163. The Control o f Growth and Development in Bombyx mori. II Genic Balance in Molting Characteristics

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1 No. 8] Proc. Japan Acad., 45 (1969) The Control o f Growth and Development in Bombyx mori. II Genic Balance in Molting Characteristics By Seijiro MOROHOSHI Faculty of Agriculture, Tokyo University of Agriculture and Technology, Fuchu-shi, Tokyo (Comm. by Yoshimaro TANAKA, M. J. A., Oct. 13, 1969) Different races of silkworms are characterized by undergoing 3, 4 or 5 molts during larval life. A variety of hypotheses have been advocated to explain the inheritance of molting behavior. Ogura ( ) interpreted it in terms of a major gene and various modifier genes, Nakamura (1932), in terms of duplicate genes, and the present author (1939), in terms of two antagonistic genes and some modifier genes. Ogura (1931) and Shimodaira (1947) found linkage between the major gene controlling the molting characteristics and the F gene or the Kp gene on the VI chromosome. The partial sex-linked inheritance of molting characteristics was first found by Nagatomo (1941) and confirmed by Ichikawa (1941) and the present author (1957), and I suggested that the maturing gene on the Z chromosome is an important modifier. Accordingly, the genic balance between the maturing gene and the major gene controlling the number of molts was newly found. (1) Autosomal inheritance o f molting characteristics. To summarize my results : the difference between each molting type is due to a series of multiple alleles, whose dominance is in the following order: Tri-> tetra-> pentamolting At present the gene symbols, M3, +M, and M5, have been given for tri-, tetra-, and pentamolting respectively. Crossing insects from a strong trimolting (3 m A) and a tetramolting race result in the F2 of a typical 3:1 segregation characteristic of the major genes. However, segregation results are very complicated in the case of a weak trimolting type (3 m B). Shimodaira (1947) found that the major gene controlling the number of molts is linked with the Kp gene on the VI chromosome. Morohoshi (1957) has also ascertained this linkage between the major gene controlling the number of molts and the Kp gene. (2) Partial sex-linked inheritance o f molting characteristics. The sex-linked factors controlling the inheritance of molting character-

2 734 S. MOROHOSHI [Vol. 45, istics have also been extensively investigated by the author. One example of the many experiments will be mentioned. A number of trimolting females appeared in the F1 of a cross between a Kp (tetramolting univoltine) (~) and a Cambodge (tetramolting multivoltine) (s). In the reciprocal cross no trimolters appeared, as shown in Table I. In the former cross, females showed shorter durations of each instar and lighter body weight than males in opposition to the normal case. Table I. Sex-linked inheritance of molting characteristics in the crosses of Kp (+M/+M, Lm) (fi)x Cambodge, c(+m/+m, Lme/Lme) (~) The sex-linked segregation of trimolters was clearly observed in the F2, as shown in Table I. The Cambodge race has the recessive early maturing gene (Lme) on the Z chromosome, but Kp individuals have the dominant late maturing gene (Lm). Somewhat fewer females than males were trimolters. It is considered that the males having two Lme genes are more apt to become trimolters than are females having one. A clear sex-linked inheritance is observed in such quantitative characteristics as larval duration, silk production, and body weight, as well as the number of molts. (3) Locus o f the maturing gene on the Z chromosome. The time spent from hatching until emergence by od and + od individuals is equal for silkworms having both` the early maturing gene, Lme, and the sex-linked gene, od (distinctly translucent skin, at 49.6 on the Z chromosome) and those having two dominant genes, Lm and +od (Morohoshi and Kikuchi, 1956). Therefore, the maturing gene is presumably located on the left proximal end, since the od gene exists on the right proximal end. Takasaki and Aratake (1956) reported that this maturing gene is linked to the Ge gene (Aruga's giant egg, at 14.0 on the Z chromo-

3 No. 8] Control of Growth and Development in Bombyx mori. II 735 some) at locus From Morohoshi and Kikuchi's and Takasaki and Aratake's experiments, the maturing gene may be located on the left proximal end, e.g., at the 0.7 ( ) on the Z chromosome. Later Takasaki and Aratake reported the locus of this maturing gene to be at 2.0 on the Z chromosome. (4) Polymorphic actions of the sex-linked maturing gene. According to studies thus far, various genes for sex-linked inheritance of quantitative characteristics of the silkworm have been assumed to be located on the Z chromosome. The author, from the above results, has arrived at the conclusion that the sex-linked inheritance of quantitative characteristics is due to a function of the maturing gene. There are two reasons for this conclusion ; one is that all quantitative characteristics, such as developmental duration, silk production, and body weight, always behave in the same direction in respect to sexlinked inheritance (see Table II). The other is that the sex-linked genes controlling the quantitative characteristics plus the maturing gene on the Z chromosome have not yet been found. Table II. Relationship between the maturing quantitative characteristics genes and Since the linkage value between the maturing gene and the os gene on the Z chromosome is about 2.0%, two larval characteristics, os and +os, represent approximately the difference of the action of maturing genes in os (+Lm) and +os (Lme) individuals (Table II, group A) or in os (+Lm) and +os (Lm) (Table II, group C). The functioning of the maturing gene controlling the quantitative

4 736 S. MOROHOsHI [Vol. 45, characteristics is clearly observed in the female of the cross shown in Table II; the early maturing gene makes the larval duration shorten, the cocoon weight, silk production, and the number of molts decrease, and the number of generations increase. On the other hand, the late maturing gene makes the larval duration lengthen, the cocoon weight, silk production, and the number of molts increase, and the number of generations decrease. (5) Relationship between the maturing gene and molting characteristics. The cross in Table II shows also the relationship between the maturing gene and molting characteristics. From the result of the backcross shown in group A of Table II, those insects having the early maturing gene (Lme) were apt to produce trimolters, while +os individuals in group B segregated few trimolters from "tetramolting larvae" as compared to no segregation of trimolters from os individuals. This result may be due to the difference of metabolism in os and +os individuals. The Lm gene did not segregate any trimolters, as seen in group C of Table II. Thus there are at least three types of maturing genes, Lm>+Lm>Lme. The relationship between different kinds of maturing genes and the segregation of tetramolters from "trimolting larvae" is shown in Table III. From Table III we can observe that the segregation of tetramolters from "trimolting larvae" is maximal in the crossing of the Lm gene (group A) and minimal in the crossing of the Lme gene (group C). Table III. Relationship between the maturing genes and the segregation of tetramolters from "trimolting larvae" As in the above results, the maturing gene controls such quantitative characteristics as the larval duration, silk production, the body weight, the number of molts, and the number of generation per year.

5 No. 8] Control of Growth and Development in Bombyx mori. II 737 Since the early maturing gene accelerates the larval and pupal development, the molting characteristics are changed to the dominant direction (M3- +ME--M5). On the other hand, since the late maturing gene lengthens the duration of the larval and pupal periods, they are changed to the recessive direction (M3--~ +M---M5). Accordingly, a genic balance is observed between the maturing gene and the major gene controlling molting characteristics, as shown in Fig. 1 A. Fig. 1. Genie balance between maturing genes and major genes controlling molting characteristics. A : genie balance, B : internal organs controlling central nervous system, C : chromosome map. Lme : early maturing gene, Lm: late maturing gene, M3: major gene controlling trimolting, +M: major gene controlling tetramolting, M5: major gene controlling pentamolting, Br: brain, SG: suboesophageal ganglion, CC: corpus cardiacum, CA: corpus allatum, Z : Z chromosome, VI: VI chromosome, M : major gene controlling molting, V : major gene controlling voltinism. The early maturing gene (Lme) diverts molting characteristics towards dominant behavior, M3 E--+M--M5. The late maturing gene (Lm) diverts molting characteristics towards recessive behavior, M'-- +M--CM, but may act secondarily to determine molting characteristics. Considering both the results of hormonal (Morohoshi and Oshiki, 1969 a, b) and genetical studies, the maturing gene seems to control the impulses from the brain, and the major gene controlling the number of molts seems to govern the secretion of the corpora allata. The secretion of the corpora allata is the strongest in trimolting (M3), intermediate in tetramolting (+M) and the weakest in pentamolting (M5). According to our recent studies (Morohoshi and Kiguchi, 1969, Morohoshi et al., 1969), the corpus allatum hormone accelerates the release of glycogen and lipid into blood from the fat body and increases the speed of the accumulation of protein into some tissues or eggs in a given period of time, and the suboesophageal ganglion hormone accelerates the accumulation of carbohydrate and lipid into the fat body or eggs and decreases the speed of the accumulation of protein into some tissues or eggs in a given period of time. Since in the early maturing strain the secretion of the corpora allata is controlled through nerve impulses from the brain, the molting

6 738 S. MoROHOSHI [Vol. 45, characteristics are directly changed to the dominant direction. Since in the late maturing strain the secretion of the suboesophageal ganglion is controlled by impulses through nerve commissures from the brain, the molting characteristics are indirectly changed to the recessive direction, as shown in Fig. 1 A. Acknowledgement. The author wishes to express his gratitude to Professor Robert C. King, Northwestern University, Illinois, for reading the manuscript. References Ichikawa, S. (1941) : An observation on trimolting in Bombyx mori. J. Sericult. Sci. Japan, 12, omrohoshi, S. (1939) : Studies on the molting character in the silkworm (Bombyx mori). I-IV. Dept. Agri. Kyushu Imp. Univ., 4, Morohoshi, S., and Kikuchi, R. (1956) : Studies on voltinism in the silkworm, Bombyx mori. II. The relationship between voltinism and the sex-linked gene (od). J. Sericult. Sci. Japan, 25, 228. Morohoshi, S. (1957) : Physiogenetical Studies on Moltinism and Voltinism in Bombyx mori. A New Hormonal Antagonistic Balance Theory on the Growth. Japan Soc. Prom. Sci., (book). Morohoshi, S., and Oshiki, T. (1969 a) : Effect of the brain on the suboesophageal ganglion and determination of voltinism in Bombyx mori. J. Ins. Physiol., 15, (1969 b) : Effect of the brain-corpora allata complex on the determination of voltinism in Bombyx mori. Proc. Japan Acad., 45, Morohoshi, S., and Kiguchi, K. (1969) : Effect of the corpus allatum hormone on lipid metabolism in Bombyx mori. Proc. Japan Acad., 45, Morohoshi, S., Iijima, T., Kikuchi, S., and Ikeda, S. (1969) : Effect of the corpus allatum hormone on carbohydrate and nitrogen metabolism in Bombyx mori. Proc. Japan Acad., 45, Nagatomo, T. (1941) : On the sex-linked appearance of trimolting in Bombyx mori. J. Sericult. Sci. Japan, 12, Nakamura, T. (1932) : On the inheritance of the molting character in the silkworm. Bull. Seri. Exp. Sta. Chosen, 3, Ogura, S. (1931) : Erblichkeitsstudien am Seidenspinner, Bombyx mori L. II. ttber die Koppelung zwischen dem Hautungsfaktor and dem Faktor F. Z. f. ind. Abst. u. Vererb., 58, ( ) : Erblichkeitsstudien am Seidenspinner, Bombyx mori L. III. Genetische Untersuchunge der Hautung (I Teil and II Teil). Ibid., 61, ; 64, Shimodaira, M. (1947) : Studies on the linkage inheritance in the silkworm. I. Relation between VI linkage and VIII linkage group. Jap. Jour. Gen., 22, Takasaki, T., and Aratake, Y. (1956) : On the locus of the sex-linked late maturing gene Lm in Bombyx mori. J. Sericult. Sci. Japan, 25,