CHROMOSOMAL DNA SYNTHESIS IN DROSOPHILA MELANOGASTER

Analysis of labeling patterns in three chromosome segments of Drosophila melanogaster has shown that the replicative activity within chromosomes is temporally ordered. Moreover, specific labeling patterns on one chromosome occur with specific patterns on another chromosome with a very high degree of correlation. This circumstance leads to the conclusion that DNA synthesis among all the regions in the three chromosome segments studied is coordinated. The various labeling patterns observed in any one chromosome and the combinations of labeling patterns observed in all three chromosome segments can be arranged in ordered arrays, if one assumes that the DNA synthesis in each chromosome region will go to completion without stopping once it has started. Such arrays can serve as models for the temporal order of DNA synthesis among chromosome regions. They predict that in any one chromosome DNA replication begins and ends at very few loci and that synthesis at a larger number of points occurs at an intermediate time.     

CYTODIFFERENTIATION IN THE ROSY MUTANT OF DROSOPHILA MELANOGASTER

In the rosy mutant of Drosophila melanogaster, two types of autofluorescent cytoplasmic inclusions are found in the cells of the posterior region of the fatbody at the prepupal stage. Bright yellow autofluorescent granules accumulating within larger inclusions clearly demarcate this area of the fatbody which also contains cobalt blue fluorescent globular material. Such inclusions were not noted in the normal Ore-R strain at this stage nor in the series of mutant strains examined other than the rosy² and maroon-like mutants. The pattern of biochemical deviation of the latter two mutants is known to be identical to that of the rosy mutant, and a portion of this mutant upset can be ascribed to the absence of xanthine dehydrogenase. These mutants lack the products of enzyme activity, uric acid and isoxanthopterin, and accumulate their precursors, hypoxanthine and 2-amino-4-hydroxypteridine. Chromatographic studies on the fatbody of rosy prepupae have shown that 2-amino-4-hydroxypteridine is limited to the posterior region; this correspondence in location as well as color of fluorescence indicates that the cobalt blue auto fluorescent globules in the fatbody contain 2-amino-4-hydroxypteridine. In the normal strain, isoxanthopterin was identified in the chromatograms of the posterior region of the fatbody, but it was not obtained from the anterior region of the fatbody. On the other hand, xanthine dehydrogenase activity could be demonstrated throughout the fatbody of the normal strain. The restriction of isoxanthopterin to a certain group of fat cells in the wild type strain and its absence from other fat cells can be explained by the differential distribution of its immediate precursor, 2-amino-4-hydroxypteridine, as displayed in the mutant rosy.     

THE EVOLUTIONARY GENETICS OF MALE LIFE-HISTORY CHARACTERS IN DROSOPHILA MELANOGASTER

Alternative models of the maintenance of genetic variability, theories of life-history evolution, and theories of sexual selection and mate choice can be tested by measuring additive and nonadditive genetic variances of components of fitness. A quantitative genetic breeding design was used to produce estimates of genetic variances for male life-history traits in Drosophila melanogaster. Additive genetic covariances and correlations between traits were also estimated. Flies from a large, outbred, laboratory population were assayed for age-specific competitive mating ability, age-specific survivorship, body mass, and fertility. Variance-component analysis then allowed the decomposition of phenotypic variation into components associated with additive genetic, nonadditive genetic, and environmental variability. A comparison of dominance and additive components of genetic variation provides little support for an important role for balancing selection in maintaining genetic variance in this suite of traits. The results provide support for the mutation-accumulation theory, but not the antagonistic-pleiotropy theory of senescence. No evidence is found for the positive genetic correlations between mating success and offspring quality or quantity that are predicted by “good genes” models of sexual selection. Additive genetic coefficients of variation for life-history characters are larger than those for body weight. Finally, this set of male life-history characters exhibits a very low correspondence between estimates of genetic and phenotypic correlations.     

MULTIPLE GENETIC MECHANISMS FOR THE EVOLUTION OF SENESCENCE IN DROSOPHILA MELANOGASTER

We present the results of selection experiments designed to distinguish between antagonistic pleiotropy and mutation accumulation, two mechanisms for the evolution of senescence. Reverse selection for early-life fitness was applied to laboratory populations of Drosophila melanogaster that had been previously selected for late-life fitness. These populations also exhibited reduced early-age female fecundity and increased resistance to the stresses of starvation, desiccation, and ethanol, when compared to control populations. Reverse selection was carried out at both uncontrolled, higher larval rearing density and at controlled, lower larval density. In the uncontrolled-density selection lines, early-age female fecundity increased to control-population levels in response to the reintroduction of selection for early-age fitness. Concomitantly, resistance to starvation declined in agreement with previous observations of a negative genetic correlation between these two characters and in accordance with the antagonistic-pleiotropy mechanism. However, resistance to stresses of desiccation and ethanol did not decline in the uncontrolled-density lines during 22 generations of reverse selection for early-life fitness. The latter results provide evidence that mutation accumulation has also played a role in the evolution of senescence in this set of Drosophila populations. No significant response in early-age fecundity or starvation resistance was observed in the controlled-density reverse-selection lines, supporting previous observations that selection on Drosophila life-history characters is critically sensitive to larval rearing density.     

COMPLEX TRADE-OFFS AND THE EVOLUTION OF STARVATION RESISTANCE IN DROSOPHILA MELANOGASTER

The measurement of trade-offs may be complicated when selection exploits multiple avenues of adaptation or multiple life-cycle stages. We surveyed 10 populations of Drosophila melanogaster selected for increased resistance to starvation for 60 generations, their paired controls, and their mutual ancestors (a total of 30 outbred populations) for evidence of physiological and life-history trade-offs that span life-cycle stages. The directly selected lines showed an impressive response to starvation selection, with mature adult females resisting starvation death 4–6 times longer than unselected controls or ancestors—up to a maximum of almost 20 days. Starvation-selected flies are already 80% more resistant to starvation death than their controls immediately upon eclosion, suggesting that a significant portion of their selection response was owing to preadult growth and acquisition of metabolites relevant to the stress. These same lines exhibited significantly longer development and lower viability in the larval and pupal stages. Weight and lipid measurements on one of the starvation-selected treatments (SB_1–5), its control populations (CB_1–5), and their ancestor populations (B_1–5) revealed three important findings. First, starvation resistance and lipid content were linearly correlated; second, larval lipid acquisition played a major role in the evolution of adult starvation resistance; finally, increased larval growth rate and lipid acquisition had a fitness cost exacted in reduced viability and slower development. This study implicates multiple life-cycle stages in the response to selection for the stress resistance of only one stage. Our starvation-selected populations illustrate a case that may be common in nature. Patterns of genetic correlation may prove misleading unless multiple pleiotropic interconnections are resolved.     

RESOURCE ACQUISITION AND THE EVOLUTION OF STRESS RESISTANCE IN DROSOPHILA MELANOGASTER

Resistance to environmental stress is one of the most important forces molding the distribution and abundance of species. We investigated the evolution of desiccation stress resistance using 20 outbred Drosophila melanogaster populations directly selected in the laboratory for adult desiccation resistance (D), postponed senescence (O), and their respective controls (C and B). Both aging and desiccation selection increased desiccation resistance relative to their controls, creating a spectrum of desiccation resistance levels across selection treatments. We employed an integrative approach, merging data on the life histories of these populations with a detailed physiology of water balance. The physiological basis of desiccation resistance may be mechanisms enhancing either resource conservation or resource acquisition and allocation. Desiccation-resistant populations had increased water and carbohydrate stores, and showed age-specific patterns of desiccation resistance consistent with the resource accumulation mechanism. A significant proportion of the resources relevant to resistance of the stress were accumulated in the larval stage. Males and females of desiccation-selected lines exhibited distinctly different patterns of desiccation resistance and resource acquisition, in a manner suggesting intersexual antagonism in the evolution of stress resistance. Preadult viability of stress-selected populations was lower than that of controls, and development was slowed. Our results suggest that there is a cost to preadult resource acquisition, pointing out a complex trade-off architecture involving characters distributed across distinct life-cycle stages.     

FRACTIONATION OF THE EYE PIGMENTS OF DROSOPHILA MELANOGASTER

Eye pigments of normal and mutant types of D. melanogaster have been extracted with water and fractionated by chromatographic adsorption on powdered talc. Spectra of all the fractions obtainable in solution have been measured and the general chemical behavior of the pigments is described. Two chemically distinct groups of pigments are found, to be identified with the earlier designated red and brown components. The red component in the wild-type eye contains three well defined pigments, two of them capable of further subdivision so that the total number of fractions obtained is five. There is also present a brown component pigment which could not be treated quantitatively by the methods employed. All members of the wild-type red component are found in cinnabar eyes, unaccompanied by the brown component. Conversely, brown eyes contain a pigment indistinguishable from the wild-type brown component, virtually alone. In sepia eyes, one red component and two brown component pigments can be distinguished, all three pigments differing from those of wild-type eyes. Pigments apparently identical with those found in wild-type melanogaster eyes have also been found in D. virilis.     

THE EVOLUTION OF DEVELOPMENT IN DROSOPHILA MELANOGASTER SELECTED FOR POSTPONED SENESCENCE

The role of development in the evolution of postponed senescence is poorly understood despite the existence of a major gerontological theory connecting developmental rate to aging. We investigate the role of developmental rate in the laboratory evolution of aging using 24 distinct populations of Drosophila melanogaster. We have found a significant difference between the larval developmental rates of our Drosophila stocks selected for early (B) and late-life (O) fertility. This larval developmental time difference of approximately 12% (O > B) has been stable for at least 5 yr, occurs under a wide variety of rearing conditions, responds to reverse selection, and is shown for two other O-like selection treatments. Emerging adults from lines with different larval developmental rates show no significant differences in weight at emergence, thorax length, or starvation resistance. Long-developing lines (O, CO, and CB) have greater survivorship from egg to pupa and from pupa to adult, with and without strong larval competition. Crosses between slower developing populations, and a variety of other lines of evidence, indicate that neither mutation accumulation nor inbreeding depression are responsible for the extended development of our late-reproduced selection treatments. These results stand in striking contrast to other recent studies. We argue that inbreeding depression and inadvertent direct selection in other laboratories' culture regimes explain their results. We demonstrate antagonistic pleiotropy between developmental rate and preadult viability. The absence of any correlation between longevity and developmental time in our stocks refutes the developmental theory of aging.     

VARIATIONS IN CUTICULAR HYDROCARBONS AMONG THE EIGHT SPECIES OF THE DROSOPHILA MELANOGASTER SUBGROUP

In addition to protecting against desiccation, some of the hydrocarbons of the waxy cuticle have previously been shown to be mating pheromones in Drosophila melanogaster and D. simulans. Therefore, cuticular hydrocarbons were compared among the eight species in the D. melanogaster subgroup. For the two cosmopolitan species and several geographic strains that were studied, all males are quite similar with very abundant monoenes. The major compound in most cases is 7-tricosene. Only three exceptions were found: D. sechellia, and the Afrotropical strains of D. melanogaster and D. simulans. A significant sexual dimorphism exists in three species: D. melanogaster, D. erecta, and D. sechellia. Greater variation was observed in females than in males. D. erecta is singular in the production of long-chain molecules (31–33 carbons). Only three species (D. melanogaster, D. erecta, and D. sechellia) produce diene in significant amounts. Such products, especially 7,11-heptacosadiene, are known to act as aphrodisiacs for D. melanogaster males. In the five other species, females show only quantitative differences from males, generally with 7-tricosene as the most abundant compound. This compound is an aphrodisiac for D. simulans males. Some species such as D. yakuba, D. teissieri, D. orena, D. mauritiana, and the Seychelles strain of D. simulans are almost identical in the chemical composition of cuticular hydrocarbons. In contrast, important variations are observed between geographic populations of D. melanogaster and D. simulans.     

THE TIME CURVE OF FACET DETERMINATION IN AN ULTRABAR STOCK OF DROSOPHILA MELANOGASTER

By a dissection of the data obtained by Driver on the effective periods at different temperatures in males and females of an ultrabar stock of Drosophila melanogaster it has been found that a symmetrical sigmoid curve satisfactorily describes the time course of the facet-determining reaction. Consequently the differences between members of the bar series in regard to this reaction do not represent merely developmental arrests of the process at some greater or lesser distance from a common upper asymptote, but the termination of the process is approached asymptotically. The velocity constant/temperature relation shows a discontinuity in the neighborhood of 21° which may be causally related to the change in the position of the effective period from the second to the third instar. The velocity constant apparently does not conform to the well known Arrhenius equation in its relation to temperature.     

EQUILIBRIUM ANALYSIS OF SEXUAL SELECTION IN DROSOPHILA MELANOGASTER

Several models for sexual selection, both by male-male competition and female choice, predict that a character which covaries with mating success should be near an equilibrium where the intensity of sexual selection opposes viability selection. This prediction was used to design experiments for estimating the intensity of sexual and viability selection on wing length in a recently captured population of Drosophila melanogaster. Observations of matings by males color-marked for wing length indicated that the standardized sexual selection differential on wing length was 0.24 under a wide range of effective sex ratios. After estimating the heritability of wing length to be 0.62, the expected standardized response due to sexual selection was calculated as 0.15 (SE = 0.15). The response due to viability selection was then estimated by comparing wing lengths of progeny of flies that had been randomly mated, thereby preventing sexual selection, with progeny of flies that had been allowed to acquire mates in a mass-mating chamber. The results support an equilibrium model in that the standardized response due to viability selection (?0.31, SE = 0.08) was opposite in sign and similar in magnitude to the estimated response due to sexual selection. Observations of females orienting in front of males which differed in wing length indicated that the mating advantage accruing to long-winged males was not due to female choice. Instead, male-male competition in which the larger of two randomly chosen males succeeded in mating, explains the observed sexual selection. An experimental analysis of genotype-environment interaction revealed that larval density had a nonlinear effect on mean wing length within sibships. If a population is displaced from equilibrium, therefore, the evolutionary trajectory of mean wing length will depend both on the intensity of selection and the environment in which that selection is operating.