Simon Verhulst

Ecological immunology : Costly parasite defences and trade-offs in evolutionary ecology

In the face of continuous threats from parasites, hosts have evolved an elaborate series of preventative and controlling measures - the immune system - in order to reduce the fitness costs of parasitism. However, these measures do have associated costs. Viewing an individuals immune response to parasites as being subject to optimization in the face of other demands offers potential insights into mechanisms of life history trade-offs, sexual selection, parasite-mediated selection and population dynamics. We discuss some recent results that have been obtained by practitioners of this approach in natural and semi-natural populations, and suggest some ways in which this field may progress in the near future.

Age-Dependent Traits: A New Statistical Model to Separate Within- and Between-Individual Effects

Evolutionary questions regarding aging address patterns of within‐individual change in traits during a lifetime. However, most studies report associations between age and, for example, reproduction based on cross‐sectional comparisons, which may be confounded with progressive changes in phenotypic population composition. Unbiased estimation of patterns of age‐dependent reproduction (or other traits) requires disentanglement of within‐individual change (improvement, senescence) and between‐individual change (selective appearance and disappearance). We introduce a new statistical model that allows patterns of variance and covariance to differ between levels of aggregation. Our approach is simpler than alternative methods and can quantify the relative contributions of within‐ and between‐individual changes in one framework. We illustrate our model using data on a long‐lived bird species, the oystercatcher (Haematopus ostralegus). We show that for different reproductive traits (timing of breeding and egg size), either within‐individual improvement or selective appearance can result in a positive association between age and reproductive traits at the population level. Potential applications of our methodology are manifold because within‐ and between‐individual patterns are likely to differ in many biological situations.

The timing of birds' breeding seasons: a review of experiments that manipulated timing of breeding

Reproductive success usually declines in the course of the season, which may be a direct effect of breeding time, an effect of quality (individuals with high phenotypic or environmental quality breeding early), or a combination of the two. Being able to distinguish between these possibilities is crucial when trying to understand individual variation in annual routines, for instance when to breed, moult and migrate. We review experiments with free-living birds performed to distinguish between the ‘timing’ and ‘quality’ hypothesis. ‘Clean’ manipulation of breeding time seems impossible, and we therefore discuss strong and weak points of different manipulation techniques. We find that the qualitative results were independent of manipulation technique (inducing replacement clutches versus cross-fostering early and late clutches). Given that the two techniques differ strongly in demands made on the birds, this suggests that potential experimental biases are limited. Overall, the evidence indicated that date and quality are both important, depending on fitness component and species, although evidence for the date hypothesis was found more frequently. We expected both effects to be prevalent, since only if date per se is important, does an incentive exist for high-quality birds to breed early. We discuss mechanisms mediating the seasonal decline in reproductive success, and distinguish between effects of absolute date and relative date, for instance timing relative to seasonal environmental fluctuations or conspecifics. The latter is important at least in some cases, suggesting that the optimal breeding time may be frequency dependent, but this has been little studied. A recurring pattern among cross-fostering studies was that delay experiments provided evidence for the quality hypothesis, while advance experiments provided evidence for the date hypothesis. This indicates that late pairs are constrained from producing a clutch earlier in the season, presumably by the fitness costs this would entail. This provides us with a paradox: evidence for the date hypothesis leads us to conclude that quality is important for the ability to breed early.

Birds sacrifice oxidative protection for reproduction.

Oxidative metabolism has reactive oxygen species (ROS) as unavoidable by–products, and the damage ROS inflicts on DNA, proteins and lipids is considered to be a major agent of senescence. Increasing reproductive effort accelerates senescence, but whether reproductive effort is increased at the expense of protection against oxidative damage has not yet been tested. We manipulated reproductive effort in zebra finches through brood size manipulation and measured the activity of two major antioxidant enzymes (superoxide dismutase (SOD) and glutathione peroxidase (GPx)) in the pectoral muscle after 19–20 days of brood rearing. Oxidative stress is reflected by the balance between oxidative protection and ROS exposure, and we therefore scaled SOD and GPx activity to daily energy expenditure (DEE) as an index of ROS production. SOD and GPx activity decreased with increasing brood size by 28% and 24%, respectively. This effect was identical in the two sexes, but arose in different ways: males did not change their DEE, but had lower absolute enzyme activity, and females increased their DEE, but did not change absolute enzyme activity. This result suggests that senescence acceleration by increased reproductive effort is at least in part mediated by oxidative stress.

Experimental evidence for a causal relationship between timing and success of reproduction in the great tit Parus m. major

SUMMARY (1) We investigated experimentally whether timing of reproduction is causally involved in the seasonal decline in reproductive success in the great tit Parus m. major L. This is important because of its implications for the optimization of reproductive decisions of the individual bird. (2) Timing of breeding was manipulated by inducing repeat clutches through removal of the first clutch. The experiment was performed in 1987 in two forests (W and 0) and followed up the year after. It was assumed that parental quality was unaffected by the ex-periment. Reproductive success of the experimental and undisturbed control clutches were compared. For forest 0, reproductive success of the experimental clutches was also compared with the expected reproductive success of first clutches laid at the same time. (3) Clutch size, fledging success and nestling weight in experimental clutches were reduced as compared with controls in forest W but not in forest 0. We conclude that late breeding causes reduced pre-fledging reproductive success in forest W but not in forest 0. (4) Recruitment of fledged young in the breeding population was strongly reduced by the experiment. We conclude that late breeding caused reduced post-fledging reproductive success in both forests. (5) Survival of females was reduced by the experiment in forest 0 relative to controls and this corresponded with the natural seasonal trend. Survival of females in W and of males in both forests was unaffected. In experimental females, clutch size in the next breeding season was reduced by 16 eggs compared with controls. The clutch size of the males was unaffected, as was the following years laying date for both sexes. We conclude that future reproductive success of females, but not of males, is also related to the timing of current reproduction. (6) Possible mechanisms underlying the relationship between date and reproductive success are discussed. It is suggested that differences in pre-fledging reproductive success induced by the experiment are related to food availability. Differences in post-fledging reproductive success are probably caused by competition between early and late young.

Telomere shortening and survival in free-living corvids

Evidence accumulates that telomere shortening reflects lifestyle and predicts remaining lifespan, but little is known of telomere dynamics and their relation to survival under natural conditions. We present longitudinal telomere data in free-living jackdaws (Corvus monedula) and test hypotheses on telomere shortening and survival. Telomeres in erythrocytes were measured using pulsed-field gel electrophoresis. Telomere shortening rates within individuals were twice as high as the population level slope, demonstrating that individuals with short telomeres are less likely to survive. Further analysis showed that shortening rate in particular predicted survival, because telomere shortening was much accelerated during a birds last year in the colony. Telomere shortening was also faster early in life, even after growth was completed. It was previously shown that the lengths of the shortest telomeres best predict cellular senescence, suggesting that shorter telomeres should be better protected. We test the latter hypothesis and show that, within individuals, long telomeres shorten faster than short telomeres in adults and nestlings, a result not previously shown in vivo. Moreover, survival selection in adults was most conspicuous on relatively long telomeres. In conclusion, our longitudinal data indicate that the shortening rate of long telomeres may be a measure of ‘life stress’ and hence holds promise as a biomarker of remaining lifespan.

Intraspecific Allometry of Basal Metabolic Rate: Relations with Body Size, Temperature, Composition, and Circadian Phase in the Kestrel, Falco tinnunculus

The relationship between body size and basal metabolic rate (BMR) in homeo therms has been treated in the literature primarily by comparison between species of mammals or birds. This paper focuses on the intraindividual changes in BMR when body mass (W) varies with different maintenance regimens. BMR varied in individual kestrels in proportion to W1.67, which is considerably steeper than the mass exponents for homomorphic change (0.667; Heusner, 1984) for interspecific comparison among all birds (0.677) or raptors (0.678), for interindividual comparison of kestrels on ad libitum maintenance regimens (0.786), and for mass proportionality (1.00). The circadian range of telemetered core temperature also varied more strongly with intraindividual than with interspecific (Aschoff, 1981a) variation in mass. This was due to reduced nocturnal core temperature at low-maintenance regimens, which was, however, insufficient to account for the excessive reduction in BMR. Carcass analysis of eight birds sacrificed revealed a disproportionate reduction in heart and kidney lean mass at low-maintenance regimens. We surmise that variation in BMR primarily reflects variation in these metabolically highly active tissues. This may account for positive correlations found between heart, kidney, and BMR residuals relative to interspecific allometric prediction, and between α and p residuals, as expected on the basis of the constant excess of BMR during α above BMR during p (Aschoff & Pohl, 1970a).

Timing of reproduction and fledging success in the Coot Fulica atra : evidence for a causal relationship

1. We investigated the relationship between hatching date and fledging success in the European coot (Fulica atra). 2. The production of fledglings per brood increased in the first half of the season and decreased in the second half, independent of clutch size or egg size. We tested experimentally whether this convex seasonal pattern is causally related to date. 3. The timing of parental care was manipulated by exchanging complete first clutches that differed in stage of incubation. Our experiments tested whether the natural variation in fledging success was due to (i) factors related to date (date hypothesis), (ii) factors related to parental and/or territory quality (parental quality hypothesis), or to a combination of both factors. 4. In the first half of the season, an experimental advance of the timing of parental care reduced fledging success, while an experimental delay raised it. In the second half of the season the opposite was found. Fledgling production by experimental pairs did not differ systematically from that of control pairs raising young at the same time. 5. Thus, the results were consistent only with the date hypothesis, and we conclude that timing of breeding and fledging success are causally related in the coot. 6. Independent of date, age of male parents was positively correlated with fledging success, suggesting that aspects of parental quality play an additional role.

Great tits growing old: selective disappearance and the partitioning of senescence to stages within the breeding cycle

Deterioration of reproductive traits with age is observed in an increasing number of species. Although such deterioration is often attributed to reproductive senescence, a within-individual decline in reproductive success with age, few studies on wild animals have focused on direct fitness measures while accounting for selective disappearance and terminal effects, and to our knowledge none have determined how senescence effects arise from underlying reproductive traits. We show for female great tits that such an approach helps understanding of the onset, impact and architecture of senescence. Cross-sectional analysis of 49 years of breeding data shows annual recruit production to decline from 3.5 years of age, this decline affecting 9 per cent of females each year. Longitudinal analyses, however, show that selective disappearance of poor-quality breeders partly masks senescence, which in fact starts at 2.8 years and affects 21 per cent of females each year. There is no evidence for abrupt terminal effects. Analyses of underlying traits show no deterioration in clutch size, but significant declines in brood size and fledgling number. Furthermore, these traits contribute −9, 12 and 39 per cent to the senescent decline in recruit production, respectively. Besides providing detailed knowledge of the patterns and architecture of senescence in a natural population, these results illustrate the importance of modelling individual variation, and facilitate study of the underlying mechanisms of senescence.

Delayed behavioral effects of postnatal exposure to corticosterone in the zebra finch (Taeniopygia guttata)

Early developmental conditions can significantly influence the growth and survival of many animal species. We studied the consequences of exposure to corticosterone (CORT), a stress hormone, during the nestling stage on two behavioral traits (neophobia, social dominance) measured when the birds had reached independence. Nestling zebra finches (Taeniopygia guttata) were exposed twice daily to exogenous CORT via oral administration for a 12-day period up until fledging. Experimental CORT administration depressed nestling growth rates, confirming results previously obtained in this species. Our data on neophobic behavior revealed a significant interaction between sex and treatment, with CORT-dosed males showing reduced latencies to approach a novel object, while there was little effect of corticosterone treatment on female neophobia. There was no significant effect of age (30 or 50 days), however, there was a non-significant trend towards an interaction between treatment and age, with neophobia increasing with age in the CORT-dosed birds, but decreasing in controls. At 50 days of age previous exposure to corticosterone resulted in reduced success in competitions for a non-food-based resource (a perch) in both sexes. There were no effects of brood size on any behavioral traits measured here, but this may be due to the small range in brood size used. Our results show that elevated levels of stress hormones during postnatal development can have significant effects on important behavioral traits, i.e., neophobia and dominance. Moreover, they confirm the importance of rearing conditions in shaping adult phenotypes.