EGG DIAPAUSE IN EPHIPPIGER CRUCIGER (ORTHOPTERA: TETTIGONIIDAE)
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1 jl exp. Biol. (1977), 66, With 1 figure Printed in Great Britain EGG DIAPAUSE IN EPHIPPIGER CRUCIGER (ORTHOPTERA: TETTIGONIIDAE) III. ABNORMAL DEVELOPMENT THROUGH THE FINAL EGG DIAPAUSE BY R. L. DEAN* AND J. C. HARTLEY Department of Zoology, University of Nottingham, England (Received 2 August 1976) SUMMARY Normally the egg of Ephippiger cruciger is subject to diapause when the embryo is almost fully developed. Most eggs die or develop erratically and slowly when chilled for some time at earlier non-diapausing stages. However, after 2 or 3 months' cooling at a stage just before catatrepsis a few eggs developed more rapidly than usual and hatched without intervention of a diapause, at a temperature that is normally too high to allow diapause development to proceed. A possible mechanism, involving the neurosecretory system, for this diapause pattern is suggested. INTRODUCTION The fully developed embryo of Epkippiger cruciger is subject to an obligatory diapause which is completed by a period of cooling (Hartley & Warne, 1972; Hartley & Dean, 1974; Dean & Hartley, 1977&). The egg-stage usually exceeds 18 months, development of the embryo requires a particular temperature regime which can only be met by the heat input from the summer months, diapause then intervenes and hatching occurs in the following spring. Embryonic development is only initiated when certain high temperature requirements have been met (Dean & Hartley, 1977 a). By the time cold weather comes the embryo has completed its first stage of development and is ready to diapause. The developing embryos are thus not normally subject to low temperatures at the wrong stage. Cooling before embryonic development has started produces a latent period of quiescence related to the length of the cooling period. As part of our programme on the development of the egg-stage of this insect, some eggs were subject to cooling at an intermediate stage of development producing aberrant development in some eggs. MATERIALS AND METHODS Eggs obtained and started into development at 20 C, as given in Dean & Hartley (1977a), were taken at stage III-12 (Warne, 1972), when the embryo is directed posteriorly and just prior to the start of catatrepsis, and cooled at 8 C. Two replicates of 100 eggs were subjected to 1, 2 and 3 months' cooling and then transferred to 25 C Present address: Department of Zoology, University of Western Ontario, London, Canada.
2 198 R. L. DEAN AND J. C. HARTLEY 100 &» 50 bo.h Jc u Days at 25 C r 140 Fig. 1. Cumulative percentage of eggs reaching stage VI-23 at 23 C after cooling at 8 C for o, 1, 3 or 3 months at stage III-12., o months' cooling (control), replicates A and B; d 1 month's cooling, replicates A and B;, 2 months' cooling, replicates A and B; D, 3 months' cooling, replicates A and B.
3 Egg diapause in Ephippiger cruciger. Ill 199 Table 1. Eggs hatching at 25 C after cooling for 2 or 3 months at stage III-12 2 months' cooling 3 months' cooling Number hatching Time at 35 C (days) 51 S Number hatching Time at 35 C (days) for further incubation. An additional two groups of the same stock were incubated directly as controls. The eggs were inspected under xylene at 10-day intervals as described previously, and the stages of development reached by the embryos recorded. RESULTS No eggs developed beyond stage III-12 in the period at 8. Evidently 8 is too low for morphogenesis even when development is initiated at higher temperatures. Figure 1 illustrates the cumulative percentage of eggs reaching stage VI-23 a * 25 0 after being cooled for o, 1, 2 or 3 months at stage III-12. The uncooled control group and those cooled for 1 month showed reasonable uniformity of response. More eggs failed to complete development in the latter group, but a proportion of the eggs successfully reaching stage VI-23 m th e early incubation period did so more rapidly than in the control group. This trend was more obvious with groups cooled for 2 and 3 months where a higher proportion of the eggs reached stage VI-23 more rapidly than the controls. However, the remainder of eggs in these groups developed much more slowly or failed to complete this phase of embryogenesis. The broken line joining the points between 50 and 90 days at 25 0 in the eggs cooled for 3 months is the consequence of a failure to appreciate one of the effects of cooling. This group was not inspected regularly after the 50th day at 25 because all the eggs which were still apparently healthy at this time had reached stage VI-23. The remaining eggs had all ceased development at a variety of intermediate stages since the 20-day inspection. Those embryos which had developed to the half-way stage were unusually small and their yolk was disintegrating in an uncharacteristic manner. In eggs where the embryos had stopped developing at earlier stages the yolk was changing from its normal form of discrete cells into oily globules like those found in nonviable newly-laid eggs (Dean, 1974). It was concluded from their lack of progress and abnormal appearance, that these eggs had been damaged at 8. However, 40 days later eye-spots were seen through the shells of some of these ' failures' so all eggs were again inspected regularly until no further development was observed. A few of the eggs cooled for 2 and 3 months at stage III-12 hatched without further cooling after reaching stage VI-23 (Table 1). No hatching occurred in eggs cooled for only 1 month or in the control group. The
4 200 R. L. DEAN AND J. C. HARTLEY first three eggs to hatch in the group cooled for 3 months were among those which reached stage VI-23 after only 20 days at 25. It is not definitely known whether the other eggs which hatched had been among the rapid developers. DISCUSSION During the course of this study, and in earlier studies involving many thousands of Ephippiger eggs there has never been any evidence to suggest that the induction of diapause at stage VI-23 ^ m an J r wav dependent upon environmental factors (Warne, 1970; Hartley & Warne, 1972; Dean, 1974; Dean & Hartley, 1977ft). It has been assumed that the diapause is an essential, and probably genetically determined stage in the embryonic development. Consequently, the results gained from eggs cooled at stage III-12 were entirely unexpected. The rate at which these eggs, and the uncooled control groups, reached stage VI-23 ^ shown in Fig. 1. The most obvious feature on the graph is the slow growth in most of the eggs after 2 or 3 months of cooling. The eggs cooled for 1 month responded in a similar way to the uncooled controls but more died before completing development. The excessive failure to complete development and the slow growth in most of the surviving eggs probably results from injury sustained at low temperature by a stage which would not normally experience it. High mortality in cooled newly laid eggs probably illustrates the same phenomenon (Dean, 1974). However, some of the eggs which had been cooled for 2 and 3 months developed more rapidly than those which had not been cooled and a small proportion of them hatched at 25 0 without further cooling. These eggs began to hatch within 40 to 50 days at 25 0 and this period included the 20 to 30 days in which the eggs developed from stage III-12 to stage VI-23. Therefore the eggs which hatched must now have been without diapause as diapause development is not completed at Diapausing eggs, with whole embryos, cooled for 2 and 3 months at 8 did not begin to hatch at 25 0 until the 25th and 18th day respectively (Dean & Hartley, 19776). By chance, three eggs which had reached stage IV-23 in only 20 days were separated from the remainder. These three eggs hatched first, so there may be an association between the rapid embryonic growth and hatching without diapause. If this is so then it is possible to speculate briefly on the nature of diapause in this species. The idea of a diapause hormone, as outlined by de Wilde (1970) for some insect eggs, is not tenable for the second or embryonic diapause of Ephippiger. It is possible that an embryonically produced diapause hormone could be effective but this would not fit well with those eggs in which diapause was eliminated by cooling at III-12. For this to be so, the hormone or its precursor would have to be present at this time, which is long before it is required. The onset of diapause is a gradual process, with observable features such as heart-beat and rate of extension and straightening of the limbs gradually slowing down to a standstill. This fits well with the system proposed by Clarke (1965) for withdrawal of the appropriate neurosecretion resulting in cessation of new growth when the current stage of the genetic programme is completed. Reactivation could be brought about by a new phase of neurosecretion that is produced at a low temperature and released after the right time period. The cooling of the eggs at stage III-12 could have brought this system into operation and thus development could have proceeded through from pre-diapause into post-diapause. Further study on this
5 Egg diapause in Ephippiger cruciger. Ill 201 phenomenon may then help to provide information on the control of this diapause system. In two species of Conocephalus, tettigoniids of a different sub-family, the diapause which normally occurs at the half-embryo stage can be prevented by cooling the egg at any time prior to the arrest of growth (Hartley & Warne, 1972). This seems to be a normal process for these species since early cooling is not accompanied by high mortality as in Ephippiger. Also, when newly laid eggs of Teleogryllus commodus are chilled they will then develop, without interruption, through the stage at which diapause normally intervenes (Browning, 1952). This suggests that the process occurring at low temperature in pre-diapause stages may be the same as those of the ' diapause development' which occurs after the inception of diapause. However, Conocephalus and Teleogryllus are then much more perfectly adapted to respond to 'pre-cooling' than Ephippiger. REFERENCES BROWNING, T. O. (1952). The influence of temperature on the completion of diapause in the eggs of Gryllus commodus Walker. Atut. J. Set. Res. B, 5, CLARKE, K. U. (1965). The control of growth in Locusta mtgratoria. J. Zool., hand. 147, DEAN, R. L. (1974). Embryonic diapause and development in Ephippiger cruciger (Fiebex). Thesis submitted to the University of Nottingham for the degree of Doctor of Philosophy. DEAN, R. L. & HARTLEY, J. C. (1977a). Egg diapause in Ephippiger cruciger (Orthoptera: Tettigoniidae). I. The incidence, variable duration and elimination of the initial diapause. J. exp. Biol DEAN, R. L. & HARTLEY, J. C. (19776). Egg diapause in Ephippiger cruciger (Orthoptera: Tettigoniidae). II. The intensity and elimination of the final egg diapause. J. exp. Biol. 66, DE WILDE, J. (1970). Hormones and insect diapause. Mem. Soc. Endocr. 18, HARTLEY, J. C. & DEAN, R. L. (1974). Ephippiger cruciger as a laboratory insect (Orthoptera: Tettigoniidae). J. Nat. Hist. 8, HARTLEY, j. C. & WARNE, A. C. (1972). The developmental biology of the egg stage of Western European Tettigoniidae (Orthoptera). J. Zool., Land. 168, WARNE, A. C. (1970). The biology of the eggs of the Tettigoniidae. Thesis submitted to the University of Nottingham for the degree of Doctor of Philosophy. WARNE, A. C. (1073). Embryonic development and the systematica of the Tettigoniidae (Orthoptera: Saltatoria). Int. J. Insect Morphol. and Embryol. i,
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