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). This flexibi•
lity of development in a genotype is an important factor in
determining the adaptive value of that genotype (Dobzhansky,
1970), since natural selection is selection for the ability of
organisms to adapt to the environment in which they must exist
(Waddington, 1957). VARIATION DUE TO MATERNAL AGE 2
Besides the genetic information furnished by the pater• nal and maternal chromosomes, the developing zygote carries with it certain cytoplasmic information, which is furnished by the mother in the course of egg formation. Its accumulation is determined by her genome and the phenotypic reactions of this genome to external and internal changes (Labeyrie, 1967).
Maternally influenced inheritance relates to the composition of egg cytoplasm or egg yolk when an egg is laid, and it re• presents a source of variability between individuals (Welling• ton, 1 9 77) .
A female may lay her eggs over a period of time. This means that her body is undergoing certain physiological chan• ges due to the aging process and due to changes which are occur• ring in the habitat and in the weather^. Her eggs therefore will be produced when her body is in different physiological states. One can see that it would be an adaptive advantage if such internal changes could help to produce offspring best able to survive in the environment in which they found them• selves. In this way their phenotypic expression, towards which selection is directed, could be altered to keep pace with environmental change. The offspring in turn would be develop• ing under different environmental conditions, and so might not need to respond to the same things, or in the same way.
See Appendix I, Section A, for information concerning the types of physiological changes which occur as a result of the aging process, and their possible influence on repro- ducti on. VARIATION DUE TO MATERNAL AGE 3
Since sensitivity to environmental factors varies among different age classes, population stability will be enhanced due to "spreading of risk" if there are many age classes in a population at any one time (Reddingius and den Boer, 1970).
The argument is that the age classes will be affected by envi• ronmental factors to different degrees, so that while some may not be favored, others will be, such that the net effect on survival within the population as a whole should not be as detrimental as in a group composed of only one age class.
This variation is also accentuated by phenotypic differences among individuals within each age class. Maternal age, as a source of variability among offspring, therefore could be a contributing factor to stability if at any one time a popula• tion housed ovipositing females of different ages.
According to Wellington (1977), we should be consider• ing how successful species are able to survive, despite their hostile environments, by attempting to discover "rules for survival". Perhaps the survival of those individuals who live to reproduce is not due to chance, as is sometimes assumed, but to their superior quality.
Parental investment, as defined by Trivers (1972), is
"any investment by the parent in an individual offspring that increases the offspring's chance of surviving (and hence re• productive success) at the cost of the parent's ability to invest in other offspring." Natural selection thus would tend to adjust parental investment so as to maximize net reproduc- VARIATION DUE TO MATERNAL AGE 4
tive success. Maternal inheritance represents an additional or alternative means by which net reproductive success of an individual could be maximized without involving the added energy costs associated with parental investment.
It may be that the reproductive system of a population is changing over time and that there are optimal times for the production of specific types of young (e.g., those best able to disperse or to enter diapause). Maternal age could also be part of a mechanism governing this change in the reproductive system.
The goal of this research project was to provide sta• tistical information concerning differences in offspring attributable to the age of the mother when she produces a batch of eggs. Since this variability could manifest itself in a number of ways, I chose to study various demographic, physio• logical, and ecological factors. The experiments were perform• ed on populations of the onion root maggot, Hy1emya a n t i q u a
(Meigen) (Diptera:Anthomyiidae) , reared under controlled laboratory conditions. A sufficiently restricted environment was necessary to al1ow elucidation of the extent to which off• spring variability is a function of maternal age. If maternal age could be shown to be a source of variability in such an environment, then it would have the potential for being an adaptively important factor influencing survival of populations under natural conditions. VARIATION DUE TO MATERNAL AGE 5
U LITERATURE REVIEW
Parsons (1962) conducted a series of experiments with
Drosophi1 a spp. to discover correlations among egg sizes and hatchabi1ity , the number of sterno-pleural chaetae, and ma•
ternal age. From his study and those of others (e.g., Miner,
1954; Durrant, 1955; Beardmore, 1960; Bodmer, 1961), he
concluded that, in general, there is an optimal maternal age when offspring will be most fit in terms of developmental
stability, viability, and reproductive ability. In a later
article Parsons (1964) suggested that this optimal maternal
age is often during the middle period of the mother's repro•
ductive life. He attempted to summarize the relevant litera•
ture up to that time, with special reference to aging in
humans and the incidence of birth defects in the offspring.
Earlier works, notably by Miner (1954, a symposium), were also
stimulated by an interest in human aging.
Lansing (1953) found that the life span of rotifer
progeny selected from young mothers increased over successive
generations, whereas the life span of those selected from old
mothers decreased. Within this "old" line, life span could
be increased by selecting for younger mothers. The fact that
such a reversal could take place indicated that the change was
not due to an accumulation of deleterious factors, but rather
to some non-genic substance transmitted through the maternal
cytopi asm.
Bateson (1963) tried to combine the idea of genotypic VARIATION DUE TO MATERNAL AGE 6
change with the ability of an individual to adapt under press• ure of the environment. He suggested that genetic changes that might also increase the available range of non-genetic flexibility would have high survival value. In 1968, den Boer advanced the theory of ".spreading of risk". He proposed four main ways in which risk could be spread through a population, two of which are by phenotypic variation and by variation between individuals in time (in rate of development and/or reproduction). Density fluctuations are stabilized by spread• ing of risk, which increases the chance of survival of the population. MacKay (1974) extended this concept to apply to the offspring of a single individual. Differences due to ma• ternal age represent one way of producing a wide variety of offspring, thus "spreading the risk of extinction of its par• ticular genetic complement as widely as possible."
At the population level, the influence of age is a means of contributing a constant supply of heterogeneous off• spring, the consequences of which can be far-reaching (Labey- rie, 1967), as Wellington (1965) has shown in his study of the western tent caterpillar, Malacosoma pluviale (Dyar)(Lepidoptera).
In Mai acosoma, the eggs are produced over a period of days during the pupal stage. Some (those produced first) receive more yolk than others. This nutritional difference is respon• sible for the appearance of different types of larvae, and they in turn affect colonial behaviour (Wellington and Maelzer,
1967). Similarly, in the fall webworm, Hyphantria cunea (Drury)
(Lepidoptera) , Morris ( 1 967) found a "strongly transmitted VARIATION DUE TO MATERNAL AGE 7
influence of parental food quality" on the viability of eggs and the survival of first-instar larvae. He stressed the importance of recognizing indirect effects of environmental factors (in this case temperature acting through food quality as the season progressed) on quality of the progeny.
The importance of age composition of females in a population has received a certain amount of attention in insect species of medical importance, especially once methods for determining physiological age (based on irreversible changes in the ovaries) were developed (Detinova, 1968; Rabinovich,
1971 & 1972b). Epidemiological risk of a population can be judged if the number of individuals of a potentially dangerous age is known. The first investigation of this sort was perform• ed on populations of the malaria mosquito, Anopheles spp. (Dip- tera)(Detinova, 1968) and its success led to a number of similar studies, some involving progeny variation due to maternal age.
Differences in the types of offspring produced by a female throughout her reproductive life have been reported for a number of characteristics and in a number of species. Table
1 is a summary of such research on insects. Most of the papers deal with demographic characteristics such as developmental rate, fecundity, longevity, and egg viability. In a few, abi• lity to resist certain types of stress has been examined.
MacKay (1974) was one of the few to study maternal-age effects in relation to ecological characteristics. She examin• ed the incidence of diapause in the sawfly Eriocampa ovata
(L .) (Hymenoptera) , and the production of alatae in the pea VARIATION DUE TO MATERNAL AGE 8
aphid, Acyrthosiphon pisum (Harris)(Homoptera). In the latter, early-born offspring of wingless aphids were shown to be more sensitive to crowding, subsequently producing more alatae than late-born offspring. The opposite trend was found in the winged form, where alatae were produced only by late-born off• spring. MacKay also provided some interesting theoretical ideas concerning the importance of maternal age as a source of variability in the biology of populations. VARIATION DUE TO MATERNAL AGE 9
Table 1
Literature summary of maternal
age studies in insect species.
SPECIES FACTOR OBSERVATION
Anoplura: Pedi culus Dev. rate -no effect human us Longevity -some early-born offspring lived longer, but there was no effect on mean length of 1 ife Fecundi ty -no effect Survival -only a few generations could be maintained when eggs were selected from very young or very old females References -Flemings and Ludwig (1964)
Coleoptera: S i t o p h i 1 u s Dev. rate -highest for mid-born off• granarius spring References -Howe ( 1 967)
Tenebri o Dev. rate -the larval period decreased moli tor as the mother aged Longevi ty -lowest for late-born off• spring Viability -greatest in eggs from young females References -Ludwig ( 1956), Tracey ( 1958), Ludwig and Fiore (1960,1961)
T e n e b r i o Dev. rate -highest for early-born off• obs curus spring, gradually decreasing as the mother aged Longevi ty -lowest for late-born offspring Size _late-born adults were the smal1 est References -Fiore ( 1960)
Tri bo 1i urn Dev. rate -highest in late-born larvae con fus urn Stress _late-born larvae endured starvation for longer References -Schneider (1940), Raychaud- huri and Butz (1965) VARIATION DUE TO MATERNAL AGE 10
LITERATURE SUMMARY continued
Di ptera: Aedes Longevi ty •lowest for offspring of mid- aegypti born females Vi abi1i ty •lowest for the first egg batches from the offspring of young females Survi val •only a few generations could be maintained when eggs were selected from late-born females References •Liles (1961)
Eretmapodi tes Stress •eggs from young females could chrystogaster withstand desiccation for longer References •Hylton (1967)
Drosophila Longevi ty -highest in early- born offspri ng s ubobs cura Fecundity -highest in early- born offspri ng References -Wattiaux (1968a)
Drosophi1 a Longevity -highest in early- born offspring pseudoobscura References -Wattiaux (1968b)
Drosophi1 a Dev. rate •highest in mid-born offspring me 1anogaster Longevity -highest in early-born offspring; late selected lines suffered most from aging Fecundi ty •early-born females were more fertile than parents and for longer; late-born females were more fertile than parents but had a shorter life span Viability •highest for eggs from middle- aged parents Size •middle-aged parents produced the smallest eggs and produced adults with the smallest wing size References •Robertson and Sang (1945), Durrant (1955), Goetsch (1956), David ( 1 959) , O'Brian (1961) , Butz and Hayden (1962), Par• sons (1962), Wattiaux and Heuts ( 1 963), O'Brian et al_. ( 1 965 ) , Delcour ( 1 969 )
Mus ca Fecundi ty •decreased as the mother aged autumnali s Vi abi1i ty •decreased as the mother aged References •Lodha, Treece and Koutz (1970) VARIATION DUE TO MATERNAL AGE 11
LITERATURE SUMMARY continued
Mus ca Dev. rate -no effect domesti ca Longevi ty -highest for early-born off• spring, gradually decreasing as the mother aged Fecundi ty -highest in mid-born females Vi abi1i ty -lowest for eggs from late- born females .early-born offspring were Stress better able to resist low humi di ti es -only a few generations could Survi val be maintained when eggs were selected from late-born fe- mal es References -Rockstein (1957, 1959), Cal• lahan (1962)
Hemi ptera: Nephotetti x Dev. rate •decreased as the mother aged ci ncti ceps Longevi ty highest in early-born off• spring Fecundi ty •late-born females were more fertile than parents but had a shorter life span Viability •highest for eggs from middle- aged females Size •middle-aged females laid the largest eggs Stress •late-born larvae were least resistant to starvation References •Murai and Kiritani (1970)
Oncopeltus Dev. rate •highest for larvae from middle- fas ci ata aged females Fecundi ty •highest for middle-aged fema- 1 es Viability •highest for eggs from middle- aged females Size .middle-aged females laid the largest eggs References .Richards and Kolderie (1957)
Tri atoma Vi abi1i ty •higher in eggs from young phy11osoma females References •Rabinovich (1972a)
Tri atoma Vi abi1i ty no differences found i nfestans References Rabinovich (1972b)
Hymenoptera: Cryptus Dev. rate -highest in mid-born offspring i nornatus References -Simmonds (1949) VARIATION DUE TO MATERNAL AGE 12
LITERATURE SUMMARY continued
Nasoni a Diapause •late middle-aged and old fema• vitripennis les produced only diapausing larvae References •Saunders (1962, 1965, 1966a, 1966b)
S p a 1 a n g i a Dev. rate •increased in non-diapausing drosophi1ae larvae as the mother aged References •Simmonds (1949)
Lepi doptera: Choristoneura Size •egg size decreased as the s_p_£. mother aged References •Campbell (1962)
Maiacosoma Acti vi ty -the first eggs laid in an p 1 u v i a 1 e egg mass (representing the first eggs produced during the pupal stage) yielded the most active, best oriented larvae References -Wellington (1965), Welling• ton and Maelzer (1967)
Porthetri a Dev. rate -late-born larvae went through d i s p a r an additional moult S i ze .egg size decreased as the mother aged References -Leonard (1970)
Orthoptera: Aulocara Dev. rate -highest for late-born off e 11 i o t i spring Fecundi ty •decreased as the mother aged References •Van Horn ( 1 966) , Vi sscher (1971) VARIATION DUE TO MATERNAL AGE 13
III EXPERIMENTAL DESIGN
Hy1emya anti qua was chosen as the experimental animal for a number of reasons. Firstly, females have been documen• ted as living 35 to 45 days in the field (Hawkes, 1972), with some living longer than 60 days (Miles, 1951). Their offspring therefore have the potential of being influenced by maternal age. Secondly, they are quite fecund, and under optimal condi• tions are capable of producing large numbers of eggs through• out most of their oviposition period. (This was a critical requirement, since a high initial egg density was required to provide a sufficient number of individuals for the various experiments.) Thirdly, all life stages are easily reared in the laboratory. Adults survive well on an artificial diet, and larvae can be reared on commercial onions. Finally, there are several different laboratory strains of H_. a n t i q u a and, in addition, a wild stock can be obtained from infested onions in the field.
Two laboratory stocks (from Simon Fraser University and from the University of Guelph), and a wild stock were used in these experiments. Adults were housed in wooden cages, 36 cm cubed. The base, back, and front of the cage were plywood, and the top and sides were screened with a fine mesh. The flies were provided with water-soaked vermiculite and food consist•
ing of 10 parts skimmed milk powder, 10 parts granulated sugar,
5 parts brewers yeast, 5 parts yeast hydrolizate, and 1 part
soya peptone. Food and water were changed twice per week. VARIATION DUE TO MATERNAL AGE 14
Rearing was done in a controlled environmental chamber maintain• ed at 22°C and a 16-hour photoperiod. There were appr-oximately
100 ovipositing females per cage.
Eggs were collected from young, middle-aged, and old
females (referred to as cohorts 1, 2 and 3, respectively) accord•
ing to the following regime. An onion, approximately 3 inches
in diameter, was cut horizontally and placed cut surface up in a 15 by 10 cm plastic container, partially filled with moist• ened silica sand. The container was placed in a cage with the
females and left for 48 hours. This period was selected for two reasons. Firstly, females exhibited a two-day oviposition cycle. Secondly, beyond 48 hours the onions began to dehydra•
te and egg mortality due to desiccation was high. Females tended to oviposit well inside the onion scales, which helped prevent desiccation for the first two days. After removal from the cage, the onion halves were separated, since the
resulting larval population form the two combined was too large to rear in one container. The onions were moistened, placed
upside down on the sand, and covered (to help maintain a suffi•
ciently high humidity). The larval cultures were checked daily and given more food when necessary.
Three such collections over six days were made per
cohort, beginning 1 week after peak emergence, with each col•
lection period being separated by 12 days. Thus, cohort 1
collections ran from day 7 through 12, cohort 2 from day 25 through 30, and cohort 3 from day 43 through 48. Within each
cohort the eggs were divided into four groups, A to D. VARIATION DUE TO MATERNAL AGE 15
Group A populations were maintained under the same tem•
perature and photoperiod as the stock cultures. Demographic
data (age at the first oviposition, fecundity, longevity,
mortality, sex ratio) were obtained from populations of emer•
ging adults, and cohort collections were made for the succeed•
ing generation. At least two successive generations were
followed to detect differences which might appear only in the
offspring of a particular age class. Group B populations were
raised under the same conditions until the mid-second instar,
at which time they were used in larval dispersal experiments.
Group C populations were taken as three-day old pupae from a
22°C chamber and placed at 3°C for a two-week period, to deter• mine their ability to survive under temperature stress. Group
D populations were raised from an early larval stage under
special temperature conditions (a day temperature of 20°C, a
night temperature of 7°C, and a 16-hour photoperiod) to induce
them to enter diapause. Diapausing pupae were kept at 3°C for
6 weeks, then allowed to emerge normally. In Groups A, C and
D, developmental rate, weight and emergence success were record•
ed.
Since nutrition is known to affect certain character•
istics of the offspring (Rockstein, 1 959 ; David et_ aj_. , 1971),
ample food was provided for both larvae and adults, and its
quality was kept constant.
Unless otherwise specified, results were analysed
using one-way and two-way Analyses of Variance, from the VARIATION DUE TO MATERNAL AGE
*ANOVAR package offered by the Computing Center at the Univer• sity of British Columbia. The data can be divided in three main ways: (1) by provenance group (SFU, Guelph, Field); (2) by population type (demographic, temperature-resistant, diap• ause); (3) by maternal age (or cohort). In the analyses, the data were first examined for provenance and/or population-type differences. If such differences were found to exist then further analyses were performed separately, within the appro• priate subgroups. Otherwise, data were pooled to increase the overall degrees of freedom in testing for maternal-age diffe• rences . VARIATION DUE TO MATERNAL AGE 17
LV THE BIOLOGY OF HYLEMYA ANTIQUA
The life cycle of Hylemya antiqua has been investigated in many different geographic regions of the world and found to be similar throughout, with the main differences being a function of environmental factors (Workman, 1958). In addition, 2 the closely related cabbage root maggot, Hylemya brassicae
(Bouche)(Diptera), has been studied in some detail and is considered quite similar in behavioral characteristics (Finlay- son, personal communication).
Time of spring emergence is a function of temperature and, related to this, depth of puparia in the soil (Workman,
1958; Eckenrode and Chapman, 1971a). The developmental thres• hold for pupae is 6°C and the day-degree accumulation for first fly emergence may vary from 235 to over 300, depending upon exact conditions (Eckenrode and Chapman, 1972). Ideal position in the soil is four inches below the surface. Deeper soil is cooler (delaying emergence) and more compact (increasing the failure rate of flies to reach the surface). Puparia close to the surface are more vulnerable to predation and other adversi• ties (Hughes and Salter, 1959; Eckenrode and Chapman, 1971b).
In British Columbia, emergence occurs during the first warm period of late April or May (Forbes, 1962). (In 1976 flies
For information on reproduction in H_. antiqua, see Appendix I, Secti on B
This species is also referred to as E r i o i sc hi a brass icae. VARIATION DUE TO MATERNAL AGE 18
were seen by April 28th_.) A weather index may be used to
predict the first and succeeding emergence patterns. Male
emergence precedes that of females by one to three days, and
the total length of the emergence period can be quite long,
resulting in considerable overlapping of generations (Workman,
1 958).
Females become receptive for mating only after their
eggs have reached a certain state of development, and will
normally mate only once. This leads one to ask whether the last
eggs produced by the female are fertilized, or if mating is a
required stimulus for egg production. Experiments conducted by
Missonnier and Stengel (1966) indicate that a female does
receive a sufficient quantity of sperm at the beginning of her
reproductive life to fertilize all the eggs she can produce.
Mating is not a prerequisite for egg production, but in the
absence of males many ovarioles become non-functional. Mating may be a stimulating factor in oviposition.
Temperature dictates when egg production will begin
after emergence, and how rapidly it will take pi ace-although once eggs are deposited in the soil and larvae reach the host
plant, they are sufficiently buffered that their development
is little affected by adverse conditions (Missonnier and Sten•
gel, 1966). It seems sufficient for normal egg production that
the individual be exposed to only a few hours of optimal
temperatures. However, this optimal range for H_. anti qua is
relatively narrow. Slightly above it, egg production is main• tained but viability drops off rapidly. Below it, both egg VARIATION DUE TO MATERNAL AGE 19
production and viability decrease (Missonnier and Stengel, 1966).
Rate of development of eggs varies among flies but re• mains fairly constant for each fly (Swailes, 1961). The flies
have a relatively long period of egg maturation, presumably cor• responding to their dispersal phase, during which they search for the appropriate host. The overwintering population need not be large for the spring population to do a great deal of damage, for they have a powerful ability to increase rapidly once they have found a sufficient quantity and quality of host plants. It is not known what proportion of females are unable to find ade• quate nutrition, but Missonnier and Stengel (1966) noted that all the spring females they captured in the field had normal ovaries fully developed, with no indication of resorption. Adults obtain water from dew (in abundance throughout the season), glucose from plant nectar or sap from trees or leaves, and proteins from pollen.
Males are capable of mating from two days of age until near death, and in the absence of competition a single male can inseminate up to seventy females (Finch and Skinner, 1973b).
Although they do not require food to begin sperm production, they must obtain proper nutrition to sustain it (Missonnier and Sten• gel, 1966). There is no relationship between age of the male and frequency of mating or fertility (Swailes , 1971 ) . Natural ste• rility averages 8% (Finch and Skinner, 1973b). Finch and Skin• ner (1973a) examined a large number of females collected from the field under a wide variety of conditions, and found the majority of them to be gravid, indicating that it is usually easy to find mates . VARIATION DUE TO MATERNAL AGE 20
Oviposition begins six to eight days after emergence and
continues until near death (Coaker and Finch, 1971). There are
some discrepancies in reports of average female longevity in the
field. It has been reported by Foott ( 1 954) as 29 days, but
between 35 and 45 days by Hawkes (1972). This variation may be
due to the different geographic locations in which the studies were conducted, specifically with respect to temperature. Some
females may live as long as 63 days (Miles, 1951). Total egg pro• duction is a linear function of time (i.e., egg. production does
not decrease as the female ages); however, viability begins to decrease once the mother approaches 40 days of age (Missonnier and Stengel, 1966). Viability for younger females varies between
86-96% under both laboratory and field conditions (Hughes and
Salter, 1959; Swailes, 1961; Finch and Coaker, 1969). Average egg production per female under laboratory conditions is 371 (Har• ris and Svec, 1966). Oviposition occurs on warm, sunny days (18-
21°C) in late afternoon (Miles, 1954; Eckenrode and Chapman, 1972).
In British Columbia, three definite peaks can be identified (May, mid-June to mid-July, mid-August to mid-September (Forbes, 1 962)).
Eggs are laid in the soil within a few centimeters of the host plant. Once eggs hatch (2-3 days after oviposition) very few^ larvae fail to find a host plant, assuming soil moisture is ade• quate. First-instar mortality may be as high as 63%, however, due to failure to become established (Hughes and Mitchell, 1960; Coaker and Finch, 1971). This failure may be related to the density of larvae already supported by the host plant and the amount of de• composition which has occurred; e.g., Workman (1958) has suggested that infested onions become broken down and water-soaked, giving VARIATION DUE TO MATERNAL AGE 21
an added dampness to the surrounding soil that promotes survival of young maggots. The majority of maggots (88%) remain within the same row of the host crop, usually settling on the first plant encountered. Some, however, cross between rows separated by as much as 14 inches before settling (Sleesman and Gui, 1931;
Workman, 1958). Second- and early third-instar larvae are res• ponsible for most of the movement in the field. The location of new host plants appears to be by chance, and depends upon the maggots' ability to move in the soil (Workman, 1958). The ave• rage duration of the three-instar larval period is 12 to 15 days at 25°C (Niemczyk , 1 964) .
Late third-instar larvae leave the host plant and burrow into the surrounding soil, where pupation takes place. Soil moist• ure is important in larval eclosion and survival in the soil
(Workman, 1958). There is no pupal diapause during the first generation. About 50% of the second-generation pupae diapause, the remaining giving rise to the third and final generation (Muk- erji and Harcourt, 1970). The non-diapausing pupal period is 9 to 14 days (Workman, 1958; Niemczyk, 1964).
Eggs are the stage most vulnerable to predation due to their exposed position and lack of motility. After larvae enter a host plant they gain a certain degree of protection (Read,
1 962). Mites, ants, carabids (notably Bembidion quadrimacul atum
(Say) and B . n i t i d u m (Kby.)(Col eoptera)) and staphylinids (Phi-
1 on thus spp. and Aleochara b i1i neata)(Gryll.)(Coleoptera)) prey on eggs and larvae. A. bi1i neata is particularly important, since it has a very high biotic potential compared with H_. antiqua VARIATION DUE TO MATERNAL AGE 22
and also because it acts as a parasite as well as a predator.
Adults destroy root-maggot eggs and larvae, and the parasitic larvae destroy root-maggot pupae (Wi shart e_t aj_. , 1 956 ; Read,
1962). Potentially, this source of mortality could be an impor• tant controlling factor, but adequate control rarely occurs-either because the predators are not present in sufficient numbers to cause real damage, or, in the case of A.biiineata, because the life cycles of prey and predator do not coincide at times when control would be most devastating (i.e., in the spring). There is little documented information on predation of adult Hy1emya, although many non-specific predators, such as hornets, are pre• sent at the same time and in high numbers (Workman, 1958). Initial adult mortality after emergence is high, followed by a period of relatively high survival until 25 and 35 days of age for males and females respectively (Workman, 1958).
The main kind of density-dependent mortality is that cau• sed by death of the host. When egg mortality is low, larval density rapidly increases. The plant may be unable to support such dense populations, and larval mortality due to lack of food ensues (Read, 1962). Denser plantings are able to support
larger larval populations, in spite of the fact that individual roots are smaller. Gravid females, in fact, are more attract• ed by thicker stands (Workman, 1958).
Workman (1958), in examining records of infestations and climatological data together with his own data on moisture requirements in H_. antiqua, concluded that high precipitation
in a prerequisite for high larval survival and, hence, for VARIATION DUE TO MATERNAL AGE
heavy damage, Heavy damage, then, could possibly be predicted from weather reports, the critical periods being the times of oviposition and hatching from the eggs. VARIATION DUE TO MATERNAL AGE 24
V " DEMOGRAPHIC FACTORS
1. Fecundity And Mortality
1.1 Introducti on
This experiment was designed to compare rate of egg production, length of the egg-laying period, and mean expect• ation of life among the offspring of young, middle-aged, and old females. These three factors, operating together, determine the contribution of a given individual to the rate of increase of the population. They may act in a compensatory fashion, in that the same net contribution may be made by two individuals, one with a high rate of egg production but short egg-laying period (or expectation of life), and the other with a lower egg-producing rate but longer period of oviposition.
However, two such individuals, although potentially contribut• ing the same number of eggs over a given period of time, may not actually be equivalent. Mean expectation of life may be affected by oviposition activity. The longer the period of time taken to produce and lay a batch of eggs, the longer the female will be exposed to hazards. On the other hand, fecund• ity puts a strain on parental metabolism, rendering the parent more susceptible to unfavorable conditions, thereby increasing the probability of dying (Calow, 1973). Thus, if females are producing eggs at a fast rate, exposure time in depositing an egg batch might be less, but so might be resistance to hazards. VARIATION DUE TO MATERNAL AGE 25
Variation in the number of days from emergence to first
oviposition may be a means of increasing the total length of
the reproductive period. The length of the pre-oviposition
period in the field is a function of temperature (Missonnier
and Stengel, 1966), although maternal age may also have an
effect.
The populations from which mortality and fecundity
data were collected were kept relatively similar in size (100±
20 ovipositing females), to avoid any density-dependent
effects. In certain species, density has been shown to mark•
edly influence egg production. For example, in a reduviid
vector of Chagas1Disease, Triatoma infestans (Klug)(Hemiptera)
(Rabinovich, 1972b), females maintained individually produced
650 eggs per time period, but only 55 when reared together
with 20-39 other females.
Age-specific mortality should be high at conception,
fall to a minimum during pre-reproductive life, then increase
with age after first reproduction. Fecundity should increase
following the first reproductive capability and then fall off
progressively with age (Emlen, 1970). According to Emlen (op.
cit.) the main selective forces for successful reproduction
(which involves selection for congenitally healthy young) will
occur as soon as reproduction begins in the life history, and
will fall off with age. Therefore, progeny from older indivi•
duals, regardless of their numbers, will be expected to be
less healthy (or more mortality-prone) than progeny from
younger parents. Where maximum reproductive rate occurs early VARIATION DUE TO MATERNAL AGE 26
in life, there will be no selection acting to keep physiologi• cal processes viable later in life, accentuating a further drop in fecundity with age. Some of these predictions could be examined in antiqua with the fecundity and mortality data col 1ected.
1.2 Materials and Methods
Females of 14. antiqua require olfactory and tactile stimuli for oviposition (Ticheler, 1969). The first is obtain• ed from the onion plant and the second is provided by some kind of support for the ovipositor. The device used in the laboratory consisted of a petri dish lined with moist filter paper, and a small container filled with pieces of onion.
Around the rim of the container, small notches (l-2mm) were cut, and then it was placed upside down on the filter paper.
The notches were too small for the females to pass through them and oviposit directly on the onion. They oviposited instead on the filter paper just inside the rim of the container. The petri dish was removed after a given period and the eggs were counted with the aid of a dissecting microscope. Since the eggs begin hatching after two to three days (Workman, 1958), this period was never longer than 48 hours. However, to ensure that no hatched larva could crawl to the onion, the plants were suspended from the top of the container in a piece of cheese cloth.
The number of days between emergence and first ovi• position was recorded, and egg-laying data were collected VARIATION DUE TO MATERNAL AGE 27
every two days thereafter throughout the reproductive life of
the population. At each collection, dead adults were removed,
sexed, and counted. This provided age-specific mortality data
which were used to calculate mean expectation of life. Initial
adult density was known, and the sex ratio was obtained as the
flies died and could be sexed. The mean rate of egg production
per female was calculated from the total number of eggs produc•
ed per unit time by the population as a whole and the average
number of females present during that period.
1.3 Results
Data on mortality and fecundity were first analysed for
provenance effects. No significant differences were found among SFU and Guelph populations, so further analyses were performed on data pooled from these provenance groups. Indivi• duals from field populations, on the other hand, were much less fecund. Their mean egg production per female per 48 hours was only 5.7 (±3.42 ) eggs, as compared with 11.9 (±2.81) eggs for individuals from both SFU and Guelph populations. Unfortun• ately, cohort sample size within field populations was not sufficiently large to allow these data to be analysed on their own.
Pre-oviposition period did not vary across provenance
(mean = 9.6 ± 1.44 days) or cohort (mean = 9.6 ± 2.30 days),
l The measure of dispersion used in this text is the standard deviation. VARIATION DUE TO MATERNAL AGE 28
indicating that maternal age does not indirectly alter the total length of the reproductive span through effects on the commen• cement of egg laying.
The mortality data collected provided the necessary information to construct a horizontal life table (Krebs, 1972).
To compare overall mortality behaviour, two different types of information from the life table were analysed. The first was the probability of being alive at age _x (Lx = Ix/lo, Rabino- vich, 1972a), and the second was the mean expectation of life at age x, or the number of days that remained to be lived by an individual after attaining age x (i.e., Ex). To detect differences in the mortality pattern across a time scale, Lx and Ex values were compared for every 10-day period up to an age of 50 days. Only female age-specific mortality was analys• ed since it is more directly related to the dynamics of the population as a whole.
The overall mean expectation of life when a fly first emerged from the puparium (EO) was 17.3 days. Significant cohort variation was found (probability = 0.02), mainly due to the shorter life expectancy of cohort 3 females. When cohorts
1 and 2 were pooled in the analysis; the, probabi1ity dropped to 0.005, indicating, that the differences observed in mean expectation of life between cohorts 1 and 2 versus cohort 3 are statistically real. See Table 2 for these results. A fly
10 days old, on average, can be expected to live another 14.1 days. No significant differences in E10 were found, although there were indications of a similar trend to that found for E0. VARIATION DUE TO MATERNAL AGE 29
TABLE 2
Mean Expectation of Life (E) at age _x, with standard deviations. Age is given in days. Analysis of Variance information for these data is given in Appendix II, Table I
FACTOR OVERALL COHORT COHORT STANDARD PROBABILITY (Ex) MEAN MEANS DEVIATION
EO 17.28 1,2 18.21 1.754 0.005 3 15.68 1.697
E10 14.10 1,2 14.41 1.439 0.207 3 13.56 1.284
E20 10.74 1,2 11.13 1.203 0.072 3 10.07 1.174
E30 7.15 1,2 7.71 1.436 0.040 3 6.20 1.547
E40 3.16 1 4.36 1.619 0.018 2 3.03 1.584 3 1.86 1.555 VARIATION DUE TO MATERNAL AGE 30
At age 20, a significant cohort difference was found when cohorts
1 and 2 (which did not differ from each other) were pooled and tested against cohort 3. The overall mean expectation of life was 10.7 days, whereas the level mean for cohort 3 was slightly less, and that for cohort 1 slightly more. The same trends were found at age 30 and 40 days; i.e., mean expectation of life was significantly higher for cohorts 1 and 2 than for cohort 3. Note that in the latter case all three cohorts dif• fered from each other. The overall mean was 3.2 days, with cohort
2 very close to this, cohort 1 greater, and cohort 3 less.
In conclusion, mean expectation of life is influenced by maternal age. Offspring from young and middle-aged mothers tend to have a longer life expectancy than do offspring from older mothers. The differences were most pronounced at the beginning of adult life, and again towards the end.
The probabilities of being alive at ages 10, 20, 30, and 40 days all showed significant differences. These results are given in Table 3. Female offspring from middle-aged mothers had a higher probability of being alive at all ages than did the offspring from older mothers. These differences were significant at least at the 0.05 probability level. Offspring from young mothers had a significantly higher probability of being alive at ages 10 and 20 days than did cohort 3 offspring
(i.e., the trend was the same as in cohort 2). However, between 20 and 30 days of age the mortality rate of cohort 1 offspring began to increase, causing the probability of being alive at age 30 days to decrease markedly. From this point on VARIATION DUE TO MATERNAL AGE
TABLE 3
Probability of Being Alive (L) at age with standard deviations. Age is given in days. Analysis of Variance information for these data is given in Appendix II, Table II.
FACTOR OVERALL COHORT COHORT STANDARD PROBABILITY (Lx) MEAN MEANS DEVIATION
L10 0.89 1,2 0.92 0.050 0.002 3 0.83 0.076
L20 0.77 1,2 0.80 0.076 0.028 3 0.72 0.063
L30 0.67 1,3 0.64 0.077 0.018 2 0.75 0.106
L40 0.56 1,3 0.53 0.095 0.023 2 0.65 0.119 VARIATION DUE TO MATERNAL AGE
the probability values for cohorts 1 and 3 were statistically
the same.
To summarize, female offspring from older mothers
throughout their lives have a lower probability of being alive
at some point in the future than do the progeny of middle-aged
mothers. This difference is most pronounced during the first
10 days of life. Offspring from young mothers pass through
their first 20 days with a comparatively low mortality rate
(similar to that found in cohort 2), which then begins to
increase quite rapidly, eventually becoming on a par with that
for cohort 3. The lower mortality rate of offspring from middle-aged mothers is maintained throughout life.
Age-specific fecundity data were analysed in two ways,
one to give on overall indication of egg-laying potential
throughout the reproductive span, and the other to allow for
detection of differences in the rate of egg-laying through
this time span. No one statistic could sufficiently express
all the relevant information. Figure 1 gives a graphic
description of fecundity characteristics in the three cohorts.
The indicator of overall performance was the average
number of eggs laid per female per 48 hours. These values were calculated by averaging the fecundity rates per 48-hour
period from the day when egg production began until it ceased.
Cessation of egg production was considered to be the day after
which there were at least three consecutive periods with no
oviposition. All three cohorts differed significantly in VARIATION DUE TO MATERNAL AGE 33
Figure 1
Reproductive characteristics (in terms of cumulative eggs/female) of early-, mid- and 1 ate-born females Days VARIATION DUE TO MATERNAL AGE 35
average fecundity (probabi1ity= 0 .008) . The overall mean was
11.9 eggs. Offspring from young mothers were much more product•
ive than this (averaging 17.4+5.24 eggs), whereas offspring
from old mothers were less fecund (averaging 7 .9 ± 1.22 eggs).
Egg production in mid-born offspring was close to average (10.7
±1.94 eggs). See Appendix II, Table III, for analysis of
vari ance res ults .
The second factor analysed was the mean rate of egg
production per female per 48 hours during given intervals (i.e.,
1-10, 11-20, 21-30, and 31-40 days) throughout the reproduct•
ive period. Due to the large degree of variability within
cohort 2 populations, significant differences in egg product•
ion between these females and those from either cohorts 1 or 3
could not be established. However, these latter groups did
show interesting differences (Table 4). During the first
10-day period, egg production was greater than the overall mean
of 14.4 eggs for cohort 1, and less than this for cohort 3,
although the probability of this difference being due to chance
alone was 0.18. From 11 to 20 days the discrepancy in egg
production was greater ( probabi 1 i ty= 0 .03), and even more pronoun•
ced for the 21-30 day interval (probabi1ity-0.005). At this
point the variability about the level means was the least.
During the final periods (31-40 and 41-50 days) egg production was very similar in the two groups.
There was consistently greater variability in egg
production among mid-born females, as indicated by their larger
standard deviations. In addition, it should be noted that egg VARIATION DUE TO MATERNAL AGE 36
TABLE 4
Mean rate of egg production per female per 48 hours for five different ranges of age. Age is given in days. For complete Analysis of Variance information see Appendi x II, Table IV .
AGE OVERALL COHORT COHORT STANDARD PROBABILITY (x) MEAN MEANS DEVIATION
1-10 14.36 1 16.37 6.570 0.182 3 12.02 4.245
11-20 15.59 1 18.41 5.587 0.028 3 12.28 3.023
21-30 14.67 1 17.89 4.609 0.005 3 10.91 1.722
31-40 14.62 1 13.90 4.920 0.475 3 15.47 1.934
41-50 9.17 1 10.27 5.029 0.290 3 7.88 1.941 VARIATION DUE TO MATERNAL AGE 37
production in cohort 1 females reached a maximum level by 20 days (18.4 eggs), which was maintained until age 30 days and then began to decline slowly. By contrast, egg production in cohort 3 females plateaued from ages 10 to 30 days at an average of 11.6 eggs per female per 48 hours, then increased to a maximum at age 40 days (15.5 eggs), dropping off rapidly immediately thereafter.
To summarize the relevant results, offspring from middle-aged mothers had the lowest sustained mortality rate throughout life. This rate was initially low in early-born mothers as well, but began rising around mid-life (30 days of age), eventually becoming comparable with that for older mothers, which was high throughout life. Early-born mothers had the highest probability of being alive at points early in life, and again towards its end. They also showed a significantly higher net rate of egg production per female per 48 hours throughout life. Older mothers produced less fecund offspring, and these differences were most pronounced during the mid- reproductive period.
2. Developmental Rate And Survival
2.1 Introduction
The purpose of this experiment was to determine the effect of maternal age on developmental rate and survival in larvae and pupae. The effect of the mother's age on egg viability in H^. antiqua has already been reported in the VARIATION DUE TO MATERNAL AGE 38
literature by Missonnier and Stengel (1966). They found that
as the age of the mother increased beyond 40 days, viability
began to decrease, although up to this age 86-96% of a female's
eggs would hatch. Viability depends firstly on successful
fertilization of eggs, and it may be that even though the
spermathecae of senescent females contain a sufficient quantity
of viable sperm (Missonnier and Stengel, 1966), the number of
functional micropylae in the chorion begins to decrease in old
age. This reduction would decrease the probability of fertil•
ization and account for the observed drop in viability, as was
found to be the case in the reduviid Rhodni us spp. (Hemiptera)
by Romoser (1973).
Since density of the adult population is known to
affect viability of eggs in certain species (e.g., in the beet
fly, Pegomyia betae (Curt.)(Diptera) (Missonnier and Stengel,
1966)), the number of individuals per cage was kept relatively
constant in these experiments.
Due to the techniques used in collecting eggs for rear•
ing (see Experimental Design), it was difficult to determine
accurately when hatching began. The eggs had been deposited well within onion tissue, and newly hatched larvae were not
easy to see. For this reason, total number of days from egg
to pupa was taken as the indicator of pre-pupal developmental
time.
Zinforlin (1969) found that rearing density affected
number of days to pupation in larvae of the flesh fly Sarco-
phaga barbata (Park.)(Diptera). Fewer days were taken to VARIATION DUE TO MATERNAL AGE 39
pupate when larval density was high. Food quality and quantity may also affect developmental rate as well as survival (Rock- stein, 1959). If food is limiting, a larva might pupate earlier than if food were plentiful. Therefore, larval density per con• tainer was maintained within certain limits (although' it could not be kept exactly equal), and food was offered in ample amounts.
Since neither number of eggs laid nor number of larvae hatched was known, survival through this initial period could not be determined directly. However, larval success could be indirectly assessed by survival and eventual emergence of the resulting pupa. As a result of normal biological variability
(and perhaps interactions among other factors), few individuals molt synchronously, even if they develop from eggs laid simulta• neously (Rabinovich, 1972b). Therefore, as development continues there will be a larger and larger overlap between stages, such that individuals with the same calendar age may belong to differ• ent instars or even different stages. What effect might these differences have on survival? For example, does a pupa which spent 20 days as a larva have the same probability of surviving as a pupa which spent only 14 days as a larva? With data on de• velopmental period from egg to pupa and the resulting pupal emer• gence success, questions such as this can be examined. If mater• nal age affects developmental rate, it may, in addition, indi• rectly affect survival at some later point.
2.2 Materials and Methods
Egg collections were made as described in the Experi- VARIATION DUE TO MATERNAL AGE 40
mental Design section, with the following alteration. In an
effort to maintain a relatively uniform larval density, the
onion halves in the collection trays taken from the older
cultures were not separated, so the resulting larvae were
reared together. Otherwise, density within these containers would be much lower than in those from young and middle-aged
females, because (1) egg viability decreases markedly when the mother passes 40 days of age, and (2) total egg production is
lower in older cultures since there are fewer females alive.
The larval cultures were given ample amounts of food,
and checked daily for pupation. When larvae were ready to
pupate they would crawl out of the onion and into the surround•
ing sand. Therefore, the presence of pupae could be checked without disturbing the remaining larvae - an important fact,
since third-instar larvae tend to pupate early if disturbed
(Workman, 1958). The times when pupation began and ended, and when maximum pupation occurred were recorded. Pupae were
collected by placing the sand in a sieve and washing it with water, thus removing the sand while leaving the pupae on the
sieve. They were counted and placed on a moist piece of
filter paper in a container to await emergence. The number of
flies which successfully emerged were then sexed and counted,
and the remaining puparia were examined to determine the number which were not viable, or from which emergence was not success•
fully completed. VARIATION DUE TO MATERNAL AGE 41
2.3 Results
The following analyses of egg to pupal period include
the data collected for temperature-resistant populations, since
these has been raised under the same conditions as the demogra•
phic cultures, up to the time of pupation. Significant prove•
nance differences in developmental rate were found at the 0.05
probability level (Table 5,A(1)). Field-derived populations had
the shortest developmental period and the least variability.
Developmental period in SFU-derived populations was equal to the overall mean, with populations from Guelph seeming to take the
longest to develop, and showing the greatest amount of varia•
bility. These latter two provenances did not, in fact, differ significantly from one another, although they both differed from
field populations. Field populations were therefore not includ•
ed in the analyses of cohort differences. They could not be
examined alone because sample size within each cohort group was too small.
Significant cohort differences were found with a proba•
bility of 0.08, showing that cohort 3 took the least time to
develop. Cohorts 1 and 2 did not differ from each other, and when these data were pooled and re-tested against cohort 3, the
probability of obtaining such a difference by chance alone dropp-
ed to 0.05 (Table 5, A(2)). These results indicate that off•
spring from older mothers develop faster than offspring from either middle-aged or young mothers, and therefore that popula•
tions composed primarily of older females would have a shorter mean generation time. VARIATION DUE TO MATERNAL AGE 42
TABLE 5
A = Developmental period from egg to pupa, in days, for demographic (DEMO) and temperature- resistant (TEMP) populations combined, and for diapause (DIAP) populations. Data were analysed within provenance and cohort groups.
B = Developmental period from pupa to adult emergence from puparium, in days, for temperature-resistant and diapause populations. Analysis of Variance information is given in Appendix II , Table V.
POPULATION OVERALL SOURCE OF LEVEL STANDARD PROBABILITY TYPE MEAN VARIATION MEANS DEVIATION
A(l) DEMO, 17 .8 SFU 1 7 .8 2 . 32 0 .041 TEMP GUELPH 19 .5 3 .74 FIELD 15 .5 1 .09
(2) DEMO, 17 .7 COH 1 ,2 18 .0 2 . 54 0 .057 TEMP COH 3 1 6 .9 1 .96
(3) DIAP 24 . 7 SFU 23 .8 4 . 1 5 0 .077 GUELPH 26 .7 4 .26 FIELD 23 .6 4 .16
(4) DIAP 24 .2 COH 1 25 .7 4 .84 0 .232 COH 2 24 .2 3 .84 COH 3 22 . 7 3 .20
B(D TEMP 1 1 .19 COH 1 11 .04 2 . 506 0 .162 COH 2 12 .12 2 .736 COH 3 10 .36 2 .499
(2) DIAP 11 .48 COH 1 12 .08 2 .985 0 .540 COH 2 10 .82 2 .442 COH 3 11 .40 2 . 793 VARIATION DUE TO MATERNAL AGE 43
There were no significant provenance differences in emergence success from puparia, so these data were pooled to increase the degrees of freedom in testing for cohort differ• ences. Total percentage emergence (i.e., of males and females combined) is not significantly affected by maternal age-the overall mean being 72.06% (Table 6, A(l)). However, a signi• ficant cohort trend in percentage of females was found
( probab i 1 i tys'QfJl ) . In cohort 1, 55% of the successfully emer• ged individuals were female, as compared with 47% and 46% from cohorts 2 and 3, respectively. These latter groups did not differ from each other, and when they were pooled and re-tested against cohort 1, the probability level dropped to 0.004 (Table
6, B(1 )) .
Maternal age thus has an influence on sex ratio, and populations derived mainly from young mothers will have a higher proportion of females than those derived from either middle-aged or older mothers. It is not likely that these sex ratio differences are related to the differences in develop• mental rate reported above. That is, the shorter develop• mental time found for cohort 3 is probably not responsible for, or related to, the lesser proportion of females in populations of emerging adults. If this were the case, then cohort 2 would either be expected to have as short a developmental period, or a greater proportion of females. VARIATION DUE TO MATERNAL AGE 44
TABLE 6
A = Total percentage emergence from puparia for all population types (DEMO = demographic, TEMP = temperature-resistant, DIAP = diapause).
B = Percentage of emerged individuals which are female, for all population types. Analysis of Variance information is given in Appendi x II, Table VI.
POPULATION OVERALL COHORT COHORT STANDARD PROBABILITY TYPE MEAN MEANS DEVIATION
A(l) DEMO 72 .06 1 68.92 18.798 0 . 597 2 75 .47 20.815 3 72 .45 16.844
(2) TEMP 64 .87 1 65 .26 1.4.304 0 .990 2 64.74 24.455 3 64.38 18.855
(3) DIAP 67 .98 1 68.22 15.481 0 .422 2 70 .20 15.509 3 62.00 21.393
B(l) DEMO 50 .83 1 54.98 8.700 0 .004 2,3 46 .68 9.454
(2) TEMP 43 .68 1 50. 74 11 .170 0 .020 2 40.45 12.781 3 40 .42 11 .848
(3) DIAP 42 .66 1 48.45 9.123 0 .087 2 44.79 10.603 3 40 .87 7 .875 VARIATION DUE TO MATERNAL AGE
VJ_ PHYSIOLOGICAL FACTORS
1.- Resistance To Environmental Stress
1.1 Introducti on
This experiment was designed to compare the degree to which offspring from mothers of different ages are buffered
against environmental stress of various kinds. The effects of
applying two types of stress were investigated-1ow temperature
on pupae, and starvation on adults.
Aestivation (a state of arrested development) is one means of coping with unfavorable environmental conditions. It
differs from diapause in that it represents an immediate reac•
tion to adverse conditions, and does not require advance
preparation. Diapause, on the other hand, involves a complex
series of physiological changes that are triggered by environ•
mental factors correlated with the onset of adverse conditions
These factors need not in themselves be unfavorable (Romoser,
1973).
Ability to aestivate is one means of increasing cold
tolerance which may result in an increased geographic range
for the species (Casagrande and Haynes, 1976). In addition,
it can promote survival in the face of extreme fluctuations
in environmental conditions, outside the normal limits of
favorabi1ity. The probability of encountering such conditions
is not uniform throughout the season, but will be higher
during periods associated with more abrupt changes in some VARIATION DUE TO MATERNAL AGE 46
factor.. Temperature, for example, changes more drastically over a given period in the spring, when flies first emerge, than it does during mid-summer. Life stages living in relat•
ively protected areas, such as the soil, may not be affected by short drops in temperature, but a cold spell of longer duration could cause serious damage unless some individuals were able to cope. Similarly, food may be scarce only at certain times in a season, and at those times, flies that can survive the longest without food are the ones most likely to survive. In other words, the chances of encountering adverse conditions may occur at times which are predictable, within certain limits. Maternal age could be responsible for the production, at those times, of individuals best able to cope.
In addition, since at any one time (especially as the season progresses) a population will contain females in many age groups, a maternal-age effect on offspring resistance to stress would act as a buffering agent for the population as a whole through spreading of risk.
Parsons ( 1 962), working with the fruit fly Drosophi1 a melanogaster (Meig.)(Diptera) , found that developmental stability in offspring changed parabolically with the age of the mother (i.e., it decreased to a r: i n i r: u r, early in life and then increased to a maximum), and that during the time of maximum stability, the individual was best buffered against environmental stress. Schneider (1940) found in the flour beetle Tribolium confusum (Duval)(Coleoptera), that late-born
larvae were able to resist starvation for longer periods than VARIATION DUE TO MATERNAL AGE 47
the early-born. On the other hand, late-born larvae of the green
rice leafhopper, Nephotettix ci neti ceps (Uh1er)(Hemiptera) , were the least resistant to starvation (Murai and Kiritani,
1 970). In the housefly, Musca domestica (L .)(Diptera) , early-
born offspring were best able to resist low humidities (Calla•
han, 1 962) and, similarly, eggs from young female Eretmapodi tes
chrystogaster (Graham)(Diptera) could withstand desiccation
for longer (Hylton, 1967). In examining cold tolerance in the
cereal leaf beetle, Oulema melanopus (L.)(Coleoptera) , Casagran-
de and Haynes (1976) found that differences among individuals
were important in determining mortality due to low temperature
exposure. They did not, however, identify the source of these
di fferences .
1.2 Materials and Methods
After pupae have reached a certain point in develop•
ment, they can be directly placed at 3°C and stored for a
period of time. The low temperature arrests development
completely, without inducing diapause. When they are again
placed at higher temperatures, development resumes and flies
emerge after the same number of warm days as when no cold
storage occurs (Ticheler, 1969). Emergence success has been
shown to be a function of state of development before storage
is initiated, and length of time stored (Workman, 1958; Tiche•
ler, 1969). Therefore, to enable comparisons to be made
between populations, these factors were kept constant. VARIATION DUE TO MATERNAL AGE 48
Cold storage was initiated at day 7 of pupal life, and maintained for 2 weeks. After removal, the pupae were first weighed and then allowed to emerge. Time taken for emergence
to begin, and emergence success (in terms of the percentages
of successful male and female individuals) were recorded. Some
of the pupae were reared as adults at 22°C and a 16-hour photo•
period to determine the effect of aestivation on their age-
specific fecundity and mortality characteristics.
Starvation experiments were performed on adult flies
under standard temperature and photoperiod conditions (see
Experimental Design). The flies were given water but no food,
and the number dying each day was recorded.
1 .3 Results
Days taken to emerge after removal from cold storage
seemed to vary across cohort, with cohort 3 taking the least
time and cohort 2 the longest. However, the probability was
0.16 (Table 5, B(l)), so the differences were not pronounced.
A very similar trend was found for the egg-to-pupa develop• mental period (Table 5, A(2)). This period was shortest for
cohort 3 cultures and longest for cohorts 1 and 2. So even
though significant differences in developmental period from
pupa to adult were not found here, perhaps there should be
more investigation before concluding that no difference exists.
There were no differences in percentage emergence
across provenance groups, so these data were pooled to increase
the sample size for cohort analyses. Total percentage emergence VARIATION DUE TO MATERNAL AGE
(overall mean = 65%) did not vary significantly among the
cohorts (Table 6, A(2)), but as in demographic and diapause
populations, the sex ratio of emerging adults showed variation
(probability = 0.02, Table 6, B(2)). Cohort 1 contained 51%
females, but within cohorts 2 and 3 the proportion of females was only 40%. .The variability about the level means was much
higher for temperature-resistant populations than for either
demographic or diapause populations.
The age-specific fecundity and mortality data did not
show significant differences across population type. These
data were then pooled and analysed together. The results
have been discussed in previous sections (Tables 2, 3, 4,
and 7) .
For the starvation experiments, there were no differ•
ences in population longevity, although death rate was found
to vary among the cohorts. In cohort 3, the majority of in•
dividuals died within the first 5 to 7 days, whereas in cohort
2 more individuals were able to resist starvation longer.
Here, the greatest mortality rate was experienced after 10
days of age. Cohort 1 was intermediate, showing its heaviest
mortality from 5 to 9 days of age. Therefore, although there
are some hardy individuals produced by females of all ages,
mid-born offspring seem generally more robust, in that a great
er proportion were able to survive longer in the absence of
food. Figure 2 shows the survivorship curves for the three
cohorts during the course of the experiment. VARIATION DUE TO MATERNAL AGE 50
0 I 2. 3 4- 5 6 7 8 *» IO (f 12 Days
Figure 2
Survivorship curves for cohort populations given water but no food from the time of emergence. VARIATION DUE TO MATERNAL AGE 51
2. Size
2.1 Introduction
It was felt that size would be an important character•
istic to investigate because of its possible effects on fecund•
ity. A small female will either lay fewer eggs of the same
size, or as many eggs but of a smaller size, than a large fe•
male of the same species. An individual may be small for
different reasons; e.g., because its parents were small, or
because of unfavorable environmental conditions during the
larval stage which caused it to pupate early at a smaller size
than normal, or because of a smaller amount of yolk in the egg
from which it developed, as a result of the age of the mother
when she produced the egg. If egg size is affected by mater•
nal age, fecundity differences could appear later as an in-
di rect result.
The age of the mother has been shown to affect the
size of her offspring in a variety of ways. In the mealworm,
Tenebrio obscurus (Fabricius)(Coleoptera) , late-born adults were found to be the smallest (Fiore, 1960). In the green
rice leafhopper, Nephotettix cincticeps (Uhler)(Hemiptera)
(Murai and Kiritani, 1970) and the milkweed bug, Oncopeltus
fas ci ata (Dal 1 as)(Hemiptera)(Richards and Kolderie, 1 957 ),
the largest eggs were laid by middle-aged females. In the
budworm Chori stoneura spp. (Lepidoptera)(Campbel 1 , 1 962) and
the gypsy moth, Porthetria dispar (L .)(Lepidoptera) (Leonard,
1970) egg size decreased as the mother aged. Finally, in VARIATION DUE TO MATERNAL AGE 52
Drosophila melanogaster middle-aged parents produced the
smallest eggs and adults with the smallest wing size (David,
1 959 ).
In Hylemya, pupal weight was used as an index of size.
Since pupae from all three population types were weighed, it was possible to compare not only the effect of maternal age within any one group but also to test for differences in size
due to different rearing regimes. An effort had been made to
keep the larval cultures about equal in size, since crowding
causes larvae to pupate early and increases competition for
the available food - both of which affect pupal size.
2.2 Materials and Methods
The weight in grams (accurate to 5 decimal places on
a Mettler H20T scale) of week-old pupae from demographic,
temperature-resistant, and diapause populations was taken to
calculate an average weight per pupa. Since pupae cannot be
sexed, it was not possible to obtain separate weight estimates
for males and females. These data were used to compare
relative sizes of individuals among populations.
2.3 Results
A significant difference in pupal weight was found
among the three provenance groups (Table 7), with SFU pupae
the smallest and field pupae the largest. Further tests
revealed that this difference was between SFU-derived cultures
versus Guelph- and field-derived cultures combined. These VARIATION DUE TO MATERNAL AGE 53
TABLE 7
Pupal weight in grams, pooled over population type. Analysis of Variance statistics are given in Appendix II, Table VII
FACTOR OVERALL LEVEL MEANS STANDARD PROBABILITY MEAN DEVIATION
Provenance 0.01190 SFU 0.01107 0.0011 0 .002 GUELPH 0.01221 0.0012 FIELD 0.01242 0.0010
Cohort 0.01221 COH 1 0.01295 0.00086 0.010 (Guelph and COH 2 0.01240 0.00118 Field) COH 3 0.01080 0 .00182
Cohort 0.01107 COH 1 0.01061 0.00110 0 .030 (SFU) COH 2 0.01097 0.00081 COH 3 0.01167 0 .00141 VARIATION DUE TO MATERNAL AGE
latter two groups proved very similar in their pupal weight characteristics. Cohort analyses were therefore performed separately within these two homogeneous subgroups.
A cohort gradient in pupal weight was found within each subgroup, although the actual trends were quite different.
In the Guelph-Field subgroup, pupal size gradually decreased as the mother aged, whereas in the SFU subgroup the largest individuals were late-born, with early- and mid-born progeny very similar in size. The size range in the former case was more than twice that in the latter. VARIATION DUE TO MATERNAL AGE 55
VII ECOLOGICAL FACTORS
1. Larval Di spersal
1.1 Introduction
This experiment was designed to answer the questions:
(1) will larvae tend to disperse more readily under crowded conditions and, if so, at what density does this intolerance appear; (2) is there a larval-age effect on dispersal and/or
intolerance (i.e., are older or younger larvae more prone to
leave the plant as density increases and is distance moved
related to age); (3) are these factors influenced by maternal age?
Morris (1964) studied dispersal movements from one
cage to another of four strains of Mus ca domes tica, under three different density regimes (100, 500, and 1000 individuals per
cage). He found that significantly more flies from the 1000-
fly cage dispersed than from the 100-fly cage. Dispersal of
European corn borer larvae, 0 s t r i n i a n u b i1 a 1i s (Hubner)(Lepi-
doptera), was shown to increase as egg density at the original
source increased (Neiswander and Savage, 1931). The authors
believed competition for food and space to be regulating
population density. Density-dependent dispersal of caddis fly
larvae, Cheumatopsyche spp. (Trichoptera), revealed that, in
those cases where small pebbles had been added to provide pro•
tection, more larvae dispersed farther as the initial number
per dish increased (Glass and Bovbjerg, 1959). The number of VARIATION DUE TO MATERNAL AGE 56
pebbles was always the same per dish, so as larval density in• creased, competition for a place near a pebble became more severe, and a greater proportion of larvae were forced to look elsewhere. When the pebbles were removed, larvae tended to move as far as possible regardless of density. Glass and
Bovbjerg (op.cit.) concluded that dispersal is a function of density and is due to aggressive behaviour associated with spacing. Watanabe et al_. ( 1 952 ) showed that the tendency to disperse as well as the distance dispersed by the Azuki bean weevil, Cal1osobruchus ch i nens i s (Coleoptera), was a function of the number of individuals released from a central point.
A review of the literature concerning distance dispersed as a function of density is offered by Wolfenbarger (1975) and will not be discussed here.
Since H_. antiqua females deposit eggs in batches, it seemed likely that larvae might exhibit either an innate tendency to disperse or dispersal behaviour triggered by some threshold density level. Contacts or collisions between larvae would be more numerous at higher densities, which might affect dispersal activity. Henson (1961) found this to be the case with the white pine cone weevil, Conophthorus coni perda
(Schwarz)(Coleoptera). The density of "dummies" (pieces of wire or grains of rice about the same size and shape as the weevils) affected dispersal in the same way as "real" weevil density, indicating that these animals were reacting to con• tact, rather than some change in the surroundings, such as food depletion, due to the presence of other individuals. VARIATION DUE TO MATERNAL AGE 57
1.2 Materials and Methods
The experimental unit for the larval dispersal test is illustrated in Figure 3. A known number of larvae of given age were released onto the central onion and left in a dark area, undisturbed. After 48 hours, the number of larvae remain• ing on the central onion and the positions of the dispersers were determined. Two age groups of larvae (mid-second and early-third instars) and larvae from young, middle-aged and old females were tested, each at four densities (10, 35, 50, and 100 individuals). The flats were uniform with respect to the initial size of the onions, since the number of larvae that can be supported by the bulb is a function of its size
(Workman, 1958). In addition, it was necessary to ensure that movement off the central onion was not due to lack of food, but because of an innate tendency to disperse or into• lerance to crowding. Thus, an onion large enough to provide an adequate food supply for that density of larvae tested during the 48-hour period was always used.
1.3 Results
A 1-way ANOVA showed that the two ages of larvae did not vary significantly from each other, so these data were pooled to increase the total degrees of freedom. A 2-way ANOVA was performed on the variables density and cohort (Table 8).
Density proved to be non-significant, but cohort means descend• ed progressively from 99.3% to 91.9%. This analysis indicated only that the two extremes were significantly different; VARIATION DUE TO MATERNAL AGE 58 o o o o o o o o 5" / 7 11 o o 0 ° o o o ) o o ONIONS o o ) o o
Figure 3
Schematic representation of the larval dispersal experimental apparatus. Onions were placed on a bed of silica sand. VARIATION DUE TO MATERNAL AGE 59
TABLE 8
Two-way Analysis of Variance performed on percentage of non-dispersers , together with individual level means and their standard deviations. Cohort data were pooled over density (number of individuals released onto the central onion), and density data were pooled over cohort.
FACTOR MEAN±STD.DEV SOURCE OF df MEAN PROB . VARIATION SQUARE
A.
COHORT 1 99.39 ± 1.501 2 95 .09 ±-6 .543 3 91 .94 ± 6.038
COHORT 2 248.569 8.5881 0.000 DENSITY 3 57.253 1.9781 0.138 INTERACTION 6 9.456 0.3263 0.919 ERROR 45 28.943
B.
DENSITY 10 96 .28 ± 5.939 35 96 .93 ± 3.918 50 96.08 ±4.166 100 92.25 ± 8.677 VARIATION DUE TO MATERNAL AGE
therefore, 1-way ANOVA's were performed on the individual cohorts, pooled over density, taken two at a time. The result was that cohorts 2 and 3 could not be distinguished from each other, although they both differed from cohort 1 (Table 8).
In other words, approximately 7% of the larvae from middle- aged and old females dispersed off the central onion, whereas larvae from young females tended not to leave so long as food remained adequate. In those flats (not included in the above analysis) in which the central onion was completely consumed during the 48-hour testing period, 90% of the larvae left in search of new food, with those onions nearest to the central plant receiving 94% of the dispersers.
Larval dispersal has been studied in the onion maggot by Sleesman and Gui (1931) and Workman (1958). They found that, although the majority of maggots seeking a host plant would settle on the first plant encountered, a relatively constant proportion passed by a number of onions before stopp• ing. My results are in general agreement with theirs, while indicating further that the source of the "dispersers" is egg batches oviposited by the female in mid- to late life.
2. Activity of Adults
2.1 Introduction
The purpose of this experiment was to test for differ• ences in activity levels in adult populations, to determine VARIATION DUE TO MATERNAL AGE 61
whether offspring activity is affected by maternal age. It was felt that this might be important both from the point of view, of dispersal and of susceptibility to predation from ambush- type predators, since it is the activity of the prey that brings it into contact with the sensory apparatus of the preda• tor. In an experiment conducted by Haynes and Sisojevic (1966) on the behaviour of the jumping spider, Phi 1odromus rufus
(Walckenaer)(Arancae), with Drosophi1 a spp., it was found that the age of the culture from which the flies emerged influenced flight activity and thus susceptibility to predation.
If predation is an important source of mortality, then one way of minimizing its effects would be to adjust fecundity and/or growth patterns such that the loss of those animals most subject to predation is less significant for the population as a whole (Slobodkin, 1974). Perhaps there is a relatively large, unproductive segment of the population which helps to remove predation pressure from the more productive individuals.
There are, of course, other ways of escaping predation; e.g., by reducing the probability that a predator will attempt capture by being more difficult to locate, or by decreasing the probability of a successful capture once an attempt has been made, by being less palatable or more dangerous (Robinson,
1969). But this "costs" the animal and the benefits may not always be worth this cost (Cody, 1966). By becoming less available to one predator the prey sometimes becomes more available to another with a different method of hunting. VARIATION DUE TO MATERNAL AGE 62
2.2 Materials and Methods
A wear index, obtained by placing individual flies in small containers for a given period and then recording relative amount of wear on the wings, was to be used as an indicator of flight activity. The more active the flies, the greater the probability of hitting the sides of the container, thus damag• ing wing tissue. This technique was not successful for H_. anti qua , however, since the isolated f1ies remained inactive until they died of desiccation or starvation. Consequently, an alternate method was decided upon which gave a different indirect indication of activity levels.
Over the course of the research project, more than 100 demographic populations were maintained. These were reared under the same conditions, in cages of similar size. Although population size varied between 75 and 200 individuals (with an average of 150), even the most dense was not crowded with respect to the size of the cage. Each population showed certain behavioural patterns associated with mating, feeding, oviposition, etc., with each activity affecting amount of wear on the wings. When such a population died, its individuals could be classified into two groups based on their accumulated wing wear. It was hoped that this grouping would provide a means of comparing adult activity among populations.
2.3 Results
Since density seemed likely to affect activity, popula- tions were arbitrarily divided into three categories (75 to VARIATION DUE TO MATERNAL AGE 63
115, 116 to 155, and 156 to 200 individuals per cage) and test•
ed for differences. No significant differences were found, so
further analyses were done on data pooled over population size.
A significant sex difference in activity was observed
at the 0.0001 level of probability (Table 9), with males being
much more active than females in all cohorts. The analyses of
cohort differences were therefore performed on males and
females separately.
Within males, both mean activity level and their
standard deviations were very similar among the cohorts (pro•
bability = 0.95). Females showed much less variability in
activity than males, yet within the female group itself, there were more differences. The three cohort means did not vary
significantly (probability = 0.16) although cohort 2 seemed
the most different, showing less wing damage than cohorts 1 or
3. When the latter were pooled and re-tested against cohort 2,
the probability decreased to 0.06. Maternal age therefore has
a slight effect on female activity, with mid-born offspring
being the least active.
The largest source of error in this method would
result from the fact that these populations did not have the
same longevity- the variation being 50 to 100 days. Thus,
if strong differences in activity had been demonstrated,
they could have been explained by this fact alone. However,
as populations age they become less active (e.g., routine care
procedures disturbed the young much more than the older
cultures). It seems probable that most wing damage would have VARIATION DUE TO MATERNAL AGE 64
TABLE 9
One-way Analysis of Variance on percentage of active individuals, with individual level means and standard deviations.
FACTOR MEAN±STD.DEV. SOURCE OF df MEAN F PROB. VARIATION SQUARE
SEX: males 60.21±22.510 SEX 1 58097.46 222.5803 0 .000
females 3 .40* 3.937 ERROR 70 261.10
COHORT: 1 59 .24±20 .909 COHORT 2 28.64 0.0535 0.948 2 59 .73±25.807 ERROR 33 535 .67
3 62.36±22.995
COHORT: 1,3 4.25± 4.431 COHORT 1 52.13 3.6153 0.066 (?) 2 1 .69± 1 .874 ERROR 34 14.42 VARIATION DUE TO MATERNAL AGE 65
occurred early in the life history, around the time when flies
were actively mating.
3. Ability To Diapause Successfully
3.1Introduction
The purpose of this experiment was to examine certain
characteristics associated with diapausing populations and to
use these parameters to compare the ability of offspring from
mothers of different ages to enter diapause. In British Colum•
bia, H. anti qua undergoes three generations per year, with
second-generation adults making the greatest contribution to
the over-wintering population (Mukerji and Harcourt, 1970).
Very often, offspring from subsequent generations do not have
time to reach the pupal stage before adverse conditions set in.
Ability to diapause thus is not always required of all
individuals, as diapausing pupae may be produced during a
relatively short period of the year. Perhaps only those
females in a particular physiological state might be responsible
for the production of diapausing offspring.
Simmonds (1949) showed that the incidence of diapause
in the offspring of the oarasites Spalancna drosophilae (Ashm.)
and Cryptus inornatus (Pratt)(Hymenoptera) gradually
increased as the mother aged. Similarly, in the parasitic wasp Nasonia vitripennis (Walk.)(Hymenoptera) non-diapausing
larvae were produced by middle-aged females, whereas only diapausing larvae were produced by older females (Saunders, VARIATION DUE TO MATERNAL AGE 66
1962 & 1966b). McNeil and Rabb (1973) found that maternal age influenced the frequency of diapausing individuals in various hyperparasites of the Tobacco hornworm, Manduca sexta (L.)
(Lepidoptera).
3.2 Materials and Methods
Diapause was artificially induced in the laboratory by rearing second-instar larvae at a day temperature of 20°C, a night temperature of 7°C, and a 16-hour photoperiod (Harris, personal communication). Developmental time from egg to pupal formation was recorded.
Resulting pupae were stored in a temperature chamber maintained at 1°C. After 6 weeks they were removed, weighed, and placed on a moist piece of filter paper at 22°C. They were left for at least one month, to emerge. Time taken for emergence to begin was noted, and the numbers of successfully emerged individuals (separated by sex) and non-emergers were recorded.
Some of these diapausing pupae were reared as adults according to standard techniques (see Experimental Design) so that data on fecundity and mortality could be collected and compared with these parameters in demographic and temperature- resistant populations.
3.3 Results
Developmental period from egg to pupa seemed to show a trend, with cohort 3 taking the least time to develop. VARIATION DUE TO MATERNAL AGE 67
However, these differences were not significant (probability =
0.23, Table 5, A(4)). Although length of the developmental period itself was different due to different rearing techniques, a similar trend was observed in demographic and temperature- resistant populations. These had been analysed together since they were raised under the same conditions until pupation
(Table 5, A(2)). The increased sample size in the latter case
(from 49 populations to 98) resulted in a significant difference in developmental time at the 0.05 probability level. The level means themselves did not differ from each other as much as the level means from diapause populations differed, but their varia• bility was less. This result suggests that the trend observed in diapause populations might, in fact, be real, although without additional data this conclusion cannot be justified.
When provenance differences in developmental period from egg to pupa were examined, a significant difference was found at the 0.01 probability level (Table 5, A(3)). Popula• tions from the Guelph stock took longer than average to develop, whereas developmental time in both SFU- and field-derived populations was below average. Developmental rate was then analysed within provenance groups but, even so, cohort differ• ences did not prove significant.
Days taken to emerge after removal from cold storage
(which is an indication of pupal developmental time) were not significantly different among the cohorts (Table 5, B(2)). If there were real differences in larval developmental time (i.e., from egg to pupa), they were not maintained during the pupal VARIATION DUE TO MATERNAL AGE 68
stage. It is interesting to note that within temperature- resistant populations, the 0.05-level cohort differences in larval developmental time were maintained during the pupal stage. Sample sizes in these two cases were approximately equal, as were standard deviations about the level means.
There were no provenance differences in emergence success from puparia, so these data were pooled for subsequent analyses. Total percentage emergence was very similar across all population types (72% in demographic, 65% in temperature- resistant, and 68% in diapause populations), and there were no distinguishable maternal-age effects (Table 6, A(3)). On the other hand, the proportion of the emerging individuals which were female showed significant cohort differences (probability
= 0.08, Table 6, B(3)). Cohort 1 populations contained a larger proportion of females (48%) than cohort 3 (40%), with cohort 2 intermediate (45%) . When cohorts 1 and 3 alone were compared, the probability that differences were due to chance alone decreased to 0.02. These same trends were found in demo• graphic and temperature-resistant populations.
Age-specific mortality and fecundity trends and pupal weight were tested for differences across population type.
Since no such differences were found, these data could be pooled across population type for other analyses, the results of which were presented in previous sections (Table 2, 3, 4 and 7). VARIATION DUE TO MATERNAL AGE 69
VIII REVIEW OF RESULTS
The following differences due to maternal age were found to exist:
1) Both the overall mean expectation of life and the expectation of life taken after 10-day intervals were lower for late-born offspring.
2) The probabilities of being alive at 10-day intervals were always highest for mid-born offspring and lowest for late- born offspring. Early-born offspring had a relatively low mortality rate for the first 20 days of life, giving them a high probability of being alive during this period. After 20 days of age their mortality rate increased, however, so that their probabilities of being alive consequently decreased.
Thus, they were initially similar to mid-born offspring, later becoming more like late-born offspring.
3) A gradient was found in average fecundity (i.e., eggs per female per 48 hours), which was highest for early-born offspring, decreasing to a minimum in late-born offspring.
4) The mean rate of egg production per 10-day period was higher for early-born than for late-born offspring for the intervals 11 to 20 and 21 to 30 days. Mid-born offspring showed a high degree of variability and were not significantly different from either of these two groups.
5) The egg to pupal developmental period was shortest for late-born offspring. This difference was clearly establish• ed only for the demographic and temperature-resistant groups. VARIATION DUE TO MATERNAL AGE 70
6) Production of female offspring was highest in popu• lations derived from early-born offspring. In the diapause population type, all three cohorts differed from each other, showing a gradient from highest in early-born to lowest in late-born offspring. In the demographic and temperature-resist• ant groups, mid- and late-born offspring were statistically similar with respect to sex ratio.
7) The death rate in populations of starved adults was lower in mid-born offspring.
8) A pupal size gradient was found, although exact trend depended on provenance of the initial stock. From the
SFU stock, late-born offspring were the largest, whereas early-born offspring were the largest from the Guelph and field stocks.
9) The proportion of dispersers versus non-dispersers in larval populations was higher in mid- and late-born off• spring.
10) Mid-born adult females were slightly less active than either early- or late-born females. VARIATION DUE TO MATERNAL AGE 71
J_X DISCUSSION
Differences in the offspring due to the age of the
mother were found in Hylemya antiqua. Their significance is
best evaluated in terms of effects on population dynamics.
Since the data were derived from laboratory populations raised
under ideal conditions, their effects on population dynamics
can be evaluated only from a theoretical point of view. How•
ever, such variation due to maternal age acting within natural
populations would result in the same type of response, although
the mechanisms producing the end result would be much more
complex. Trends therefore are comparable in the two situations,
even though actual values may not be.
The population consequences of the statistically signi•
ficant decrease observed in the number of eggs laid per female
per day in offspring from middle-aged and from old mothers can
be evaluated by means of the Lotka equation used to estimate
the intrinsic rate of natural increase, r_. This equation is
b e"rxLxMx = 1
x = a where L_x is the probability of being alive at age x (or the
proportion of the total population which is still alive at age x) , M_x is the average number of eggs laid by a female of age x, a_ is the age at first reproduction, and b_ is the age at last reproduction. VARIATION DUE TO MATERNAL AGE 72
In the iterative evaluation of _r using this equation, it is assumed that the age-specific mortality and fecundity schedules are fixed, i.e., that all individuals are identical.
But this is clearly not the case if offspring from young mothers are more fecund than offspring from middle-aged and old mothers, or if an individual born from a young female has a higher survival probability, or mean expectation of life, than an individual borne by an older female, as in H_.' anti qua.
In other words, the probability of being alive at age 20 days for a female originating from an egg batch laid when her mother was, say, 15 days old, would be much higher than if her mother had been 40 days old. The same would be true for her average egg. production.
The significance of this effect on the rate of increase depends upon the following two factors: (1) the age of the mother at the point when her offspring begin to have a decreased probability of surviving, and (2) her fecundity value at that age. The younger the age class at which the effect begins to operate, the larger will be the survival probability of the mother, and therefore the more important her egg contribution will be to the growth rate of the population.
Similarly, the higher her egg production for the ages affected, the greater her contribution to population growth. If the female is making a significant egg contribution at those ages, the more pronounced will be the reduction in the rate of in• crease. Also, r_ may be significantly reduced if the mother is relatively young (or fecund) when the mean expectation of VARIATION DUE TO MATERNAL AGE 73
life for her offspring begins to decrease (Rabinovich, 1971).
In the case of H_. an ti qua, when the mother is young the offspring she produces have a high survival probability and begin (after 10 days of age) to have a high fecundity.
When these offspring reach mid-life their mortality rate begins to increase quickly and their fecundity decreases. Never• theless, they exhibit a comparatively long mean expectation of life. As the mother passes into middle-age, however, her off• spring show the lowest sustained mortality rate with a long mean expectation of life. Their overall fecundity is slightly less than that for their younger-born sisters, and their rate of egg production is more variable throughout life. When the mother reaches old age, her offspring have the lowest mean expectation of life, the highest mortality rate, the lowest average fecundity, and differ significantly in their rate of egg production (from 11 to 30 days) from their siblings born when their mother was young. In other words, the late-born progeny make the least net contribution of offspring to succeed• ing generations. Thus, it seems that these effects of the aging process are most pronounced when the mother is in old age. Nevertheless, her net reproductive rate at this time is still quite high, even though statistically lower than it was in early- and mid-reproductive life. A significant reduction in the overall rate of increase would still be expected, and, in fact, was found.
The rates of increase for early-, mid- and late-born offspring were 1.5432, 1.4395 and 1.2115, respectively. If VARIATION DUE TO MATERNAL AGE 74
all individuals were assumed to be identical with average characteristics, the r value would be only 1.3981. If one considers the growth of a population of given size, or the new density after a certain period of population increase, the net effect of these different rates of increase becomes more obvious.
This was done using the equation
N = No ert,
where N£ is the size of the initial population, t^ is the amount of time elapsed, and _r is the rate of increase of the population.
Table 10(A) shows population growth from 1 through 10 genera• tions, starting with one adult female, and using the above values for r.
Population growth in the cohorts is remarkably different.
For example, by the tenth generation in Table 10(A), cohort 1 population density is almost ten times as high as that for cohort 3, and considerably higher than that for the average populati on.
In these calculations of _r, a 50:50 sex ratio in the offspring was assumed. However, in H_. antiqua the sex ratio of the offspring is subject to modification due to the age of the mother. If sex ratio is averaged over all population types
(i.e., demographic, temperature-resistant, and diapause) it is found that 51% of early-born offspring are female, whereas only 43% and 42% of mid- and late-born offspring respectively are female. Taking these differences into consideration results in an even steeper downward gradient in r. from early- VARIATION DUE TO MATERNAL AGE 75
TABLE 10
Growth of populations from 1 through 10 generations, considering different rates of natural increase, jr. The initial density in all populations was one adult female. A considers no maternal-age effects. B_ considers a maternal-age effect on sex ratio. C_ considers a maternal-age effect on both sex ratio and mean generation time.
COHORT 1 COHORT 2 COHORT 3 AVERAGE
r = 1 .5432 4 .6 r=l .4395 4 .2 r-1 .2115 3 .3 r=l .3981 4 .0 21 .8 1 7 .7 11 .2 16 .3 102 .4 75 .0 37 .8 66 .3 479 .5 316 .7 127 .2 268 .3 2243 .9 1 336 .0 427 .3 1086 .2 1 0500 .7 5636 .3 1435 .1 4396 .6 491 38 .5 23777 .6 4819 .8 1 7795 .4 229946 .0 100307 .9 16187 . 5 72027 .2 1076041 .9 423157 .6 54366 .3 291530 . 5 5035382 .2 1785126 .7 182590 .2 1179970 .5
r = 1 .5589 4 .7 r = l .3221 3 .7 r-1 .0842 2 .9 r = l .3217 3 .7 22 . 5 14 .0 8 .7 14 .0 107 .4 52 .7 25 .8 52 .7 510 .6 198 .0 76 .4 197 .7 2427 .2 742 .8 226 .1 741 .3 11 537 .9 2786 .6 668 .6 2779 .9 54846 .8 1 0453 .5 1977 .1 1 0424 .3 260719 .3 39214 .4 5846 .5 39089 .1 1239352 .9 146104 .7 1 7288 .5 146576 .0 5891375 .1 551832 .5 51123 .5 549629 .6
r- 1 .5009 4 .4 r-1 .3712 3 .9 r = l .2874 3 .6 r = l .3865 4 .0 20 .1 15 .5 1 3 .1 16 .0 90 .2 61 .1 47 .5 64 .0 404 .8 241 .0 1 72 .3 256 .2 1816 .1 949 . 5 624 .5 1025 .0 8146 .9 3741 .3 2262 .8 4101 .0 36545 .0 14741 .1 8199 .2 16407 .6 163930 .8 58081 .3 29708 .8 65643 .9 735348 .6 228849 .9 107645 .6 262629 .6 3298571 .3 901666 .5 390038 .2 1050734 .4 VARIATION DUE TO MATERNAL AGE 76
through late-born progeny. The new values are 1.5589 for early-born, 1.3221 for mid-born, and 1.0842 for late-born off• spring. The resulting effects on population growth are shown
in Table 10(B). Density differences in this case are, as expected, even more pronounced.
One could also consider the average number of female offspring produced by an individual during her life span (i.e., the net reproductive rate, _Ro) . Ro_ is calculated as follows:
b Ro = ^ LxM'x, x = a where M'x is the average number of female offspring produced by an individual of age _x. It is calculated from the average egg production per female at age x_, and the proportion of these eggs which will potentially give rise to female offspring. The other parameters are as previously defined. In discrete, non- overlapping generations IRo is the amount by which the population increases each generation. For the same reasons as given above, Ro^ will be reduced by a significant amount if the age of the mother at which the proportion of her offspring that are female begins to decrease is also associated with a high egg contribution. The later in life that this effect comes into operation, the less will be the reduction in net reproduct• ive rate.
In H_. antiqua, by the time the mother passes into middle-age the percentage of her offspring that are female has dropped considerably, yet her net fecundity is still relatively VARIATION DUE TO MATERNAL AGE 77
high. This situation results in rather large differences in the net reproductive rate among the cohorts; e.g., 13.09,
10.48 and 7.54 for early-, mid- and late-born offspring, respectively. Thus, a population of early-born offspring could potentially increase its size by 13 times each generation, whereas a population of late-born offspring could increase by only 7.5 times, approximately half as much. All other factors being equal, this difference represents a pronounced variation in population growth. However, in H_. antiqua, other factors are not equal and the interpretation of Ro_ is more complex.
A population's capacity for increase is inversely related to mean generation time (Barnes, 1976). According to
Barnes (op.cit.), variation in mean generation time has more effect on the rate of increase than variation in net reproduct• ive rate. Within my demographic and temperature-resistant populations, late-born offspring had a significantly shorter egg-to-pupa developmental period. Since all other developmental periods were similar, this means that late-born offspring have a shorter mean generation time. To what extent would this counter-balance their lower rate of increase?
A rate of increase can also be calculated by using Ro, although this method is not as accurate as the one discussed previously. It is interesting, nevertheless, in that it takes into consideration mean generation time, as follows:
1 r = logg Ro GT" , VARIATION DUE TO MATERNAL AGE 78
where GJ_ is mean generation time. Data from the present series of experiments indicate that real generation time (i.e., the period from the birth of the parents to their first reproduct• ion) for late-born offspring is only 91% of that for early- and mid-born offspring, giving new _r values of 1.5009 , 1.371 2 and 1.2874 for cohorts 1, 2, and 3, respectively. (See Table
10(C) for effects on population growth.) In all, Table 10 shows that only small variations in _rwill have pronounced effects on density. Even considering growth in an "average" population, the final density is considerably lower than it potentially could be.
The progressive changes in the rate of increase as maternal-age effects were taken into consideration can be summarized as follows:
Rl R2 R3 COHORT 1 1.5432 1.5589 1 .5009 COHORT 2 1 .4395 1.3221 1.3712 COHORT 3 1.2115 1.0842 1.2874 AVERAGE 1.3981 1 .3217 1.3865
where Rl considers no maternal-age effects (i.e., a 50:50 sex ratio and equal generation times are assumed), R2 considers the maternal-age effect on sex ratio only, and R3 considers both sex ratio and mean generation time as being modified by maternal age.
From these results it is apparent that the faster turn-over rate of late-born offspring does ameliorate their lower rate of increase, but not sufficiently to counteract VARIATION DUE TO MATERNAL AGE 79
their inferior fecundity (both in terms of number of eggs pro•
duced, and the proportion of those which will be female) and
their higher mortality rate. The difference in r_ within one
cohort level caused by considering their different generation
times are still not as pronounced as the differences in r. among
the three cohorts.
A final question which might be asked is, what value
has a female of a given age to the population in terms of the
number of female offspring she is likely to contribute for the
rest of her life? The reproductive value, V_x, can be used to measure her worth: it is the number of female offspring that
remain to be born for a female of given age, and is estimated relative to its value at birth, as follows:
erx k ryLj,M y Vx . ]T e- ' ' u y=x
where x represents the age of the female and y represents the age categories she will yet pass through from age >< to the end of her reproductive span. A reproductive value of 5, for example, means that a female which has reached that age can be expected to produce five times as many female offspring as a female which has just been born. This difference is a func• tion of mortality rate and is due to the fact that not all newly born females will live to reach age )< and produce off• spring. VARIATION DUE TO MATERNAL AGE 80
The reproductive curves for early-, mid- and late-born offspring are shown in Figure 4. These were calculated using the _r values in which the maternal-age effects on sex ratio and mean generation time were considered. In all three cases the curves first increase to plateaus of variable length and then decrease at variable rates. The maximum J7x_ values are
5.7, 4.2, and 3.3 for early-, mid- and late-born progeny, respectively. Thus, a population consisting of representatives from each of these cohort groups, which would be the usual case, would be heterogeneous with respect to the reproductive value of each member. The loss of an early-born individual would have a more substantial influence on population growth than the loss of a late-born individual. This might be impor• tant to consider in pest-management practices.
A management policy should concentrate on attacking the age groups with the highest reproductive values, to de• crease population growth as rapidly and as efficiently as possible. If other characteristics of those individuals with the high reproductive values were considered, it might be possible to identify when or where they are most likely to occur, to what mortality factor they are particularly suscep• tible, or some other circumstance that might make different• ial mortality possible to achieve in a control program.
Predators may very well exploit these differences in an opposite sense, as they sometimes seem to select those indivi• duals with the lowest reproductive values, thereby substract- ing as little as possible from the future density of their VARIATION DUE TO MATERNAL AGE 81
6 i
0 10 20 30 +o 50
Age (days)
Figure 4
Reproductive value curves for early-, mid- and late-born females. VARIATION DUE TO MATERNAL AGE 82
prey population. Phenomena involving qualitative differences
such as these have rarely been given sufficient emphasis in
analysing control strategies and evaluating control programs
(Wellington, 1 977) .
An important concept in pest management is the economic
threshold. When the density of the pest population reaches this level, control measures must be initiated to prevent crop damage and economic loss. The more modern techniques of pest management involve the use of predictive pest/crop models which allow the manager to initiate corrective action before damage actually occurs, or before density increases to a level where an outbreak is inevitable. Because models are only abstractions of a real system, there will be deviations between actual behaviour and that predicted by the model. For example, there will inevitably be a time lag between the instant when the model recognized a need for corrective measures and when that need first appeared. Thus small errors can be introduced into the timing of control operations. Yet in certain pest/crop complexes a delay of more than two or three days between the occurrence of an event and the implementation of the appropriate control strategy cannot be tolerated if this strategy is to be effective (Haynes, Brandenburg and
Fisher, 1973). The prediction, to be valuable, therefore must be accurate. One neglected means of increasing the accuracy of the model and therefore its predictions is to take into consideration biological variability. In the case at hand, the slight differences in rates of increase alter population VARIATION DUE TO MATERNAL AGE 83
growth significantly, and at certain times, this pheonmenon would be critically important.
Enough of the biology of H. an ti qua is known to be able to model population growth for predictive purposes while taking differences due to maternal age into account. If data concern• ing temperatures and soil states at critical periods were availa• ble to characterize initial conditions, changes in the pest popu• lation could be predicted relatively accurately. In this way the model could monitor the preponderance of individuals with high reproductive values, allowing control measures to be geared accordi ngly.
Interesting differences due to maternal age were found in pupal size. In Guelph-and field-derived populations, the smallest pupae were produced from late-born offspring, whereas in SFU-derived populations late-born offspring produced the largest pupae. To evaluate this difference it is necessary to consider how being "small" affects an individual. No fecund• ity differences were found between the SFU and Guelph prove• nance groups, regardless of their size difference. Further• more, field-derived females were the largest, yet least fecund^.
Finally, SFU and Guelph groups had similar developmental rates, whereas field populations developed significantly faster. This was the only additional provenance difference found, so it seems
^ This inferior fecundity may be an indirect result of aggressive behaviour normally acting to keep flies spaced in the environment. Biggs (1972) hypothesizes that such behaviour is not always evident in cultures which have been raised for many generations in the laboratory (e.g., SFU- and Guelph-derived populations) since selection there favors decreased defense of personal space. i
VARIATION DUE TO MATERNAL AGE 84
that size itself is not associated with other characteristics evaluated in these experiments.
The fact that fecundity characteristics were quantitati• vely similar in SFU- and Guelph-derived populations suggests that, in H_. antiqua, an individual reacts to a smaller size by producing smaller, not fewer, eggs. Assuming comparable efficiences in energy conversion and utilization, the amount of food required to produce a given number of eggs would be a function of their size. The resulting combination of size and number of eggs therefore represents a reproductive strategy, perfected by natural selection and geared to the conditions in which the individuals find themselves. For this reason, size differences among individuals originating from different areas should be expected.
The size of the original parents was always closer to the larger cohort size. Thus it could be interpreted that maternal age has an effect on size only when the mother is young to middle-aged in SFU populations, or when she is middle- aged to old in Guelph and field populations. This arrangement would be another aspect of the survival strategy, in that the ability to pupate successfully at a smaller size would be selected in populations experiencing food shortages from time to time, and the development of this response would be tuned to the particular conditions under which it formed. In the
Cinnabar moth, Tyri a jacobaeae (L.)(Lepidoptera), the size threshold for successful pupation varies among individuals and appears to be related to size of the food plants (Myers, VARIATION DUE TO MATERNAL AGE 85
personal communication).
When populations of newly emerged adults were given water, but no food, mortality rate differed, although longevity was comparable among the three cohorts. Mid-born offspring were the most robust, in the sense that the majority survived the first 10 days of starvation and then died rather quickly.
Late-born offspring, on the other hand, experienced their highest mortality rate much earlier. Early-born offspring were intermediate. Therefore, during short periods of food stress a greater proportion of individuals would survive in a mid-born than in a late-born population. And in a mixed population there would be a differential mortality rate favor• ing those individuals with the higher reproductive values
(i.e., the early- and mid-born offspring). If individuals of a species varied in their ability to resist starvation, this strategy would be most effective as a precaution against periods of food shortage if the surviving individuals had the highest reproductive value. The loss of late-born individuals has far less effect on subsequent population growth than the loss of early- or mid-born individuals. The fact that the most resistant individuals have an intermediate reproductive value however, implies that robustness requires a compromise between reproductive abilities and certain others, such that more hardy but slightly less fecund individuals are produced..
Parsons (1962, 1964) suggested that during the middle period of her reproductive life, a female often produces off• spring most fit in terms of developmental stability, viability, VARIATION DUE TO MATERNAL AGE 86
and reproductive ability. According to Emlen (1970) the main
selective forces for successful reproduction and the product•
ion of congenitally healthy young will occur as soon as
reproduction begins and will fall off with age. Thus, progeny
from old females would be less healthy (or more mortality-prone)
than progeny from young females. In HL antiqua the best off•
spring, in terms of reproduction, are early-born. They have
the highest mean expectation of life, a relatively low mortal•
ity rate up to 30 days of age, the highest average fecundity,
the highest mean rate of egg production (from ages 11 to 30
days), and they produce the highest proportion of femage off•
spring. On the other hand, the best offspring in terms of
survi val are mid-born. Their mean expectation of life is
comparable with that for early-born offspring, they show the
lowest sustained mortality rate, and they are the most hardy
individuals with respect to ability to survive food-stressed
situations. They show intermediate fecundity characteristics.
From Emlen's definition, and contrary to his prediction, mid-
born progeny should be considered the most healthy in that
they are the least mortality-prone. Late-born offspring,
however, are as predicted. They have the lowest mean expect•
ation of life, the highest mortality rate throughout life,
the least ability to survive starvation (i.e., the most mortality-prone), and they have the lowest net fecundity and
rate of egg production (i.e., they are least reproductively
fit).
Clearly, in considering which offspring are the most
"fit", the most "reproductively successful", or the "health- VARIATION DUE TO MATERNAL AGE 87
iest" it is important to state from what point of view. Each type of offspring has something to contribute to the survival of the population as a whole, and from this point of view the
idea of the "best" offspring is less meaningful. One could postulate, for example, that when conditions are good rapid increases in population density should be primarily due to the
reproductively superior early-born offspring. When conditions are less favorable, the hardier mid-born offspring would ensure that a segment of the population will survive. And when condi• tions mediate faster development, late-born offspring should make their contribution. Their shorter generation time might be a way of maximizing fitness in the face of a deteriorating environment over the course of a season. With a longer genera• tion time they might leave fewer offspring. (Or these individuals, being the most mortality-prone, should be more susceptible to predation, thereby removing predation pressure from the reproduct-
ively more valuable segment of the population). In other words,
this variability in offspring can represent a strategy for survival of the population.
Emlen ( 1 970) suggests that fecundity should ri|se after
reproductive capability begins and then should fall off progres• sively with age. Mortality should be at a minimum just before
first reproduction and then should begin rising with age.
These trends were more or less apparent in all cohort populations
of H_. anti qua, although the progressive decrease in fecundity
and increase in mortality with age occurred relatively slowly
at first, and were followed by more pronounced VARIATION DUE TO MATERNAL AGE
changes later in life. In addition, early-born offspring changed most drastically , with fecundity quickly increasing to a high level after first reproduction, and mortality rate
increasing most quickly around mid-reproductive life.
Certain ecological characteristics were also evaluated for their response to maternal age. A small percentage of
larvae in populations of H_. an ti qua appear to have an innate tendency to disperse (Sleesman and Gui, 1931; Workman, 1958).
Maternal age has been shown to be the source of heterogeneity in activity and dispersal ability among offspring in other species - e.g., in Maiacosoma pluvi ale (Wellington, 1965).
The present study demonstrated a maternal-age effect on larval dispersal in H_. antiqua, identifying the source of those individuals with a greater tendency to disperse as the egg batches from middle-aged and older mothers.
Within an onion crop, the resource is such that larval utilization this year does not affect the availability of food for next year's generation. According to Monro (1967) the chance of survival in such cases will be the greatest when the resource is used to produce the largest number of progeny i.e., it will be most advantageous to increase as rapidly as possible during favorable periods. A uniform distribution would be expected since it would prevent egg wastage on over• crowded plants, thus promoting most efficient utilization of the food crop (Myers, 1976). According to Myers (op.cit) a uniform distribution requires (1) some kind of marking mechanism, detectable by ovipositing females, to identify VARIATION DUE TO MATERNAL AGE 89
places where eggs have already been laid, or (2) larval competition to ensure that only the number that can survive will remain on the plant.
Larvae of H_. antiqua seem capable of tolerating very crowded conditions until their food supply is depleted. Then the individuals disperse in all directions in search of a new host plant. Even the smallest larvae can move relatively large distances when searching for food (Workman, 1958; Iyer, personal communication; personal observation). However, the main factor responsible for spacing within an onion patch is the oviposition behaviour of adult females. Females are able to distinguish between infested and non-infested onions and prefer to oviposit on infested plants (Kendall, 1932; Sleesman and Gui , 1931; Workman, 1 958 ; personal observation). Workman
(op.cit.) suggests that odor is the most probable responsible factor. Since the preference appears even before onion break• down begins (i.e., before larval attack), a pheromone may be involved (Myers, personal communication). As was found with Drosophila melanogaster (Del Solar and Palomino, 1966) and D_. pseudoobscura (Meig.)(Del Solar, 1968), there may be optimal densities for maximal egg production, and subsequent larval viability, developmental rate, and/or longevity. In other words, larvae may have a favorable conditioning effect on the medium in which they live. Workman (1958) points out that infested onions become broken down and water soaked, giving an added dampness to the surrounding soil which seems to promote survival of young maggots. VARIATION DUE TO MATERNAL AGE 90
If this conditioning is an important survival factor,
then optimal densities are not at the lowest levels. Nor is it
likely that they are at the highest levels, since first-instar
larvae would not readily compete with the larger, older maggots,
and such unequal competition could affect survival, speed of
development, and weight of emerging adults. If food were over-
exploited, mortality due to starvation would be high and the
net contribution to the succeeding generation low. In the
extreme case, all eggs would be concentrated in a single ovi-
position site with large suitable areas left unexploited (Del
Solar, 1968).
According to Myers (1976), dispersal will be favored when egg distribution is moderately clumped and batch size is
small, yet larger than the plant can support. Dispersal at
such timeswould lead to higher overall population densities
and thus to stability. In H_. antiqua, egg production per
female is high and batch size is small (Missonnier and Stengel,
1966). Eggs are laid in a clumped pattern (since females are
attracted to preinfested plants), and larval dispersal occurs
at a relatively low rate. The attraction of femalesto pre•
infested plants could result in over-clumping (and therefore over-exploitation of food and high larval mortality), unless
there were some mechanism operating to prevent this.
There are a number of mechanisms through which inter• mediate densities could be achieved. Biggs (1972) hypothesized
that aggressive behaviour, arising beyond a certain adult VARIATION DUE TO MATERNAL AGE 91
density, would keep flies spaced in the environment so that egg and larval aggregation would remain optimal. He pointed out that such aggressive behaviour is not always evident
in laboratory cultures, which are raised at unnaturally high population densities, since selection there favors decreased defense of personal space. Secondly, although females may be attracted by infested plants, they may deposit only a few of their eggs at that spot and then move on to additional ovi- position sites. (This seems to be how the cabbage root fly,
E r i o i s c h i a brassica, achieves a fairly uniform distribution of eggs throughout a brassica crop (Hughes and Salter, 1959).)
A final possibility is that females may be repulsed by heavily infested onions once density on such plants increases beyond some critical level. Certain observations on their ovipositing behaviour indicate that this might be happening.
For example, cohort collections were made by leaving one or two onion trays (each containing two onion halves) in a cage for 48 hours. If egg production was low, the majority of eggs would be deposited on only one of the onion halves. The higher the egg production, the more evenly distributed the eggs were. But if two trays were placed in a cage, and production was high, eggs would be deposited first on one onion half and then the next, within the same container, before females would move on to the second container. Females would even deposit eggs on the watering dish, or in the corners of the cage, rather than add to the density in the onion tray. VARIATION DUE TO MATERNAL AGE 92
Unless survival of dispersers is low, density-dependent
dispersal would decrease population stability (in cases where
the host plant can be over-exploited) and therefore would not
be selected (Myers, 1 976). In H_. an ti qua, survival of dispers•
ing larvae is probably quite high, since food plants in onion
fields are closely spaced and gravid females are more attracted
to the denser atands (Workman, 1958). This means that (1)
larvae would have a high probability of locating a new plant
and (2) mortality of dispersers due to predation by mites,
ants, carabids, and staphylinids would be low, since the time
the maggots would spend searching for a new host would be
relatively short. Density-dependent dispersal proved to be
non-significant in these experiments, which is what would be
expected on the basis of Myers' work. Reddingius and den
Boer (1970) found density-dependent dispersal to have as
stabilizing an effect on population fluctuations as density-
independent di spersal , but they were considering only those
cases in which the food resource could not be over-exploited.
According to the larval dispersal experiments, approxi• mately 1% of the offspring from middle-aged and old mothers
had an innate tendency to disperse. If this tendency is carried over to the adult stage, one would expect to find
that adult activity • varied in the same proportions. Experiments
showed that maternal age in fact could affect the activity
level of adult female offspring, in that mid-born offspring were significantly less active than either early- or late-born
progeny. But the results, did not coincide with results from VARIATION DUE TO MATERNAL AGE 93
the larval dispersal experiments, indicating that the tendency
to disperse in larvae is probably not related to activity level
in adults, at least with respect to effects of maternal age.
All adult females of Eri oi schia brass i cae disperse soon
after mating and prior to oviposition (Hawkes, 1972). If this
is also true to H_. antiqua, the observed differences in adult
activity level could indicate that all early- and late-born
female offspring disperse, whereas mid-born females remain
near the place of emergence and mating. One might also expect
to find differences in pre-oviposition period, however, if
this were so because a dispersing female would not begin to
lay eggs as soon as a non-dispersing one, and therefore her
pre-.ov i pos i ti on period would be longer. No such differences were found, so the evidence did not consistently support the
idea that a specific segment of the adult population might
be more prone to disperse. The different activity levels
observed could be due to factors totally unrelated to dis•
persal, a safer conclusion, considering how questionable this
technique was for evaluating activity in adults.
Diapause was also examined for maternal-age differ•
ences. It is a state of arrested development which physiologic•
ally prepares the animal, in advance, for approaching un-
favorable conditions (McHaffey, 1972). Thus it acts as a
physiological timing mechanism, not only providing for resist•
ance to adverse conditions, but also for resumption of develop•
ment at more favorable times (in synchrony with the host plant), VARIATION DUE TO MATERNAL AGE 94
and for synchronization of adult emergence for mating. The
environmental factors triggering diapause need not in them•
selves be unfavorable, but merely correlated with the onset
of unfavorable conditions. Adult H. antiqua emerging from
diapausing pupae in the spring produce the succeeding summer
generations. Diapause populations therefore were also examined
for age-specific fecundity and mortality characteristics to
compare their reproductive capability with non-diapausing
•popul ati ons .
The specific physiological causes of diapause are not
fully understood, although they are thought to be associated
with the absence of growth hormones-an indirect result of
environmental changes acting through neurosecretory cells.
Probably the most important cue is length of day, since it
represents the most accurate and invariable means of obtain•
ing synchrony with environmental change. Temperature may act
in association with photoperiod. Other factors that have been
shown to be important in specific cases are nutrition, moist•
ure content of food, crowding, desiccation, and maternal age
at oviposition.
The stimulus for the biochemical changes associated
with diapause may be received by the adult female during
oogenesis. McHaffey (1972) observed a maternal-age effect
on egg diapause in the floodwater mosquito, Aedes ni gromaculi s
(Ludlow)(Diptera). He found that only females of a particular
age responded to appropriate photoperiods and temperatures VARIATION DUE TO MATERNAL AGE 95
by producing diapausing offspring. Similarly, in other species
producing diapausing eggs it has been shown that a neuro•
hormone, liberated by the subesophageal ganglion in response
to environmental stimuli when the mother is at a particular
stage of egg development, is the inducer of diapause in her
offspring. Saunders ( 1 966a & 1 966b), in his work with Nasoni a
vi tri penn i s , hypothesized that older females (which produced
diapausing larvae) may be reacting differently to temperature,
photoperiod, and availability of the host than middle-aged
females.
A mother's age, then, may influence the incidence of
diapause in her offspring in three ways: (1) by affecting the
response of her offspring to the environmental cues associated with the onset of adverse conditions; (2) by affecting her
own response to these cues, enabling her to prepare her off•
spring to enter diapause; or (3) by a combination of these
factors - the age of the mother affecting her own response to
environmental cues and, depending on whether she responds in
the appropriate way, also affecting the response of her off•
spring to the same cues.
In Hy1emya brassicae the changes associated with
diapause are triggered in the mother and must be re-activated
in her offspring during the pupal stage (Read, 1965). The
females are responding to changes in photoperiod and temperature,
and particular temperature conditions precisely determine the
intensity of the diapause. H_. anti qua pupae can be artificial•
ly induced to enter diapause by altering their temperature VARIATION DUE TO MATERNAL AGE 96
regime in the laboratory. However, under field conditions the
mother may play a more important role in preparing her off•
spring for diapause, as in H_. brassicae.
Whatever the mechanisms involved, the external environ•
ment plays a central role in diapause control, acting through
neurosecretory cells and affecting hormonal levels in the body.
Internal physiological changes associated with aging, and
independent of external conditions, by themselves could only
potentially affect the offsprings' ability to receive and
react appropriately to environmental cues. If more complicated
interactions are involved, and it seems likely that under
natural conditions they may be, an experimental design in which
adult females are maintained under constant conditions would
not detect them. Only limited conclusions can be drawn from
my experiments, therefore, regarding the effect of maternal
age on offspring diapause in H_. an ti q ua.
The criterion for "successful" diapause in these
experiments was percentage emergence from puparia. Since total
emergence (i.e., of males and females combined) did not differ
significantly among the three cohorts, it would appear that
the age of the mother does not influence the ability of her
offspring to diapause when subjected to a 1ow-temperature
rearing regime.
Since HL a th t i qua has overlapping generations within a
season, and since diapausing pupae are produced over a relat•
ively short period, it would seem likely that maternal age would have to act in combination with environmental cues even VARIATION DUE TO MATERNAL AGE 97
if it were involved in pupal diapause. There would be adult
females of given critical ages present in.the population for long
periods, but only those present when external conditions were within a given range would be stimulated to produce diapausing
offspring • :Otherwise non diapausing offspring would form. And
if onjy maternal age were operating, diapausing pupae would appear
over a much longer span than is actually observed.
A sequence of physiological processes are called into
action when an individual undergoes diapause. Do these
processes alter the performance of the individual with respect
to characteristics that are not associated with diapause it•
self? In my experiments, the parameters studied (larval and
pupal developmental rates, emergence success, sex ratio, pre- oviposition period, fecundity, mortality, and size) in diapau• sing populations were comparable with those found in demographic and temperature-resistant populations. Although analyses were
performed separately, the same trends were evident throughout; e.g., the maternal-age effect on sex ratio was found through• out the population types, and was not peculiar to any one.
Such similarity indicates that the diapausing process does not affect population parameters, and that diapausing populations do not differ from non-diapausing ones. In addition, since the same trends were found independently during three different approaches, their recurrence adds confidence to the reality of any differences observed.
This research project examined a series of the components of H_. a n t i q u a ' s total behaviour. Even though the VARIATION DUE TO MATERNAL AGE 98
assembled system (i.e., the insect population within its natural environment) can not be fully characterized by only one such segment, the individual components are still demonstrably important to its functioning (Tummala, Ruesink and Haynes,
1975). I suggest that the variability in offspring elucidated in this study has an important role to play in the population dynamics of this species.
Populations of antiqua exhibit overlapping generations, and at any one time will contain ovipositing females of differ• ent ages. Maternal age has been shown to be a source of vari• ability among offspring in this species-a variability known to contribute to stability (den Boer, 1968). When a female alters the characteristics of her offspring as a function of her age, this alteration represents a strategy for spreading the risk of extinction of her genetic complement (MacKay, 1974). In addition, since it introduces phenotypic variation, it also represents a strategy for survival of the population as a whole. VARIATION DUE TO MATERNAL AGE 99
X CONCLUSION
The hypothesis that maternal age is a source of vari• ation among offspring was examined in populations of Hylemya antiqua. A series of experiments were performed under control• led laboratory conditions to test for qualitative differences among early-, mid- and late-born cohorts of offspring. A variety of characteristics were studied to determine the extent to which the age of the mother when she produces a batch of eggs can affect heterogeneity in her offspring.
Early-born offspring were found to be the reproductively most successful. They had the longest mean expectation of life, a relatively low mortality rate into mid-life, the highest ave• rage fecundity, the highest mean rate of egg production, and they produced the highest percentage of female offspring. On the other hand, mid-born offspring seemed hardiest. They also showed a long mean expectation of life, comparable with that for early-born offspring but, in addition, they had the lowest sustained mortality rate and showed the greatest ability to survive food stress. Their robustness may have been acquired at the expense of certain reproductive capabilities however, in that their average fecundity was lower than their early- born siblings', and their rate of egg production was more variable. Late-born offspring were the most mortality-prone and the least fecund, but they had the shortest mean generation time. These differences were evaluated in terms of their effect on the rate of natural increase and on population VARIATION DUE TO MATERNAL AGE 100
growth. The relevance of such qualitative differences in programs of pest management was also discussed.
Maternal age was found to influence pupal size, al• though the provenance groups differed significantly from each other and, in fact, showed opposite trends within their respect• ive cohort groups. It is suggested that size itself, and the ability of a species to alter the size at which it pupates, are characteristics which have evolved to fit a specific set of environmental conditions. Thus, variations in the strategy employed (i.e., the manner in which size varies) are functions of those conditions under which the phenomenon arose.
A greater proportion of dispersers was found among mid- and late-born larvae than among early-born larvae. Previous studies had indicated that certain larvae show an innate tend• ency to disperse while others do not. The present study sup• ported this idea, suggesting further that the source of these dispersers were egg batches produced by middle-aged and older mothers. Such dispersal characteristics seemed not to be carried over to the adult stage. Differences in activity level were found among adult females (mid-born offspring being the least active) but these did not correspond to dif• ferences in larval activity. This fact, together with results from other experiments-e.g. , the length of the preoviposition period-led to the conclusion that activity level in adults as determined by this technique was not related to dispersal abi1i ty . VARIATION DUE TO MATERNAL AGE 101
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APPENDIX I
A. Reproduction and Aging
That ovarian activity is under the control of secretions
from the corpora allata was established by Wigglesworth in 1936.
The corpora allata are the producers of juvenile hormone during
the larval stage, but since expression of adult characters is
inhibited in the presence of juvenile hormone, allatal activity
must cease just prior to pupation, in the last larval instar.
In cases where oogenesis takes place after metamorphosis, as
in the Diptera, the corpora allata then must be re-activated.
Allatal secretions stimulate vitel1ogenesis and regulate
the synthesis of proteins incorporated into the oocyte in late
oogenesis (i.e., the vitellogenins) by the fat body (de Wilde
and de Loof, 1973). During vitel1ogenesis there is a rapid
increase in cell volume of the oocyte resulting from the in•
flow of nutritive material. Follicle cells, which provide yolk, increase in number. This yolk may not be supplied in
its finished form, but may be modified by elements of the oocyte itself (Missonnier and Stengel, 1966).
It may be that the allata assure proper structural
conditions for the energy metabolism associated with vitello- genesis (Romoser, 1973), in addition to controlling the release of lipids stored in the fat body and their transfer to the oocyte. They may also influence yolk deposition indirectly
by their effects on feeding behaviour (Strangways-Dixon, 1961). VARIATION DUE TO MATERNAL AGE
A fly is stimulated to eat a high sugar diet at the beginning of oogenesis when the corpora allata show a maximum of secret• ory activity, and a high protein diet towards its completion, at which time protein-yolk is deposited by the follicles.
Activity of the corpora allata is influenced by neurosecretory cells in the brain, which may also act by directly stimulating protein synthesis, a prerequisite for protein yolk formation (de Wilde and de Loof, 1973). The pathway shown in Figure I (originally from Minks, 1967, but taken here from de Wilde and de Loof, 1973) is probably valid for many insect species. The neurosecretory cells, in turn, are affected by external environmental conditions, notably photoperiod, temperature, food (both quality and quantity) and interactions between these factors (de Wilde and de Loof,
1973). In the absence of neurosecretory cells, egg production decreases, although in certain species a few mature eggs can still be produced.
Finally, feedback mechanisms are involved in endocrine regulations and thus the state of the internal milieu (e.g., the activity of the ovaries, or the level of hormones circul• ating in the body) influences the functioning of the endocrine system. In Mus ca domesti ca, a hormone released by the ovary inhibits the release of secretions from the corpora allata, thereby indirectly affecting yolk deposition in young oocytes
(Adams, 1970).
Physiological state can be altered through aging.
Aging is a process involving those time-dependent changes in VARIATION DUE TO MATERNAL AGE
NSC
CC
CA
Ovary
Figure I
Schematic representation of endocrine relations in adult locusts (Locusta migratoria). NSC= neurosecretory cells; CC= corpora cardiaca; CA = corpora allata; a=activation of protein synthesis; b= specific modification of protein synthesis; c= water balance; d- follicle cell activity in yolk deposition. VARIATION DUE TO MATERNAL AGE 114
structure and function which occur from the beginning of life
to its termination. Such changes are predictable and reproduc•
ible. Aging should not be confused with senescence, which
forms only one part of the total aging process, and is ultima•
tely responsible for the death of the individual (Rockstein
and Miguel , 1 973) .
There are a number of theories of aging but these fall
into two main categories, one based on genetic factors and the
other on environmental factors, as the agents of change
through time (Rockstein and Miguel, 1973). Some of the possible
genetic mechanisms which decrease the likelihood of surviving
as time progresses are: (1) a programmed slowing down of growth,
specifically of brain and muscle tissue, causing a decreasing metabolic rate and irreversible age-related changes in fibrous
protein (Lansing, 1952); (2) the decline of a juvenile or
growth substance responsible for the maintenance of a non-
senescing state; (3) depletion of essential substanceswithin
a cell; (4) the accumulation of an aging factor or hormone,
and (5) the accumulation of substances which may be chemically
harmful to the organism. Each of the following environmental
factors has been proposed as a major cause of aging in general,
and senescence in particular: (1) the cumulative effects of
extrinsic radiation; (2) the cumulative effects of viruses or
bacteria of a pathological nature, and (3) the cumulative
effects of a changing environment. However, since aging and
senescence involve a complex series of time-dependent changes
in many organs, and since death results from the interaction VARIATION DUE TO MATERNAL AGE 115
of both genetic and environmental factors, these two theories should not be considered mutually exclusive (Rockstein and
Miguel ,1973).
It becomes evident, then, that although under natural conditions when a multiplicity of factors affecting survival are operating, individuals rarely live to the point where senescence begins to appear, they will always experience changes due to aging.
Many of the known internal changes which occur as an individual ages could logically affect egg quality. For example, within the circulatory system the volume of the blood and its qualitative and quantitative composition is changing, as is the rate and the amplitude of the heart beat, which affects circulation of the haemolymph through the body and, hence, the distribution of nutritive material (Arnold, 1959).
It has been shown that the synthetic ability of follicle and fat body cells decreases with age (Miguel e_t al_, 1 972 ;
Haydak, 1957). Haydak (op. cit.) also showed an age-related accumulation phenomenon in the worker honey bee. Hormonal levels and types of hormones found in the body change with age, both as a function of the internal biochemical milieu (in the form of feedback mechanisms) and external environmental conditions-mainly with respect to temperature, photoperiod and nutrition. Nutrient composition in the diet is changing both in quantity and quality, as the food plants themselves age (de Wilde and de Loof, 1973). It is also possible that the individual may be reacting differently to the nutrients VARIATION DUE TO MATERNAL AGE 116
ingested (Rockstein and Miguel, 1973). Finally, it would seem that egg quality must be directly influenced by the environ• mental factors associated with aging and senescence. All these factors could affect enzyme patterns, accumulation of metabolic by-products, organ development, and/or levels of particular proteins. Enzyme levels and their distribution have been shown to change with age in a number of insect species (Lang,
1967; Raychaudhuri and Butz, 1965; Rockstein and Farrell, 1972), as has the distribution of glycogen (Samis e_t aj_, 1971; Nettles and Betz, 1965; Rockstein and Srivastava, 1967). Reproduction itself puts a strain on parental metabolism and can be consi• dered an element of aging (Calow, 1973).
To summarize, hormone production from the corpora allata, the controlling agents of vitel1ogenesis , is affected by: (1) the internal mi 1ieu of the body (which is changed through time due to the aging process), and (2) neurosecretory cells from the brain (which are affected by the external environment). A feedback mechanism is thus formed, since hormonal levels themselves alter internal conditions. Allatal hormone production has a direct influence on yolk and egg cytoplasmic formation. Other factors may carry an indirect influence (e.g., by affecting composition of food reserves).
As a result, yolk and/or cytoplasm may vary slightly in compo• sition, and this may lead to the production of different types of young. VARIATION DUE TO MATERNAL AGE 117
LITERATURE CITED
Adams, T.S. 1970. J. Insect Physiol. 16:349
Arnold, J.W. 1959. Ann. Ent. Soc. Am. 52:229
Calow, P. 1973. Am. Nat. 107:559
De Wilde, J. and A. De Loof. 1973. Physiol, of Insecta 1:12
Haydak, M.H. 1957. Bee World 38:197
Lang, CA. 1 967. J. Gerontol. 22:55
Lansing, A.I. 1952. "Cowdry's Problems of Aging" 3rd ed. Williams and Wilkins, Baltimore, Maryland
Minks, A. K. 1 967. Arch. Neer. Zool . 17:175
Miquel, J., K. G. Bensch, D.E. Phil pott and H. Atlan. 1 972. Mech. Aging Develop. 1:71
Missonnier,. J. and M. Stengel. 1 966. Curt. Ann. Epiphyties 17:5
Nettles, W.C. and N.L. Betz. 1965. Ann. Ent. Soc. Am. 58:721
Raychaudhuri , A. and A. Butz. 1 965. Ann. Ent. Soc. Am. 58:541
Rockstein, M. and G.J. Farrell. 1972. J. Insect Physiol. 18:737
Rockstein, M. and J. Miquel. 1973. Physiol, of Insecta 1:371
Rockstein, M. and P.N. Srivastava. 1967. Experientia 23:1
Romoser, W.S. 1973. "The Science of Entomology". MacMillan Publ . Co., New York
Samis, H.V., F.C. Erk, and M.B. Baird. 1971. Exp. Gerontol. 6:9
Strangways-Dixon, J. 1961. J. Exp. Biol. 38:637
Wigglesworth, V.B. 1936. Quart. J. Microsc. Sci. 79:91-121 VARIATION DUE TO MATERNAL AGE 118
B. Reproduction in Hylemya antiqua
In HyTemya antiqua there are between 25 and 35 ovarioles.
Development of a particular follicular set occurs simultaneously
across all ovarioles, but within any one, the growth phase of
one follicle must be totally completed before the growth phase
of the next can begin.'
The rhythm of oviposition is strongly influenced by
the environment, notably by temperature and nutrition. All
the eggs belonging to a given ovarian cycle can be laid
(usually in small bathces) within 24 hours, or can be retained within the ovary while those from the following follicular set
are maturing, and laid at any time during this period (7 to
10 days under ideal conditions). Thus, the rhythm of egg
laying is not always a sign of the maturation rhythm of the
ovaries. Ripe eggs sitting in the ovary are apparently not
altered during this time.
By the time of imaginal maturation, an individual
possesses very few nutritive reserves, and must eat to survive.
No eggs are produced under conditions of poor nutrition. It
seems that a complete diet is necessary before egg development will take place. If fed solely on a diet of sugar water,
females exhibit a normal longevity, but the follicles remain
in a juvenile state of development. When conditions are ideal,
fecundity rapidly approaches the physiological maximum. If
conditions remain favorable, there will not be a slowing down
in the rhythm of the ovaries or in egg production as a female
^ This information was taken from Missonnier and Stengel, 1966. VARIATION DUE TO MATERNAL AGE 119
ages. (This is not to say that egg production in the offspring of a female is not affected by her age when she produces a particular egg batch.)
Unfavorable conditions, such as high temperature and/ or poor nutrition, provoke follicular resorption but do not influence functioning of the germarium. Resorption occurs only during the beginning of vitel1ogenesis , and may act as a regulatory mechanism in egg production. Thus, oogenesis seems to be composed of two phases. The first is oocyte production and the onset of vitel1ogenesis . The second is the complet• ion of vitel1ogenesis . The resorption of a follicle and the beginning of the growth phase of the next occur simultaneously, suggesting that a transfer of material is involved. The proportion of follicles which are resorbed is a function of the intensity of the adverse conditions. Low temperatures
(unless they occur for an extended period of time) do not cause resorption of follicles, but only retard development.
Physiologically fluctuations in the functioning of the ovarioles are evident. These are correlated with cyclic secretory activity in the corpora allata, although it is not clearly understood how this feedback mechanism operates.
Ovariole activity may be indirectly controlled by environmental factors such as food, since females tend to choose their nutrition in relation to their physiological .state. VARIATION DUE TO MATERNAL AGE 120
APPENDIX II
TABLE I
One-way Analysis of Variance on Mean Expectation of Life (E) at age x^. Age is given in days.
FACTOR SOURCE OF df MEAN SQUARE PROBABILITY (Ex) VARIATION
EO COHORT 1 28.1321 9.3555 0.005 ERROR 28 3.0070
E10 COHORT 1 3 .2024 1.6665 0.207 ERROR 28 1.9216
E20 COHORT 1 4.9845 3.5013 0.072 ERROR 28 1 .4236
E30 COHORT 1 10.0577 4.6174 0 .040 ERROR 28 2.1782
E40 COHORT 2 11.7614 4.6599 0.018 ERROR 27 2.5239 VARIATION DUE TO MATERNAL AGE 121
TABLE II
One-way Analysis of Variance on Probability of Being Alive (L) at age x. Age is given in days.
FACTOR SOURCE OF df MEAN SQUARE PROBABILITY (Lx) VARIATION
LIO COHORT 1 0 .0414 11.7670 0 .002 ERROR 28 0 .0035
L20 COHORT 1 0 .0277 5 .3649 0 .028 ERROR 28 0 .0051
L30 COHORT 1 0 .0463 6 .3070 0.018 ERROR 28 0 .0073
L40 COHORT 1 0 .0603 5 .7856 0 .023 ERROR 28 0 .0104
TABLE III
One-way Analysis of Variance on mean number of eggs per female per 48 hours .
SOURCE OF df MEAN SQUARE F PROBABILITY VARIATION
COHORT 2 94.7801 8.6664 0.001 ERROR 27 10.9365 VARIATION DUE TO MATERNAL AGE 122
TABLE IV
One-way Analysis of Variance on mean number of eggs produced per female per 48 hours, for five different age ranges. Age is expressed in days.
AGE SOURCE OF df MEAN SOUARE F PROBABILITY VARIATION
1-10 COHORT 1 61.2666 1.9307 0.182
ERROR 1 8 31.7330
11-20 COHORT 1 121.4390 5.7342 0.028 ERROR 1 8 21.1 779
21-30 COHORT 1 156.9100 12.1296 0.003 ERROR 18 12.9361
31-40 COHORT 1 7.9282 0.5320 0.475 ERROR 18 14.9031
41-50 COHORT 1 18.4239 1.1882 0.290 ERROR 18 15.5058 VARIATION DUE TO MATERNAL AGE 123
TABLE V
Analysis of Variance Statistics A = Developmental period from egg to pupae (in days), analysed across provenance group and cohort. B = Developmental period from pupa to adult emergence from puparium (in days). Cohort data were pooled over SFU and Guelph provenance groups.
POPULATION SOURCE OF df MEAN SQUARE PROBABILITY TYPE VARIATION
A(l) DEMO Provenance 2 21.4088 3.2987 0 .041 TEMP Error 90 6.4900
(2) DEMO Cohort 1 22 .0387 3.7531 0.057 TEMP Error 97 5 .8721
(3) DIAP Provenance 2 47.5567 2.7044 0.077 Error 47 1 7 .5852
(4) DIAP Cohort 2 27 .771 4 1.5071 0.232 Error 47 18.4271
B(l) TEMP Cohort 2 12.4681 1.8810 0.162 Error 54 6.6285
(2) DIAP Cohort 2 4.7408 0.6233 0 . 540 Error 56 7 .6061 VARIATION DUE TO MATERNAL AGE 124
TABLE VI
Analysis of Variance Statistics : Total percentage emergence from puparia B = Percentage of emerged individuals which are female. Cohort data were pooled over SFU and Guelph provenance groups.
POPULATION SOURCE OF df MEAN SQUARE PROBABILITY TYPE VARIANCE
A(l) DEMO Cohort 2 187.5941 0.5215 0.597
Error 46 359.7297
(2) TEMP Cohort 2 3 .901 7 0.0102 0.990 Error 61 381.1340
(3) DIAP Cohort 2 239 .0865 0.8750 0.422 Error 59 273 .2534
B(l) DEMO Cohort 1 802.0999 9.5329 0.004 Error 47 84.1404
(2) TEMP Cohort 2 61 7 .7551 4.2225 0.020 Error 51 146 .3003
(3) DIAP Cohort 2 232 .2859 2 . 5420 0.087 Error 59 91 .3784 VARIATION DUE TO MATERNAL AGE 125
TABLE VII
Analysis of Variance Statistics on weight per pupa (in grams). Data were pooled across population type.
* z Guelph and field provenance groups.
** = SFU provenance group.
SOURCE OF df MEAN SQUARE PROBABILITY VARIATION
Provenance 2 0.86565 6 .5992 0 .002 Error 80 0.13117
Cohort* 2 0.86052 5.3701 0.010 Error 30 0 .1 6024
Cohort ** 2 0.47739 3.7799 0.030 Error 48 0.12629