Japanese Journal of Ichthyology 魚 類 学 雑 誌 Vol. 35, No. 2 1 9 8 8 3 5 巻 2 号 1988 年

Genetic Divergence and Relationship among Fifteen Species of Genera Trachurus, Decapterus, Selar and Selaroides

Akihiro Kijima, Nobuhiko Taniguchi and Akira Ochiai (ReceivedOctober 9, 1987 )

Abstract Geneticdistance and the relationshipsamong 15 speciesof genera Trachurus, Decapterus , Selar, and Selaroideswere estimatedfrom 18 electrophoreticallydetectable isozyme genes. Es - timates of geneticdistance (D) betweenevery pair of specieswithin the genus Trachurusran g e d from 0.005to 0.560with a mean of 0.322,and from 0.484to 1.868with a mean of 1.022with in the genus Decapterus. Betweenspecies of differentgenera, estimates of D ranged from 0.78 6 to 2.863 with a mean of 1.784. From these results, Decapterusspecies could be considereda s havingevolved over a long periodwhile Trachurus is a newlyarisen genus. A relationshipamo n g species suggeststhat the Decapterusspecies are expandedto offshoreand deep area after bein g dividedinto some groups,and that the Trachurusspecies are dividedpresumably into at least tw o groups, one group of which is coastal and the other of which is offshore. Trachurusjaponi c u s and Trachurusnovaezelandiae could be consideredsubspecies on the basis of allelicdistributi o n and geneticdistan c e .

In the previous report (Kijima et al., 1986a) the the present study are to estimate the degree of subfamily Caranginae could be divided into two genetic divergence and to investigate relationships large group on the basis of electrophoretically among species on the basis of electrophoretically detectable isozyme genes, one of which was fusi- detectable isozyme genes. Moreover relationships form including the genera Trachurus, Decapterus, among species are discussed from the view point Selar, and Selaroides and the other was corn- of adaptive radiation as compared with morpho- pressiform. Isozyme genes were very useful for logical studies. analyzing the relationship within a certain taxono- mic level as shown by Kijima et al. (1986a). Materials and methods Because of too many species in many genera survey- ed in the previous paper, the number of loci avail- Table 1 shows fish species, number of fish tested able were limited for making a thorough analysis and their sampling sites. The Trachurus species of the relationship among the species within a except T. japonicus were commercially imported genus. from several countries as food or research The fusiform group was also morphologically samples. They were transported in frozen state. somewhat highly specialized, adapting to long The other species including T. japonicus were migration around offshore water (Suzuki, 1962; collected from the southeast coast of Japan. Vergara, 1972). This is one of the main evolu- Fish samples were immediately frozen and stored tionary trends in the family Carangidae. There below -20•Ž until they were tested. Taxonomy are many species in the genera Trachurus and and identification of species followed Berry and Decapterus of the four genera. Although a lot Cohen (1974), Shavoneyev (1980) and Gushiken of morphological and ecological studies among (1983). species were published (Matsubara, 1955; Suzuki, Eleven enzymes were surveyed in the liver, 1962; Kishida, 1974; Berry and Cohen, 1974; muscle and heart by two buffer-systems as shown Stephenson and Robertson, 1977; Shavoneyev, in Table 2. The procedure for starch gel electro-

1980; Gushiken, 1983), taxonomic relationships phoresis, detection of isozymes, and nomenclature among species have not yet been thoroughly of locus followed the same methods as previously estimated. It would be necessary to analyse reported (Kijima et al., 1986a, b). Since MDH relationships among them by using another marker isozymes cannot be confirmed as soluble or index such as isozyme genes. The objectives of mitochondrial form, they are designated with

•\1 6 7 魚類学雑誌 Japan. J. Ichthyol. 35(2), 19 8 8

numbers. Alleles were numbered consecutively locus, 10 (A-J) at aGpd-A, 11 (A-K) at aGpd-B, as A, B, C,•c. from the most anodal to the most 15 (A-O) at Aat-A, 8 (A-H) at Aat-B, 12 (A-L) at cathodal. Allele frequency was calculated to three Idh-A and Idh-B, 8 (A-H) at Ldh-A, 3 (A-C) at of four decimal points by directly counting pheno- Ldh-B, 7 (A-G) at Mdh-1, 5 (A-E) at Mdh-2, 4 types. Calculation of genetic distance, and con- (A-D) at Mdh-3, 5 (A-E) at Mdh-4, 9 (A-I) at Me-A,

struction of dendrograms also followed previous 11 (A-K) at Pgm, 10 (A-J) at 6Pgd, 17 (A-Q) at

reports (Kijima et al., 1986a, b). Sdh and 2 (A-B) at Sod, considering all species. Allelic divergence was remarkably large at Aat-A and Sdh, and small at Ldh-B and Sod. The Results observed number of phenotypes is consistent with

Fig. 1 shows electropherograms of 11 enzymes that expected at all loci examined.

surveyed in the liver, muscle and heart. The In order to estimate the degree of genetic di-

isozymes detected are summarized in Table 2. vergence quantitatively, the genetic distance be-

Only one zone appeared in ADH, PGM, 6PGD, tween every pair of species in 4 genera was cal-

SDH and SOD in all of the species examined, culated from allele frequencies as shown in Table

indicating one locus coding for each enzyme 4. The minimum genetic distance was observed

(Fig. 1). In aGPD and IDH, different bands between Trachurus japonicus and Trachurus were observed between liver and muscle, indicating novaezelandiae (D=0.005), and the maximum

different isozymes in each tissue. Two or more between Trachurus declivis and Decapterus tabl different zones were observed in the same tissue (D=2.863). The genetic distance among species in AAT, LDH, MDH and ME, indicating that ranged from 0.005 to 0.560 with a mean of 0.322

some isozymes coded by different loci were active within 15 pairs of the genus Trachurus, and from

in the same tissue (Fig. 1). From the results, 0.484 to 1.868 with a mean of 1.022 within 21 pairs

eighteen isozymic loci were estimated from 11 of the genus Decapterus. The genetic distance

enzymes examined as shown in Table 2.

Allele distributions and frequencies at the 18 Table 2. Enzymes surveyed, tissues and buffer-

loci in 15 species belonging to 4 genera are shown systems used, isozymes detected and loci coded. in Table 3. There are 9 alleles (A-I) at the Adh

Table 1. Sampling site and the number of

individuals in each species of the genera

Trachurus, Decapterus, Selar and Selaroides examined.

•\1 6 8 •\ Kijima et al.: Genetic Divergence of Caranginae among species of different genera ranged from of amino acid substitution is considered to be 0.786 to 2.863 with a mean of 1.784 in 69 pairs. large in proportion to evolutionary time. Genetic The genetic distance in the present study generally distance corresponds to the number of allelic increased on higher taxonomic levels. change or the rate of amino acid substitution and A dendrogram revealing the relationships among therefore should increase in proportion to evolu- them was constructed on the basis of the genetic tionary time. Genetic distances between De- distances as shown in Fig. 2. From the dendro- capterus species were distinctively larger than those gram, 15 species were clearly divided into two between Trachurus species. It suggests that the groups at a distance of 2.313, one of which in- genus Decapterus has arisen long over the past cluded all Decapterus species tested and the other while Trachurus is a newly arisen one. In fact, group was divided into two other groups, one of morphological differences among Trachurus spe- which was the genus Trachurus at a distance of cies are so small that some taxonomic controversy 1.555. The remaining group which includes two in species or subspecies levels have not been settled genera, Selar and Selaroides, was divided at a yet (Berry and Cohen, 1974; Shavoneyev, 1980). distance of 0.786 The degree of genetic divergence Genetic relationship among Decapterus species. between species, however, was largely different in Of the Carangidae, Decapterus species are con- each genus. The genus Decapterus was the most sidered as the group which is morphologically and divergent species group, and Trachurus was the ecologically more highly adapted to migrate least. around offshore areas. Morphological adaptability The dendrogram also revealed that the species for offshore areas is characterized by the body of Trachurus could be divided into three groups, shape such as low body depth and by the large namely 1) T. declivis and T. murphyi, 2) T. trach- first dorsal fin. Although the size of the first urus, and 3) T. trecae, T. novaezelandiae and T. dorsal fin compared to the second one is not japonicus at genetic distances of 0.468 and 0.410 obviously different, the body depth of D. macarellus respectively. Also there were four groups in the is the lowest and next to D. russelli, D. macrosoma, genus Decapterus, namely 1) D. russelli and D. D. muroadsi, D. tab!, D. akaadsi and D. maruadsi maruadsi, 2) D. macarellus, D. muroadsi and D. from the data of Gushiken (1983). akaadsi, 3) D. tabl, and 4) D. macrosoma. Kishida (1974) investigated the habitat of five Decapterus species in the East China Sea. Ac- Discussion cording to his conclusion, D. maruadsi has in- habited the coastal water, D. akaadsi and D. tabl Genetic distance and relationships among genera. have inhabited areas of 200m depth or less at the Kijima et al. (1986a) have estimated an average front part of the continental shelf, while D. macro- genetic distance of 0.880 for every pair of species, soma's habitat ranges from coastal water to the 2.046 for every pair of genera in 35 carangid spe- surface of the front part of the continental shelf. cies. They also indicated that these values were D. russelli has not been caught in the Kyushu and considered to be reasonable in comparison with Shikoku area but in Okinawa, mixed with D. the other fish species. Comparing these data macrosoma. Morphological characters are well with those of this study, infinite values of genetic correlated with habitat in each species. Com- distance estimated in the previous report were paring the present data with the data reported by calculated as 1.462 (D. macrosoma and D. macarel- Kishida (1974), deep sea type and offshore type lus), 1.868 (D. macrosoma and D. tabl), and 2.819 are together in the same group. This suggests (D. macrosoma and Selaroides leptolepis), respec- that the Decapterus species have expanded to tively. The values between the other pairs were offshore and deep areas after dividing into some not very different from each other. The relation- species groups. It could be reasonable because ships between genera agreed well with the previous of the general tendency of long term evolution report. The present data thus support the previous of fishes from coastal water to offshore or deep study. sea. Isozymic alleles are changed by occurrence of Genetic relationship among Trachurus species. amino acid substitution and are considered neutral Shavoneyev (1980) proposed that the genus or nearly neutral for natural selection. The rate Trachurus colud be divided into three groups, that

•\1 6 9 •\ 魚類学雑誌 Japan. J. Ichthyol. 35 (2), 1988

•\1 7 0 •\ Kijima et al.: Genetic Divergence of Caranginae

Fig. 1. Examples of electropherogram of 11 enzymes. See the text for nomenclature of allele . TTC, Trachurus trecae; TJP, T. japonicas; TNV, T. novaezelandiae; TDV, T. declivis; TTR, T. trachttrus; TMP, T. murphyi; DRL, Decapterus russelli; DMS, D. macrosoma; DML, D. macarellus; DMU , D. muroadsi; DMA, D. maruadsi; DAK, D. akaadsi; DTB, D. tabl; SCP, Selar crumenophthalmus; SLL, Selaroides leptolepis.

•\1 7 1 •\ 魚類学雑誌 Japan. J. Ichthyol. 35 (2), 1988

•\1 7 2 •\ Kijima et al.: Genetic Divergence of Caranginae

•\1 7 3 •\ 魚類学雑誌 Japan. J. Ichthyol. 35 (2), 1988

Fig. 2. Genetical relationship among 15 species of the genera Trachurus, Decapterus, Selar, and Selaroides. is, "mediterraneus", "trachurus" and "picturatus" and T. japonicus is just in agreement with both on the basis of morphological and ecological reports. These two next appeared to be close to characters. According to his hypothesis, mem- T. trecae of Shavoneyev's "mediterraneus" group bers of the "mediterraneus" group (T. mediter- while T. declivis appeared close to T. murphyi and raneus, T. Trecae, T. lathami and T. indicus) is consistent with Berry and Cohen's (1974) re- characterized by small scutes, high body depth port. These results suggest that the size of the and coastal area habitat are the most primitive. scute is not very clearly correspondent with evolu- The members of the "picturatus" group (T. pic- tionary features and are against the hypothesis of turatus, T. symmetricus and T. murphyi) char- Shavoneyev (1980). In fact, "picturatus" group acterized by low body depth, a large number of is different from the other groups in number of scutes and habitat far beyond the continental rays and scutes and body depth, but the "tra- shelf are the most advanced and phylogenetically churus" and "mediterraneus" groups are different close to members of the "mediterraneus" group, from each other only in the depth of the largest possibly linked by a common origin. The mem- scute according to the data from Shavoneyev bers of the "trachurus" group (T. trachurus, T. (1980). Therefore, there are at least two groups delagoa, T. novaezelandiae and T. japonicus) char- in the Trachurus species and they would be a- acterized by large scutes and by remnants of many daptively radiated offshore such as the "picturatus" primitive characters are an independent trend of species. T. declivis may have been derived from development. He also suggested that T. declivis an ancestor of T. murphyi. As only one individual would be more properly regarded as an aberrant of T. declivis could be tested, a deviation of allele form, the evolution of which has occurred as a frequency cannot be exactly estimated. How- different course from that of all other members of ever, because the probability of the appearance of Trachurus. His hypotheses are different at some a common allele at all loci should be high, a points from the report of Berry and Cohen (1974). relationship between species could be assumed. Berry and Cohen (1974) revealed that T. novae- These suggest that the two species in the south zelandiae and T. japonicus belonging to the Pacific Ocean could be considered to come from "trachurus" group of Shavoneyev (1980) w ere different origins. morphologically similar to T. lathami which be- There is no completely divergent locus between longs to the "mediterraneus" group. They also T. japonicus and T. novaezelandiae, and the genetic revealed that T. declivis appeared to be closer to distance between them is too small to be at the T. murphyi which belongs to the "picturatus" species level (Kijima, et al., 1986b, Taniguchi et group. Comparing these reports with the present al., 1986). Moreover there is no morphologically study, a close relation between T. novaezelandiae significant difference between them (Stephenson

•\1 7 4 •\ Kijima et al. : Genetic Divergence of Caranginae and Robertson, 1977). There are two closely Matsubara, K. 1955. Fish morphology and hierarchy, related subspecies inhabiting different areas south I. Ishizaki Shoten, Tokyo, xi+789 pp (In Japanese.) and north part of the earth, i.e. T. trachurus Shavoneyev, Ye. 1980. Systematics, morpho-ecologi- trachurus and T. trachurus capensis in the Atlantic cal characteristics and origin of carangids of the Ocean and T. symmetricus symmetricus and T. genus Trachurus. J. Ichthyol., 20(6): 15-25. Stephenson, A. B. and D. A. Robertson. 1977. The symmetricus murphyi in the south and north part New Zealand species of Trachurus (Pisces: Carang- of the east side of the Pacific Ocean (Shavoneyev, idae). J. Roy. Soc. New Zealand, 7(2): 243-253. 1980). On the west side of the Atlantic Ocean, Suzuki, K. 1962. Anatomical and taxonomical studies only one species (T. lathami) has inhabited both on the carangid fishes of Japan. Rep. Fac. Fish. parts. These are considered to be newly arisen Pref. Univ. Mie, 4(2): 42-232. and adaptively radiated north and south along the Taniguchi, N., M. Fujita and M. Akasaki. 1986. coast in each area. From these evidences, we Genetic divergence and systematics in sparid fish could conclude that the two species, T. novae- from Japan. Proceedings of the Second Internation- zelandiae and T. japonicus, are subspecies, and al Conference on Indo-Pacific Fishes, p. 849-858. that they adaptively radiated from the Indian Vergara, R. 1972. Analysis taxonomico y con- sideraciones filogeneticas sobre las especies Cubanas Ocean to the Pacific Ocean and then north and del genero Caranx. (Teleostei, Perciformes, Car- south along the coastal area. angidae). Cent. Invest. Pseq. Cuba, Contrib., 34: 1-138. Acknowledgement (Department of Cultural Fisheries, Faculty of Agricul- We wish to thank Mr. F. Nishioka of the Tokai ture, Kochi University, Monobe B-200, Nankoku Regional Fisheries Research Laboratory, Mr. K. 783, Japan; AK, present address: Department of Takeshita of the Seikai Regional Fisheries Re- Fisheries, Faculty of Agriculture, Tohoku University, search Laboratory, Mr. S. Wada of the Fishery Tsutsumi-dori Amemiya-cho, Sendai 980, Japan) Research Institute of Shizuoka Prefecture, and

Mr. S. Gushiken of the Gushiken Ichthyology マ ア ジ 属,ム ロ ア ジ 属,メ ア ジ 属,ホ ソ ヒ ラ ア ジ 属15 Laboratory, for supplying the fish samples. This 種 の 遺 伝 的 分 化 と 類 縁 関 係 work was supported in part by grants-in-aid from 木 島 明 博 ・谷 口 順 彦 ・落 合 明 the Ministry of Education, Science and Culture, ア ジ 亜 科 で 紡 錘 形 の グ ル ー プ と さ れ る マ ァ ジ 属,ム ロ Japan (60760148). ア ジ 属,メ ア ジ 属 お よ び ホ ソ ヒ ラ ア ジ 属 の 合 計4属15 種 間 に お け る 遺 伝 的 分 化 お よ び 類 縁 関 係 を18ア イ ソ ザ Literature cited イ ム 遺 伝 子 を 標 識 と し て 調 べ た.そ の 結 果,遺 伝 的 距 離 は マ ア ジ 属6種 間 で0.005-0.560,平 均0.322,ム ロ Berry, F. H. and L. Cohen. 1974. Synopsis of Trach- ア ジ 属7種 間 で0.484-1.868,平 均1.022で あ っ た. urus (Pisces, Carangidae). Quart. J. Florida Acad. 4属 間 の 遺 伝 的 距 離 は0.786-2.863,平 均1.784と な Sci., 35(4): 177-211. り,分 類 群 が 高 次 に な る に 従 っ て 遺 伝 的 距 離 が 大 き く な Gushiken, S. 1983. Revision of the carangid fishes っ た.遺 伝 的 距 離 を も と に 作 成 し た 枝 分 れ 図 は 各 属 が そ of Japan. Galaxea, 2: 135-264. れ ぞ れ1つ の グ ル ー プ を 形 成 す る こ と を 示 し,形 態 に よ Kijima, A., N. Taniguchi and A. Ochiai. 1986a. る 分 類 を よ く 反 映 し た.こ れ ら の こ と か ら,ム ロ ア ジ 属 Genetic relationships in the family Carangidae. は よ り古 い 年 代 に 分 化 し,マ ア ジ 属 は よ り新 し い 年 代 に Proceedings of the Second International Conference 分 化 し た と 推 定 さ れ た.ま た マ ア ジ 属 は 沿 岸 性 と沖 合 性 on Indo-Pacific Fishes, p.840-848. の 少 な く と も2つ の グ ル ー プ に 大 別 さ れ た.日 本 の マ ア Kijima, A., N. Taniguchi and A. Ochiai. 1986b. ジ と ニ ュ ー ジ ー ラ ン ドの マ ア ジ は 最 も 新 し い 年 代 に 適 応 Genetic divergence and morphological difference 放 散 に よ っ て 西 方 よ り沿 岸 づ た い に 東 進 し,太 平 洋 で 南 between the spotted and common mackerel. Japan. 北 に 分 化 し て で き た 種 と考 え ら れ,こ れ ら は 亜 種 レ ベ ル J. Ichthyol., 33(2): 151-161. に あ る と推 定 され た. Kishida, S. 1974. Fisheries biology of the scads (genus Decapterus)in the East China Sea-II. Specific (783南 国 市 物 部 乙200高 知 大 学 農 学 部;木 島,現 所 属: distributoin and annual catch. Bull. Seikai Reg. 980仙 台 市 堤 通 雨 宮 町1-1東 北 大 学 農 学 部) Fish. Res. Lab., 45: 1-14. (In Japanese.)

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