon Salmo salar and the brown trout The karyotypes with a chromosome number about S. trutta, which are far apart by chromosome number, 80 have independently originated in Coregonidae and are similar by DNA content in the cells [7]. The distinc- Salmonidae. Evidently, these karyotypes have also tion between these species by chromosome number is independently appeared in phyletic lines of taimen related to chromosome fusion or partition rather than (Hucho) and other Salmonidae. Both taimen and lenok polyploidy [8]. (Brachymystax) species, which are distinguished by a Shortly afterwards, several authors [9–11] supposed relatively great chromosome number, have a group of that all species of Salmonidae, Coregonidae, and Thy- four pairs of small metacentric chromosomes, which is mallidae have a tetraploid origin. This viewpoint was absent in other Salmonidae [14]. confirmed by further studies. It was revealed that The forms with the karyotypes including about 60 genome duplication had occurred before the separation chromosomes have independently originated in at least of three groups; that is, they had a common tetraploid six (!) different phyletic lines of Salmonidae and Core- ancestor (see [12] for review). The analysis of karyo- gonidae. These are species of the genera Oncorhynchus types of related diploid species suggested that the com- and Parasalmo, the Sakhalin taimen Parahucho perryi, 1022-7954/02/3810-1115 $27.00 © 2002 MAIK “Nauka /Interperiodica” 1116 ZELINSKY, MAKHROV (a) 2n 100 90 80 70 60 50 SALMONIDAE . NF Reference Brachymystax . B. lenok . ** . 102Ð124 [3, 14Ð16] Hucho . H. hucho . *. 106Ð114 [3, 17] H. taimen . ***. 112 [13] Oncorhynchus . O. gorbuscha . *** 100Ð104 [3, 13, 17] O. keta . * . 94Ð102 [3, 17Ð19] O. kisutch . *****. 100Ð112 [3, 13, 17Ð21] O. masou . * . 100Ð104 [3, 17, 22] O. nerka . *** 100Ð104 [3, 17] O. tschawytscha . * . 100Ð104 [3, 17, 18, 23] Parahucho . P. perryi . *. 100 [3, 17] Parasalmo . P. apache . * 106 [17] P. aquabonita . .***** 104 [13, 17] P. chrysogaster . .* 102Ð104 [17, 30] P. clarki . ***** . 104 [13, 30] P. gilae . * 106 [30] P. mykiss . ********. 104Ð108 [17, 19, 24Ð31] P. sp. * . 104 [30] Salmo . S. carpio . * . 98 [31] S. ischchan . *** . 96Ð100 [31] S. letnika . * . 104 [31] S. marmoratus . * . 108 [31] S. salar . 72Ð74 [31, 32] S. trutta . ****.*** * . 92Ð104 [31, 33Ð35] Salmothymus . S. obtusirostris . *. 94 [3, 17] Salvelinus . S. albus . .***** . 98Ð100 [13, 17, 36] S. alpinus . *. **** . 96Ð100 [3, 6, 13, 17, 37Ð39] S. boganidae . *** . 98 [13] S. confluentus . * . 100 [17] S. elgyticus . *** . 98 [13] S. fontinalis . *** . 100 [3, 13, 17] S. kronocius . ****.* . 100 [13] S. lepechini . .* . 100 [40] S. leucomaenis . *** . 100 [3, 13, 17] S. levanidovi . .*** . 98 [17] S. malma . **** . *** . 98Ð100 [3, 17, 36] S. namaycush . * . 100 [17] S. pluvius . *** . 100 [17] S. schmidti . ***** . 98 [13] S. taranetzi . *** . 98 [13] S. sp. *. 98 [17] Salvethymus . S. svetovidovi . * 98 [13] 2n 100 90 80 70 60 50 Fig. 1. Chromosome number (2n) and the number of chromosome arms (NF) in different Salmonoidei species: (a) family Salmo- nidae; (b) families Coregonidae and Thymallidae. RUSSIAN JOURNAL OF GENETICS Vol. 38 No. 10 2002 HOMOLOGOUS SERIES BY CHROMOSOME NUMBER 1117 (b) 2n 100 90 80 70 60 50 ëOREGONIDAE . NF Reference Coregonus . C. albula . ****** . 96Ð97 [6, 13, 17] C. anaulorum . *** . 98 [13] C. artedii . *** . 94Ð106 [13, 17] C. autumnalis . **** . 96Ð104 [13, 16, 17] C. chadary . ***** . 98Ð100 [16, 17] C. clupeaformis . * . *** 94 [17] C. hoyi . * . 94 [17] C. lavaretus . ********* . 94Ð104 [3, 13, 16, 41Ð48] C. muksun . ***** . 100 [13, 17] C. nasus . .*** 92Ð98 [13, 17] C. nigripinnis . * . 94 [17] C. peled . * ******* . 92Ð96 [13, 16, 17] C. tugun . *** . 106 [16] C. reighardi . * . 100 [17] C. sardinella . ** . 96Ð100 [13, 17] C. schinzii . * . [3] C. ussuriensis . *** . 100 [13, 17] C. wartmanni . * . [3] C. zenithicus . * . 94Ð98 [3, 17] Prosopium . P. abyssicola . * . 100 [17] P. coulteri . ** . 100Ð102 [13, 17] P. cylindraceum . * . 96Ð100 [13, 17] P. gemmiferum . * . 100 [17] P. spilonotus . * . 100 [17] P. williamsoni . * . 100 [17] Stenodus . S. leucichthys . 92Ð108 [13, 16, 17] . *** . THYMALLIDAE . Thymallus . T. arcticus ***** . 146Ð168 [3, 16, 17] T. brevirostris *** . 150 [16] T. grubei *** . 148Ð150 [16, 17] T. thymallus **** * * . 150Ð170 [3, 16, 17, 42, 49] 2n 100 90 80 70 60 50 Fig. 1. (Contd.) the Atlantic salmon, the longfinned char Salvethymus tion of karyotypes. White [1] justified the principle of svetovidovi, the broad whitefish Coregonus nasus, the homologous change, though he renamed this concep- Bonneville cisco Prosopium gemmiferum. tion later. Bulatova [51] described “karyological chains that are basically homologous.” Bogdanov [52] described the series of homologous variation by spe- DIVERSITY OF CHROMOSOME NUMBER cific features of meiosis. AS MANIFESTATION OF THE LAW OF HOMOLOGOUS SERIES Several authors reported parallelism of chromo- The series of forms of Salmonoidei with a chromo- somal rearrangements in different taxa of Salmonoidei. some number close to 80 and 60 can be considered a The trend toward decreasing chromosome number, particular case of homologous series described by which is exhibited in the evolution of Salmonidae and Vavilov [50]. As we know, homologous series by chro- Coregonidae, is related to genome diploidization in mosome number have not so far been detected. How- these families, which are tetraploid by origin (see [17] ever, similar concepts were used to describe the evolu- for review). RUSSIAN JOURNAL OF GENETICS Vol. 38 No. 10 2002 1118 ZELINSKY, MAKHROV Salmonidae and Coregonidae may have undergone such a rearrangement with the possible exception of the tungen (Coregonus tugun) and lenok species, whose distinction from Thymallidae is not very marked. Earlier, we scrutinized the possible mechanisms for the formation of karyotypes with a chromosome num- ber near 60 exemplified by the Atlantic salmon and salmon species belonging to the genus Parasalmo [31]. Note that the species with such karyotypes are charac- terized by a higher chromosomal variability than related species with a chromosome number near 80. Apparently, this is related to the fact that karyotypes with a chromosome number near 60 formed relatively recently and the “balancing” of their chromosome set has not yet been completed. For example, the embryos of the broad whitefish C. nasus, compared to other Coregonidae, are charac- terized by a very high frequency of such chromosomal 2n 100 90 80 70 60
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