Experimentally increased brood size accelerates actuarial senescence and increases subsequent reproductive effort in a wild bird population

The assumption that reproductive effort decreases somatic state, accelerating ageing, is central to our understanding of life-history variation. Maximal reproductive effort early in life is predicted to be maladaptive by accelerating ageing disproportionally, decreasing fitness. Optimality theory predicts that reproductive effort is restrained early in life to balance the fitness contribution of reproduction against the survival cost induced by the reproductive effort. When adaptive, the level of reproductive restraint is predicted to be inversely linked to the remaining life expectancy, potentially resulting in a terminal effort in the last period of reproduction. Experimental tests of the reproductive restraint hypothesis require manipulation of somatic state and subsequent investigation of reproductive effort and residual life span. To our knowledge the available evidence remains inconclusive, and hence reproductive restraint remains to be demonstrated. We modulated somatic state through a lifelong brood size manipulation in wild jackdaws and measured its consequences for age-dependent mortality and reproductive success. The assumption that lifelong increased brood size reduced somatic state was supported: Birds rearing enlarged broods showed subsequent increased rate of actuarial senescence, resulting in reduced residual life span. The treatment induced a reproductive response in later seasons: Egg volume and nestling survival were higher in subsequent seasons in the increased versus reduced broods' treatment group. We detected these increases in egg volume and nestling survival despite the expectation that in the absence of a change in reproductive effort, the reduced somatic state indicated by the increased mortality rate would result in lower reproductive output. This leads us to conclude that the higher reproductive success we observed was the result of higher reproductive effort. Our findings show that reproductive effort negatively covaries with remaining life expectancy, supporting optimality theory and confirming reproductive restraint as a key factor underpinning life-history variation

Elevational variation in body-temperature response to immune challenge in a lizard

Immunocompetence benefits animal fitness by combating pathogens, but also entails some costs. One of its main components is fever, which in ectotherms involves two main types of costs: energy expenditure and predation risk. Whenever those costs of fever outweigh its benefits, ectotherms are expected not to develop fever, or even to show hypothermia, reducing costs of thermoregulation and diverting the energy saved to other components of the immune system. Environmental thermal quality, and therefore the thermoregulation cost/benefit balance, varies geographically. Hence, we hypothesize that, in alpine habitats, immune-challenged ectotherms should show no thermal response, given that (1) hypothermia would be very costly, as the temporal window for reproduction is extremely small, and (2) fever would have a prohibitive cost, as heat acquisition is limited in such habitat. However, in temperate habitats, immune-challenged ectotherms might show a febrile response, due to lower cost/benefit balance as a consequence of a more suitable thermal environment. We tested this hypothesis in Psammodromus algirus lizards from Sierra Nevada (SE Spain), by testing body temperature preferred by alpine and non-alpine lizards, before and after activating their immune system with a typical innocuous pyrogen. Surprisingly, non-alpine lizards responded to immune challenge by decreasing preferential body-temperature, presumably allowing them to save energy and reduce exposure to predators. On the contrary, as predicted, immune-challenged alpine lizards maintained their body-temperature preferences. These results match with increased costs of no thermoregulation with elevation, due to the reduced window of time for reproduction in alpine environment.This work was funded by the Spanish Ministerio de Ciencia e Innovación [project CGL2009-13185]. FJZC [AP2009-3505] and SR [AP2009-1325] were supported by two pre-doctoral grants from the Ministerio de Ciencia e Innovación (FPU programme). FJZC was partially supported by a Ramón Areces Foundation postdoctoral fellowship. GMR was partially supported by a grant of the Ministerio de Ciencia e Innovación (Juan de la Cierva programme)

Costs and benefits of immune system activation on physiology, behavior and offspring phenotype from an immunoecological perspective

Pathogen challenges and host immune defenses can have substantial impact on life history patterns of animals. Biotic and abiotic factors may affect immunity in wild animals, influencing e.g., population dynamics and sexual selection. The overall aim of this thesis was to assess costs and benefits of immune system activation on physiology, behavior and offspring phenotype. The conducted research has been in two of the major branches within the field of immunoecology; (i) direct and indirect effects related to the costs induced by immune system activation and (ii) different aspects of maternal transfer of antibodies to offspring. We found that immune-challenged zebra finches (Taenopygia guttata) demonstrated some of the general sickness behaviors, such as reduction in appetite and activity. However, zebra finches showed a circadian pattern in their thermoregulatory response, manifested as fever at night and hypothermia at day. In addition, they reduced their energy consumption several days after the immune-challenge. Immune-challenged zebra finch mothers also increased investment in the current breeding event, in line with a ‘terminal investment’ strategy. When examining the effects of immune system activation on the energy budget on wild birds during winter, we found that immune-challenged great tits (Parus major) attenuated their energy saving nighttime hypothermia and immune-challenged blue tits (Cyanistes caeruleus) were more inclined to expose themselves to perceived predation risk in order to save energy by using nest boxes for nighttime roosting. When assessing maternal antibody transmission to offspring, we found that immune-challenged zebra finch mothers transferred antigen-specific antibodies to their offspring in relation to antibody concentration in her circulation by the time of egg laying. These maternal antibodies persisted in the offspring until at least 5 days of age. In addition, we demonstrated that mothers are able to transfer functional antigen-specific antibodies to their offspring five months after the mothers were exposed to the antigen. Collectively, this work shows how immune system activation can have significant effects on physiology, behavior and offspring phenotype, with important implications for avian life history evolution

Immune challenge induces terminal investment at an early breeding stage in female zebra finches

The "terminal investment" hypothesis proposes that individuals with low future survival prospects will gain from increasing investment in the current reproductive event even though it will reduce the chances of future reproduction even further. Such investments have previously been found to occur mainly during the late stages of the breeding event, that is, encompassing a short period of elevated parental care close to offspring independence. Our aim was to study if a simulated mild bacterial infection can induce a terminal investment already at egg laying (i.e., at an early breeding stage). Therefore, we challenged female zebra finches (Taeniopygia guttata) before egg laying with a tetanus-toxoid vaccine mimicking a bacterial infection. Immune-challenged females increased the total clutch mass by 20%, primarily through laying clutches that were 17% larger than control females. Although the immune-challenged females produced more eggs, they kept the same investment strategy in relation to egg laying order as did control females. Our study implies that female birds can use a nonpathogenic immune challenge as an indication of declining survival prospects, and consequently increase clutch size. These investment decisions by immune-challenged mothers are in line with "terminal investment" conducted at an early stage of breeding, challenging the traditional view that terminal investment should occur at late breeding stages

eggs

This file contains all individual eggs Female = Female identity Treatment = Injection with either phosphate buffered saline (PBS) or tetanus-toxoid vaccine Exp = Control females (1); tetanus-injected females (2) Body mass = Body mass (g) of the female Clutch size = Number of eggs in the clutch Egg day = Number of days after the production of the first egg (egg day = 1) that each egg in the clutch were produced. Egg order = The order in which the eggs were produced Rel egg order = The egg order divided by clutch size to adjust egg order for variation in clutch size. Yolk mass = The yolk mass of each individual egg Egg mass = The total mass of each individual egg Albumen mass = The albumen mass of each individual egg Yolk Proportion = The proportion of yolk in relation to egg mass of each individual egg Yolk prop. arcsin = Arcsine transformed yolk proportions of each individual egg Scaled index = Condition index of the femal

all birds

This file includes all the females that got two injections and was offered a nesting opportunity.ID = Identity of the bird Treatment = Injection with either phosphate buffered saline (PBS) or tetanus-toxoid vaccine Tarsus length = Tarsus length (mm) of the female Body mass = Body mass (g) of the female Scaled index = Condition index of the femal

Data from: Immune challenge induces terminal investment at an early breeding stage in female zebra finches

The ‘terminal investment’ hypothesis proposes that individuals with low future survival prospects will gain from increasing investment in the current reproductive event even though it will reduce the chances of future reproduction even further. Such investments have previously been found to occur mainly during the late stages of the breeding event, i.e., encompassing a short period of elevated parental care close to offspring independence. Our aim was to study if a simulated mild bacterial infection can induce a terminal investment already at egg laying (i.e., at an early breeding stage). Therefore, we challenged female zebra finches (Taeniopygia guttata) prior to egg laying with a tetanus-toxoid vaccine mimicking a bacterial infection. Immune-challenged females increased the total clutch mass by 20 %, primarily through laying clutches that were 17 % larger than control females. Although the immune-challenged females produced more eggs, they kept the same investment strategy in relation to egg laying order as did control females. Our study implies that female birds can use a non-pathogenic immune challenge as an indication of declining survival prospects, and consequently increase clutch size. These investment decisions by immune-challenged mothers are in line with ‘terminal investment’ conducted at an early stage of breeding, challenging the traditional view that terminal investment should occur at late breeding stages

exp birds

This file only includes those females that started to produce a clutch. ID = Identity of the bird Treatment = Injection with either phosphate buffered saline (PBS) or tetanus-toxoid vaccine Exp = Control females (1); tetanus-injected females (2) Body mass = Body mass (g) of the female Days to first egg = The time period between first presented with a nest box and nesting material and the production of the first egg by the females. Number of eggs = Clutch size Mean egg mass = Mean egg mass (g) of the eggs in each clutch Total egg mass = Total mass (g) of all eggs in a clutch Mean yolk mass = Mean yolk mass (g) of the eggs in each clutch Mean yolk proportion = Mean proportion of yolk in relation to egg mass in each clutch Arcsin mean yolk prop. = Arcsine transformed mean yolk proportion Diff body Mass = Initial body mass taken on the day of the second injection minus body mass after completion of egg laying. Days btw bm measurements = Number of days between the two body mass measurements Scaled index = Condition index of the female Age = Age of the female; 1 = One year old; 2 = Two years old Tetanus = Tetanus antibody concentrations (mODmin-1) Log (tet) = The logarithm of tetanus antibody concentration

Effects of prenatal testosterone exposure on antioxidant status and bill color in adult zebra finches.

Permanent offspring modification through maternal hormone transfer is thought to be a tool for mothers to influence life-history trajectories of individual offspring. In birds, yolk hormones influence numerous aspects of the offspring's physiology, including antioxidant status, an important physiological measure that is linked to growth, reproductive effort, and survival. While it is evident that yolk hormones can affect antioxidant status of nestlings, it is not known whether their effect extends beyond the nestling stage. In this study, we use the zebra finch (Taeniopygia guttata) to test experimentally whether exposure to elevated yolk testosterone (T) levels can result in long-term effects on antioxidant status and traits likely to be associated with this measure. Our data show a significant but sex-specific effect with respect to a period from fledging to the age of 7 mo; T males had higher antioxidant status than control males, whereas antioxidant levels did not differ among females and were intermediate compared with the two male groups. Bill color, a trait associated with carotenoids (a specific group of antioxidants) and known to be under the control of circulating levels of T, was not affected by our yolk T manipulation. Bill color (alone or in covariation with egg treatment or sex) did not predict immune responsiveness or antioxidant status. Moreover, there was only weak evidence that antioxidant status predicted the strength of different immune responses. Antioxidant status (in covariation with egg treatment and sex) predicted levels of circulating total antibody levels but did not predict the strength of cell-mediated and humoral immune responses. Our results suggest that yolk T affects antioxidant status independently of these other traits