STUDIES on the COPULATORY BEHAVIOUR of the FREE-LIVING NEMATODE PANAGRELLUS REDIVIVUS (GOODEY, 1945). by C.L. DUGGAL M.Sc. (Hons

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STUDIES on the COPULATORY BEHAVIOUR of the FREE-LIVING NEMATODE PANAGRELLUS REDIVIVUS (GOODEY, 1945). by C.L. DUGGAL M.Sc. (Hons STUDIES ON THE COPULATORY BEHAVIOUR OF THE FREE-LIVING NEMATODE PANAGRELLUS REDIVIVUS (GOODEY, 1945). by C.L. DUGGAL M.Sc. (Hons. School) Panjab University A thesis submitted for the degree of Doctor of Philosophy in the University of London Imperial College Field Station, Ashurst Lodge, Sunninghill, Ascot, Berkshire. September 1977 2 AtSTRACT The copulatory behaviour of Panagrellus redivivus is described in detail and an attempt is made to relate copulation with the age and reproductive state of the nematodes. Male P. redivivus show both pre- and post-insemination coiling around the female and they use their spicules for probing and for opening the female gonopore. Morphological studies on the spicules have been made at both the light microscope level and the scanning electron microscope level in order to understand their functional importance during copulation. The process of insemination has been studied in some detail and the morphological changes occurring in the sperm during their migration from the seminal vesicle to the seminal receptacle have been recorded. It was found that during migration the sperm formed long chains by attaching themselves anterio-posteriorly, each sperm producing pseudopodial-like projections. The frequency of copulation in the male nematodes and its influence on the number of sperm produced and on the nematode life- span was examined, and compared with the development and longevity of aging virgin males. The number of sperm shed into the uterus of the female at the time of copulation was found to increase with increasing intervals between copulations. Similar observations were also made on the life-span and oocyte production in copulated and virgin females. The phenomenon 3 of sex attraction was studied in relation to oocyte development in the female's reproductive tracts and was investigated using 4th stage larval females, and virgin and non-virgin females of varying age and reproductive states. Virgin females were found to be attractive to and respondent towards the adult males whereas copulated females neither attracted nor responded to adult males. The timing of the first copulation of the newly moulted female was studied in relation to the number of available males. The possible effects of age on the first copulation of a virgin female was also noted. Further copulation in inseminated females was studied in relation to storage of the oocytes and the number of sperm present from the previous copulation. It was found that large numbers of sperm can delay further copulation considerably but that aged sperm in the seminal receptacle did not prevent further copulation. 4 ACKNOWLEDGEMENTS My thanks are due primarily to my supervisors, Professor N.A. Croll for suggesting the problem; Dr. A.A.F. Evans for his continual interest and advice; and Dr. D.J. Wright for his constant help, advice, and encouragement throughout this work. My appreciations are due to Professor T.R.E. Southwood for providing work space and facilities at the Field Station. My thanks are also due to Mrs. A.J. Budd for typing this manuscript and all those at Imperial College Field Station who have helped me in so many ways. Finally, my special thanks go to the Government of India for providing me with a scholarship during the tenure of this work. CONTENTS Page Abstract 2 Acknowledgements 4 Contents 5 Introduction 10 General copulatory behaviour and physiology in nematodes 10 Sex attraction in nematodes 16 Female copulatory activity in nematodes 18 Males copulatory activity in nematodes 22 Sex ratio in nematodes 25 Conclusions 27 Section I - The experimental animal and its culture 30 in the laboratory I.A. Panagrellus redivivus (Goodey, T., 1945), 30 Order Rhabditida (Oerley, 1880), Family Panagrelaimidae (Thorne, 1937) I.B. Monoxenic culture 30 I.C. Preparation of agar plates 31 I.D. Observation on P. redivivus at low magnification 32 I.E. Observation on P. redivivus at high magnification 32 I.F. Scanning electron microscopy 34 1.Tail region of adult male P. redivivus 34 2. Sperm 34 Section II - Observations on the general reproductive 36 biology of P. redivivus II.A. The male reproductive system 36 6 Page II.B. Male accessory reproductive organs 40 1.The spicules 40 2. The gubernaculum 40 3. Caudal papillae 43 II.C. The female reproductive system 43 II.D. General copulatory behaviour of P. redivivus 45 1. Pre-insemination coiling of the male 45 2. Penetration 49 3. Insemination 49 4. Insemination in the post-vulvar uterine sac 51 5. Post-insemination coiling of the male and its 52 attachment to the female II.E. Maturation of sperm in the female 53 1.Introduction 53 2. Experimental procedure 55 3. Observations 56 Section III - Copulatory behaviour of male P. redivivus 66 III.A. Post-moulting copulatory behaviour of adult 66 male P. redivivus 1.Experimental procedure 66 2. Results 66 III.B. The rate of copulation, the number of sperm 68 transferred and the life span of normally copulating males 1.Experimental procedure 68 2. Results 68 7 Page III.C. Development and life span of virgin male 71 1.Experimental procedure 71 2. Results 72 III.D. Effect of short isolation periods on the 73 copulatory behaviour of•male P. redivivus 1.Experimental procedure 73 2. Results 73 2a. The duration of pre-insemination coiling 76 2b. The number of sperm transferred per copulation 76 2c.Duration of post-insemination coiling 79 and attachment III.E. Effect of long isolation periods on the 80 libido of male P. redivivus 1.Experimental procedure 80 2. Results- 81 Section IV - Development and life span in female P. redivivus 83 IV.A.1. Introduction 83 2. Experimental procedure 83 3.Results 84 3a.Development in virgin females 84 3b.Development in copulated female 92 3c.Mortality of virgin and copulated females 93 Section V - Sex attraction in P. redivivus 95 V.A. Introduction 95 V.B. Test apparatus for sex attraction experiments 95 and experimental procedure 8 Page V.C. Results 98 1.Response of virgin females and adult males 98 towards E. coli 2. Homosexual attraction and response of virgin 100 females and adult males 3. Attraction and response of fourth-stage larval 100 females to adult males 4. Attraction and response of normally copulating 102 females to adult males 5. Attraction and response of aging virgin females 102 to adult males P. redivivus Section VI - Copulatory behaviour of females P. redivivus 107 VI.A. Time of first copulation in female 107 1.Introduction 107 2. Experimental procedure 107 3. Results 108 VI.B. The effect of aging on the first copulation 110 of the virgin female 1.Introduction 110 2. Experimental procedure 110 3.Results 111 VI.C. Factors influencing the second copulation 111 1. Introduction 111 2. Experimental procedure 114 2a. The influence of male copulatory activity on 114 the copulatory behaviour of once-copulated females 9 Page 2b.Number and aging of sperm in the uterus 114 2c. Number and aging of oocytes in the female 115 3. Results 115 3a.The influence of male copulatory activity 115 on the copulatory behaviour of once-copulated females 3b.The number and aging of sperm in the uterus 117 3c.The number and aging of oocytes in the females 121 VI.D. The third copulation of female P. redivivus 124 1. Experimental procedure 124 2. Results 124 VI.E. Behaviour of sperm of P. redivivus in vitro in the 126 presence of oocytes 1.Introduction 126 2. Experimental procedure 126 3.Results 126 General Discussion 127 Copulatory behaviour and the role of the spicules and 127 caudal papillae during copulation Functional maturation of sperm in nematodes 129 Copulatory behaviour of male nematodes 133 Sexual development of adult female nematodes 135 Sex attraction in nematodes 138 Copulatory behaviour of female nematodes 142 Conclusions 146 References 149 Appendices 158 10 INTRODUCTIO N The reproductive physiology of nematodes has recently been reviewed by Anya (1976) and Lee and Atkinson (1976). It is apparent that little is known about the factors influencing copulation in nematodes and that the process of copulation itself has been described in relatively few species. General copulatory behaviour and physiology in nematodes In most of the nematode species examined the male coiled its tail around the vulval region of the female using its specialised copulatory muscles to form a loop through which the female moved forwards and backwards several times prior to copulation (Greet, 1964; Chin and Taylor, 1969; Trudgill, 1976). In a few species, however, the male appeared to move the ventral surface of its cloacal region backwards and forwards over the cuticular surface of the female until it located the vulval opening (Fisher, 1972; Chuang, 1962; Anderson and Darling, 1964; Jones, 1966; Sommerville and Weinstein, 1964; Somers, Shorey and Gaston, 1977). At copulation the anterior end of the male and female Nematospiroides dubius were found to point in opposite directions (Sommerville and Weinstein, 1964), whereas in Cylindrocorpus spp. they were at right angles (Chin and Taylor, 1969). During copulation the head of the male and female of Ditylenchus destructor were never seen to be parallel (Anderson and Darling, 1964). 11 During pre-insemination coiling or probing of the male in Rhabditis teres (Chuang, 1962), Pelodera teres (Jones, 1966), Cylindrocorpus spp. (Chin and Taylor, 1969), Rhabditis pellio (Somers, Shorey and Gaston, 1977), the spicules were periodically protruded to make contact with the cuticle of the female. Such a periodic extension of the spicules has not been observed in other species of nematode. Mueller (1930) reported that during copulation in Ascaris lumbricoides the spicules were withdrawn into their sheaths and he thought that they played no part in insemination. However, this was based on fixed worms found in the coital position and more recent work on the copulatory behaviour of living specimens of several nematode species has shown that the spicules remained inside the vagina during the whole process of insemination, no matter how long this process took (Chuang, 1962; Greet, 1964; Anderson and Darling, 1964; Jones, 1966, Sommerville and Weinstein, 1964; Fisher, 1972; Chin and Taylor, 1969; Trudgill, 1976; Somers, Shorey and Gaston, 1977).
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