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Abortive Development in the Crested Newt Triturus Cristatus

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Abortive Development in the Crested Newt Triturus Cristatus Development 100, 65-72 (1987) 65 Printed in Great Britain © The Company of Biologists Limited 1987 Abortive development in the crested newt Triturus cristatus H. WALLACE Department of Genetics, University of Birmingham, PO Box 363, Birmingham BIS 2TT, UK Summary Crested newts exhibit a balanced lethal system which abortive embryo. causes development to abort in 50 % of tailbud em- Two possible modes of origin for the balanced bryos. The main features of arrested embryos are lethal system are discussed, either from ancestral described, shown to be constant in a range of culture autosomes or from sex chromosomes. The latter is conditions and found to be unchanged by parabiosis favoured because it involves fewer assumptions. The or extirpation of the central nervous system or heart. subsequent evolution of the system should inevitably Two categories of abortive embryos can be dis- lead to progressively earlier embryonic mortality by tinguished in some spawnings. A corresponding seg- an accumulation of multiple recessive lethal factors on regation of an easily identified marker chromosome each chromosome variant. confirms previous reports that chromosome 1 carries the recessive lethal factors. The marker chromosome Key words: developmental genetics, embryonic lethality, is tentatively associated with the blistered form of sex chromosomes, Triturus cristatus, newt. Introduction and death in T.c. carnifex tailbud embryos, together with some experimental tests of whether or not a In one of the earliest descriptions of amphibian primary defect is localized in any particular tissue. development, Rusconi (1821) remarked that almost The data reported here were accumulated over the half the embryos of Triturus cristatus perished at the last three years, mainly while checking an anomalous tailbud stage. He concluded that the development of spawning that showed high embryonic survival. Most this species must be relatively sensitive to culture of the observations were obtained by breeding a conditions, as he encountered no such mortality second generation from this stock, which showed a among T. palmatus embryos. Spemann (1921), Gliick- regular 50% embryonic mortality and the corre- sohn (1932) and Stief (1940) also noticed a high sponding segregation of a distinctive marker chromo- mortality of T. cristatus embryos, without attempting some. to explain it. Macgregor & Homer (1980) redis- covered this embryonic mortality and established its genetic basis, as a consequence of finding that adult Materials and methods crested newts were invariably heterozygous for a heterochromatin pattern on the largest pair of All observations were made on T.c. carnifex, using six pairs purchased from Xenopus Ltd as a single importation and chromosomes. This chromosome 1 heteromorphism their descendents. Adult females were identified by the is apparently maintained by a balanced-lethal system pattern of ventral spots and isolated when laying. Paternity in natural populations of crested newts, including was uncertain for most spawnings, as a succession of males three subspecies of T. cristatus and the closely related were used to ensure successful courtship. Matings were T. marmoratus (Sims, Macgregor, Pellatt & Horner, induced by injecting chorionic gonadotrophin (100-200 i.u. 1984). Different culture conditions and temperature Pregnyl) in winter or occurred spontaneously in late spring. regimes have failed to alleviate the embryonic mor- Grass was provided for the spawning initially, so that eggs tality or to distinguish between the presumed two could be collected daily by cutting off folded grass blades. types of lethal homozygote (Wallace, 1984; Horner & This technique was later improved by substituting nylon Macgregor, 1985). ribbons for the grass, scraping the eggs off each ribbon daily and culturing batches of up to 20 eggs in a Petri dish. The The following account provides details of the eggs were then completely visible and less often damaged in developmental defects associated with retardation laying or collection. 66 H. Wallace Before operations, the egg capsule was surface sterilized in 70 % ethanol for 15 s and removed with fine forceps in Steinberg solution (Rugh, 1962) containing penicillin and streptomycin. Extirpations and parabiosis were performed in the same medium on 2 % agar using tungsten needles (Popiela, 1976; Wallace, 1962). Embryos used for histology were also decapsulated, fixed in neutral formalin or Bouin, processed as 8/wn serial sections and stained either with haematoxylin and eosin or Feulgen and light green. Mitotic metaphases were accumulated by culturing decapsulated wounded embryos for up to 24 h in colchicine (0-5 ragml"1 Steinberg) in small plastic weighing dishes. The isolated heads of these embryos were then swollen in diluted medium for 15 min before fixation in methanol-acetic acid (3:1). Squashed preparations of the heads were subjected to a variety of C-banding techniques and stained with Giemsa (Gurr's R66). The technique described by Sims et al. (1984) provided the best results after brief fixation. Material stored in fixative at — 20 °C for 3-18 months only Fig. 1. Camera-lucida drawings of normal embryos responded to more severe alkaline extraction, 0-07 M- (A-D) aged 4, 5, 7 and 10 days at 20°C; Harrison stages barium hydroxide at 65°C for 30-60min. 24, 30, 35 and 38. Defective embryos (E-H) at the same ages show increasing retardation, dorsal blisters (E-G) and less regular pigmentation (G,H). Capsules shown in Results A and E are 5 mm long. Normal development Mated females typically lay 200-300 eggs during a onset of retardation even when comparing virtually period of 2-3 weeks. Even at the height of spawning, synchronous embryos. Several spawnings, however, they lay less than 40 eggs in one night and relatively have revealed an early manifestation of the defective few during the day. It is therefore more convenient to syndrome in head-process embryos (stage 24). Be- time development from the first cleavage, about 6h tween 10 % and 30 % of the embryos then carry after deposition at 20°C. Successive cleavages occur dorsal blisters over the brain and spinal cord at 90 min intervals. The ensuing morula (12-18 h) has (Fig. 1E-G). Almost all such embryos become ar- a corrugated animal hemisphere before the blastocoel rested, generally at an earlier tailbud stage than the enlarges dramatically at 22—24 h. Gastrulation occu- remaining defective embryos which lack blisters. A pies all the second day and neurulation all the third comparison of blistered specimens with contempor- day. The neurula first elongates by forming a head ary normal embryos suggests that at least some are process at 80-96 h (Harrison stages 21-26; Fig. 1A) already retarded at the head process stage. All before the tailbud becomes visible. Elongation of the defective embryos show subnormal tail growth, only trunk and tail then causes the embryo to become form the primordia of balancers and gills (Fig. 1H), arched within its capsule (stages 27-32; Fig. IB). and rarely show a heart beat, circulation or spon- Only half of these tailbud embryos show continued taneous movement. They are most easily dis- growth and an intensified pigmentation in two dorsal tinguished from younger normal embryos by their stripes, widely separated over the head (Fig. 1C,D). pigmentation, which covers the hindbrain instead of The heartbeat is usually evident by 6 days and blood separating into two dorsal stripes. Their development circulates through the growing gills by 7 days in these is virtually arrested after 7 days, but many survive for normal embryos which generally hatch at 9-12 days. most of the following week and become oedematous This description corresponds to the normal table before degenerating or succumbing to fungus. constructed by Horner & Macgregor (1985) using The main symptoms of retardation and tailbud stages derived from Xenopus and thus indirectly from arrest occur at all the temperatures tested, which Harrison stages. The latter were found suitable for approach the limits of embryonic survival. Uncleaved T. cristatus and extended to include larval life by eggs tolerate gradual warming to 25 °C, to cleave 5 h Gliicksohn (1932), and are reproduced in Rugh later and then at hourly intervals. The temperature (1962), so it seems preferable to use them here. can be safely increased to 28 °C only after gastru- lation. In both cases, tailbud embryos become pig- Abnormal development mented by 4 days and half of them are clearly No abnormality is evident prior to the closure of the retarded at 5-6 days. Eggs chilled to 12°C cleave at neural tube (stage 20) and it is difficult to pinpoint the roughly 5h intervals, complete neurulation after 7 Balanced lethal factors in newts 67 Table 1. Summary of spawnings showing numbers of that the presence or absence of dorsal blisters dis- hatched larvae and arrested tailbud embryos after tinguishes the expected two types of lethal homozy- development at the indicated temperatures gote. Line Hatched Arrested 1 7 matings of purchased adults (12-25 °C) 352 333 (48 %) Experimental studies 2 1 mating as above: (a) at 20°C 50 52 (51 %) The possibility that much of the defective syndrome (b) at 25-28 °C 41 21 (34 %) 3 9 matings of survivors from line 2b: could result from failure to establish a blood circu- (a) at 20 °C 233 222 (49 %) lation (Wallace, 1984) has been tested in two ways. (b) at 24 °C 493 457 (48 %) Random pairs of embryos were joined in parabiosis at (c) at 28 °C 308 314 (50 %) stages 26-28. Only 21 twins out of 40 operations 4 8 matings of F] from purchased stock 317 293 (48 %) remained attached 2 days later, when defective em- (20 °C) 5 Samples from line 4 isolated as: bryos were already distinctly retarded. Six twins were (a) normal head process (hp) embryos 193 81 (21 %) both normal, ten were both defective and five con- (b) hp embryos with dorsal blisters 2 103 (27 %) sisted of a defective embryo attached to a normal one.
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