Pat Monaghan

Compensation for a bad start: grow now, pay later?

Nutritional conditions during key periods of development, when the architecture and modus operandi of the body become established, are of profound importance in determining the subsequent life-history trajectory of an organism. If developing individuals experience a period of nutritional deficit, they can subsequently show accelerated growth should conditions improve, apparently compensating for the initial setback. However, recent research suggests that, although compensatory growth can bring quick benefits, it is also associated with a surprising variety of costs that are often not evident until much later in adult life. Clearly, the nature of these costs, the timescale over which they are incurred and the mechanisms underlying them will play a crucial role in determining compensatory strategies. Nonetheless, such effects remain poorly understood and largely neglected by ecologists and evolutionary biologists.

Oxidative stress as a mediator of life history trade-offs: mechanisms, measurements and interpretation

The concept of trade-offs is central to our understanding of life-history evolution. The underlying mechanisms, however, have been little studied. Oxidative stress results from a mismatch between the production of damaging reactive oxygen species (ROS) and the organisms capacity to mitigate their damaging effects. Managing oxidative stress is likely to be a major determinant of life histories, as virtually all activities generate ROS. There is a recent burgeoning of interest in how oxidative stress is related to different components of animal performance. The emphasis to date has been on immediate or short-term effects, but there is an increasing realization that oxidative stress will influence life histories over longer time scales. The concept of oxidative stress is currently used somewhat loosely by many ecologists, and the erroneous assumption often made that dietary antioxidants are necessarily the major line of defence against ROS-induced damage. We summarize current knowledge on how oxidative stress occurs and the different methods for measuring it, and highlight where ecologists can be too simplistic in their approach. We critically review the potential role of oxidative stress in mediating life-history trade-offs, and present a framework for formulating appropriate hypotheses and guiding experimental design. We indicate throughout potentially fruitful areas for further research.

Early growth conditions, phenotypic development and environmental change

Phenotypic development is the result of a complex interplay involving the organisms own genetic make-up and the environment it experiences during development. The latter encompasses not just the current environment, but also indirect, and sometimes lagged, components that result from environmental effects on its parents that are transmitted to their developing offspring in various ways and at various stages. These environmental effects can simply constrain development, for example, where poor maternal condition gives rise to poorly provisioned, low-quality offspring. However, it is also possible that environmental circumstances during development shape the offspring phenotype in such a way as to better prepare it for the environmental conditions it is most likely to encounter during its life. Studying the extent to which direct and indirect developmental responses to environmental effects are adaptive requires clear elucidation of hypotheses and careful experimental manipulations. In this paper, I outline how the different paradigms applied in this field relate to each other, the main predictions that they produce and the kinds of experimental data needed to distinguish among competing hypotheses. I focus on birds in particular, but the theories discussed are not taxon specific. Environmental influences on phenotypic development are likely to be mediated, in part at least, by endocrine systems. I examine evidence from mechanistic and functional avian studies and highlight the general areas where we lack key information.

Why don't birds lay more eggs?

Fifty years ago David Lack put forward a key hypothesis in life-history theory: that avian clutch is ultimately determined by the number of young that parents can provide with food. Since then, a plethora of brood manipulations has shown that birds can rear more young than the number of eggs they lay, and prompted a search for negative effects of increased effort on future reproduction. However, recent studies have shown that the demands of laying and incubating eggs generally omitted from experiments, could affect parental fitness. Lacks hypothesis, and the tests of its validity, need to be extended to encompass the full demands of producing and rearing the brood.

Telomere length in early life predicts lifespan

The attrition of telomeres, the ends of eukaryote chromosomes, is thought to play an important role in cell deterioration with advancing age. The observed variation in telomere length among individuals of the same age is therefore thought to be related to variation in potential longevity. Studies of this relationship are hampered by the time scale over which individuals need to be followed, particularly in long-lived species where lifespan variation is greatest. So far, data are based either on simple comparisons of telomere length among different age classes or on individuals whose telomere length is measured at most twice and whose subsequent survival is monitored for only a short proportion of the typical lifespan. Both approaches are subject to bias. Key studies, in which telomere length is tracked from early in life, and actual lifespan recorded, have been lacking. We measured telomere length in zebra finches (n = 99) from the nestling stage and at various points thereafter, and recorded their natural lifespan (which varied from less than 1 to almost 9 y). We found telomere length at 25 d to be a very strong predictor of realized lifespan (P < 0.001); those individuals living longest had relatively long telomeres at all points at which they were measured. Reproduction increased adult telomere loss, but this effect appeared transient and did not influence survival. Our results provide the strongest evidence available of the relationship between telomere length and lifespan and emphasize the importance of understanding factors that determine early life telomere length.

Neonatal nutrition, adult antioxidant defences and sexual attractiveness in the zebra finch

Early nutrition has recently been shown to have pervasive, downstream effects on adult life–history parameters including lifespan, but the underlying mechanisms remain poorly understood. Damage to biomolecules caused by oxidants, such as free radicals generated during metabolic processes, is widely recognized as a key contributor to somatic degeneration and the rate of ageing. Lipophilic antioxidants (carotenoids, vitamins A and E) are an important component of vertebrate defences against such damage. By using an avian model, we show here that independent of later nutrition, individuals experiencing a short period of low–quality nutrition during the nestling period had a twofold reduction in plasma levels of these antioxidants at adulthood. We found no effects on adult external morphology or sexual attractiveness: in mate–choice trials females did not discriminate between adult males that had received standard– or lower–quality diet as neonates. Our results suggest low–quality neonatal nutrition resulted in a long–term impairment in the capacity to assimilate dietary antioxidants, thereby setting up a need to trade off the requirement for antioxidant activity against the need to maintain morphological development and sexual attractiveness. Such state–dependent trade–offs could underpin the link between early nutrition and senescence.

Telomere dynamics rather than age predict life expectancy in the wild

Despite accumulating evidence from in vitro studies that cellular senescence is linked to telomere dynamics, how this relates to whole-organism senescence and longevity is poorly understood and controversial. Using data on telomere length in red blood cells and long-term survival from wild Alpine swifts of a range of ages, we report that the telomere length and the rate of telomere loss are predictive of life expectancy, and that slow erosion of relatively long telomeres is associated with the highest survival probabilities. Importantly, because telomere dynamics, rather than chronological age, predict life expectancy, our study provides good evidence for a mechanistic link between telomere erosion and reduced organism longevity under natural conditions, chronological age itself possibly not becoming a significant predictor until very old ages beyond those in our sample.

Nutritional constraints on egg formation in the lesser black-backed gull : an experimental study

The use of supplementary feeding experiments to investigate the relationship between food supply and clutch and egg size in birds has yielded disparate results, some authors showing an advancement in laying date and/or increased clutch size in response to additional food whereas other studies have found no effect. Here we investigate the nutritional requirements of egg formation in lesser blackbacked gulls Larus fuscus L., through a series of feeding experiments providing additional food of different quality

Fecundity and survival in relation to resistance to oxidative stress in a free-living bird.

Major life history traits, such as fecundity and survival, have been consistently demonstrated to covary positively in nature, some individuals having more resources than others to allocate to all aspects of their life history. Yet, little is known about which resources (or state variables) may account for such covariation. Reactive oxygen species (ROS) are natural by-products of metabolism and, when ROS production exceeds antioxidant defenses, organisms are exposed to oxidative stress that can have deleterious effects on their fecundity and survival. Using a wild, long-lived bird, the Alpine Swift (Apus melba), we examined whether individual red cell resistance to oxidative stress covaried with fecundity and survival. We found that males that survived to the next breeding season tended to be more resistant to oxidative stress, and females with higher resistance to oxidative stress laid larger clutches. Furthermore, the eggs of females with low resistance to oxidative stress were less likely to hatch than those of females with high resistance to oxidative stress. By swapping entire clutches at clutch completion, we then demonstrated that hatching failure was related to the production of low-quality eggs by females with low resistance to oxidative stress, rather than to inadequate parental care during incubation. Although male and female resistance to oxidative stress covaried with age, the relationships among oxidative stress, survival, and fecundity occurred independently of chronological age. Overall, our study suggests that oxidative stress may play a significant role in shaping fecundity and survival in the wild. It further suggests that the nature of the covariation between resistance to oxidative stress and life history traits is sex specific, high resistance to oxidative stress covarying primarily with fecundity in females and with survival in males.

Resource allocation between reproductive phases: the importance of thermal conditions in determining the cost of incubation

Changes in the resources allocated to particular stages of reproduction are expected to influence allocation to, and performance in, subsequent reproductive stages. Experimental manipulation of individual investment patterns provides important evidence that such physiological trade‐offs occur, and can highlight the key environmental variables that influence reproductive costs. By temporarily altering the thermal properties of starling nests, we reduced the energetic demand of first‐clutch incubation, and examined the effect of this manipulation on performance during the same and the subsequent reproductive attempts. Compared with controls, starlings investing less in incubation were more successful in fledging young, and were more likely to hatch all their eggs if a subsequent reproductive attempt was made. Our results show that incubation demands can limit reproductive success, and that resources saved during incubation can be reallocated to later stages of the same reproductive attempt and to future reproductive attempts. This study also shows that small changes in thermal environment can affect breeding success by altering the energetic demands imposed on incubating parents, independently of the effect of temperature on other environmental variables such as food supply.