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Evolutionary effects of selection on age at reproduction in larval and adult Drosophila melanogaster.

Abstract. - 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.

Key words. - Aging, Drosophila melanogaster, larval development, mutation accumulation, pleiotropy, reproduction, selection, survival.

Aging is a drop in survival probability and fecundity with age after the onset of reproduction (Charlesworth, 1980). Its occurrence can be explained by a drop in the force of natural selection on mutations with fitness effects expressed later in life (Medawar, 1952; Hamilton, 1966; Charlesworth, 1980). Mutations with age-specific deleterious effects can therefore reach a higher equilibrium frequency under mutation-selection balance if they are expressed later in life. Mutations can also be pleiotropic by affecting fitness at more than one age, and selection will act with greater force on earlier than on later fitness effects. Aging could then evolve as a deleterious side-effect of mutants selected as a result of their beneficial earlier effects (Medawar, 1946; Williams, 1957).

Empirical tests of these theories of aging have been made mainly in laboratory studies of Drosophila. Most work has been with females, and longevity and age-specific fertility have been examined. Approaches have included analysis of outbred populations (e.g., Rose and Charlesworth, 1981a), chromosome extraction (e.g., Hughes and Clark, 1988) and artificial selection on age at reproduction (e.g., Rose and Charlesworth, 1981b; Rose, 1984; Luckinbill et al., 1984; Mueller, 1987; Service et al., 1988; Partridge and Fowler, 1992). The results suggest that both mutation accumulation and pleiotropy may be important in the evolution of aging in Drosophila.

One aim of this study was to extend the investigation to males. Artificial selection on age at reproduction can extend male lifespan (e.g., Wattiaux, 1968; Rose, 1984; Partridge and Fowler, 1992). Wattiaux (1968) recorded a drop in male mating activity in one such selection line of D. subobscura, supporting the idea of pleiotropy, while Kosuda (1985), using chromosome extraction, demonstrated higher genetic variance for male mating activity in older D. melanogaster, possibly supporting the idea of mutation accumulation, although the effects could have been nonadditive. We have examined age-specific reproductive success of males from replicate lines of D. melanogaster artificially selected by age at reproduction. The males from the |young' and |old' selection regimens differ in longevity (Partridge and Fowler, 1992) and the present study tested for a direct response to selection in late life fertility in the |old' lines, and for a possible correlated response in the form of a decrease in early fertility or in pre-adult performance.

The second aim was to investigate whether the pattern of differences between the |young' and |old' lines was a consequence of responses and correlated responses to selection on age at reproduction, or instead an artefact of other, uncontrolled differences between the selection regimes. Hybrids between the lines within each selection regimen (to remove any effects of inbreeding depression) were compared with each other and with the base stock, to determine if evolution for each character had occurred in the |young' lines, the |old' lines or both. Because the base stock had been in laboratory culture for 16 years before these experiments commenced, evolution of life-history characters should have been very much more rapid in the selection lines than in it. Any evolution of a character in the selection lines should therefore be apparent as a difference from the base stock, and any genetic correlation between characters should be reflected in the pattern of correlated responses relative to the base stock.

A final aim was to examine whether the results were more consistent with the mutation accumulation or pleiotropy theories of aging. Mutation accumulation in the |young' lines rather than selection response in the |old' lines, could explain why female longevity and late fertility were higher in the |old' lines (Partridge and Fowler, 1992; Charlesworth, 1982).

Materials and Methods

Base Stock, Selection Lines and

Fly Handling

The base stock of D. melanogaster was collected in Dahomey (now Benin) West Africa in 1970, and has since been maintained in mass culture in population cages on a 12 hr: 12 hr light/dark cycle at 25 [degrees] C with uncontrolled humidity, by introducing three fresh culture bottles containing 60 ml of food medium once a week and removing them after four weeks.

The selection lines have been described elsewhere (Partridge and Fowler, 1992). In brief, they were derived from the Dahomey base stock, and three replicate |young' and |old' lines were produced, with selection commencing in March 1986. The |young' lines were propagated using parents that emerged in the culture bottles up to day 17, with eggs being collected from days 14 to 17 (= days 0 to 3 of the next generation). In the |old' lines, the adults of the previous generation eclosing up to day 17 were subsequently kept in mixed-sex groups in population cages over three bottles of weekly renewed food medium. Initially the egg-collections were made from adults 28 to 31 days old, then the age of the parents was gradually increased to 70 to 73 days as the lines responded to selection. The |young' lines were propagated at higher larval densities than the |old' lines, because the breeding adults were more numerous and fertile when the eggs from the |young' lines were collected (Partridge and Fowler, 1992).

A stock carrying the recessive mutant marker scarlet in approximately Dahomey genetic background was produced by two rounds of backcrossing of both sexes of a scarlet stock to the Dahomey base stock, with selection of scarlet parents in the two [F.sub.2] generations. The resulting |Dahomey-scarlet' stock was then kept in a population cage identical to that of the Dahomey base stock, starting in January 1989.

The flies were handled at room temperature, and anaesthesia of adults was with carbon dioxide on flies not less than 3 hr after eclosion.

Measurement of Longevity and

Reproductive Success of Males

Male longevity and reproductive success were measured in generations 31 (|old') and 99 (|young') of selection. Reproductive success was estimated as the proportion of wild type progeny when scarlet-eyed males competed with pure line males, with [F.sub.1] hybrid males from crosses between the lines within a selection regime or with base stock males for matings with scarlet-eyed females. The hybridization of replicate lines should have removed any effects of inbreeding depression. Parents of the experimental males and of the |Dahomey-scarlet' flies were reared at standard low larval density (< 300 adult emergees/bottle) in culture bottles and collected as virgins. To make hybrids between the lines within a selection regime, females of line 1 were crossed with males of line 2, females of line 2 with males of line 3 and females of line 3 with males of line 1; these and the pure line and base stock parents were allowed to lay eggs on grape juice medium (Fowler and Partridge, 1986) for three hours. At 24 hours from the midpoint of egg-laying, first instar larvae were set up at a standard density of 100/food vial, and flies were then collected as virgins. For each pure and hybrid line and sample of the base stock, 10 virgin scarlet females together with three experimental and seven scarlet males were set up in each of 13 replicate pots (80 mm x 35 mm diam) containing 7 ml of food medium with a small smear of active yeast paste. The flies were transferred to fresh pots on a weekly cycle of intervals of one day, two days, one day, three days. Deaths of wild type males were recorded daily. All of the scarlet females were replaced with new three-day-old virgins once every two weeks. Male fertility was measured as the proportion of wild type adult progeny emerging from twice weekly 24 hr samples of eggs from the two one-day transfer intervals. The plug of food together with its eggs were transferred from the pot to a bottle of culture medium with an excess of yeast paste, to yield culture conditions in which larval mortality was low (<10%) and did not differ between lines. The genotypes of the progeny emerging from these bottles were scored. For this measurement of fertility, a subsample of 10 of the 13 pots was used, and the number and genotypes of the flies in them were kept as described, by replacing dead experimental and scarlet flies with individuals from the remaining 3 pots. In these three pots, dead scarlet flies but not experimental flies were replaced from a pool of virgins. The total number of pots for each replicate line was reduced as the experimental flies died. Eventually sufficient death had occurred that fewer than 10 fertility pots could be kept with their full complement of flies, and the number of pots in the fertility sample was then reduced accordingly.

Our measure of male reproductive success therefore combined the effects of male mating success, fertility and sperm competition. Because the males in the selection lines are kept in mixed-sex populations and under conditions where females can remate several times, it is appropriate to measure male reproductive success in this way, rather than, for instance, exclusively with virgin females or in the absence of competition from other males.

Measurement of Longevity and

Fertility of Females

Female longevity and fertility were measured in generations 44 (|old') and 125 (|young') of selection. Pure and hybrid line females and base stock males and females were produced as for the measurement of male longevity and fertility. For each pure and hybrid line and each sample of the base stock, 100 females were set up in batches of 10 with 10 base stock males in food pots. Base stock males were used to standardize any male effects on the longevity or fertility of females. The flies were transferred to fresh pots every two days, and the plug of food from the vacated pot was removed and transferred to a low-density culture bottle as described for the measurement of male fertility. The adults emerging from these bottles were counted to give an estimate of the number of fertile eggs the females had laid on the food plugs. Deaths were recorded daily, and dead males were replaced at transfer as necessary to keep the sex ratio even in each pot. All of the males were replaced with three-day-old virgins once every two weeks. As females died, the number of replicate pots was reduced to keep the fly density as constant as possible.

Measurement of Development Time and

Larval Viability of Pure Lines,

Hybrid Lines and the Base Stock

Development time and thorax length of the pure lines, of the hybrids between them and of the base stock were measured in generations 43 (|old') and 123 (|young') of selection. Thorax length was taken as a measure of body size, because it shows strong, positive phenotypic and genetic correlations with other measures such as wing length, tibia length and body weight (Robertson, 1963; Wilkinson et al., 1990). First instar larvae were set up in seven replicate culture vials (with 80 larvae each) for each pure and hybrid line and the base stock. The eclosing adults were collected and counted every 12 hours, and their thorax lengths were measured under a compound microscope to the nearest 0.04 mm.

Larval viability was measured in the same generations as development time, by competing experimental and |Dahomey-scarlet' larvae. First instar larvae of the selection lines, their hybrids, the base stock and the scarlet stock were collected, and vials were set up with a mixture of one third wild type and two thirds scarlet larvae at three larval densities: five replicates of 30 wild type + 60 scarlet (= density 90), five replicates of 60 wild type + 120 scarlet (= density 180) and three replicates of 200 wild type + 400 scarlet (= density 600). The wild type and scarlet adults emerging from each vial were then counted.

Results

Longevity and Reproductive Success of

Males and Females

The median longevities of the pure, hybrid and base stock males and females (Table 1) suggested that there were(effects) of both selection regimen and inbreeding. The data were not normally distributed, and for statistical analysis a distribution-free method, the log rank test (Miller, 1981), was used. This test uses life table data to cumulate, for each successive sampling interval (day), both the observed number of deaths in each group being compared, and the expected number for each group, calculated by allocating the total number of deaths observed in each sampling interval to the groups in proportion to the number of individuals entering that sampling interval. The total observed and expected deaths can then be used to generate a chi-squared value with one degree of freedom. For each comparison, the three replicates were paired according to the line numbers allocated to them at the beginning of the experiment (or the numbers of the mothers of the hybrids) and, if the differences between paired replicates were all in the same direction, the probabilities from the three independent comparisons were combined (Sokal and Rohlf, 1969) to give an overall probability for the comparison. If the directions of the differences differed, then the normal distribution of chi was used to obtain an overall probability. These are given, corrected for multiple comparisons (Rice, 1989), in Table 2. In both pure and hybrid lines of both sexes, flies from the |old' selection regimen lived significantly longer than those from the |young' regimen. In both sexes, hybrid |old' flies lived significantly longer than base stock flies, and both pure and hybrid |young' females lived significantly less long than the base stock females. In males, the |old' lines and in females the |young' lines showed evidence of inbreeding depression, with pure line flies living less long than hybrids.

For the measurement of male reproductive success, for each sample bottle the percentage of the total flies emerging that was wild type in each sampling interval was calculated. The figure for each sample pot was used to calculate a mean figure for each replicate, and the average values of these replicate line means are shown in Figure 1A. For females, the number of flies emerging from each sample pot was divided by the number of females in the pot that survived the sampling interval, to give a mean number of progeny per female for each sample. These figures were used to calculate a mean fertility for each replicate line and, as for the males, the averages of these means are displayed in Figure 1B.

[TABULAR DATA OMITTED]
Table 2. Survival of males and females. Table-wide
significance values for paired comparisons between regimes.

                            Males   Females

Hybrid old > Hybrid young    ***      ***
Pure old > Pure young        ***      ***

Hybrid old > Base stock      ***      ***
Hybrid young < Base stock    NS        **

Hybrid young > Pure young    NS        **
Hybrid old > Pure old         *        NS

 < = The direction of the difference. * P = 0.05. ** P = 0.0 1.
*** P
0.001. NS = not significant.


To minimize problems both with non-independence of the individual samples because the same individuals were present in each, and with diminishing sample sizes later in the experiment, for comparison of the lines two time intervals, early and late, were used for analysis. The early interval was chosen to cover the peak period of early fertility, and the late interval to cover as much as possible of the period when fertility started to decline, but ending when more than 20% of the flies had died in the replicate line with the highest mortality rate. For the males, the early sample was from days 2 to 5 and the late sample from days 19 to 23, while for the females, the corresponding intervals were days 2 to 7 and days 10 to 22. The data from the individual sampling intervals during these times were averaged for each replicate line, and the replicate line means were then used in a one-way analysis of variance. The informative pairwise comparisons were then made, and their probabilities adjusted appropriately for the number of comparisons. The results are shown in Table 3. In males in the early sample, the hybrid young lines were significantly more fertile than the base stock, and marginally nonsignificantly (0.05 < P < 0. 1) more fertile than the hybrid old lines. In the late sample, the hybrid old lines were significantly more fertile than the base stock and the hybrid young lines, and the pure old lines were significantly more fertile than the pure young lines. For the females in the early sample, the base stock was significantly more fertile than the hybrid |old' lines and marginally nonsignificantly (0.05 < P < 0. 1) more fertile than the hybrid |young' lines. For females in the late sample, no statistical comparisons involving the pure |young' lines were possible because the variance between replicate lines was significantly greater than that for the other groups. For the remaining groups, the hybrid |young' lines were significantly less fertile than both the base stock and the hybrid |old' lines. There was thus no evidence for significant inbreeding depression for fertility in either sex, although this could not be tested for the late interval for females of the |young' lines.
Table 3. Paired comparisons of age specific measures of
fertility for the pure |young' and |old', hybrid |young'
and |old', and base stock regimes. The direction of difference
and statistical significance of each comparison is
given for early and late measures of fertility males (a.) and
females (b.).

           Early                            Late

a. Males
Hybrid old-Hybrid young        Hybrid old > Hybrid young(*)
Pure old-Pure young            Pure old > Pure young(*)

Hybrid old-Base stock          Hybrid old > Base stock(*)
Hybrid young > Base stock(*)   Hybrid young-Base stock

Hybrid young-Pure young        Hybrid young-Pure young
Hybrid old-Pure old            Hybrid old-Pure old

b. Females
Hybrid old-Hybrid young        Hybrid old > Hybrid young(*)
Pure old-Pure young

Hybrid old < Base stock(*)     Hybrid old-Base stock
Hybrid young-Base stock        Hybrid young < Base stock(*)

Hybrid young-Pure young
Hybrid old-Pure old            Hybrid old-Pure old

 < = The direction of the difference.

 (*) P0.05.


Development Time, Larval

Viability and Thorax Length

The numbers of male and female adults eclosing in each vial were probit transformed to give a mean development time, and these vial means were then used to generate the line means in Table 4. Inspection of the confidence limits about the regimen means (the means of the line means) shows that for both sexes of both pure and hybrid lines the |old' lines took significantly longer to develop than the |young'.

[TABULAR DATA OMITTED]

Comparison between the selection regimens and the base stock for development time took a different form from the comparisons involving adults, because only a single base stock replicate was present. The replicate lines within a regimen were therefore tested for heterogeneity using nested analysis of variance and, provided that the result was not statistically significant, contrasts between each regimen and the base stock were conducted using t-tests. Each vial from the base stock and the replicate lines was treated as one replicate in the t-test. The pure and hybrid |young' line males and females and the hybrid |old' line males and females all developed significantly (P < 0.001) faster than the base stock. One-way nested analysis of variance revealed that there, was also an effect of inbreeding depression in the |old' lines, with both males (P < 0.05) and females (P < 0.01) of the hybrid lines developing significantly more quickly than the pure lines.

The percent of wild type adults emerging from each larval competition vial (Table 5) was angular transformed for further analysis. The data at each culture density were analyzed exactly as for development time. One-way nested analysis of variance on the effect of selection regimen was carried out for the pure and hybrid lines at each larval density. At density 90, larval viability was significantly (P < 0.05) lower in the hybrid |old' than in the hybrid |young' lines, at density 180 the differences between |young' and |old' lines were in the same direction but marginally nonsignificant (P < 0.1) in both cases, while at density 600 there were highly significant (P < 0.01) effects in the same direction in both pure and hybrid lines. The hybrid lines were subjected to a two-way analysis of variance, to test for an interaction between the effects of culture density and selection regimen, which was highly significant (P < 0.001). Inspection of the data shows that this interaction was contributed to overwhelmingly by the very large difference in performance between |young' and |old' line hybrids at culture density 600. Comparisons with the base stock using t-tests revealed that at density 90, differences were nonsignificant, at density 180 the pure |young' lines had significantly (P = 0.025) higher and the hybrid |young' lines marginally nonsignificantly (P = 0.06) higher viability than the base stock, while neither the pure or hybrid |old' lines differed significantly from the base stock. At density 600, the hybrid |young' lines again had significantly (P < 0.01) higher viability than the base stock while the pure |young' lines (P = 0.082) and the pure and hybrid |old' lines did not differ significantly from it. To test for inbreeding depression, one-way analysis of variance revealed that at densities 90 and 180 there was no evidence of significant inbreeding depression in flies from either selection regimen, while at density 600 there was no significant effect in the |young' lines, but in-the |old' lines pure line larvae had significantly (P < 0.05) lower viability than hybrids".

[TABULAR DATA OMITTED]

To compare thorax length, five males and five females were chosen at random from adults emerging in each of the standardized density vials used to measure development time. The figures were used to calculate a mean for the males and females from each vial, and these were then used to calculate the replicate means in Table 6. There were no significant differences in thorax length between selection regimens for pure or hybrid males or females. Comparisons with the base stock using t-tests revealed that both the pure (P = 0.013) and the hybrid (P = 0.03) |young' females had significantly smaller thoraxes, while there were no significant differences in the males.

[TABULAR DATA OMITTED]

Discussion

Inbreeding Depression

Both the |young' and the |old' lines showed some evidence of inbreeding depression, with longevity affected in both |young' line females and |old' line males, and development time and larval viability at high larval densities affected in the |old' lines. The greater evidence for inbreeding depression in the |old' lines may be attributable to persistently lower effective population sizes in them, associated with a lower number of less fertile breeders (Partridge and Fowler, 1992). Because of the presence of inbreeding depression, analysis of the fitness characters and their correlations was carried out using the hybrid lines and the base stock. A similar study (Hutchinson and Rose, 1991) did not find evidence for inbreeding depression in selection lines, which is interesting in view of the greater antiquity and smaller population sizes in them compared with those used in the present study.

The previously reported (Partridge and Fowler, 1992) lower larval fitness of the |old' lines does not appear to have been an artefact of greater levels of inbreeding depression, because the same differences between the selection regimens were apparent in the hybrid lines in the present study.

Males from the Selection Regimens

Comparison of the hybrid males from the two selection regimens showed that |old' line males lived longer, were more fertile late in life, developed more slowly and had lower larval viability at high densities than did the |young' line males. This pattern of responses closely parallels that seen in the hybrid females in the present study and in the pure line females in the earlier study (Partridge and Fowler, 1992). It therefore extends those findings to males.

Trade-offs within the Adult Period

Previous studies (e.g., Rose, 1984; Clare and Luckinbill, 1985; Luckinbill et al., 1987) have found evidence of a negative genetic correlation, or trade-off, between fertility early in the adult period on one hand, and longevity and fertility late in life on the other. The results of a previous study (Partridge and Fowler, 1992) with the pure lines together with the evidence from the hybrid lines in the present study has failed to confirm these findings for either females or males. |Old' line flies were longer-lived and more fertile late in life than |young' line flies, with no corresponding drop in their early fertility.

It is possible that flies from both selection regimens have evolved independently for the characters in respect of which they differ. Comparison with the base stock, which has presumably evolved considerably more slowly for these characters over the time period since the selection lines were established, could therefore reveal any trade-offs. Comparison of the hybrid lines with the base stock failed to reveal evidence of trade-offs within the adult period. |old' line males lived longer and were more fertile than the base stock but did not differ significantly from it in early fertility. The |old' line males presumably had higher lifetime reproductive success than the males from the base stock, but the design of the present experiments precluded statistical testing, because fertility scores were not available for individual males. The hybrid |young' line males had significantly higher early fertility than did the base stock, presumably a direct response to selection. There was no significant correlated response in either longevity or late fertility. Had the base stock not been examined, the marginally nonsignificant difference in early fertility and the significant difference in late fertility between the |young' and |old' line males could have been mistakenly interpreted as indicative of a possible trade-off between these two characters.

The hybrid |old' line females had greater longevity than the base stock, and also lower early fertility than it. These data could therefore be used to deduce a possible trade-off between early fertility and survival. However, caution is indicated by the finding that the hybrid |young' line females had a marginally nonsignificant tendency toward lower early fertility than the base stock, but had lower longevity and late life fertility than it did, the opposite difference to that predicted by a trade-off.-these results taken together suggest that the drop early in fertility in the hybrid |old' line females relative to the base stock may not have been a correlated response to selection on their late life performance. Rather, it may have been attributable to selection on a character other than age at reproduction per se, and one which was at least partly experienced in common with females from the |young' selection regimen.

Trade-offs between the

Pre-adult and Adult Period

Both sexes from the hybrid |old' lines performed better than those from the |young' lines as adults, had longer development times and had lower larval viability especially at higher larval density. These data could therefore indicate a trade-off between larval and adult performance. However, comparison with the base stock did not support this idea. The hybrid |old' lines performed better than the base stock as adults, but they also performed at least as well as it as larvae, with faster rates of development in both sexes and no significant reduction in larval viability or adult thorax length.

Comparison of the hybrid |young' lines with the base stock also failed to support the idea of a trade-off between the adult and larval period. The hybrid |young' line larvae developed much faster and had higher viability than those of the base stock, yet they also gave rise to fitter male adults, with higher early fertility and unimpaired late fertility and longevity. In females, in contrast, they gave rise to less fit adults with lower longevity and fertility and smaller thoraxes, which is consistent with the idea of a trade-off. The directions of evolutionary change in adult fitness relative to the base stock were opposite for the sexes, yet they both out-performed the base stock as larvae. The pre-adult period may therefore have evolved in response to some aspect of the selection regimens other than age at reproduction per se.

An undetected difference in development time between flies from two selection regimes could produce spurious evidence of differences in early fertility between them, especially in females, if adults from the two regimens were collected for testing at a fixed time after the egg stage rather than after eclosion from the pupa. Flies from the slower developing lines would be more recently eclosed, and hence less fertile.

Inadvertent Selection

The evolution in pre-adult characters in the |young' and |old' lines could have arisen as a correlated response to selection on age at reproduction or, instead, as a result of other uncontrolled differences between the |young' and |old' selection regimens and between both selection regimens and the base stock. It seems highly likely that both sets of selection lines, and especially the |young' lines, were under intense selection to develop rapidly. |Young' line flies were under selection to reach their peak fertility between days 14 and 17 from the egg, when the next generation of eggs was collected. In addition, larval densities were probably higher in the |young' lines (Partridge and Fowler, 1992) and larval development would therefore have been slowed, making selection on development time more intense. Females have to feed in order to mature their ovaries and commence egg production, which causes a delay of a few days between emergence and peak fertility, while males emerge from the pupa with both sperm and accessory fluid present in the reproductive glands and peak in fertility at 12 hours of age (Ashburner, 1989). The |young' line males may therefore have been under less intense selection than the females to develop rapidly. The |young' hybrid females showed the most rapid development of all groups.

The inadvertent selection on the pre-adult period may explain some of the apparently anomalous findings with adults. Hybrid |young' line females showed a significant reduction in thorax length relative to the base stock, and may have sacrificed growth for rapid development, with a deleterious effect on the adult soma apparent as low longevity and low fertility at all ages relative to the base stock. In contrast, hybrid |young' line males increased in early fertility with respect to the base stock, perhaps because this direct response to selection was not so strongly opposed by selection for rapid development. Some selection on development time evidently also occurred in the |old' lines, presumably because only flies emerging before day 17 contributed to the adult population, but despite the fact that the |old' line hybrids developed more rapidly than the base stock, they gave rise to fitter adults.

The results suggest that if artificial selection on age at reproduction is to be fully informative about the pattern of correlated responses, larval densities must be standardized, and all adults must be allowed to emerge and mature in both |old' and |young' lines before the lines are propagated. It is possible that there were genuine correlated responses to selection present in the pre-adult period in these lines, but that they were masked by the effects of unequal selection intensity on the developmental period in the| young' and |old' lines and in males and females.

Mutation Accumulation and Pleiotropy

Hybrid |old' line males had improved in adult performance relative to the base stock with no loss in larval fitness or in early adult fertility. The data therefore strongly suggest that the |old' lines achieved their adult advantage over the base stock by a reversal of the effects of mutation accumulation, and not by a change in the frequency of mutants with pleiotropic effects. For |old' line females the picture was confused by their lower early fertility than the base stock females. The data from the |young' lines were also ambiguous, with some evidence that the |young' line females had traded off rapid development against adult fertility and longevity. In contrast, the |young' line males appeared to have increased in early fertility at no significant cost elsewhere in the life history. Interpretation of the changes is complicated by the finding that pre-adult characters were changing anyway in response to altered direct selection on larval development time.

The data do not support the idea that the lower longevity and late life fertility of the |young' lines relative to the |old' lines could be accounted for by the effects of mutation accumulation in the |young' lines. If the hybrid |young' males are compared with the base stock, they did not differ significantly from it in longevity or late fertility. The data therefore support the idea that the difference between the |young' and |old' lines was attributable to a direct response to selection in the 'old' lines. In females, the hybrid |young' lines lived significantly less long than the base stock, and had lower late fertility than it. These results are consistent with the effects of mutation accumulation. However, they could also be attributable to the effects of direct selection for rapid development.

Our results point to the need to avoid inadvertent direct selection on characters other than those intended. In the present context, standardization of larval density and avoidance of selection pressure for rapid development are clearly important. The data also point to the need for a base stock that allows examination of where the direct and correlated responses to selection have occurred. Unfortunately, unlike E. coli (e.g., Bennett et al., 1992), D. melanogaster stocks cannot at present be revived from freezing. A long established base stock kept under constant conditions is therefore a desirable point of reference.

Literature Cited

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Author:Roper, Caroline; Pignatelli, Patricia; Partridge, Linda
Publication:Evolution
Date:Apr 1, 1993
Words:6331
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