The physiological costs of reproduction in small mammals

Abstract

Life-history trade-offs between components of fitness arise because reproduction entails both gains and costs. Costs of reproduction can be divided into ecological and physiological costs. The latter have been rarely studied yet are probably a dominant component of the effect. A deeper understanding of life-history evolution will only come about once these physiological costs are better understood. Physiological costs may be direct or indirect. Direct costs include the energy and nutrient demands of the reproductive event, and the morphological changes that are necessary to facilitate achieving these demands. Indirect costs may be optional 'compensatory costs' whereby the animal chooses to reduce investment in some other aspect of its physiology to maximize the input of resource to reproduction. Such costs may be distinguished from consequential costs that are an inescapable consequence of the reproductive event. In small mammals, the direct costs of reproduction involve increased energy, protein and calcium demands during pregnancy, but most particularly during lactation. Organ remodelling is necessary to achieve the high demands of lactation and involves growth of the alimentary tract and associated organs such as the liver and pancreas. Compensatory indirect costs include reductions in thermogenesis, immune function and physical activity. Obligatory consequential costs include hyperthermia, bone loss, disruption of sleep patterns and oxidative stress. This is unlikely to be a complete list. Our knowledge of these physiological costs is currently at best described as rudimentary. For some, we do not even know whether they are compensatory or obligatory. For almost all of them, we have no idea of exact mechanisms or how these costs translate into fitness trade-offs.

Figure 1

(a) Food intake each day throughout pre-breeding, pregnancy and lactation phases for MF1 mice. Data averaged across 71 litters. (b) Daily food intake averaged over the last days of lactation (10–18) plotted against litter size in MF1 mice. (c) Pup mass in relation to litter size in MF1 mice. (d) Histogram showing the frequency at birth of different litter sizes across 71 litters of MF1 mice.

Figure 2

(a) Peak energy intake of female small rodents, when not breeding (black), pregnant (red) and lactating (green). There was no significant elevation in intake during pregnancy, but intake during lactation was significantly elevated compared with both non-breeders and pregnant individuals. (b) Residual energy intake in lactation was significantly associated with litter size. Data from small rodents are given in table 1.

Figure 3

(a) Food intake at peak lactation (grams over 3 days) in relation to litter size in Peromyscus leucopus (drawn from tabulated data in Millar 1978). (b) Energy intake during lactation (kJ d⁻¹) in relation to litter size in Sigmodon hispidus (drawn from tabulated data in Rogowitz 1998).

Figure 4

Mean mass at weaning of male (grey) and female (white) pups of (a) rats and (b) mice when fed on diets of varying protein content (from 16.3% to 9.4% protein). Drawn from data in Goettsch (1960).

Figure 5

(a) Food intake and (b) wheel-running activity of rats during pregnancy and lactation. Days are expressed relative to the day of parturition (day =0) also indicated by the dotted line. Data are split between those raising large (n>6; open squares) and those raising small (n<6; filled squares) litters. Note how food intake in the larger litters increases dramatically a few days before weaning probably due to intake by the offspring (plots from data presented in tables 2 and 3 of Slonaker 1924).

Figure 6

Body temperatures of a single female MF1 mouse measured at 1-minute intervals using an implanted body temperature transmitter (e-mitter Minimitter Inc) for 7 days prior to breeding and for 7 days at peak lactation. Data are screened to include only times when the animals are at rest, and then averaged over 30-minute periods within each day. The error bars refer to the s.d. for day-to-day variability (n=7 for each data set). During lactation, the body temperature is consistently elevated approximately 1.5°C higher than that prior to breeding during the light phase and much of the dark phase. Dark bar indicates period when lights out (J. R. Speakman, K. Drerrer, F. J. Munro & C. T. Troup 2005, unpublished data).