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

Criscuolo, François; Monaghan, Pat; Nasir, Lubna; Metcalfe, Neil B.

doi:10.1098/rspb.2008.0148

Cited by 174 publications

(154 citation statements)

References 46 publications

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“…2006; Criscuolo et al. 2008), which are essential components of fitness, is predicted to produce ROS and also draws limited resources away from AOX defense and repair systems. This is hypothesized to induce OS and, ultimately, lead to an accumulation of damage, reduced maintenance function, and organismal senescence (Harman 1956; Beckman and Ames 1998; Isaksson et al.…”

Section: Introductionmentioning

confidence: 99%

Plasma markers of oxidative stress are uncorrelated in a wild mammal

Christensen

Selman

Blount

et al. 2015

Ecology and Evolution

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Oxidative stress, which results from an imbalance between the production of potentially damaging reactive oxygen species versus antioxidant defenses and repair mechanisms, has been proposed as an important mediator of life‐history trade‐offs. A plethora of biomarkers associated with oxidative stress exist, but few ecological studies have examined the relationships among different markers in organisms experiencing natural conditions or tested whether those relationships are stable across different environments and demographic groups. It is therefore not clear to what extent studies of different markers can be compared, or whether studies that focus on a single marker can draw general conclusions regarding oxidative stress. We measured widely used markers of oxidative damage (protein carbonyls and malondialdehyde) and antioxidant defense (superoxide dismutase and total antioxidant capacity) from 706 plasma samples collected over a 4‐year period in a wild population of Soay sheep on St Kilda. We quantified the correlation structure among these four markers across the entire sample set and also within separate years, age groups (lambs and adults), and sexes. We found some moderately strong correlations between some pairs of markers when data from all 4 years were pooled. However, these correlations were caused by considerable among‐year variation in mean marker values; correlation coefficients were small and not significantly different from zero after accounting for among‐year variation. Furthermore, within each year, age, and sex subgroup, the pairwise correlation coefficients among the four markers were weak, nonsignificant, and distributed around zero. In addition, principal component analysis confirmed that the four markers represented four independent axes of variation. Our results suggest that plasma markers of oxidative stress may vary dramatically among years, presumably due to environmental conditions, and that this variation can induce population‐level correlations among markers even in the absence of any correlations within contemporaneous subgroups. The absence of any consistent correlations within years or demographic subgroups implies that care must be taken when generalizing from observed relationships with oxidative stress markers, as each marker may reflect different and potentially uncoupled biochemical processes.

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Section: Introductionmentioning

confidence: 99%

Plasma markers of oxidative stress are uncorrelated in a wild mammal

Christensen

Selman

Blount

et al. 2015

Ecology and Evolution

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“…In most cases these effects are related to the feeding conditions of nestlings; however, the exact physiological mechanisms (other than changes in body size) whereby early nutrition affects adults are usually more difficult to identify (Monaghan, 2008). Although some studies have found that nestling nutrition may exert long-lasting effects on physiological traits in adulthood (Blount et al, 2003;Verhulst et al, 2006;Criscuolo et al, 2008), others have revealed that after fledging birds can fully compensate for the negative effect(s) of early nutrition on such important parameters as immune function (Birkhead et al, 1999) or stress response (Lendvai et al, 2009).…”

Section: Introductionmentioning

confidence: 99%

Fully reversible phenotypic plasticity of digestive physiology in young house sparrows: lack of long-term effect of early diet composition

Brzęk

Kohl

Caviedes‐Vidal

et al. 2011

Journal of Experimental Biology

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SUMMARYFeeding conditions during the nestling period may significantly affect whole-life fitness in altricial birds but little is known about the physiological mechanisms responsible for these effects. Permanent changes (irreversible developmental plasticity) in digestive physiology caused by the neonatal diet may form such a mechanism. We previously showed that the lack of starch in the diet of house sparrow (Passer domesticus) nestlings between 3 and 12days post-hatching significantly decreased the activity of intestinal maltase, an enzyme essential for starch digestion. To check whether diet-induced variation in maltase activity in young house sparrows is reversible, we raised them under laboratory conditions from 3 until 30days of age on diets with either 0% starch or 25% starch, with some individuals experiencing a switch in their assigned diet at 12days of age. We found evidence for the presence of an internal, presumably genetic, program for changes in the activity of maltase and sucrase, which was, however, significantly affected by diet composition (i.e. environmental factor). Digestive enzyme activity in 30day old birds was not influenced by diet composition prior to day12 but instead depended only on diet that was fed between days 12 and 30. We conclude that plasticity in the activity of intestinal disaccharidases in house sparrow nestlings represents completely reversible phenotypic flexibility that can help young sparrows to cope with unpredictable variation in food composition during ontogeny without long-term effects on their digestive system. However, comparison with other species suggests that the magnitude of digestive flexibility in young passerines may be evolutionarily matched to species-specific variation in feeding conditions.

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“…Factors associated with the rearing environment, such as maternal investment, can have subsequent effects on an offspring's adult physiology and reproductive success (Machin and Page, 1973;Mousseau and Fox, 1998;Burness et al, 2000;Criscuolo et al, 2008). Sexual signalling is an important contributor to lifetime reproductive success, signalling information about an individual's health and status to competitors and potential mates (Hurst, 1990;Rich and Hurst, 1998;Maynard Smith and Harper, 2003;Malone et al, 2005).…”

Section: Introductionmentioning

confidence: 99%

Experimental evidence that litter size imposes an oxidative challenge to offspring

Gibson

Garratt

Brooks

2015

Journal of Experimental Biology

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The post-natal environment in which young develop can substantially impact development, adult phenotype and fitness. In wild mice, competition among litter-mates affects development rate and adult behaviour. We manipulated post-natal litter size in a cross-fostering design to investigate the effects of enlarged and reduced litter sizes on sexual signalling, oxidative stress and the links between them. Oxidative stress causes somatic damage that can limit reproductive success and lifespan, and is predicted to mediate investment in life-history traits, including sexual signals. We predicted that litter enlargement would cause an increase in potential oxidative stress, inhibit growth and reduce sexual signalling in male mice. Males reared in enlarged litters were smaller at weaning and, despite rapid growth immediately after weaning, remained smaller at 10 weeks of age than those reared in smaller litters. Females from enlarged litters were consistently smaller throughout post-weaning development and showed no increase in growth rate compared with females from reduced litters. In enlarged litters, protein thiol concentration was lower at weaning in the liver and kidneys, with this trend continuing at 10 weeks of age in the kidneys only. Aconitase enzyme activity was also lower in mice from enlarged litters at weaning and 10 weeks of age in the kidneys. Male mice from enlarged litters scent marked more frequently and had larger preputial glands than those from reduced litters, indicating greater sexual signalling investment irrespective of this increased oxidative challenge. The results of this study are the first to reveal oxidative costs of developmental stress in small mammals.

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

Cited by 174 publications

References 46 publications

Plasma markers of oxidative stress are uncorrelated in a wild mammal

Plasma markers of oxidative stress are uncorrelated in a wild mammal

Fully reversible phenotypic plasticity of digestive physiology in young house sparrows: lack of long-term effect of early diet composition

Experimental evidence that litter size imposes an oxidative challenge to offspring

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