Early nutrition and phenotypic development: 'catch-up' growth leads to elevated metabolic rate in adulthood

Abstract

Resting metabolic rate (RMR) is responsible for up to 50% of total energy expenditure, and so should be under strong selection pressure, yet it shows extensive intraspecific variation and a low heritability. Environmental conditions during growth are thought to have long-term effects through 'metabolic programming'. Here we investigate whether nutritional conditions early in life can alter RMR in adulthood, and whether this is due to growth acceleration or the change in diet quality that prompts it. We manipulated dietary protein levels during the main growth period of zebra finches (Taeniopygia guttata) such that an episode of poor nutrition occurred with and without growth acceleration. This produced different growth trajectories but a similar adult body mass. Only the diet that induced growth acceleration resulted in a significant (19%) elevation of RMR at adulthood, despite all the birds having been on the same diet after the first month. This is the first study to show that dietary-induced differences in growth trajectories can have a long-term effect on adult metabolic rate. It suggests that modification of metabolic efficiency may be one of the mechanisms mediating the observed long-term costs of accelerated growth, and indicates links between early nutrition and the metabolic syndrome.

Figure 1

Body mass gain (g d⁻¹) of zebra finch chicks reared (a) initially on a low (L)- or high (H)-quality diet during the first 15 days, (b) then re-allocated to H or L diets until the age of 30 days (HH, high throughout; HL, high for 15 days then low, etc) and (c) thereafter put on the same diet and followed until the age of 200 days. Asterisks indicate significant diet treatment differences (^*p<0.05; ^**p<0.01; ^***p<0.001, see table 1 and text for further details and statistics).

Figure 2

Resting metabolic rate (W g⁻¹) of zebra finches in relation to early diet (see figure 1 and text for description of diets). Energy consumption is shown per g of body mass for illustrative purposes, but all the analyses were based on consumption per bird, with body mass included as a covariate. The measurements of metabolic rate were made when the birds were (a–c) 15, 30 and 200 days old before any diet switch (H, high-quality diet; L, low-quality diet; ^*p<0.05; ^**p<0.01; ^***p<0.001, see table 2 for statistics). (filled circle, HH; open circle, HL; filled triangle, LH; open triangle, LL; filled square, H; open square, L).