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Keywords:

  • Drosophila melanogaster;
  • geographical variation;
  • larval growth efficiency;
  • temperature

Abstract

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

Geographic clines in ectotherm species including Drosophila melanogaster have been found throughout the world, with genetically larger body size and shorter development time occurring at high latitudes. Temperature is thought to play a major role in the evolution of this clinal variation. Laboratory thermal selection has effects similar to those seen in geographical clines. Evolution at low temperatures results in more rapid development to larger adult flies. This study investigated the effects of geographical origin and experimental temperature on larval growth efficiency in D. melanogaster. Larvae from populations that had evolved at high latitudes were found to use limited food more efficiently, so that the overall adult body size achieved was larger. Larvae reared at a lower experimental temperature (18 °C) used food more efficiently than those reared at a higher temperature (25 °C). The increases in growth efficiency found in populations from high latitudes could explain their increased body size and more rapid development.


Introduction

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

Latitudinal clines in body size have been found in a number of ectotherm species; these include Apis mellifera (honey bee) (Alpatov, 1929), Musca domestica (house fly) (Bryant, 1977), Myrmeleon immaculatus (ant lion) (Arnett & Gotelli, 1999) and Scottolana canadensis (a crustacean copepod) (Lonsdale & Levinton, 1985); in these species larger body size occurs at high latitudes. Latitudinal clines in a related trait, growth rate, have been found in a number of species of fish, including Morone saxatilis (striped bass) (Conover et al., 1997), Fundulus heteroclitus (mummichog) (Schultz et al., 1996) and Menidia menidia (Atlantic silverside) (Conover & Present, 1990). Similarly to body size, growth rate increases with increasing latitude. Latitudinal clines in body size have also been found in a number of species of Drosophila, including Drosophila melanogaster (David & Bocquet, 1975; Watada et al., 1986; Coyne & Beecham, 1987; Imasheva et al., 1993; James et al., 1995; Van ′t Land et al., 1999), D. robusta (Stalker & Carson, 1947), D. simulans (Watada et al., 1986) and D. subobscura (Huey et al., 2000). Flies from populations that evolved at higher latitudes achieve a larger adult body size than those from populations that evolved at lower latitudes.

In addition to the variation in body size of D. melanogaster with latitude, shorter development time, larger egg size and higher ovariole number have been reported at higher latitudes in more than one continent (development time, Australia and South America (James & Partridge, 1995; Van ′t Land et al., 1999) egg size, Australia and South America (Azevedo et al., 1996), ovariole number, Australia, Japan and France/Africa (Watada et al., 1986; Capy et al., 1993; Azevedo et al., 1996)). The repeatability of the clines in these traits in different continents suggests that they are the result of natural selection. However, it is not yet clear what selective agent is responsible for these clines or which traits are the targets of selection.

Latitudinal clines in the characters of ectotherms are largely caused by the environment which they occupy. The environment can have both short-term and long-term effects, from an immediate developmental response to evolutionary adaptation over a number of generations. There are a number of environmental factors which vary with latitude and which could therefore be responsible for the latitudinal variation. The strongest candidate for the selective agent in these clines is temperature. Temperature is highly correlated with latitude in all continents. Laboratory studies of Drosophila provide evidence which implicates temperature as the selective agent involved in the clines. The suite of traits that shows latitudinal clines is similarly affected by laboratory thermal evolution. Flies that evolve at lower temperatures in the laboratory are larger (Anderson, 1966; D. pseudoobscura;Cavicchi et al., 1985; D. melanogaster;Partridge et al., 1994a; D. melanogaster), have a shorter development time (Anderson, 1966; D. pseudoobscura;James & Partridge, 1995; D. melanogaster) and lay larger eggs (Azevedo et al., 1996; D. melanogaster). As well as the evolutionary effect, temperature has a direct environmental effect on these traits; D. melanogaster reared at lower temperatures have larger body size and egg size and longer development time (Azevedo et al., 1996; James et al., 1997). Growth to larger adult body size at lower temperatures is a general characteristic of ectotherms (Ray, 1960; Atkinson, 1994).

The underlying physiological basis of the variation of these traits with latitude and temperature is at present not understood. In vertebrate populations, although some research has been performed on geographical differences in physiology, very few studies were designed to establish whether differences found were genetic or purely environmental (see Garland & Adolph, 1991 for review). In invertebrates, the majority of the research on latitudinal variation in physiology has focused on Drosophila. The main focus of these physiological studies in Drosophila is the metabolic rate which has been seen to increase with latitude (Giesel et al., 1991; Berrigan & Partridge, 1997).

How efficiently an animal can make use of the food resources available to it in terms of growth can have a large impact on its fitness. The ability to grow efficiently where limited resources are available can provide an animal with a great advantage over its fellows. Efficiency of growth in ectotherms has most commonly been measured in fish species. Efficiency of growth in the Atlantic silverside increases with latitude of origin (Present & Conover, 1992). When provided with excess food, a fish which has evolved at high latitude can grow more efficiently than one which has evolved at low latitude (Present & Conover, 1992; Billerbeck et al., 2000). How-ever, when the fish were given limited food there was no difference in the growth efficiency of the populations (Billerbeck et al., 2000). The increase in efficiency with latitude could in part explain the difference in growth rate with latitude (Conover & Present, 1990), however, food consumption also increases with latitude (Present & Conover, 1992; Billerbeck et al., 2000). Efficiency of growth could be a major target of selection in the latitudinal variation of these fish.

Studies of growth efficiency have been performed in D. melanogaster which have evolved at different temperatures in the laboratory. Drosophila melanogaster larvae adapted to low temperature in the laboratory require less food resources to produce a given overall adult size (Neat et al., 1995). This result suggests that growth efficiency may be the main target of selection in thermally adapted populations. Changes in growth efficiency could also account for the changes in other characters. A larva with a higher efficiency of conversion of food resources to adult body size may be able to achieve a larger overall adult size more rapidly, if metabolic efficiency is limiting for growth rate. An increase in metabolic efficiency may also cause a change in reproductive efficiency, thus increasing egg size and ovariole number. It is therefore important to know if this evolution of higher growth efficiency in Drosophila also occurs in natural populations living at higher latitudes. If higher growth efficiency occurs in D. melanogaster at high latitudes as it does in the Atlantic silverside, this could indicate that efficient growth may be widespread in ectotherm species at high latitudes. The first aim of this study was to investigate whether larval growth efficiency is affected by latitude of origin in D. melanogaster originating from a wide latitudinal range in two continents.

A study on the effect of developmental temperature on growth efficiency in the Atlantic silverside, indicated that growth efficiency was higher at low temperatures (Present & Conover, 1992). However, a study of the effect of developmental temperature on laboratory thermally evolved D. melanogaster showed that larval growth efficiency was greater at an experimental temperature of 25 °C than at 16.5 °C (Neat et al., 1995). This contrasted with the evolutionary effects found in the same study, where larvae from low temperature selection lines were found to use food more efficiently than those from high temperature selection lines. However, the reduction in growth efficiency at the lower temperature could have been as a result of the stressful combination of a very low temperature and a very low food level. Although it has been demonstrated repeatedly that the adult body size of a number of species of Drosophila that are fully fed as larvae, increases with decreasing developmental temperature (e.g. Ray, 1960; Powell, 1974; Coyne & Beecham, 1987; Partridge et al., 1994a), this trend is reversed at extremely low temperatures (David et al., 1994; David et al., 1997; Karan et al., 1998; Morin et al., 1999), suggesting that very low temperatures limit growth. Neat et al. (1995) found no difference in adult body size between adults reared at the two experimental temperatures (16.5 and 25 °C) when the larvae had been fully fed, suggesting that the lower temperature used here was too low. Furthermore, the levels of food that the larvae consumed in this experiment were extremely low, which may have further compromised growth, particularly at the low temperature. The second aim of the present study was to determine the effect of developmental temperature on larval growth efficiency of D. melanogaster. A low temperature of 18 °C was used, rather than 16.5 °C, because this temperature is sufficiently different from 25 °C for any temperature related differences to be apparent and size under full feeding is maximal at 18 °C (David et al., 1994; James et al., 1997; Karan et al., 1998; Morin et al., 1999).

The repeated occurrence of both the evolutionary and plastic responses of ectotherm body size to temperature demonstrates that fundamental features of their physiology are responsible. Identification of the processes at work will therefore reveal important constraints on function.

Materials and methods

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

Fly populations

The 10 South American populations of D. melanogaster have been described elsewhere (Azevedo et al., 1996; Van ′t Land et al., 1999; Zwaan et al., 2000). They were collected in 1995 along a latitudinal range from 2.22°S to 41.50°S. The South American populations exhibit latitudinal variation in body size and development time (Van ′t Land et al., 1999) and egg size (Azevedo et al., 1996). The Australian population samples were collected in January 1997, from sites at Cygnet (Tasmania, 43.08°S), Flowerpot (Tasmania, 43.15°S), Innisfail (Queensland, 17.30°S) and Darwin (Northern Territory, 12.23°S). The Australian populations form part of a cline that has previously been found to exhibit latitudinal variation in body size (James et al., 1995), development time (James & Partridge, 1995), egg size and ovariole number (Azevedo et al., 1996). These populations were maintained from collection in bottle culture at 25 °C. The Dahomey population was collected in 1970 and was maintained from collection in population cage culture with overlapping generations at 25 °C. All experiments were carried out at constant temperature and constant day length (12 h light, 12 h dark).

Measurement of larval growth efficiency

To collect eggs, flies were placed in laying pots with yeasted grape juice medium for a 24-h acclimatization period, then transferred to fresh grape juice medium for 2 h to encourage the laying of any retained eggs. The flies were then allowed to lay on fresh grape juice medium for two consecutive periods of 2.5 h. Eggs were picked from the surface of the medium using a needle and placed individually in vials (12 × 50 mm, 110 vials per population) containing 1 mL of agar (5 g L–1) which had been autoclaved and onto the surface of which had been pipetted 35 μL of aqueous solution containing 1.5 mg of yeast. This quantity of yeast was provided because previous studies have shown that this is a sufficient amount of food for the majority of the larvae to reach adulthood, but it produces a substantial reduction in body size compared with ad lib feeding (see Neat et al., 1995 for response curves). For example, mean female wing area for Innisfail (Australia) with 1.5 mg of yeast=1.06 mm2, with 10 mg of yeast (excess food)=1.28 mm2, for Cygnet with 1.5 mg of yeast=1.21 mm2, with 10 mg of yeast=1.49 mm2. The vials were checked regularly for eclosing adults and all flies were removed and frozen soon after emergence. The left wings of all of the emerged flies were then removed and mounted on microscope slides. Wing area was measured using Object Image 1.60p software (by Norbert Vischer, based on the public domain NIH Image program, available at http://simon.bio.uva.nl/object-image.html) on a PowerMacintosh 8600/200 computer with a video camera attached to a compound microscope.

To ensure that any differences in size between populations were not caused by the differences in the amount of food ingested by the larvae rather than differences in growth efficiency, a further test was performed. The addition of a further egg to vials already utilized by experimental larvae allowed us to determine the amount of yeast remaining that would be available for larval consumption. Individual eggs from the two South American cline end populations (Guayaquil and Puerto Montt) were placed in vials containing agar and 1.5 mL yeast solution as in the previous experiment. When pupariation had occurred, the pupae were removed from the experimental vials. Any vial in which no pupa was found was discarded. One freshly laid egg from a standard laboratory stock (Dahomey) was then added to each of the vials. The Dahomey eggs had been collected on a Petri dish containing grape juice medium that had been placed in the cage for 2.5 h. The vials containing the eggs were then left for 3 days (72 h). On the third day, the Dahomey larvae were removed from the vials and were weighed to the nearest 0.002 mg using a Sartorius micro balance. It was not possible to retrieve larvae from all the vials. In some cases it was apparent that very young larvae had crawled up the side of the vial, presumably in search of food and had died. These larvae were not weighed. There was no significant difference in the number of larvae retrieved from the vials that had been previously occupied by the two populations. This method provided us with a measure of the amount of yeast remaining that was available for larval consumption and whether this differed between the two populations.

Experimental groups and treatments

Larval growth efficiency was measured in all 10 South American and all four Australian populations at 25 °C; it was also measured at two temperatures, 18 and 25 °C, for two cline end populations from each continent (Australia: Innisfail 17.30°S and Cygnet 43.08°S, South America: Guayaquil 2.22°S and Puerto Montt 41.50°S). In order to control parental effects, the parents of the experimental individuals were also reared at the experimental temperature.

Statistical analysis

All statistical analysis was performed using JMP 3.2.2 for the Macintosh (SAS, 1997).

Larval growth efficiency method

A Wilcoxon rank sum test was performed to establish if there were differences in size between the larvae raised in the vials that had previously been vacated by larvae of the two South American populations.

Larval growth efficiency in clines from Australia and South America

The variances of the wing area measurements for different sites within each sex were found to be homogeneous. The Australian populations can be considered to be two replicate populations each from high and low latitudes and they were therefore analysed using an analysis of variance (ANOVA), with replicate sites nested within latitude (high or low). The South American populations form a continuous latitudinal cline and they were therefore analysed using least squares regression ANOVA, to look for a relationship between wing area and latitude.

Larval growth efficiency at 2 temperatures

In order to determine if there were differences between lines and between temperatures, two way-ANOVA were performed on each sex with line and temperature as main effects.

Results

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

Larval growth efficiency method

There was no significant difference in weight between the Dahomey larvae reared in the vials previously occupied by Guayaquil or Puerto Montt larvae (Wilcoxon statistic Z=–0.722, P =0.470, Guayaquil mean= 0.0890 ± 0.021 mg (95%), n=45, Puerto Montt mean = 0.090 ± 0.015 mg (95%) n=48), indicating that there was no significant difference in the amount of food available for larval consumption in the vials previously occupied by the larvae from the two populations.

Larval growth efficiency in clines from Australia and South America

In both continents, wing area and therefore larval growth efficiency, increased with latitude. In the South American populations, for both males and females, there were highly significant (P < 0.001) differences between populations and standard least squares regression showed a significant increase in wing area with latitude (female P < 0.05, male P < 0.01) (Fig. 1a,b, Table 1). Analysis of variance of the data from both sexes in the Australian populations showed a significant effect of latitude (P < 0.001) but no significant difference between replicate populations (Fig. 1c,d, Table 2).

image

Figure . 1. Wing area and 95% confidence intervals for adult flies produced from food-restricted larvae: (a) Female, South America; (b) Male, South America; (c) Female, Australia; (d) Male, Australia.

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Table 1.  Least squares regression ANOVA of wing area of food restricted flies among South American populations. Thumbnail image of
Table 2.  Analysis of variance of wing area of food restricted Australian populations with replicate populations nested within latitude. Thumbnail image of

Larval growth efficiency at two temperatures

The wing areas of each of the lines at the two temperatures are shown in Fig. 2.

image

Figure . 2. Mean wing area and 95% confidence intervals of food restricted flies against temperature. (a) Female, (b) Male.

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For both South America and Australia, wing area (and larval growth efficiency) was higher at the lower temperature and in the high latitude lines. For both males and females of Australian and South American origin there were highly significant effects of both temperature and line (P < 0.001) (Table 3). For Australian males there was also a significant interaction effect between line and temperature (P < 0.005).

Table 3.  Analysis of variance of wing area of food restricted Australian and South American populations at 18 and 25 °C. Thumbnail image of

Discussion

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

These experiments were designed to measure larval growth efficiency, the ability of a larva to turn a fixed amount of food into adult body size. The accuracy of the measurement of larval growth efficiency is dependent on their being no differences in the amount of food consumed by larvae from different populations. Our study showed that there was no difference in the amount of food consumed by high and low latitude larvae. Mean weights of Dahomey larvae when removed from the vials 72 h after laying, were higher than would be expected of freshly hatched larvae (Guayaquil=0.089 ± 0.021 mg, Puerto Montt=0.090 ± 0.015 compared with freshly hatched weight of 0.02 mg, data from Partridge et al., 1994b) indicating that there was a small amount of food remaining in the vials. However, the amount of growth achieved by the Dahomey larvae was not affected by the geographical origin of the previous occupant of the vial, indicating that the amount of food consumed by the larvae from the two populations did not differ. These results therefore indicate that our study provides a true measure of larval growth efficiency.

A latitudinal cline in larval growth efficiency was seen in D. melanogaster from South America and Australia. The populations studied originated from a wide latitudinal range in two independent continents, suggesting this is probably a worldwide trend. An increase in larval growth efficiency has previously been found in cold-adapted laboratory thermal selection populations (Neat et al., 1995). The effects found in our study parallel those of laboratory thermal selection and imply that the clines found are the result of natural selection. Our results further implicate temperature as a selective force in the cline (see Introduction). Larval growth efficiency was found to be greater in high latitude populations as a result of natural selection. The increase in efficiency may occur because it is more beneficial for a larva to grow efficiently at low temperatures (high latitudes) or because low temperatures increase the potential for growth and hence make it easier to achieve higher efficiency.

Temperature has been shown to have developmental effects on the size of Drosophila as well as on that of numerous other ectotherms (for review see Atkinson, 1994): D. melanogaster reared at low temperature reach a larger size and lay larger eggs but develop more slowly (Zwaan et al., 1992; Azevedo et al., 1996; James et al., 1997). In the present study, temperature was demonstrated to have an environmental effect on growth efficiency, with larvae raised at 18 °C being more able to convert food into larger adult size than those raised at 25 °C. This result may underlie the evolutionary response of growth efficiency to temperature, with patterns of allocation of nutrients possibly becoming genetically altered. The mechanisms underlying the response of growth efficiency to experimental temperature are not understood and warrant further investigation.

In laboratory thermal selection, as in latitudinal clines, development time has been seen to be slower in populations from higher selection temperatures (Anderson, 1966; James & Partridge, 1995). The increase in body size and accompanying faster development of flies that have evolved at lower temperatures (or higher latitudes) could be explained by the increase in growth efficiency. Greater efficiency could enable a fly to reach a larger size in shorter time. The increase in efficiency of food use may also explain the variation of reproductive characters (ovariole number and egg size) with latitude. An increase in larval growth efficiency could lead to the formation of more ovarioles and the maintenance of this increased efficiency in the adult could lead to the production of larger eggs. If both growth efficiency and reproductive efficiency are increased, then the amount of resources available for reproductive function will be increased.

An increase in larval growth efficiency, as seen in flies originating from high latitudes and at low temperatures, appears to confer an unconditional advantage to the flies. If this was the case, we would expect to see lower latitude flies also evolving higher larval growth efficiency. The cline in growth efficiency suggests the presence of a trade off, with low latitude flies having a lower growth efficiency in order to produce some other trait more advantageous within their environment. Establishing what is involved in this trade off is a challenge for the future.

The increase in larval growth efficiency which we have found in D. melanogaster with both increase in latitude of origin and at low developmental temperatures corresponds to that found in another ectotherm. The growth efficiency of Atlantic silverside fish, increases with increasing latitude when excess food is provided, although not when only limited food is provided (Present & Conover, 1992; Billerbeck et al., 2000). Growth efficiency of the Atlantic silverside also increases at low temperatures. These similarities in growth efficiency variation in these two very different ectotherm species may have implications for other ectotherms. Variation in latitude and in temperature have large effects on ectotherm species but the effects of variation in latitude tend to be similar across species. Body size increases with increasing latitude in a large number of ectotherms (e.g. Alpatov, 1929; Bryant, 1977; Lonsdale & Levinton, 1985; Arnett & Gotelli, 1999). Underlying this increase in body size in ectotherms may be an increase in growth efficiency similar to that which we have demonstrated in D. melanogaster and which has been demonstrated in the Atlantic silverside (Present & Conover, 1992). Many parallels can be drawn between latitudinal variation in Drosophila and other ectotherms, further work in a number of species will enable us to understand similarities in the responses of ectotherms to variation in temperature and latitude.

The discovery that a change in efficiency of growth underlies the plastic response of ectotherm body size to temperature implies that low temperature provides the opportunity for more efficient growth. Understanding the underlying mechanisms of this change in efficiency is likely to identify processes that constrain ectotherm energy budgets. The evolutionary change in efficiency could involve a re-allocation of resources towards growth. Identification of the genes responsible is likely to reveal mechanisms by which allocation of nutrients is controlled.

Acknowledgments

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

We thank BBSRC and NERC for financial help, Jan van ′t Land and Ary Hoffman for fly populations, Ricardo Azevedo for statistical advice, Bas Zwaan and Kevin Fowler for helpful comments and the members of the Partridge group for help picking eggs.

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  2. Abstract
  3. Introduction
  4. Materials and methods
  5. Results
  6. Discussion
  7. Acknowledgments
  8. Bibliography
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