SEARCH

SEARCH BY CITATION

Keywords:

  • body size;
  • Drosophila melanogaster;
  • fertility;
  • longevity;
  • temperature

Abstract

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Genetic variation of body size along latitudinal clines is found globally in Drosophila melanogaster, with larger individuals encountered at higher latitudes. Temperature has been implicated as a selective agent for these clines, because the body size of laboratory populations allowed to evolve in culture at lower temperatures is larger. In this study, we investigated the hypothesis that larger size is favoured at lower temperature through natural selection on adult males. We measured life-span and age-specific fertility of males from lines of flies artificially selected for body size at two different experimental temperatures. There was an interaction between experimental temperature and body size selection for male fitness; large-line males were fitter than controls at both temperatures, but the difference in fitness was greater at the lower experimental temperature. Smaller males did not perform significantly differently from control males at either experimental temperature. The results imply that thermal selection for larger adult males is at least in part responsible for the evolution of larger body size at lower temperatures in this species. The responsible mechanisms require further investigation.


Introduction

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Geographical clines of body size have been observed in several species of ectotherms, with larger individuals found in populations derived from higher latitudes, both in nature and when reared in common conditions (e.g. the house fly Musca domestica ( Bryant, 1977), the honey bee Apis melifera ( Alpatov, 1929), a copepod Scottolana canadensis ( Lonsdale & Levinton, 1985), the Atlantic silverside Menidia menidia ( Conover & Present, 1990), and several Drosophila species (e.g. David & Bocquet, 1975; Coyne & Beecham, 1987)). The appearance of clinal variation under standard experimental conditions indicates that it has a genetic basis. Latitudinal, genetic clines of body size in Drosophila melanogaster have been described in several different parts of the world (e.g. Australia ( James & Partridge, 1995), South America ( van’t Land, 1997), Western Europe and Africa ( Capy et al., 1993 ), Japan ( Watada et al., 1986 ), North America ( Coyne & Beecham, 1987; Capy et al., 1993 ) and Eastern Europe and central Asia ( Imasheva et al., 1994 )). The repeatability of clines both within and between species strongly suggest that the clinal genetic variation is maintained by natural selection. It is important therefore to identify the selective agents maintaining the clines, and to determine if they are the same in different species.

Two lines of evidence implicate temperature as a major factor responsible for evolution of body size along geographical clines in Drosophila. Firstly, genetic changes conferring increased body size have also been reported with increasing altitude in Drosophila (e.g. Stalker & Carson, 1948; Bitner-Mathéet al., 1995 ). Secondly, in laboratory studies in which replicated populations of Drosophila are maintained at different temperatures, body size evolves to be larger in populations maintained at lower temperatures (e.g. Anderson, 1966, 1973; Cavicchi et al., 1985 , 1989; Partridge et al., 1994 ).

Although temperature is implicated as a selective agent in latitudinal clines, the identity of the targets of selection is less clear, and body size per se may not be included. Other traits show latitudinal clines (e.g. development time ( James et al., 1995 ) and growth efficiency (S. Robinson and L. Partridge, unpublished data)), and also respond to laboratory thermal selection (e.g. development time ( Anderson, 1966; James & Partridge, 1995) and growth efficiency ( Neat et al., 1995 )). Body size could evolve as a correlated response to selection on one of these other traits. To determine if thermal selection acts on body size, the trait must be manipulated without these correlated responses to thermal selection, and the fitness effects examined. Neither lines produced by laboratory thermal selection (e.g. Partridge et al., 1995 ), nor lines from nature expressing genetic difference in size (e.g. Tantawy & El-Helw, 1970), can be used to infer the effects of thermal selection on body size per se. Such lines will exhibit differences in other aspects of adaptation to temperature, from which the role of body size cannot be disentangled. Investigation of the effect of body size using rearing temperature to produce variation in size (e.g. Zamudio et al., 1995 ; Nunney & Cheung, 1997) is also potentially problematic, because rearing temperature affects other traits, such as growth efficiency, that influence adult fitness at different temperatures.

One way to approach the problem is to manipulate body size by artificial selection. One study has performed this, manipulating body size by selecting for increased and decreased wing area ( McCabe & Partridge, 1997). In these selection lines cell size was kept constant, in accordance with the pattern of latitudinal variation in size ( James et al., 1995 ). Artificial selection can itself result in correlated responses, but they are in general different from those seen with thermal selection on body size. Neither pre-adult development time ( Azevedo et al., 1997 ) nor growth efficiency (J. Pelage, J. McCabe and L. Partridge, unpublished data) were altered by artificial selection. These selection lines therefore did not show the pattern of correlated responses to body size change seen with latitudinal and thermal selection ( James & Partridge, 1995). McCabe & Partridge (1997) demonstrated that the fitness of the adult female stage of life history in D. melanogaster is implicated in the evolution of larger size at lower temperature. They found a strong interaction between body size selection and environmental temperature for both survival and lifetime reproductive success, with larger females living relatively longer and producing relatively more offspring than controls at the lower experimental temperature ( McCabe & Partridge, 1997).

No comparable investigation has been carried out on the adult male stage of the life history. As the physiology and behaviour of female and male D. melanogaster are very different, we might not expect the relationship between their fitness and their body size to respond in the same way to environmental temperature. There are precedents for interactions between sex and temperature in the determination of adult fitness in Drosophila ( Vieira et al., 2000 ). Males produce many small gametes, whereas females produce relatively few large ones, and so males are capable of fertilizing more eggs than the total eggs produced. Males hence compete for females, and are therefore under strong selection to find and court females. The main cost of reproduction in male Drosophila is behavioural ( Cordts & Partridge, 1996), whereas that in females is associated with egg-production and the consequences of mating (e.g. Maynard Smith, 1958; Lamb, 1964; Chapman et al., 1995 ). In Drosophila there is a quite pronounced sexual dimorphism, with female flies significantly larger than males. Thermal selection on adult body size might therefore be expected to differ between the sexes. Body size of both sexes evolves in response to latitude and laboratory thermal selection, but male size could be a correlated response to selection on females, as there is a strong genetic correlation between the size of the two sexes ( Cowley & Atchley, 1990).

We have therefore tested the hypothesis that larger size evolves at lower temperatures in part through selection on adult males. We looked for an interaction between effects of genetically determined body size and environmental temperature for male longevity and fertility. The replicated selection lines had been artificially selected for increased and decreased wing area ( McCabe et al., 1997 ). The selection lines expressed correlated responses in thorax length ( McCabe et al., 1997 ), and adult dry weight ( Azevedo et al., 1997 ), confirming that the selection on wing size conferred differences in body size. In order to examine male fitness traits, the selected males were competed with a standard, mutant-marked, random-bred competitor strain, to produce a biologically realistic set of measures of adult male competitive reproductive success.

Materials and methods

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Selection lines and competitor stock

The selection lines have been described elsewhere ( McCabe & Partridge, 1997; McCabe et al., 1997 ). They were derived from a random-bred, wild-type stock collected in Dahomey, West Africa, in 1970, maintained as in cage culture at 25 °C. In 1996, three replicate large-, control- and small-sized lines were artificially selected for wing area with constant cell area. For each selection line, the wing area and cell area of 25 pairs of flies were measured in each generation. For the three control lines, 10 males and 10 females were selected at random. For the large- and small-size selection lines, flies with the 10 largest or smallest wing areas for each sex were selected as the parents of the next generation, while ensuring that the mean cell area of these pairs corresponded with the mean cell area of the controls. Each replicate line was propagated by setting up 100 first instar larvae in a bottle of 70 mL medium seeded with live yeast. Selection was continued for eight generations, after which the lines were maintained in bottle culture at 18 °C, under standard low larval density (<300 emergees per bottle), for a year before this experiment was carried out.

The competitor stock used in the experiment carried the recessive mutant marker scarlet in an approximately Dahomey genetic background. It had been produced, in 1988, by two rounds of back-crossing of the scarlet mutant into the Dahomey genetic background. The line had been maintained at 25 °C in population cage culture.

Measurement of male life-history traits

In order to assess the fitness of adult male flies from the selection lines, longevity and age-specific fertility were measured. Fertility was estimated as the proportion of wild-type progeny when selection line males competed with scarlet-eyed males for matings with scarlet-eyed females. Hence, this measurement of fertility incorporates male mating success, sperm competition and fecundity. To determine the influence of environmental temperature, the experiment was carried out at two different temperatures; 18 and 25 °C, with the experimental flies and competitors being reared and tested at the experimental temperature. These measurements were based on those used by Roper et al. (1993 ).

The selection lines and the scarlet competitor stock were maintained in standard, low larval density, bottle culture at each experimental temperature for at least two generations prior to the experiment, to avoid the parental and early embryonic effects of temperature and temperature shift ( Huey et al., 1995 ; Crill et al., 1996 ). Twenty pairs of flies were taken from each selection line population to be the parents of the experimental flies, and were transferred to laying pots containing yeasted grape juice medium. After an acclimatory period of 48 h at 18 °C or 24 h at 25 °C, the flies were transferred to fresh medium for a 2-h pre-lay period and then transferred again to fresh medium for egg collection, which lasted for 8 h at 18 °C and 4 h at 25 °C. First instar larvae were collected 46 h after the midpoint of the lay at 18 °C, and 23 h after the midpoint at 25 °C. Fifty larvae were placed in vials containing 7 mL medium, with four vials per selection line. Collection of emerging virgin male flies from these vials was carried out by anaesthesia over ice within 8 h of eclosion. For the scarlet competitor stock, six laying pots were set up as for the selection line populations, each with 20 pairs of flies. Ten vials of 50 larvae were collected from each laying pot. Emerging virgin 50 of both sexes were collected from these vials in a similar manner to the selection line flies.

At each temperature, for each selection line, 10 virgin scarlet females, three selection line males, and seven scarlet males were set up in each of 13 replicate bottles, each containing 70 mL of food medium and active yeast. This design ensured that the selection-line males competed mainly with scarlet males, rather than with each other. Flies in each bottle were transferred to fresh bottles every 4 days at 18 °C, and every other day at 25 °C, to compensate for the increased rate of living at the higher temperature. The bottles from which the selection line flies were removed were kept at 18 °C. Deaths of selection line males were recorded when flies were transferred, and the longevities of the first 37 flies to die from each line were noted. All scarlet flies were replaced with virgins every 4 weeks at 18 °C, and every 2 weeks at 25 °C. Male fertility was recorded as the proportion of adult progeny that were wild-type emerging from the bottles from which the selection line flies had been removed. A subsample of 10 of the 13 bottles was examined, and the numbers and genotypes of flies in these bottles were maintained by replacing dead flies with individuals from the remaining three bottles. In these three bottles, dead scarlet flies, but not selection line flies, were replaced from a group of virgins. When sufficient death had occurred that fewer than 10 bottles could be maintained with a full complement of flies, the number of bottles in the experiment was reduced accordingly. When fewer than three flies remained in a line, that line was no longer maintained. Adult flies were handled at room temperature, and anaesthesia was carried out with carbon dioxide.

To provide an estimate of male fitness for each replicate selection line, the total number of wild type flies emerging from all of the bottles from each line was counted. This gave a measure of total lifetime competitive reproductive success for the males of each replicate selection line. This measure was used rather than a measurement of the proportion of progeny sired by the selection line males, because it takes the survival of the selection line males as well as their fertility into account. A measure based on the proportion of wild type progeny produced would reflect only fertility and would also be biased by the declining fertility of the selection line males relative to their younger scarlet competitors as the experiment proceeded.

Wing size

To give an indication of the body size of the lines, the wing size of the selection line males used in the experiment was measured. A sample of 10 male flies was taken from each of two of the vials of virgin selection line flies collected at the time of initiation of the experiment at each experimental temperature. The right wings of these sample flies were fixed in propanol and mounted in Aquamount on microscope slides. The areas of the mounted wings were digitized using a camera attached to a microscope at ×50 magnification, and analysed using Object-Image version 1.62 for the Macintosh. The area within six landmarks around the edge of the wing, where veins intersected with the boundary, was measured for each wing.

Statistical analysis

The longevity, fertility, fitness and wing size data were subjected to analyses of variance. After transformation of the data, if appropriate, homogeneity of variance was confirmed in all cases with the O’Brien test, which performs an analysis of variance on a new variable, created using group sample variances from the data, to compare spread in the groups. Normality of the error distribution was confirmed with the Shapiro–Wilk test.

The variances among environmental temperatures were significantly heterogeneous for longevity. Environment heteroscedasticity was eliminated by transformation following the procedure outlined by Dutilleul & Potvin (1995; eqn 6). The data were subjected to an analysis of variance, treating experimental temperature and selection regime as fixed main effects, and replicate lines as a random effect, nested within selection, and individual fly death times as the unit of replication. Linear contrast analyses were used to compare the longevity of pairs of selection regimes.

The assessment of fertility involved repeated measures on at least some of the same individuals. To minimize pseudoreplication, while examining the temporal patterns of reproduction in lines from different regimes, the data were divided into ‘early’ and ‘late’ phases of adult life. ‘Early’ data consisted of the total number of wild-type flies emerging from each bottle of each line in the first five sampling intervals (up to day 20 at 18 °C, and day 10 at 25 °C), divided by the total number of flies (wild-type and scarlet) emerging from the same bottle. ‘Late’ data consisted of the data collected at subsequent sampling intervals, up to the interval at which more than 20% of the flies had died in the replicate line with the highest mortality rate. The fertility data were subjected to an analysis of variance, with temperature and selection regime as fixed main effects, and replicate lines as a random effect nested within selection, and with bottles as the unit of replication. Linear contrast analyses were used to compare the fertility of pairs of selection regimes.

The fitness data were subjected to a two-way analysis of variance, with temperature and selection as fixed main effects, and replicate lines as the unit of replication.

The wing size data were subjected to an analysis of variance, with temperature and selection as fixed main effects, and replicate lines as a random effect nested within selection. There was no significant between-vial variance, and so data from individual body size measurements were used in the analysis.

All analyses were carried out using JMP statistical package version 3.2.2 for the Macintosh (SAS 1997).

Results

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

Longevity

There were significant effects of both temperature and selection regime upon longevity ( Fig. 1). Flies lived significantly longer at the lower experimental temperature. The large-size selection lines lived for significantly longer than flies from the control-size selection lines at both temperatures (18 °C: F1,6=63.3563, P < 0.001; 25 °C: F1,6=9.8780, P < 0.05). The small-size selection lines and the control-size selection lines did not differ significantly from each other in longevity at either temperature (18 °C: F1,6=1.7911, NS; 25 °C: F1,6= 0.0026, NS). There was a significant interaction between temperature and selection regime, mainly attributable to greater survival of the large-size selection lines relative to the other lines at the lower experimental temperature. There was significant variation between the lines within the selection regimes for survival, but there was no significant interaction between temperature and lines within selection regime.

image

Figure 1 Mean lifespan, transformed using the procedure outlined in Dutilleul & Potvin (1995; eqn 6) (±95% CL) of males from the large-, control- and small-size selection lines reared and tested at 18 and 25 °C. Results of ANOVA on transformed longevity; Temperature: F1,6=2455.743, P < 0.001, Selection Regime: F2,6=23.732, P < 0.01, Lines within selection: F6,648=6.675, P < 0.001, Temperature × selection: F2,6=13.111, P < 0.01, Temperature × lines within selection: F6,648=2.01. 6, P=NS.

Download figure to PowerPoint

Male fertility

Both temperature and selection regime had a significant effect on both ‘early’ and the ‘late’ male fertility ( Fig. 2). Fertility was higher at the lower experimental temperature. Males from the large-size selection lines sired a greater proportion of progeny than both the small- and control-size selection lines. The small- and control-size selection lines did not differ significantly from one another in fertility at either experimental temperature, in either phase of adult life. The analysis of variance also revealed a highly significant interaction between temperature and selection regime in both phases, mainly because the large-size selection line males had a greater fertility-advantage at the lower experimental temperature. There was a significant effect on male fertility of lines within selection, but there was no significant interaction between the lines within selection and temperature, for either phase.

image

Figure 2 Mean fertility (±95% CL) of males from the large-, control- and small-size selection lines reared and tested at 18 and 25 °C. Data is split into (a) ‘early’ and (b) ‘late’ fertility. ‘Early’ fertility is the sum of the proportions of progeny sired by the selection line flies in the first five sampling intervals at each temperature, and ‘late’ fertility is the sum of the proportions of progeny sired by the selection line flies at subsequent sampling intervals. Results of ANOVA on ‘early’ fertility; Temperature: F1,6=119.5031, P < 0.001, Selection Regime: F2,6=17.6771, P < 0.001, Lines within selection: F6,162=2.5741, P < 0.05, Temperature × selection: F2,6=25.3115, P < 0.001, Temperature × lines within selection: F6,162=0.4021, P=NS. Results of ANOVA on ‘late’ fertility; Temperature: F1,6=40.9683, P < 0.001, Selection Regime: F2,6=26.2688, P < 0.01, Lines within selection: F6,162=2.3688, P < 0.05, Temperature × selection: F2,6=29.8356, P < 0.001, Temperature × lines within selection: F6,162. =0.4463, P=NS.

Download figure to PowerPoint

Male fitness

Temperature did not have a significant effect on fitness (Table 1). Selection regime, however, did have a significant effect, with large-size selection lines being significantly fitter than controls. Small-size selection lines were not significantly different in fitness from the control lines. There was also a significant interaction between temperature and selection regime, mainly because of the increased fitness of the large size selection lines when reared and tested at the lower temperature. There was no significant effect of lines within selection.

Table 1.   Two-way nested analysis of variance on fitness of males from the large-, control- and small-size selected lines reared and tested at 18 or 25 °C. Replicate lines were treated as random effects, nested within selection regime, and selection regime and temperature were analysed as fixed effects. Thumbnail image of

Wing size

There was a highly significant difference in wing area between flies from the different selection regimes ( Fig. 3). Experimental temperature also had a highly significant effect on wing area, which was greater at the lower temperature for all three selection regimes. There was a significant interaction between selection and temperature, mainly owing to a reduction in the size-differences between the different selection regimes at 25 °C. There was also a significant effect of lines within selection, and of the interaction between temperature and lines within selection.

image

Figure 3 Wing size of the males from the size selected lines which were used in the experiment at 18 and 25 °C. Each point corresponds to the mean (±95% CL) of the 20 samples from each of the three replicate lines within each selection regime. Results of ANOVA on wing size; Temperature: F1,6=374.1518, P < 0.001, Selection Regime: F2,6=42.2314, P < 0.001, Lines within selection: F6,342=20.4897, P < 0.001, Temperature × selection: F2,6=8.5210, P < 0.05, Temperature × lines within selection: F6,3. 42=10.1876, P < 0.001.

Download figure to PowerPoint

Discussion

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

The results implicate male body size as a target of thermal selection in Drosophila. Males from the large-size selection lines lived longer than controls and sired relatively more offspring than them at both experimental temperatures, and the extent of their advantage was greater at the lower experimental temperature. The fitness advantage of the large lines was hence greater at the lower experimental temperature. The results implicate body size per se, or some trait genetically correlated with it, as the target of thermal selection. It will be important to determine what aspect of body size is important. The size of most external body parts is altered by selection on wing area ( Wilkinson et al., 1990 ), and the size of at least some internal structures must also be changed.

The results for male fitness parallel those previously found for females of these selection lines ( McCabe & Partridge, 1997) and show that, despite the very different behaviour and physiology of females and males, thermal selection acts on their body size in a similar way. Some basic aspect of biological function must therefore be affected. Within a single temperature, increased body size is associated with an increase in lifespan of both males and females, both as a genetic correlation (e.g. Tantawy & Rakha, 1964; Tantawy & El-Helw, 1966; Partridge & Fowler, 1992) and as a phenotypic correlation (e.g. Partridge & Farquhar, 1981, 1983; Partridge et al., 1986 ). The mechanisms at work could be similar in the sexes, and might lead to a parallel response to temperature, but it is not clear why temperature affects either relationship. Positive genetic (e.g. male: Ewing, 1961; Wilkinson, 1987; female: Tantawy, 1961; Tantawy & Rakha, 1964; Tantawy & El-Helw, 1966; Hillesheim & Stearns, 1992) and phenotypic (e.g. male: Partridge & Farquhar, 1981, 1983; Partridge et al., 1987a , b; female: Tantawy & Vetukhiv, 1960 ; Partridge et al., 1986 ) correlations between body size and fertility have also been reported for both sexes. The mechanisms at work in the two sexes are likely to be different, with ability to accrue nutrients and convert them into eggs important for females ( Maynard Smith, 1958; Lamb, 1964) and mating success playing a more important role for males ( Cordts & Partridge, 1996). Again, the reasons why temperature should affect the relationships between body size and fertility are unclear.

Two possible explanations for these observations are based on body size per se. Firstly, the relationship between male fitness and body size may change in response to environmental temperature. Secondly, when reared at the lower experimental temperature, the large-size selection lines were larger than any of the other selection line flies at either experimental temperature, and may have entered a size range in which fitness increases more rapidly with increase in body size. To test which of these explanations is most plausible, it would be necessary to produce lines of flies with a wide range of body sizes, and compare their performance as adults at the two experimental temperatures, so that the effects of phenotypic size and experimental temperature could be separated. Whatever the explanation, the results provide direct evidence for an interaction between genetically determined body size and environmental temperature in the determination of adult male fitness.

Fitness was measured on adult males, but it is possible that the interaction between temperature and genetic variation for size in the determination of adult fitness occurs during the pre-adult period. Lower environmental temperature during growth increases growth efficiency (S. Robinson and L. Partridge, unpublished observations), and in the present experiment led to larger adult body size at the lower experimental temperature for all lines ( Fig. 3), as has been observed previously (e.g. Alpatov, 1930; Robertson, 1959; Partridge et al., 1994 ). This increased growth efficiency may be particularly beneficial to the adult fitness of individuals that are, for genetic reasons, capable of achieving larger adult size, and may have contributed to the gene-by-environment interaction for body size observed in the present study. This variation in the pattern of plasticity of body size in response to developmental temperature may have played a role in the determination of adult fitness. The difference in male body size between the large and control selection lines was reduced at the higher experimental temperature ( Fig. 3). This phenomenon was not observed for female body size one year previously ( McCabe & Partridge, 1997; Fig. 2). Therefore, this interaction has either evolved in the intervening time, or was always the case for male body size, the plasticity of which has not previously been examined in these lines.

Whatever the mechanism producing the effect of environmental temperature on the fitness advantage of the large line males, it could be important in nature. One study of a latitudinal cline in body size in Eastern Australia found that, in flies collected directly from nature, the genetic cline for body size with increasing latitude was steepened by the direct effects of environmental temperature ( James et al., 1997 ). Flies from higher latitudes were both genetically and environmentally larger. If the interaction relationship between genetically determined size and environmental temperature in the determination of adult fitness is operative in nature, then selection for genetically increased body size may be more intense in the lower temperatures at higher latitudes, either because the phenotypic plasticity of body size during development is especially beneficial to genetically large individuals, or because it takes genetically large flies into a higher range of body size before selection acts on the adults. The first explanation is not supported by the finding that phenotypic plasticity of body size shows very little clinal variation ( James et al., 1997 ; Morin et al., 1999 ). A major unanswered question is the identity of the mechanisms responsible for the phenotypic plasticity of body size of ectotherms generally in response to growth temperature ( Atkinson, 1994).

Latitudinal size clines have been found in several invertebrates and vertebrates: the house fly Musca domestica ( Bryant, 1977), the honey bee Apis melifera ( Alpatov, 1929), an ant lion Myrmeleon immaculatus ( Arnett & Gotelli, 1999), a copepod Scottolana canadensis ( Lonsdale & Levinton, 1985) and several species of fish (the Atlantic silverside Menidia menidia ( Conover & Present, 1990; Billerbeck et al., 2000 ); the striped bass Morone saxatilis ( Brown et al., 1998 ) and the Mummichog Fundulus heteroclitus ( Schultz et al., 1996 )). The selective agents responsible for these latitudinal clines may or may not be the same across different taxa. The size clines in the three fish species are all associated with increased rate of growth and growth efficiency, as in Drosophila, which may indicate that there are common mechanisms at work.

Acknowledgments

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References

We thank C. Sgrò, G. Shreeves and W. J. Kennington for discussion, G. Geddes for practical advice and the Natural Environment Research Council for financial support.

References

  1. Top of page
  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. References
  • 1
    Alpatov, W.W. 1929. Biometrical studies on variation and races of the honey bee (Apis melifera) . Q. Rev. Biol. 4: 1 58.
  • 2
    Alpatov, W.W. 1930. Phenotypical variation in body and cell size of Drosophila melanogaster. Biol. Bull. 58: 85 103.
  • 3
    Anderson, W.W. 1966. Genetic divergence in M. Vetukhiv’s experimental populations of Drosophila pseudoobscura. III. Divergence in body size . Genet. Res., Cambridge 7: 255 266.
  • 4
    Anderson, W.W. 1973. Genetic divergence in body size among experimental populations of Drosophila pseudoobscura kept at different temperatures. Evolution 27: 278 284.
  • 5
    Arnett, A.E. & Gotelli, N.J. 1999. Geographic variation in life-history traits of the ant lion, Myrmeleon immaculatus: evolutionary implication of Bergmann’s rule . Evolution 53: 1180 1188.
  • 6
    Atkinson, D. 1994. Temperature and organism size: a biological law for ectotherms? Adv. Ecol. Res. 25: 1 58.
  • 7
    Azevedo, R.B.R., French, V., Partridge, L. 1997. Life-history consequences of egg size in Drosophila melanogaster. Am. Nat. 150: 250 282.
  • 8
    Billerbeck, J.M., Schultz, E.T., Conover, D.O. 2000. Adaptive variation in energy acquisition and allocation among latitudinal populations of the Atlantic sliverside. Oecologia 122: 210 219.
  • 9
    Bitner-Mathé, B.C., Peixoto, A.A., Klaczko, L.B. 1995. Morphological variation in a natural population of Drosophila mediopunctata: altitudinal cline, temporal changes and influence of chromosome inversions . Heredity 75: 54 61.
  • 10
    Brown, J.J., Ehtisham, A., Conover, D.O. 1998. Variation in larval growth rate among striped bass stocks from different latitudes. Trans. Am. Fish Soc. 127: 598 610.
  • 11
    Bryant, E.H. 1977. Morphological adaptation of the housefly, Musca domestica L., United States. Evolution 31: 580 596.
  • 12
    Capy, P., Pla, E., David, J.R. 1993. Phenotypic and genetic variability of morphometric traits in natural populations of Drosophila melanogaster and Drosophila simulans: 1. Geographic variations . Genet. Select. Evol. 25: 517 526.
  • 13
    Cavicchi, S., Guerra, D., Giorgi, G., Pezzoli, C. 1985. Temperature-related divergence in experimental populations of Drosophila melanogaster. I. Genetic and developmental basis of wing size and shape variation . Genetics 109: 665 689.
  • 14
    Cavicchi, S., Guerra, D., Natali, V., Pezzoli, C., Giorgi, G. 1989. Temperature-related divergence in experimental populations of Drosophila melanogaster. II. Correlation between fitness and body dimensions . J. Evol. Biol. 2: 235 251.
  • 15
    Chapman, T., Liddle, L.F., Kalb, J.M., Wolfner, M.F., Partridge, L. 1995. Cost of mating in Drosophila melanogaster females is mediated by male accessory-gland products. Nature 373: 241 244.
  • 16
    Conover, D.O. & Present, T.M.C. 1990. Countergradient variation in growth rate: compensation for length of the growing season among Atlantic silversides from different latitudes. Oecologia 83: 316 324.
  • 17
    Cordts, R. & Partridge, L. 1996. Courtship reduces longevity of male Drosophila melanogaster. Anim. Behav. 52: 269 278.
  • 18
    Cowley, D.E. & Atchley, W.R. 1990. Development and quantitative genetics of correlation structure among body parts of Drosophila melanogaster. Am. Nat. 135: 242 268.
  • 19
    Coyne, J.A. & Beecham, E. 1987. Heritability of two morphological characters within and among natural populations of Drosophila melanogaster. Genetics 117: 727 737.
  • 20
    Crill, W.D., Huey, R.B., Gilchrist, G.W. 1996. Within-generation and between-generation effects of temperature on the morphology and physiology of Drosophila melanogaster. Evolution 50: 1205 1218.
  • 21
    David, J.R. & Bocquet, C. 1975. Similarities and differences in latitudinal adaptation of two Drosophila sibling species. Nature 257: 588 590.
  • 22
    Dutilleul, P. & Potvin, C. 1995. Among environment heteroscedasticity and genetic autocorrelation: implications for the study of phenotypic plasticity. Genetics 139: 1815 1828.
  • 23
    Ewing, A.W. 1961. Body size and courtship behaviour in Drosophila melanogaster. Anim. Behav. 9: 93 99.
  • 24
    Hillesheim, E. & Stearns, S.C. 1992. Correlated responses in life history traits to artificial selection for body weight in Drosophila melanogaster. Evolution 46: 745 752.
  • 25
    Huey, R.B., Wakefield, T., Crill, W.D., Gilchrist, G.W. 1995. Within- and between-generation effects of temperature on early fecundity of Drosophila melanogaster. Heredity 74: 216 223.
  • 26
    Imasheva, A.G., Bubli, O.A., Lazebny, O.E. 1994. Variation in wing length in Eurasian natural populations of Drosophila melanogaster. Heredity 72: 508 514.
  • 27
    James, A.C., Azevedo, R., Partridge, L. 1995. Cellular basis and developmental timing in a size cline of Drosophila melanogaster. Genetics 140: 659 666.
  • 28
    James, A.C., Azevedo, R., Partridge, L. 1997. Genetic and environmental responses to temperature of Drosophila melanogaster from a latitudinal cline. Genetics 146: 881 890.
  • 29
    James, A.C. & Partridge, L. 1995. Thermal evolution of rate of larval development in Drosophila melanogaster in laboratory and field populations. J. Evol. Biol. 8: 315 330.
  • 30
    Lamb, M.J. 1964. The effects of radiation on the longevity of female Drosophila subobscura. J. Insect Physiol. 10: 487 497.
  • 31
    Van’T Land, J. 1997. Latitudinal variation in Drosophila melanogaster. On the maintenance of world-wide polymorphisms for Adh, αGpdh and In (2L) t, PhD Thesis, University of Groningen, The Netherlands.
  • 32
    Lonsdale, D.J. & Levinton, J.S. 1985. Latitudinal differentiation in copepod growth: an adaptation to temperature. Ecology 66: 1397 1407.
  • 33
    Maynard Smith, J. 1958. The effects of temperature and egg-laying on the longevity of female Drosophila subobscura. J. Exp. Biol. 35: 832 842.
  • 34
    McCabe, J., French, V., Partridge, L. 1997. Joint regulation of cell size and cell number in the wing blade of Drosophila melanogaster. Genet. Res., Cambridge 69: 61 68.
  • 35
    McCabe, J. & Partridge, L. 1997. An interaction between environmental temperature and genetic variation for body size for the fitness of adult female Drosophila melanogaster. Evolution 51: 1164 1174.
  • 36
    Morin, J.P., Moreteau, B., Pétavy, G., David, J.R. 1999. Divergence of reaction norms of size characters between tropical and temperate populations of Drosophila melanogaster. J. Evol. Biol. 12: 329 339.
  • 37
    Neat, F., Fowler, K., French, V., Partridge, L. 1995. Thermal evolution of growth efficiency in Drosophila melanogaster. Proc. Roy. Soc. London B 260: 73 78.
  • 38
    Nunney, L. & Cheung, W. 1997. The effect of temperature on body size and fecundity in female Drosophila melanogaster: evidence for adaptive plasticity . Evolution 51: 1529 1535.
  • 39
    Partridge, L., Barrie, B., Barton, N.H., Fowler, K., French, V. 1995. Rapid laboratory evolution of adult life-history traits in Drosophila melanogaster in response to temperature. Evolution 49: 538 544.
  • 40
    Partridge, L., Barrie, B., Fowler, K., French, V. 1994. Evolution and development of body-size and cell-size in Drosophila melanogaster in response to temperature. Evolution 48: 1269 1276.
  • 41
    Partridge, L. & Farquhar, M. 1981. Sexual activity reduces lifespan of male fruitflies. Nature 294: 580 582.
  • 42
    Partridge, L. & Farquhar, M. 1983. Lifetime mating success of male fruitflies (Drosophila melanogaster) is related to their size . Anim. Behav. 31: 871 877.
  • 43
    Partridge, L. & Fowler, K. 1992. Direct and correlated responses to selection on age at reproduction in Drosophila melanogaster. Evolution 46: 76 91.
  • 44
    Partridge, L., Fowler, K., Trevitt, S., Sharp, W. 1986. An examination of the effects of males on the survival and egg production rates of female Drosophila melanogaster. J. Insect Physiol. 32: 925 929.
  • 45
    Partridge, L., Hoffmann, A., Jones, S.J. 1987a. Male size and mating success in Drosophila melanogaster and D. pseudoobscura under field conditions. Anim. Behav. 35: 468 476.
  • 46
    Partridge, L., Ewing, A., Chandler, A. 1987b. Male size and mating success in Drosophila melanogaster: the roles of male and female behaviour . Anim. Behav. 35: 555 562.
  • 47
    Robertson, F.W. 1959. Studies in quantitative inheritance. XII. Cell size and number in relation to genetic and environmental variation of body size in Drosophila. Genetics 44: 869 896.
  • 48
    Roper, C., Pignatelli, P., Partridge, L. 1993. Evolutionary effects of selection on age at reproduction in larval and adult Drosophila melanogaster. Evolution 47: 445 455.
  • 49
    Schultz, E.T., Reynolds, K.E., Conover, D.O. 1996. Countergradient variation in growth among newly hatched Fundulus heteroclitus: Geographic differences revealed by common-environment experiments . Func. Ecol. 10: 366 374.
  • 50
    Stalker, H.D. & Carson, H.L. 1948. An altitudinal transect of Drosophila robusta Sturtevant. Evolution 2: 295 305.
  • 51
    Tantawy, A.O. 1961. Effects of temperature on productivity and genetic variance of body size in Drosophila melanogaster. Genetics 46: 227 238.
  • 52
    Tantawy, A.O. & El-Helw, M.R. 1966. Studies on natural populations of Drosophila. V. Correlated response to selection in Drosophila melanogaster. Genetics 53: 97 110.
  • 53
    Tantawy, A.O. & El-Helw, M.R. 1970. Studies on natural populations in Drosophila. IX. Some fitness components and their heritabilities in natural and mutant populations of Drosophila melanogaster. Genetics 64: 79 91.
  • 54
    Tantawy, A.O. & Rakha, F.A. 1964. Studies on natural populations in Drosophila. IV. Genetic variances of and correlations between four characters in Drosophila melanogaster. Genetics 50: 1349 1355.
  • 55
    Tantawy, A.O. & Vetukhiv, M.O. 1960. Effects of size on fecundity, longevity and viability in populations of Drosophila pseudoobscura. Am. Nat. 94: 395 403.
  • 56
    Vieira, C., Pasyukova, E.G., Zeng, Z., Hackett, J.B., Lyman, R.F., Mackay, T.F.C. 2000. Genotype–environment interaction for quantitative trait loci affecting lifespan in Drosophila melanogaster. Genetics 154: 213 227.
  • 57
    Watada, M., Ohba, S., Tobari, Y.N. 1986. Genetic differentiation in Japanese populations of Drosophila simulans and Drosophila melanogaster II. Morphological variation. Jap. J. Genet. 61: 469 480.
  • 58
    Wilkinson, G.S. 1987. Equilibrium analysis of sexual selection in Drosophila melanogaster. Evolution 41: 11 21.
  • 59
    Wilkinson, G.S., Fowler, K., Partridge, L. 1990. Resistance of genetic correlation structure to directional selection in Drosophila melanogaster. Evolution 44: 1990 2003.
  • 60
    Zamudio, K.R., Huey, R.B., Crill, W.D. 1995. Bigger isn’t always better: body size, developmental and parental temperature and male territorial success in Drosophila melanogaster. Anim. Behav. 49: 671 677.