Copyright 0 1985 by the Genetics Society of America
GENETICS O F FACTORS AFFECTING T H E LIFE
HISTORY O F
DROSOPHILA MELANOGASTER.I. FEMALE PRODUCTIVITY
YUCHIRO HIRAIZUMI
Department of Zoology, The University of Texas, Austin, Texas 78712
Manuscript received June 1 1 , 1984 Revised copy accepted February 21, 1985
ABSTRACT
Starting from four basic strains of Drosophila melanogaster, two laboratory strains (cn bw, Tokyo) and two isofemale lines (B-102, B-103) originated from a wild population in Texas, we constructed by repeated backcrosses through females for 20 or more generations a total of 16 strains of all possible combi- nations between the chromosome sets and cytoplasmic classes. Females from these 16 synthesized strains were then examined for their reproductive per- formance during their entire life span.-The chromosome set from the cn bw strain was found to associate with the highest female productivity when the age of females was very young, but these females ceased their reproduction and died relatively earlier, resulting in a smaller number of total progeny. The B-102 and B-103 chromosome sets, on the other hand, were associated with the lowest productivity when the females were young, but they lived and con- tinued reproduction longer, resulting in a larger number of total progeny. The Tokyo chromosome set was associated with female productivity intermediate between the other two groups.-Cytoplasmic factors were found to affect the productivity of young females, with the cytoplasm from the cn bw strain asso- ciated with the highest productivity. Longevity was not cytoplasmically af- fected.-There was a clear interaction in female productivity between the Tokyo chromosome set and the cytoplasm from the Texas isofemale lines; the lifetime female productivity, as well as longevity, associated with the Tokyo chromosome set was found to increase considerably when it was substituted into the cytoplasm of the Texas isofemale lines. This chromosome-cytoplasm interaction appeared to be independent of the two systems of hybrid dys- genesis.
HE fitness of a genotype consists of many components that interrelate in
T
a particular complicated way to determine the total fitness or adaptedness of the genotype. Among various components of fitness, perhaps the most es- sential would be viability and fertility. T h e former is important for the survival of an individual at a given generation, whereas the latter is important for the production of the next generation. How these two components interact in determining the total fitness is a difficult question to answer. Their relative importance will depend not only upon genotypes but also upon environmental conditions. T h e present author studied the relationship between developmental time (period from egg laying to adulthood) and female productivity (number454 Y . HIRAIZUMI
of progeny produced by a female) in Drosophila melanogaster and he found that these two components of fitness correlated negatively within a range of certain levels such that a genotype with a faster developmental time tended to show a lower productivity and vice versa (HIRAIZUMI 1961). Based upon these observations he suggested that, given a certain environmental condition, there might exist the best combination or combinations between developmental time and female productivity that maximized the total fitness as measured by the Malthusian parameter m (FISHER 1930) and natural selection would select for such a combination, but not necessarily for a faster developmental time or a higher productivity. HIRAIZUMI (1 96 1 ) further suggested, by comparing the m
values for several model cases, that relative contributions of developmental time and productivity to the total fitness would differ depending upon the environmental conditions. For example, under an environment in which the life cycle of the organism slowed down, the developmental time would become relatively more important and, when the productivity decreased to a lower level, it would become more important relative to the developmental time. A negative correlation between female productivity and viability (or their related characters) has also been reported by several other investigators (GOWEN and JOHNSON 1946; SIMMONS, PRESTON and ENCELS 1980; ROSE and CHARLES-
During the past few decades, many studies have been made on various components of fitness in Drosophila such as developmental time, female pro- ductivity, viability and longevity (for a review see LAMB 1978), but, in most cases, those studies were made for each component separately, and genetic studies of the whole life history of Drosophila have been rather scarce. A series of investigations were initiated a few years ago in this laboratory to study the genetics of factors affecting the life history of
D.
melanogaster and to obtain a better understanding of the structure of fitness-how the components interact in determining the total fitness. T h e present paper, the first of this series of studies, will report the modes of progeny production by females of different genotypes throughout their entire reproductive life spans. Special attention will be paid to a possible effect of a cytoplasmic factor or factors on female productivity.WORTH 1981).
MATERIALS AND METHODS
Strains: T h e strains of D . melanogaster used in this study are as follows.
cn bw is a standard laboratory strain in which the second chromosome is marked with two recessive mutants, cn (cinnabar eyes, 2R-57.5) and bw (brown eyes, 2R-104.5). T h e cn bw genotype is white eyed. This strain has been used in this laboratory as a standard for various other experi- ments in the past.
Tokyo is a standard wild-type laboratory strain that was originally established from flies captured in a wild population in Tokyo, Japan, more than 30 yr ago. This strain has been kept in this laboratory by mass transfer of a relatively small population size.
B-102 and B-103 a r e isofemale lines each of which was established from a wild-inseminated female captured in a wild population in Brownsville, Texas, in 1979. Each of these lines has since been kept in this laboratory by mass transfer in a couple of dozen small culture vials.
FEMALE PRODUCTIVITY IN DROSOPHILA 455
cross were then crossed to five males from the corresponding basic strain from which the parental males were taken. Four replications were made for each combination. This procedure was repeated for at least 20 generations to substitute the chromosome set from one basic strain into cytoplasm of the other. A total of 16 such “backcross” strains were synthesized in this way. In this report the origin of the chromosome set will be indicated by writing the basic strain symbol before the parentheses and that of the cytoplasm within the parentheses. For example, the synthesized strain with a chromosome set from the B-102 and cytoplasm from the cn bw strain will be symbolized as
Exferimental procedures: A group of ten to 20 virgin females was collected within a 6-hr period from each of the 16 synthesized strains at the 20th backcross generation and aged in culture vials for an additional 24 hr. Each virgin was then crossed to three cn bw males, 2-4 days of age, taken from the standard cn bw strain. Parents were kept in each vial for 2 days for the first brood and then transferred to the new culture vials for another 2 days for the second brood. This transfer procedure was continued until the parental female died. Three young cn bw males were added in the seventh, 14th and 21st broods so that there were sufficient numbers of fertile males in each mating. The same experiment was repeated at the 23rd to 25th generation of backcross by taking additional virgin females from each of the 16 strains such that the total number of females tested per strain in the two sets of experiments became 30. An additional two to three extra replications were included in the second set to back up any accidental loss of experimental females. More than 500 females were examined in the two sets of experiments among which only one female of the type B-102 (B-102) was found to be completely sterile and this female was excluded from the analyses. For many strains, the total number of replications completed was more than 30, and in such cases the replications in excess of 30 (usually one or two) were excluded randomly. Since the data from the two sets of experiments were homogeneous in young and lifetime female produc- tivity as well as in longevity, they were pooled for statistical analyses of these variables.
At the 28th to 30th generation of backcross, a total of 22 virgin females were collected from each strain and, after aging them for 24 hr, they were individually mixed with three cn bw males for 1 day to ensure copulation. The female and males were then transferred to a fresh culture vial to allow the female to oviposit for 24 hr. The number of eggs layed and the number of emerged adult flies were recorded for each vial separately.
A standard cornmeal-agar medium was used for all experiments at a room temperature of 23- 24”.
B-102 (cn bw).
RESULTS
Total number of progencj produced: Table 1 summarizes the average number of lifetime progeny per female in each strain. This table also includes the results of variance analysis. Not surprisingly, there was a statistically significant heterogeneity in the total number of progeny produced among the chromo- some sets. T h e chromosome set from the standard cn bw strain was associated with the lowest female productivity, whereas the set from the Tokyo strain was intermediate and the sets from the B-102 and B-103 strains were associated with the highest female productivity. There was no significant difference in female productivity among different cytoplasmic classes, but there was a sig- nificant interaction between chromosome sets and cytoplasmic classes. Since the interaction term was significant, further analyses were made by testing homogeneity in female productivity among cytoplasmic classes within each chromosome set. T h e only chromosome set that showed a significant hetero- geneity was that of Tokyo (F = 5.23; d.f. = 3, 116, P
<<
0.01); the Tokyo (B-102) and Tokyo (B-103) strains produced more progeny than did the Tokyo456 Y . HIRAIZUMI
TABLE 1
Average number of total progeny perfemale an each strain
~
~~ ~
Chromosome set
<:ytopla\m cn bw Tokyo B-IO2 B-103 Mean
(cn bw) 142.00 170.97 349.33 329. 13 247.86
(Tokyo) 118.77 165.17 323.90 321.20 232.26 (B-102) 134.53 240.20 295.03 274.07 235.94 (B-103) 141.43 246.10 274.23 344.03 251.45
Mean 134.17 205.61 310.63 317.11 241.88
Sourre of‘ variation MS d.f. F P
Among chromosomes 9321 18.92 3 67.20 <<0.01 Among cytoplasms 10206.62 3 0.74 NS Interaction 366 1 1.27 9 2.64 <0.01
Error 13869.87 464
NS = not significant.
any significant interaction (F = 1.33; d.f. = 6, 348; P = 0.25). Based on these results, it seems reasonable to conclude that the significant interaction shown in Table 1 is in fact due to an interaction between the Tokyo chromosome set and the four cytoplasmic classes. One easy explanation for the increased productivity in the Tokyo (B-102) and Tokyo (B-103) strains might be to assume “heterosis” between chromosome segments, one from the Tokyo and the other from the B-102 or B-103 strains, and such heterozygosities still remained in these synthesized strains even after 20 or more generations of backcross matings. However, this possibility is less likely since their reciprocal combinations, B-102 (Tokyo) and B-103 (Tokyo), did not show any such tend- encies.
Longevity: T h e longevity of each female was measured by the number of broods in which she was still alive. Average survival length was then computed for each genotype and it is shown in Table
2,
together with the results of variance analysis. T h e cn bw chromosome set was associated with the shortest and Tokyo with the intermediate, and the B-102 and B-103 chromosome sets were associated with the longest survival length. There were statistically sig- nificant differences in longevity among chromosome sets, but no difference was demonstrated among different cytoplasmic classes, and there was no sig- nificant interaction between chromosomal and cytoplasmic factors. It should be noted, however, that there was a considerable increase in longevity when the Tokyo chromosome set was placed into t h e B-102 or B-103 cytoplasm.FEMALE PRODUCTIVITY IN DROSOPHILA
TABLE 2
Average longevity of females in each strain
457
Chromosome set
Cytoplasm cn bw Tokyo B-102 B-103 Mean
(cn bw) 9.53 13.03 16.73 16.23 13.88
(Tokyo) 10.07 12.93 16.27 16.47 13.93
(B-102) 9.43 15.37 16.10 14.90 13.95 (B-103) 10.60 15.93 15.07 16.30 14.48
Mean 9.91 14.32 16.04 15.98 14.06
Source of variation MS d.f. F P
Among chromosomes 995.86 3 43.16 <<0.01
Among cytoplasms 9.26 3 0.40 NS
Interaction 34.24 9 1.48 NS
Error 23.07 464
Longevity was measured by the number of broods after which the females were found alive. N S = not significant.
Brood
FIGURE 1.-Average number of progeny produced in each brood for each chromosome set. An average was calculated over the four cytoplasmic classes for each chromosome set, except for the Tokyo set for which the average was taken for the cn bw and Tokyo cytoplasmic classes in one group and for the B-102 and B-103 in the other, since these t w o groups showed heterogeneous female productivity.
In the above analyses, however, only the total number of progeny produced by a female through her entire life span was examined. Further analyses were conducted to examine the distribution of progeny production along the whole life span of the females.
458 Y. HIRAIZUMI
TABLE 3
Average value of d f o r each strain
Chromosome set
Cytoplasm en bw Tokyo B-102 B- 103 Mean
(cn bw) -5.40** -4.30** 6.47** 0.77 -0.62 (Tokyo) -1.97 -7.07** 9.47** 3.87** 1.08 (B-102) -0.50 -5.37** 6.70** 0.33 0.29 (B-103) -2.17 -3.00* 1.27 7.03** 0.78
Mean -2.51** -4.93** 5.98** 3.00** 0.38
Source of variation MS d.f. F P
Among chromosomes 2989.69 3 45.77 <<0.01
Among cytoplasms 65.87 3 1.01 NS
Interaction 264.47 9 4.05 <<0.01
Error 65.32 464
d = (number of progeny produced in the second brood)
-
(number of progeny produced in the first brood).*
P < 0.05.**
P c 0.01.mosome set except for that of Tokyo in which the average was taken for the cn bw and Tokyo cytoplasmic classes in one group and for the B-102 and B- 103 in the other, since these two groups showed heterogeneous female pro- ductivity. Several interesting points can be seen in this figure. First, although it is apparent that the number of progeny produced over the entire reproduc- tive period is the largest for B-102 and B-103, intermediate for Tokyo and the smallest for the cn bw chromosome set, this order is entirely reversed when productivity of the first brood alone is considered: female productivity is the highest for cn bw, intermediate for Tokyo and the lowest for the B-102 and B-103 chromosome sets. A detailed analysis of the effects of chromosome sets upon young female productivity, together with the effect of cytoplasmic fac- tors, will be presented later.
FEMALE PRODUCTIVITY IN DROSOPHILA 459
FIGURE 2.-Average number of progency produced in each brood for each cytoplasmic class. An average was taken over the three chromosome sets (cn bw, B-102 and B-103) for each cyto- plasmic class. The Tokyo chromosome set was not included in this figure since there was a significant chromosome-cytoplasm interaction involving this set.
B-103 chromosome sets, both showing consistently positive d values (F = 5.98;
d.f. = 3, 116; P
<<
0.01 and F = 2.98; d.f. = 3, 116; P<
0.05 for theB-
102 and B-103 chromosome set, respectively), but there appeared to be no
clear-cut pattern between these two sets in the order of d values over the cytoplasmic classes. There is, therefore, a suggestion for the presence of chro- mosome-cytoplasm interaction of an irregular type with respect to the d value. Since, as mentioned in MATERIALS AND METHODS, the females tested were collected within a 6-hr period, there could be a chance of some degree of heterogeneity in the average age of females tested among strains, and this may well be the main cause of the significant interaction in the d value. Whether it is due to a real chromosome-cytoplasm interaction or to experimental errors as mentioned above is not known at this time, but it seems to be well estab- lished that different chromosome sets show different magnitudes of d values.
Figure 2 shows the number of progeny produced in each brood for each cytoplasmic class. An average was taken over the three chromosome sets for each cytoplasmic class. T h e Tokyo chromosome set was not included in this figure since there was a significant chromosome-cytoplasm interaction involving this set. In general, the four lines run closely along the entire reproductive
Y . HIRAIZUMI 460
T A B L E 4
Average number of progeny produced in the first brood of each strain
Chromosome set
Cytoplasm cn bw Tokyo B-102 B-103 Mean
( c n bw) 26.13 18.17 14.77 20.23 19.83
(Tokyo) 18.47 18.17 9.60 12.87 14.78
(B-102) 19.20 17.40 12.03 12.37 15.25
(B- 103) 22.33 18.47 13.93 14.53 17.32
Mean 21.53 18.05 12.58 15.00 16.79
Source of variation MS d.f. F P
A m o n g chromosomes 1799.48 3 36.34 <<0.01
Aniong cytoplasms 636.82 3 12.86 <<0.01
Interaction 94.91 9 1.92 <0.05
Error 49.52 464
102 and B-103 sets showed the lowest productivity. As described earlier, there was no main effect of cytoplasmic factors on the total number of progeny produced through the entire life span of the females, but they in fact affect the productivity of young females in the first and probably a few more suc- ceeding broods. Since there was a significant chromosome-cytoplasm interac- tion, an additional analysis was made for each chromosome set separately. T h e Tokyo chromosonie set was the only one that showed homogeneous female productivity among cytoplasmic classes in this brood; all others showed signif- icant heterogeneity. When the strains with the Tokyo chromosome set were excluded from the analysis, the interaction term for the remainder became not significant ( F = 1.01; d.f. = 6 , 348; P
>
0.25), although the main effects of chromosome sets and of cytoplasmic classes remained highly significant. Whether the significant interaction involving the Tokyo chromosome set is real or due to experimental errors such as a slightly heterogeneous age of the females tested is not understood at this time.FEMALE PRODUCTIVITY IN DROSOPHILA 461
T A B L E 5
Average egg-to-adult percentage for each strain
Chromosome set
Cytoplasm cn bw Tokyo B-102 8-103 Mean
(cn bw) 82.9 89.6 79.7 86.7 84.7
(Toky 0) 74.6 78.7 79.2 85.0 79.4
(B- 102) 78.7 88.7 77.5 84.5 82.4
(B- 103) 81.3 79.2 85.0 86.6 83.1
Mean 79.4 84.1 80.4 85.7 82.4
Source of variation s.s d.f. X 2 P
Among chromosomes 862.22 3 23.10 KO.01 Among cytoplasms 899.60 3 24.1 1 <<0.01
Interaction 423.76 9 11.36 NS
Error 37.32*
For the procedures of statistical analysis, see text. NS = not significant. * 821122 = 37.32
analyses are also shown in Table
5.
There were statistically significant differ- ences among chromosome sets as well as among cytoplasmic classes, but the chromosome-cytoplasm interaction term was not significant. T h e (Tokyo) cy- toplasm and the cn bw chromosome set appeared to associate with somewhat reduced egg-to-adult proportions. There are, therefore, some indications of differential larval stage viability caused by either cytoplasmic or chromosomal factors. T h e magnitude of reductions, however, are not so large in both cases to account for the large differences in the female productivity found in the previous experiments, and it appears reasonable to conclude that the observed differences in productivity are largely due to differences in the numbers of egg production. It should be noted at this point that the absence of chromo- some-cytoplasm interaction indicates the absence of the effect of the SF sterility (reduced egg hatchability) due to the I-R system of hybrid dysgenesis.DISCUSSION
Although the number of genotypes examined in the present study was small and, therefore, the information extracted from the results was rather limited, there were several useful findings worthy of summarization here. First, the “shape” of the distribution of progeny production along the whole life span of
462 Y. HIRAIZUMI
of female genotypes among which some produce more progeny at a young age period but cease reproduction relatively earlier and the others produce fewer progeny when they are young but continue their reproduction longer resulting in larger numbers of total progeny. If these genotypes coexist in a population, they will be exposed to the pressure of natural selection. Which type could have selective advantage will depend upon the environmental conditions. Un- der the environment in which the population maintains itself with overlapping generation time, perhaps the genotypes that produce more progeny at a young age, even if the potential total number of progeny is smaller, may be selected for. On the other hand, under the environment in which the generation times are somewhat separated, the genotypes with the larger number of progeny produced during the entire life span may become selectively advantageous. At this point, one may wonder whether the highest productivity of the cn bw (cn bw) females in the first brood is not due to female genotype per se but, rather,
is due to male genotype (cn bw) that may interact in mating behavior with the genotypes of females. For example, the cn bw males may tend to copulate with the cn bw (cn bw) females more quickly than with the other genotype females, thus allowing the cn bw (cn bw) females to produce fertilized eggs earlier. This point was examined as follows. Virgin females, 24-30 hr of age, from the four strains of cn bw (cn bw), Tokyo (Tokyo), B-102 (B-102) and B-103 (B-103), were individually crossed to three cn bw males, 2-4 days of age. N o anesthetic was used during these procedures. Immediately after the two sexes were placed together in a culture vial, the occurrence of copulation was watched in each vial for 5 hr. T h e parental flies, regardless of whether or not they copulated during this period, were kept in each vial for 2 days to form the first brood and then discarded. T h e females tested were classified into two groups, A and B; group A included those females that copulated within the 5-hr period and group B included the rest of females. T h e results were as follows. The pro- portion of females included in group A was heterogeneous among the four strains
(xg
= 43.75, P<<
0.01): it was the highest (48 of 50 females) for the cn bw (cn bw) strain, intermediate (16 of 30 females) for Tokyo (Tokyo) and lowest (ten of 30 and 26 of 62 females) for the B-102 (B-102) and the B-103 (B-103) strains, respectively. T h e average number of progeny per female in group A was, as might be expected, larger than that in group B for each strain, although the weighted average of the differences, 1.70, over the four strains did not deviate significantly from zero ( F = 1.21; d.f. = 1, 164; P>
0.25). T h e strain-group interaction term was not statistically significant ( F =0.39; d.f. = 3, 164; P
>
0.75), but the difference among strains was significant with the cn bw (cn bw) strain showing the highest female productivity (F =FEMALE PRODUCTIVITY IN DROSOPHILA 463
the cn bw (cn bw) females in the first brood, at least a large portion of it, is due to their highest genetic potential in producing progeny in the first brood but not due to an interaction with the cn bw males used.
T h e second point that emerged from this study is that cytoplasmic factors can affect female productivity, although to a much lesser extent than do the chromosomal factors. T h e main effects of cytoplasmic factors seem to be lim- ited to relatively young females. Generally speaking, the females of the cn bw cytoplasmic class show somewhat higher productivity than those having the other cytoplasmic classes when the age of females is young, but, in addition to such a simple main effect, there is a significant interaction between the chro- mosomal and cytoplasmic factors. At this point, one may wonder whether this interaction is in fact related to either of the two systems of hybrid dysgenesis, P-M (KIDWELL, KIDWELL and SVED 1977) and I-R (for review see BREGLIANO et al. 1980) systems. T h e latter possibility (reduced egg hatchability) was al- ready ruled out in the previous section (Table
5).
T h e former possibility (in- terruption in gonadal development in females) was examined by raising the tested females at 28.5", and the results were completely negative.T h e third point, which is possibly related to the first, is that the Tokyo and the cn bw chromosome sets are associated with a peculiar pattern of female productivity; the number of progeny for the second brood decreases when compared with that of the first brood, but then progeny number increases in the third and succeeding broods. T h e biological mechanism causing this trend is not clear at this time, but it appears that, during the past many generations under the laboratory culture conditions, the procedures of maintaining these strains might have operated to select for such a genotype associated with an increased productivity in the first brood.
T h e present investigation covered only a part of the whole life history of a genotype, and more observations of other characters, as well as of other gen- otypes, are needed to better understand the total fitness, adaptation and evo- lution of species. Those are left for future studies.
This work was supported by research grant AG-01934 from the National Institute on Aging.
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FISHER, R. A., 1930
GOWEN, J. W. and L. E. JOHNSON, 1946 On the mechanism of heterosis. I . Metabolic capacity of different races of Drosophila melanogaster for egg production. Am. Nat. 8 0 149-179. HIRAIZUMI, Y., 1961 Negative correlation between rate of development and female fertility in
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KIDWELL, M . G., J. F. KIDWELL and J . A. SVED, 1977 Hybrid dysgenesis in Drosophila melano- gaster: a syndrome of aberrant traits including mutation, sterility and male recombination. Genetics 86: 813-833.
Ageing. pp. 43-104. In: The Genetics and Biology of Drosophila, Vol. 2c, Edited by M. ASHBURNER and T. R. F. WRIGHT. Academic Press, New York.
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ROSE, M. R. and B. CHARLESWORTH, 1981 Genetics of life history in Drosophila melanogaster. 1.
Pleiotropic effects of fitness o f mutations Sib analysis of adult females. Genetics 97: 173-186.
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