Metabolic rate and hypoxia tolerance are affected by group interactions and sex in the fruit fly (Drosophila melanogaster): new data and a literature survey

Abstract

Population density and associated behavioral adjustments are potentially important in regulating physiological performance in many animals. In r-selected species like the fruit fly (Drosophila), where population density rapidly shifts in unpredictable and unstable environments, density-dependent physiological adjustments may aid survival of individuals living in a social environment. Yet, how population density (and associated social behaviors) affects physiological functions like metabolism is poorly understood in insects. Additionally, insects often show marked sexual dimorphism (larger females). Thus, in this study on D. melanogaster, we characterized the effects of fly density and sex on both mass-specific routine oxygen consumption (V̇O₂) and hypoxia tolerance (P_Crit). Females had significantly lower routine V̇O₂ (∼4 µl O₂ mg^-1 h^-1) than males (∼6 µl O₂ mg^-1 h^-1) at an average fly density of 28 flies·respirometer chamber^-1 However, V̇O₂ was inversely related to fly density in males, with V̇O₂ ranging from 4 to 11 µl O₂ mg^-1 h^-1 at a density of 10 and 40 flies·chamber^-1, respectively (r²=0.58, P<0.001). Female flies showed a similar but less pronounced effect, with a V̇O₂ of 4 and 7 µl O₂ mg^-1 h^-1 at a density of 10 and 40 flies·chamber^-1, respectively (r²=0.43, P<0.001). P_Crit (∼5.5 to 7.5 kPa) varied significantly with density in male (r²=0.50, P<0.01) but not female (r²=0.02, P>0.5) flies, with higher fly densities having a lower P_Crit An extensive survey of the literature on metabolism in fruit flies indicates that not all studies control for, or even report on, fly density and gender, both of which may affect metabolic measurements.

Keywords: Drosophila; Oxygen consumption; Respirometry techniques; Sex; Social interaction.

Fig. 1.

Wet and dry body mass in female and male D. melanogaster. Mean±s.e. are plotted, but standard errors are too small to be visible (see text). N=703 for females, 529 for males. Different lower case italic letters indicate significance differences between groups at the P<0.01 level (t-test).

Fig. 2.

Wet and dry mass-specific routine oxygen consumption (V̇O₂) in male and female D. melanogaster. Mean values±s.e. are presented. Also indicated are n values, where each value contributing to n is a separate trial comprising multiple flies in each respirometer. The average number of flies in the respirometer (density) for n runs, was 18±3 for males and 29±3 for females. Different lower case italic letters indicate significance differences between groups at the P<0.01 level (t-test).

Fig. 3.

Mass-specific routine V̇O₂ in normoxia as a function of density in male and female D. melanogaster. Density is shown on both a per respirometer and per ml of respirometer basis. Separate linear regressions for male (n=18) and female (n=25) flies are provided, along with the correlation coefficient and P value for each. Dashed lines represent the extrapolation of each relationship back to the value for a single fly. The slope of the two lines was significantly different (P<0.02, least squares method).

Fig. 4.

P_Crit determination in adult D. melanogaster. (A) A scatter plot of 11 P_Crit trials (211 females in total). (B) Representative routine V̇O₂ data derived from a single experimental trial of a respirometer containing 17 female flies. Also shown are the values for a respirometer blank. The intersection of the two linear regressions indicates the P_Crit value, identified on the X-axis by the vertical dashed arrow (see text for details of P_Crit calculation and statistics).

Fig. 5.

P_Crit as a function of respirometer fly density in male and female D. melanogaster. Density is shown on both a per respirometer and per ml of respirometer basis. Separate linear regressions for male (n=14) and female (n=25) flies are provided, along with the correlation coefficient and P value for each (least squares method). Dashed lines represent the extrapolation of each relationship back to the value for a single fly. The slope of the line for female flies was not significant (P>0.05), indicating that P_Crit in females as lines was unaffected by fly density.

Fig. 6.

Relationship between P_Crit and routine V̇O₂ in male and female D. melanogaster. N=17 trials for males and 25 trials for females (least squares method). Average fly density of all trials was 29±2 flies respirometer⁻¹.