A STUDY OF THE VARIATION DUE TO MATERNAL AGE IN HYLEMYA ANTIQUA by GEORGIA J. GOTH B.Sc. Hon., University of Alberta, 1969 M.Sc, University of Oklahoma, 1972 THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF DOCTOR OF PHILOSOPHY THE FACULTY OF GRADUATE STUDIES INSTITUTE OF ANIMAL RESOURCE ECOLOGY and DEPARTMENT OF PLANT SCIENCE We accept this thesis as conforming to the required standard THE UNIVERSITY OF BRITISH COLUMBIA June, 1977 Georgia J. Goth, 1977 In presenting this thesis in partial fulfilment of the requirements for an advanced degree at the University of British Columbia, I agree that the Library shall make it freely available for reference and study. I further agree that permission for extensive copying of this thesis for scholarly purposes may be granted by the Head of my Department or by his representatives. It is understood that copying or publication of this thesis for financial gain shall not be allowed without my written permission. Department of ?(«ttt ScAt&C*. The University of British Columbia 2075 Wesbrook Place Vancouver, Canada V6T 1W5 Date ftuq 2.6; H77 VARIATION DUE TO MATERNAL AGE i THESIS ABSTRACT In 1928, Jennings and Lynch found that the individuals of a clone of rotifers were not intrinsically alike, but varied in fertility and life span depending on the nature of the eggs from which they came. Lansing (1953) suggested that this di• versity was due to an aging factor transmitted to the offspring through the eggs of middle-aged and old mothers. He thought that this aging factor would accelerate the rate of aging in the offspring. This led to a number of similar studies in which attempts were made to demonstrate a "Lansing-effect" in other species. However, there was still a need for a better under• standing of the extent to which maternal aging might be a source of variability among offspring, and the effect of this variability on population dynamics. This was the goal of the present research project. Maternal-age effects on a variety of life history traits were studied in populations of Hy1emya anti qua, the onion root maggot, raised in the laboratory under controlled conditions. A number of differences were elucidated. When the mother is young, she produces her most repro- ductively successful offspring. These offspring have a high survival probability until they reach mid-life, at which point their mortality rate begins to increase more rapidly. ~ Never• theless, they have a long mean expectation of life. They have the highest net fecundity (i.e., average number of eggs produ• ced per female per 48 hours) and at certain ages (11 to 30 days) VARIATION DUE TO MATERNAL AGE show the highest rate of egg production. A higher percentage of the total offspring they produce throughout their reproduc• tive spans are female. These qualities all contribute to give them the highest innate capacity-of natural increase (1.5009) in comparison with later born offspring. As the mother passes into middle-age, her offspring display reduced reproductive capabilities, but their overall survival capabilities are maximal. These young show the low• est sustained mortality rate throughout life and have as long a mean expectation of life as their early-born sisters. They are also the hardiest in terms of their ability to survive food stress-a greater proportion are able to survive starva• tion longer. Their net fecundity is intermediate between that for early-born and that for late-born offspring, as indicated by their rate of increase (1.3712). A mother in old age produces her least viable offspring (i.e., those with the highest mortality rate and the shortest mean expectation of life), and her least fecund offspring (both in terms of net fecundity and rate of egg production). These offspring however have the fastest turn-over rate (mean gene• ration time). Nevertheless, they make the least contribution to succeeding generations, with a rate of increase of 1.2874. These maternally influenced differences in rate of increase have a remarkable effect on population growth; e.g., after ten generations in a constant environment a population of early- born offspring could potentially be 10 times as dense as a late- born population. VARIATION DUE TO MATERNAL AGE iii A young mother produces either her largest or her small• est offspring (depending on provenance) in terms of pupal size. Age-specific fecundity and mortality differences, however, are not related to these size differences. Finally, maternal age also affects the dispersal abi• lity of larvae and the activity of adult females. A certain percentage (7%) of larvae from middle-aged and older mothers show an innate tendency to disperse, whereas those from young mothers tend to remain on the original food source. Trends in adult activity do not coincide with these larval activity dif• ferences. As adults, mid-born females are slightly less acti• ve than either early- or late-born females. Maternal age, therefore, is a source of variability among offspring in this species. Populations of Hylemya anti- qua exhibit overlapping generations, and at any one time will contain ovipositing females of different ages. When a female alters the characteristics of her offspring as a function of her age, it not only represents a strategy of spreading the risk of extinction of her own genetic complement, but it introduces phenotypic variation, thereby representing a stra• tegy for survival of the population as a whole. VARIATION DUE TO MATERNAL AGE TABLE OF CONTENTS Page THESIS ABSTRACT 1 List of Tables vi Li st of Fi gures V11 ACKNOWLEDGEMENTS viii I INTRODUCTION 1 II LITERATURE REVIEW 5 III EXPERIMENTAL DESIGN 13 IV THE BIOLOGY OF HYLEMYA ANTIQUA 17 V DEMOGRAPHIC FACTORS 24 24 1. Fecundity and Mortality 24 1.1 Introduction 1.2 Materials and Methods 26 1 .3 Results • • 27 •37 2. Development Rate and Survival • 37 2.1 Introducti on 39 2.2 Materials and Methods 2.3 Results 41 VI PHYSIOLOGICAL FACTORS '• • 45 45 1. Resistance to Environmental Stress 45 1.1 Introducti on 47 1.2 Materials and Methods 1 .3 Resul ts 48 2. Size 51 51 52 2.12 MaterialIntroductios ann d Methods VARIATION DUE TO MATERNAL AGE V TABLE OF CONTENTS (cont.) Page 2.3 Results 52 VII ECOLOGICAL FACTORS 55 1. Larval Dispersal 55 1 .1 I ntroducti on 55 1.2 Materials and Methods 57 1 .3 Results 57 2. Activity of Adults 60 2.1 Introduction 60. 2.2 Materials and Methods 62 2.3 Results 62 3. Ability to Diapause Successfully 65 3.1 Introduction 65 3.2 Materials and Methods 66 3 .3 Resul ts 66 VIII REVIEW OF RESULTS 69 IX DISCUSSION 71 X CONCLUSION 99 XI LITERATURE CITED 101 APPENDIX Ill VARIATION DUE TO MATERNAL AGE Yi List of Tab!es Page 1. Literature summary of maternal-age studies i n i nsects 9 2. Mean expectation of life at age x, with standard deviations 29 3. Probability of being alive at age >c, with standarddeviations 31 4. Mean rate of egg production for different ranges of age 36 5. (A) Developmental period from egg to pupa 42 (B) Developmental period from pupa to adult emergence from puparium 42 6. (A) Total percentage emergence from puparia 44 (B) Percentage of emerged individuals that are female 44 7. Pupal weight in grams, with standard deviations 53 8. Analysis of Variance statistics for percentage of non-dispersers, with level means and their standarddeviations . 59 9. Analysis of Variance statistics for percentage of active individuals, with level means and their standard deviations 64 10. Growth in cohort populations using different intrinsic rates of natural increase 75 VARIATION DUE TO MATERNAL AGE List of Figures Reproductive characteristics of early-, mid-and late-born females Survivorship curves for cohort populations Schematic representation of experimental apparatus for testing larval dispersal Reproductive value curves for early-, mid-and late-born females VARIATION DUE TO MATERNAL AGE ACKNOWLEDGEMENTS I wish to thank Drs. B.D. Frazer, J.H. Myers, V.C. Runeckles, and C.F. Wehrhahn, the members of my thesis comm• ittee, for their helpful suggestions throughout the course of my research project, and for reviewing and criticising my manuscript. I am also indebted to Elaine Goth, Joe de Silva and Ann Edmondson for their technical assistance, and to Rosemary Iyer for her interest and encouragement. Finally, I am extremely grateful to Dr.. W.G. Wellington, my thesis super• visor, for his guidance, support, criticisms, and encouragement. It has been a valuable learning experience for me to work with Dr. Wellington in this capacity and I wish to thank him very m uch . VARIATION DUE TO MATERNAL AGE 1 I INTRODUCTION Natural selection acts on phenotypes, affecting an indi• vidual's ability to produce viable offspring. The chance of a population surviving is determined by its ability to cope with environmental variation in space and time, and thus on the variability it houses within it (den Boer, 1968). In addition, variability in the offspring of a single female may be important in determining the survival of her particular genome (MacKay, 1 9 74) . A population may be flexible (i.e., variable) because (1) it possesses a large amount of genetic variation, or (2) the phenotypic expression of a given genotype may be altered depending upon environmental conditions. I am concerned here with flexibility of the second type. An organism possesses developmental flexibility if its genotype can be modified in adaptively valuable ways (i.e., to produce different phenotypes) in response to environmental change (Thoday, 1953). These exogeneous adaptations are pro• duced by the capacity to respond in the appropriate way, and it is the genetic constitution which determines the degree of response which is possible (Haddington, 1957).