Temperature-size rule is mediated by thermal plasticity of critical size in Drosophila melanogaster

Abstract

Most ectotherms show an inverse relationship between developmental temperature and body size, a phenomenon known as the temperature-size rule (TSR). Several competing hypotheses have been proposed to explain its occurrence. According to one set of views, the TSR results from inevitable biophysical effects of temperature on the rates of growth and differentiation, whereas other views suggest the TSR is an adaptation that can be achieved by a diversity of mechanisms in different taxa. Our data reveal that the fruitfly, Drosophila melanogaster, obeys the TSR using a novel mechanism: reduction in critical size at higher temperatures. In holometabolous insects, attainment of critical size initiates the hormonal cascade that terminates growth, and hence, Drosophila larvae appear to instigate the signal to stop growth at a smaller size at higher temperatures. This is in contrast to findings from another holometabolous insect, Manduca sexta, in which the TSR results from the effect of temperature on the rate and duration of growth. This contrast suggests that there is no single mechanism that accounts for the TSR. Instead, the TSR appears to be an adaptation that is achieved at a proximate level through different mechanisms in different taxa.

Figure 1.

Complete growth curves from larval hatching to adult eclosion at 25°C (black curve) and 17°C (grey curve). Circles are larval and pupal masses and squares are final adult masses. The difference between final pupal mass and adult mass is owing to loss of pupal case. Error bars are standard errors and are obscured by the markers in some cases. Upper panels show duration of each developmental stage at the two temperatures, with vertical lines indicating when 50% of larvae have made the developmental transition (L1, first larval instar; L2, second larval instar; L3, third larval instar).

Figure 2.

Effect of temperature on key size-regulating developmental parameters. Black bars depict values for 25°C, grey bars depict 17°C. (a) Critical size calculated using the breakpoint method. (b) Logarithmic growth rate during TGP. (c) Duration of TGP and TTP_CS. (d) Mass gained during TGP. (e) Mass loss during pupariation and metamorphosis. (f) Wet weight at eclosion. All error bars are 95% CIs. See text for details of statistical comparisons.

Figure 3.

Time to pupariation as a function of converted larval weight at starvation. The dashed lines show the breakpoint in the data and indicate the critical size at 25°C (white) and 17°C (grey and black).