114. Sex Reversal in the Japanese W rasse, By Yo K. OKADA, M.J.A. (Comm. Oct. 12, 1962)

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1 e 508 [Vol. 38, 114. Sex Reversal in the Japanese W rasse, Halichoeres poecilopterus By Yo K. OKADA, M.J.A. (Comm. Oct. 12, 1962) The Labridae are a group of fish mostly assuming beautiful colouration or colour patterns which vary considerably not only among different species but according to the sex in the same species. Not infrequently, the sexual difference is so marked that the two sexes of the same fish are regarded as different species. Halichoeres poecilopterus is one of such examples. The green coloured Aobera and the red coloured Akabera were once regarded as different species, the former being referred to Julis poecilopterus and the latter Julis pyrrhogramma, but it is now well established that the two are only sexual colour varieties of the same fish, Halichoeres poecilopterus. The so-called Aobera or blue wrasse is comparatively large. Those found in Tokyo Bay usually measure 160 to 215 mm in body length, smaller ones being rarely encountered. The body is coloured dark green on the back and paler below with a large blackish brown spot behind the pectoral fin. Moreover, there is a dark brown longitudinal band on both sides of the body, accompanied by two or three rows of brownish spots above and three or four rows of yellowish spots below. The width of the band increases with the length of the body. However, the band becomes lighter in colour as the fish increases in length, so that the band of larger fishes is less distinct than that of smaller ones. Furthermore, in smaller and accordingly younger fishes, a similar dark brown band is also found on the head, but in larger fishes the band is replaced by elongated spots and longitudinal light blue bars with dark brown margin, one extending between the tip of the snout and the eye, others distributing on the cheek and the side of the head. Another characteristic of the Aobera is that the caudal fin exhibits five or six wavy stripes of reddish brown colour. The red wrasse or Akabera, on the other hand, is tinted red all over the body as the name indicates. It differs from Aobera not only in colour and colour patterns, but also in size. They seldom exceed 150 mm, and lack the black spots on the breast which are characteristic of the blue wrasse. A longitudinal band running along the side of the body as that seen in the blue wrasse is narrow but dark in colour and distinct, the tone being the same throughout the whole length to the tip of the snout. Three rows of brownish spots

2 No. 8] Sex Reversal in the Japanese Wrasse, Halichoeres poecilopterus 509 above the band and the four rows of yellowish spots below are also distinct but the reddish wavy stripes on the caudal fin are less developed as compared with those of the blue wrasse. Bluish horizontal lines and spots under the eyes are indistinct in their outline. As early as 1902, Jordan and Snyder pointed out that the characteristics of these two kinds of Japanese wrasse are merely the differences between the two sexes of the same species. Kinoshita verified this view by his experiments carried out in He observed that the blue wrasses rapidly lose their sexual characteristics after castration, while the red wrasses are not affected by extirpation of the sexual glands at any developmental stage. However, if a testis is transplanted to the red wrasses, they transform after several months into blue wrasses (1938). Transplantation of an ovary to the blue wrasses causes no changes in colouration in the recepients (1939). It is evident from these experiments that the blue and red wrasses are males and females of the same species, respectively. However, there are some problems to be solved. Are both sexes separate from the time of hatching, colour and colour patterns peculiar to the male sex becoming developed at a certain stage of growth? So far as my observation is concerned, the so-called Akabera (red wrasse) from different parts of Japan have always been females with the ovary, no matter whether they are mature or immature. The question arises, therefore, as to whether the species passes the young stage as the female and later reverses into the male. There is an interesting passage in the article by Kinoshita in "Shokubutsu oyobi Dobutsu" (Botany and Zoology) Vol. IV, No. 6, He states, "The external appearance of a wrasse, 156 mm in length, taken out from an aquarium in the state of hibernation showed characteristics intermediate between the male and female. The sexual gland of the fish was apparently a normal testis to the naked eye, but when studied in sections, there were innumerable egg-like cells distributed over the whole tissue" (l.c., fig. 4). According to Kinoshita, this specimen failed to display the male sex characters and he attributed the failure to the antagonizing effect exerted by the egg-like cells on the action of the testicular hormone. In the same article, Kinoshita further states that he observed a structural change in the sexual gland of a young fish which suggests a transformation of the female elements into the male. These observations and discussions are, of course, far from satisfactory, since they were based upon only one specimen out of twentyseven, and the mentioned egg-like cells were regarded as the testis-ova.

3 510 YO K. OKADA [Vol. 38, I carried out experiments in this wrasse on the formation of spermatozoaa in the female gonad following administration of androgenic hormone. I inserted a small amount of crystalline methyltestosterone under the scales of some twenty red wrasses of various developmental stages, ranging from young fishes measuring about 100 mm to mature ones about 140 mm in length. The experiments were not successful in inducing sperm formation, but caused a change in the secondary sex characters in all the fish; the red wrasses invariably transformed into the blue wrasses. Fig. 1 shows three representatives; a Fig. 1. Three representatives of changed colour patterns in red morasses of different developmental stage after insertion of crystalline methyltestosterone under scales. All in same proportion. young (upper), an adult (lower), and a mediumsized specimen (middle). The photographs were taken one month after the treatment which was carried out on October 3, In each case the dark brownish spot characteristic of the blue wrasse is distinctly observed just behind the pectoral fin. The stripes on the head and the wavy lines on the caudal fin are also clearly seen, but the longitudinal band on the body side is still narrow and dark in colour, and extends anteriorly to the tip of the snout. Another characteristic worthy of note was that mature specimens reacted faster than younger ones in the course of the experiment. Recently I obtained the following results after making an examination of the relationship between the length of the body (degree of growth) and the sex ratio in materials from both the Seto Inland Sea and Tokyo Bay. The body lengths of 26 specimens from the Seto Inland Sea varied from 111 to 167 mm and those measuring over 140 mm were males or regarded as males. Therefore, the sex ratio was 16 ~ :10g. The fishes from Tokyo Bay were generally larger than those from the Seto Inland Sea, ranging from 112 to 215 mm in length. Among them, those measuring from 140 to 150 mm were females, smaller ones being young fish, and those above

4 No. 8] Sex Reversal in the Japanese Wrasse, Halichoeres poecilopterus mm males. Among those measuring from 160 to 170 mm there were a considerable number of fishes which were apparently sexually intermediate. Thus the sex ratio of those from Tokyo Bay, except for 7 young fishes, was 17 : 9 : 24g. Fig. 2 shows two cases of the intermediate type. In the case a (upper in the figure) the scales forming the black spot on the breast are slightly developed, and the irregular stripes on the head have become faintly visible. In the case b (lower) the dark brownish longitudinal band extending caudally from the pectoral fin is of a considerable width, and the irregular stripes on the cheek are also conspicuous, Fig. 2. colour Two patterns examples between of fish red having and blue intermediate wrasseṣ but the dark brownish band still remains along the head. The black spots on the breast are not yet fully developed. The process of natural transformation from the red wrasses into the blue wrasses as represented by these two specimens seems to be slightly different from that caused by insertion of crystalline methyltestosterone. In the former case it seems likely that the longitudinal band on the body side becomes wider and paler in colour prior to the formation of the black spot on the breast. The gonad of these intermediate fishes was next examined in sections. The results are shown for the briefness'sake by accompanying figures. The first and the last figures of the plate are a mature ovary and a testis filled with spermatozoa, respectively, which are presented here for comparison. The wrasses lay eggs in June or July in southern Japan, and from August to October in Tokyo Bay. After that, the ovary diminishes in size to one-third of the original. The second figure of the plate shows an ovary just after spawning, each of the ovarian lobes being filled with young o cytes. In this state the wrasse is supposed to enter the hibernation. One may conjecture that the egg cells remain undeveloped until the next spring. However, as the third figure of the plate indicates, an infiltration of a considerable amount of white blood corpuscles (phagocytes) into the connective tissue has occurred in each of the ovarian lobes at a little later stage where the ovary has undergone regres-

5 512 YO K. OKADA [Vol. 38, Explanation of Plate 1. Matured ovary with fully grown egg cells. 2. Spent ovary immediate after ovulation. 3. Ovarian lobes at the beginning of transformation of sexual elements. 4. The same in advanced stage. 5. Ovary transformed into testis, no longer showing remains of female elements. 6. Testis filled with spermatozoa. Magnification: 3 and 4 x 120, others x 30. Abbreviation : By, blood vessel; Oc, oocyt; Oc', degenerated oocyt; Ov, ovum; Ph, phagocyte; Sc, spermatocyt; St, spermatid; Sz, spermatozoa; Vd, vas deferens.

6 No. 8] Sex Reversal in the Japanese wrasse, Halichoeres poecilopterus 513 sive changes to a considerable degree. In addition to degenerating egg cells, sperm cells are found in the same genital epithelium especially near the free end of the ovarian lobes. The fourth figure of the plate depicts the state in which the sex gland has been further transformed. At this stage the sex gland is no longer an ovary, hardly and oocytes being found in each lobe. Most of the egg cells have been replaced by masses of sperm cells. The fifth figure represents a further advanced stage. The gonad is now completely transformed into a testis. It is likely that the wrasse hibernates in this state and functions as a male in the next reproductive season. The above is the description of the sex reversal in Halichoeres poecilopterus based upon observations of external transformation of sex characters and internal changes of the gonad. In summary, it may be that the Japanese wrasse, after reaching maturity, first functions as a female, and then transforms into a male following drastic changes in the gonad, the remaining egg cells undergoing degeneration and spermatozoa being formed from reserved primitive germ cells. Consequently the ovary is transformed into a testis, and the fish now comes to function as male. Thus, the appearance of sperm cells in the ovary of incompletely developed blue wrasses is not an abnormal phenomenon. It is merely a case of protogynous transitional hermaphroditism. It is said that the red wrasse readily goes into hibernation if the temperature is lowered in the aquarium, but the blue wrasse hardly does so and most of them cannot stand the low temperature. According to a recent information from Prof. S. Kawaguti of the Okayama University most of the red wrasses which had been kept in the Tama Aquarium since last autumn, 30 out of 40 fishes turned into the blue wrasses in the course of 40 days from June 15 to July 23. All these facts indicate that the wrasse is hatched out as a female and dies as a male, and the sex reversal is an ordinary phenomenon taking place during its life cycle. I should like to close the present report by expressing my hearty thanks to Mr. S. Yagi of the Matsuyama Museum and to Dr. Y. Haneda, Director of the Kurihama Natural History Museum, for their kind supply of the material of respective district. References Jordan, D. S. and Snyder, J. 0. (1902): Proc. U.S. Nat Mus., 24, Kinoshita, Y. (1934) : Jour. Sci. Hiroshima Univ., B, Div. 1, 3. (1935a) : Bot. Zool., 3(7), 35-. (1935b) Jour. Sci. Hiroshima Univ., B. Div. 1, 4, (1936) : Bot & Zool., 4(6), 35-. (1938) : Zool Mag. (Japan), 50(4), (1939) : Ditto, 51(2), 131. &