DIRECT AND CORRELATED RESPONSES TO SELECTION ON AGE AT REPRODUCTION IN DROSOPHILA MELANOGASTER

Aging may be a consequence of mutation accumulation or of negative pleiotropic correlations between performance late and earlier in the lifespan. This study used artificial selection on flies derived from two different base stocks to produce “young” and “old” lines, propagated by breeding from young and old adults respectively. Virgin and mated adults of both sexes from the “old” lines lived longer than “young” line flies. “Young” and “old” mated females did not differ in fecundity or fertility early in the lifespan, but “old” line females had higher fecundity and fertility late in life. The results therefore suggested either that the response to selection had revealed the effect of mutation accumulation, or that pleiotropy involving characters other than early fecundity must have been involved. Development time from egg to adult was longer in the “old” lines. Competition of selected line larvae from one base stock against mutant marked larvae from the same base stock revealed that, at a wide range of larval densities, “old” line larvae showed lower survival rates than “young” line larvae. Thorax length and wet weight were significantly greater in the “old” line flies from one base stock. The results may imply that the selection regime in the “old” lines favored extended growth during development to produce a more durable adult soma, despite the cost in increased larval mortality and delayed reproduction, because the potential reproductive benefits later in life were increased. However, the differences between larvae from “old” and “young” lines could also be attributable to density differences, and this possibility needs systematic investigation.     

CORRELATED RESPONSES IN LIFE-HISTORY TRAITS TO ARTIFICIAL SELECTION FOR BODY WEIGHT IN DROSOPHILA MELANOGASTER

Drosophila melanogaster that had been successfully selected on rich and poor larval medium for increased and decreased fresh weight at eclosion were tested on an intermediate medium for correlated responses in longevity, fertility, and hatchability. Larger flies laid more eggs early in life and lived shorter lives than smaller flies, which not only lived longer but also laid more eggs later in life. This supports the notion of a mortality cost of reproduction in Drosophila. The total number of eggs laid per lifetime did not differ between the two groups. The percentage of offspring hatched started at normal levels (about 50% of eggs laid), then declined rapidly in large flies. In small flies, hatchability started at a lower level early in life (40-65%), but declined less rapidly, and later in life was higher than the hatchability of eggs laid by larger flies.     

SELECTION FOR KNOCKDOWN RESISTANCE TO HEAT IN DROSOPHILA MELANOGASTER AT HIGH AND LOW LARVAL DENSITIES

Responses to short-term selection for knockdown resistance to heat (37°C) in Drosophila melanogaster reared under stressful (high larval density) and nonstressful (low larval density) conditions were compared. No difference in selection response between density treatments was found. A test of heat resistance (39°C) after pretreatment (37°C) did not reveal an increase in survival for selected lines as compared to controls. Flies reared at high density had higher knockdown resistance throughout the experiment. Resistance to heat was not associated with body size.     

EVOLUTION AND DEVELOPMENT OF BODY SIZE AND CELL SIZE IN DROSOPHILA MELANOGASTER IN RESPONSE TO TEMPERATURE

We examined the evolutionary and developmental responses of body size to temperature in Drosophila melanogaster, using replicated lines of flies that had been allowed to evolve for 5 yr at 25°C or at 16.5°C. Development and evolution at the lower temperature both resulted in higher thorax length and wing area. The evolutionary effect of temperature on wing area was entirely a consequence of an increase in cell area. The developmental response was mainly attributable to an increase in cell area, with a small effect on cell number in males. Given its similarity to the evolutionary response, the increase in body size and cell size resulting from development at low temperature may be a case of adaptive phenotypic plasticity. The pattern of plasticity did not evolve in response to temperature for any of the traits. The selective advantage of the evolutionary and developmental responses to temperature is obscure and remains a major challenge for future work.     

THE RESPONSES OF DROSOPHILA MELANOGASTER TO ARTIFICIAL SELECTION ON BODY WEIGHT AND ITS PHENOTYPIC PLASTICITY IN TWO LARVAL FOOD ENVIRONMENTS

To investigate the potential response to natural selection of reaction norms for age and size at maturity, fresh body weight at eclosion was mass selected under rich and poor larval food conditions in Drosophila melanogaster. The sensitivity of dry weight at eclosion to the difference between rich and poor larval food was selected using differences in sensitivities among families. For both experiments, the correlated response to selection of age at eclosion was examined. The flies were derived from wild populations and had been mass cultured in the lab for more than six months before the experiments started. These flies responded to selection on body weight upwards and downwards on both rich and poor larval food. Selection on increased or decreased sensitivity of body weight was also successful in at least one direction. Sensitivity was reduced by selection upwards in a poor environment and downwards in a rich environment.     

ARTIFICIAL SELECTION FOR DEVELOPMENTAL TIME IN DROSOPHILA MELANOGASTER IN RELATION TO THE EVOLUTION OF AGING: DIRECT AND CORRELATED RESPONSES

A wild-type strain of Drosophila melanogaster was successfully selected for both fast and slow larval development. The realized heritabilities (h²) ranged from 0.20 to 0.30 for the fast lines and 0.35 to 0.60 for the slow lines. The selection applied is relevant in relation to the evolution of aging. The longevity of adults, either virgin or mated, was not affected by selection for developmental time, indicating that developmental time is not a causal determinant of life span, thus confirming the results of the studies on environmental effects on aging (Zwaan et al. 1991, 1992). However, adult body weights were higher in the slow developmental lines and lower in the fast lines, relative to the control flies. Furthermore, slow females showed relatively high early fecundity and low late fecundity, as compared with control and fast females. Mated longevities and total lifetime progeny productions were not statistically different. Previous results obtained by other authors from selection experiments on age at reproduction either supported the mutation accumulation or the negative pleiotropy theory of aging (Luckinbill et al. 1984; Rose 1984b). The impact of the reported results on the interpretation of these studies is discussed, and it is noted that direct selection on adult longevity is needed to settle this issue.     

EVOLUTIONARY EFFECTS OF SELECTION ON AGE AT REPRODUCTION IN LARVAL AND ADULT: DROSOPHILA MELANOGASTER

Two sets of three replicate lines of Drosophila melanogaster were artificially selected by reproduction at either a ‘young’ or an ‘old’ age. The pure lines, the hybrids between the lines within a selection regimen and the base stock from which the lines were derived were compared for longevity, early and late fertility, development time, larval viability and adult thorax length. Comparison of hybrid with pure lines showed some evidence for inbreeding depression in the lines from both selection regimes. Comparison of hybrid lines with the base stock did not provide evidence for any trade-off in either males or females between early fertility on the one hand and late life fertility and longevity on the other. Nor was there any clear evidence of a trade-off between pre-adult and adult fitness components. There was evidence of inadvertent selection for rapid development in both selection regimens, especially in the females of the ‘young’ lines, and this complicated the interpretation of the responses and correlated responses to selection. An improvement in adult performance in the ‘old’ line males relative to the base stock appeared to be attributable to reversal of mutation accumulation. Comparison of the hybrid ‘young’ and ‘old’ lines with the base stock did not support the idea that the superior longevity and late life fertility of the ‘old’ lines relative to the ‘young’ lines could be accounted for by the effects of mutation accumulation in the ‘young’ lines. The results point to the need to compare selected lines with their base stock when deducing responses and correlated responses to selection and to avoid unintentional selection. In this type of experiment, larval density should be standardized during selection, and adults should not be under pressure for rapid maturation.     

CROSS-RESISTANCE FOLLOWING ARTIFICIAL SELECTION FOR INCREASED DEFENSE AGAINST PARASITOIDS IN DROSOPHILA MELANOGASTER

An increase in resistance to one natural enemy may result in no correlated change, a positive correlated change, or a negative correlated change in the ability of the host or prey to resist other natural enemies. The type of specificity is important in understanding the evolutionary response to natural enemies and was studied here in a Drosophila-paxasitoid system. Drosophila melanogaster lines selected for increased larval resistance to the endoparasitoid wasps Asobara tabida or Leptopilina boulardi were exposed to attack by A. tabida, L. boulardi and Leptopilina heterotoma at 15°C, 20°C, and 25°C. In general, encapsulation ability increased with temperature, with the exception of the lines selected against L. boulardi, which showed the opposite trend. Lines selected against L. boulardi showed large increases in resistance against all three parasitoid species, and showed similar levels of defense against A. tabida to the lines selected against that parasitoid. In contrast, lines selected against A. tabida showed a large increase in resistance to A. tabida and generally to L. heterotoma, but displayed only a small change in their ability to survive attack by L. boulardi. Such asymmetries in correlated responses to selection for increased resistance to natural enemies may influence host-parasitoid community structure.     

RAPID LABORATORY EVOLUTION OF ADULT LIFE-HISTORY TRAITS IN DROSOPHILA MELANOGASTER IN RESPONSE TO TEMPERATURE

Three replicate lines of Drosophila melanogaster were cultured at each of two temperatures (16.5°C and 25°C) in population cages for 4 yr. The lifespans of both sexes and the fecundity and fertility of the females were then measured at both experimental temperatures. The characters showed evidence of adaptation; flies of both sexes from each selection regime showed higher longevity, and females showed higher fecundity and fertility, than flies from the other selection regime when they were tested at the experimental temperature at which they had evolved. Calculation of intrinsic rates of increase under different assumptions about the rate of population increase showed that the difference between the lines from the two selection regimes became less the higher the rate of population increase, because the lines were more similar in early adulthood than they were later. Despite the increased adaptation of the low-temperature lines to the low temperature, like the high temperature lines they produced progeny at a higher rate at the higher temperature. The lines may have independently evolved adaptations to their respective thermal regimes during the experiment, or there may have been a trade-off between adaptation to the two temperatures, or mutation pressure may have lowered adaptation to the temperature that the flies no longer encountered.     

DENSITY-DEPENDENT NATURAL SELECTION IN DROSOPHILA: EVOLUTION OF GROWTH RATE AND BODY SIZE

Drosophila melanogaster populations subjected to extreme larval crowding (CU lines) in our laboratory have evolved higher larval feeding rates than their corresponding controls (UU lines). It has been suggested that this genetically based behavior may involve an energetic cost, which precludes natural selection in a density-regulated population to simultaneously maximize food acquisition and food conversion into biomass. If true, this stands against some basic predictions of the general theory of density-dependent natural selection. Here we investigate the evolutionary consequences of density-dependent natural selection on growth rate and body size in D. melanogaster. The CU populations showed a higher growth rate during the postcritical period of larval life than UU populations, but the sustained differences in weight did not translate into the adult stage. The simplest explanation for these findings (that natural selection in a crowded larval environment favors a faster food acquisition for the individual to attain the same final body size in a shorter period of time) was tested and rejected by looking at the larva-to-adult development times. Larvae of CU populations starved for different periods of time develop into comparatively smaller adults, suggesting that food seeking behavior in a food depleted environment carries a higher cost to these larvae than to their UU counterparts. The results have important implications for understanding the evolution of body size in natural populations of Drosophila, and stand against some widespread beliefs that body size may represent a compromise between the conflicting effects of genetic variation in larval and adult performance.     

AN INTERACTION BETWEEN ENVIRONMENTAL TEMPERATURE AND GENETIC VARIATION FOR BODY SIZE FOR THE FITNESS OF ADULT FEMALE DROSOPHILA MELANOGASTER

Abstract. — Drosophila and other ectotherms show geographic genetic variation in body size, with larger individuals at higher latitudes and altitudes. Temperature is implicated as an important selective agent because long-term laboratory culture of Drosophila leads to the evolution of larger body size at lower temperatures. In this paper, we tested the hypothesis that, in Drosophila melanogaster, larger size is favored at lower temperatures in part because of selection on adult females. We used replicated lines of D. melanogaster artificially selected for increased and decreased wing area with constant cell area. The resulting size differences between the selected lines were due solely to differences in cell number, and thereby were similar to the cellular basis of clinal variation in body size in nature. We examined life-history traits of adult females at 18 and 25°C. Rearing for two generations at the two temperatures did not affect the extent of the size differences between lines from the different selection regimes. There was a strong interaction between temperature and size selection for both survival and lifetime reproductive success, with larger females living significantly longer and producing more offspring over their lifetime only when reared and tested in the colder environment. There was also an increase in average daily progeny production in large-line females relative to the control and small lines again, only in the colder environment. Thus, the females from the large selection lines were relatively fitter at the colder temperature. At both experimental temperatures, especially the lower one, the small- line females rescheduled their progeny production to later ages. Larger body size may have evolved at higher latitudes and altitudes because of the advantages to the adult female of being larger at lower temperatures.     

DIRECTIONAL AND STABILIZING DENSITY-DEPENDENT NATURAL SELECTION FOR PUPATION HEIGHT IN DROSOPHILA MELANOGASTER

Six populations of Drosophila melanogaster have been kept at extreme population densities, three high and three low, for 175 generations. Larvae from the high density populations pupate 50%-100% higher than larvae from the low density populations. At high larval test densities there is both a directional and a stabilizing component to selection, with viabilities ranging from 0.14 to 0.992, depending on the choice of pupation site. The directional component is stronger on the populations which have evolved at low densities, while the stabilizing component is stronger on the populations which have evolved at high densities. There is no indication that the evolution of this trait, in response to density, has altered its phenotypic plasticity.     

THE EFFECT OF TEMPERATURE ON BODY SIZE AND FECUNDITY IN FEMALE DROSOPHILA MELANOGASTER: EVIDENCE FOR ADAPTIVE PLASTICITY

The reaction norm linking rearing temperature and size in Drosophila melanogaster results in progressively larger flies as the temperature is lowered from 30°C to 18°C, but it has remained unclear whether this phenotypic plasticity is part of an adaptive response to temperature. We found that female D. melanogaster reared to adulthood at 18°C versus 25°C showed a 12% increase in dry weight. Measurements of the fecundity of these two types of fly showed that the size change had no effect on lifetime fecundity, regardless of the adult test temperature. Thus the phenotypic plasticity breaks the usual positive correlation between body size and fecundity. However, at a given temperature, early fecundity (defined as productivity for days 5 through 12 after eclosion at 25°C and days 7 through 17 at 18°C) was highest when the rearing and test temperatures were the same. The early fecundity advantage due to rearing at the test temperature was 25% at 18°C and 16% at 25°C, a result consistent with the overall phenotypic response to temperature being adaptive. This conclusion is further supported by the finding that the temperature treatments resulted in a trade-off between early fecundity and longevity, a trade-off that parallels the known genetic correlation. Another parallel is that both the temperature-induced and genetic effects are independent of total fecundity. By contrast, within the temperature treatments, the phenotypic correlation between early fecundity and longevity was positive, illustrating the danger of assuming that phenotypic and genetic correlations are similar, or even of the same sign.     

DIRECT SELECTION ON LIFE SPAN IN DROSOPHILA MELANOGASTER

An important issue in the study of the evolution of aging in Drosophila melanogaster is whether decreased early fecundity is inextricably coupled with increased life span in selection experiments on age at reproduction. Here, this problem has been tackled using an experimental design in which selection is applied directly to longevity. Selection appeared successful for short and long life, in females as well as males. Progeny production of females selected for long life was lower than for short-lived females throughout their whole life. No increase of late-life reproduction in long-lived females occurred, as has been found in selection experiments on age at reproduction. This discrepancy is explained in terms of the inadequacy of the latter design to separate selection on life span from selection on late-life fecundity. Moreover, starvation resistance and fat content were lower for adults selected for short life. In general, the data support the negative-pleiotropy–disposable-soma theory of aging, and it is hypothesized that the pleiotropic allocation of resources to maintenance versus to reproduction as implicated in the theory might involve lipid metabolism. It is argued that further research on this suggestion is urgent and should certainly comprise observations on male reproduction because these are for the greater part still lacking. In conclusion, the longevity of D. melanogaster can be genetically altered in a direct-selection design, and such an increase is accompanied by a decreased general reproduction and thus early reproduction.     

WITHIN- AND BETWEEN-GENERATION EFFECTS OF TEMPERATURE ON THE MORPHOLOGY AND PHYSIOLOGY OF DROSOPHILA MELANOGASTER

We investigated the effects of developmental and parental temperatures on several physiological and morphological traits of adult Drosophila melanogaster. Flies for the parental generation were raised at either low or moderate temperature (18°C or 25°C) and then mated in the four possible sex-by-parental temperature crosses. Their offspring were raised at either 18°C or 25°C and then scored as adults for morphological (dry body mass, wing size, and abdominal melanization [females only]), physiological (knock-down temperature, and thermal dependence of walking speed), and life history (egg size) traits. The experiment was replicated, and the factorial design allows us to determine whether and how paternal, maternal, and developmental temperatures (as well as offspring sex) influence the various traits. Sex and developmental temperature had major effects on all traits. Females had larger bodies and wings, higher knock-down temperatures, and slower speeds (but similar shaped performance curves) than males. Development at 25°C (versus at 18°C) increased knock-down temperature, increased maximal speed and thermal performance breadth, decreased the optimal temperature for walking, decreased body mass and wing size, reduced abdominal melanization, and reduced egg size. Parental temperatures influenced a few traits, but the effects were generally small relative to those of sex or developmental temperature. Flies whose mother had been raised at 25°C (versus at 18°C) had slightly higher knock-down temperature and smaller body mass. Flies whose father had been raised at 25°C had relatively longer wings. The effects of paternal, maternal, and developmental temperatures sometimes differed in direction. The existence of significant within- and between-generation effects suggests that comparative studies need to standardize thermal environments for at least two generations, that attempts to estimate “field” heritabilities may be unreliable for some traits, and that predictions of short-term evolutionary responses to selection will be difficult.     

THE SYMMETRY OF CORRELATED SELECTION RESPONSES IN ADAPTIVE EVOLUTION: AN EXPERIMENTAL STUDY USING DROSOPHILA

The relationship between the processes of density-dependent and age-specific selection has been investigated by examining a common phenotype, urea resistance, which has apparently evolved in response to each of these selection mechanisms. Twenty populations that have experienced differing levels of age-specific selection show differences in egg-to-adult viability in environments with high levels of urea. Among this group of populations, it appears that resistance to urea is correlated with longevity, but not development time. Ten populations kept at extreme larval densities for many generations also show responses to urea: those kept at high larval densities appear to be most resistant to urea. However, these populations show no differences in adult longevity. An additional five populations were selected directly for urea resistance by adding this compound to the larval food environment. Again, there was a strong response to this artificial selection, with urea resistance increasing dramatically, but these populations showed no response in adult longevity or resistance to crowding when compared to five control populations. There is clearly no simple relationship between longevity and larval urea resistance. It may be that age-specific and density-dependent selection induce similar changes in this phenotype, but do so through different genetic and physiological pathways. We suggest that these data are not consistent with the view of constant and symmetric genetic variance-covariance matrices. These data support a more prominent role for observations of evolutionary trajectories rather than static measurements of genetic components of variance.