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Experimental Studies of the Reproductive Behaviour of Xenopus Laevis

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[An account is given of certain descriptive and experimental observations on part of the reproductive behaviour of Xenopus laevis (Daudin), the South African clawed frog. The animals were maintained in conditions constant with respect to temperature, minimal water volume and feeding, the three environmental factors believed to be important for breeding in Xenopus. They were observed under standardised conditions in small glass aquaria. In these conditions, as in pregnancy diagnosis laboratories, ovulation in the female is under the experimenter's control, occurring only in response to injected gonadotrophin or other sex hormones. Gonadotrophin is known also to.affect the reproductive behaviour of the male. The endocrinological background is discussed. Chorionic gonadotrophin was prepared and assayed specially for this research, and used throughout. The mating behaviour of isolated pairs of Xenopus individuals in these conditions is described at length. When a 'treated' male (= injected with gonadotrophin in Xenopus saline) is placed with a treated female, he eventually assaults her and remains clasping her until after fertilisation, that is for a period of many hours. When placed with an 'untreated' female (not injected, or injected with saline alone) or with a treated or untreated male, he assaults, remains clasping for a variable period of minutes, unclasps, and after an interval assaults again, this sequence being many times repeated. Vocalisations by the 'passive partner' are described-that is, by the animal assulted-, namely Ticking in the untreated female and Sawing in the male. The treated female is silent when assaulted. Two movements described as Flicking and High-kicking are reported; these movements occur during feeding and moulting, but also, especially in the male, in the mating aquaria during observations with untreated females and males as passive partners, tending to occur in these latter conditions at the beginning and end of spells of clasping. The circumstance that males isolated with passive partners other than treated females perform repeated spells of clasping makes possible a particular method of experiment and modes of measurement. 16 separate pairs could be observed simultaneously for a period of observation constituting a 'Test'. This period was constant—3 hours—for all 'Tests' within a given experiment, and all experiments here described. The sum of the durations of the clasping spells within this period—T. R. T.—and the mean duration of these spells—M. C. T.—were measured for each pair in each Test. Since their variance was high, while individual animals could be marked, most experiments involved balanced designs with several replicate Tests. On statistical grounds a logarithmic transformation was performed on the crude values obtained for T.R.T. and M.C.T. Two experiments were performed, using untreated females as passive partners, with balanced Graeco-Latin square designs permitting determination of the contribution to the variance of the two measures from differences between individual males, differences between individual untreated females, and dosage of gonadotrophin injected into the males. These experiments gave identical results—in the second one of high significance. It was found that the variance of both measures depended significancy on differences between individual males, but that differences between females affected M.C.T. and not T.R.T., while hormone dose given to the male affected T.R.T. and not M.C.T. Further experiments showed that when the passive partner was a male M.C.T. was significantly lower than when it was an untreated female, while T.R.T. was unchanged. When the passive partners were all males, neither measure was affected by injecting the passive males with gonadotrophin or by selecting them on the basis of their T.R.T. scores when tested in the active role. These results are subjected to a detailed causal analysis according to the principles and methods put forward by RUSSELL, MEAD & HAYES (1954) After a full examination of the data, an interpretation of the Acts of Flicking and High-kicking as displacement activities, and an account of neurological results of other authors on Rana species, it is concluded that the central nervous mechanism in the male Xenopus underlying the observed behaviour must consist of three basic units, defined as the Clasping Correlation Unit, the Unclasping Correlation Unit and the Clasping Coordination Unit. The two former must have no direct interaction with each other, though both influence the Clasping Coordination Unit. Other hypotheses are successively eliminated, and it is shown that with a few plausible assumptions about operation the definitive one will account satisfactorily in detail for all the factual results. The demonstration of this mechanism is rigorous and the finding that gonadotrophin influences the Clasping but not the Unclasping Correlation Unit is particularly critical evidence for the specificity of hormone action on the central nervous system., An account is given of certain descriptive and experimental observations on part of the reproductive behaviour of Xenopus laevis (Daudin), the South African clawed frog. The animals were maintained in conditions constant with respect to temperature, minimal water volume and feeding, the three environmental factors believed to be important for breeding in Xenopus. They were observed under standardised conditions in small glass aquaria. In these conditions, as in pregnancy diagnosis laboratories, ovulation in the female is under the experimenter's control, occurring only in response to injected gonadotrophin or other sex hormones. Gonadotrophin is known also to.affect the reproductive behaviour of the male. The endocrinological background is discussed. Chorionic gonadotrophin was prepared and assayed specially for this research, and used throughout. The mating behaviour of isolated pairs of Xenopus individuals in these conditions is described at length. When a 'treated' male (= injected with gonadotrophin in Xenopus saline) is placed with a treated female, he eventually assaults her and remains clasping her until after fertilisation, that is for a period of many hours. When placed with an 'untreated' female (not injected, or injected with saline alone) or with a treated or untreated male, he assaults, remains clasping for a variable period of minutes, unclasps, and after an interval assaults again, this sequence being many times repeated. Vocalisations by the 'passive partner' are described-that is, by the animal assulted-, namely Ticking in the untreated female and Sawing in the male. The treated female is silent when assaulted. Two movements described as Flicking and High-kicking are reported; these movements occur during feeding and moulting, but also, especially in the male, in the mating aquaria during observations with untreated females and males as passive partners, tending to occur in these latter conditions at the beginning and end of spells of clasping. The circumstance that males isolated with passive partners other than treated females perform repeated spells of clasping makes possible a particular method of experiment and modes of measurement. 16 separate pairs could be observed simultaneously for a period of observation constituting a 'Test'. This period was constant—3 hours—for all 'Tests' within a given experiment, and all experiments here described. The sum of the durations of the clasping spells within this period—T. R. T.—and the mean duration of these spells—M. C. T.—were measured for each pair in each Test. Since their variance was high, while individual animals could be marked, most experiments involved balanced designs with several replicate Tests. On statistical grounds a logarithmic transformation was performed on the crude values obtained for T.R.T. and M.C.T. Two experiments were performed, using untreated females as passive partners, with balanced Graeco-Latin square designs permitting determination of the contribution to the variance of the two measures from differences between individual males, differences between individual untreated females, and dosage of gonadotrophin injected into the males. These experiments gave identical results—in the second one of high significance. It was found that the variance of both measures depended significancy on differences between individual males, but that differences between females affected M.C.T. and not T.R.T., while hormone dose given to the male affected T.R.T. and not M.C.T. Further experiments showed that when the passive partner was a male M.C.T. was significantly lower than when it was an untreated female, while T.R.T. was unchanged. When the passive partners were all males, neither measure was affected by injecting the passive males with gonadotrophin or by selecting them on the basis of their T.R.T. scores when tested in the active role. These results are subjected to a detailed causal analysis according to the principles and methods put forward by RUSSELL, MEAD & HAYES (1954) After a full examination of the data, an interpretation of the Acts of Flicking and High-kicking as displacement activities, and an account of neurological results of other authors on Rana species, it is concluded that the central nervous mechanism in the male Xenopus underlying the observed behaviour must consist of three basic units, defined as the Clasping Correlation Unit, the Unclasping Correlation Unit and the Clasping Coordination Unit. The two former must have no direct interaction with each other, though both influence the Clasping Coordination Unit. Other hypotheses are successively eliminated, and it is shown that with a few plausible assumptions about operation the definitive one will account satisfactorily in detail for all the factual results. The demonstration of this mechanism is rigorous and the finding that gonadotrophin influences the Clasping but not the Unclasping Correlation Unit is particularly critical evidence for the specificity of hormone action on the central nervous system.]

Affiliations: 1: Department of Zoology and Comparative Anatomy, University of Oxford

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