Compensatory Growth Is Accompanied by Changes in Insulin-Like Growth Factor 1 but Not Markers of Cellular Aging in a Long-Lived Seabird.

AbstractDeveloping organisms often plastically modify growth in response to environmental circumstances, which may be adaptive but is expected to entail long-term costs. However, the mechanisms that mediate these growth adjustments and any associated costs are less well understood. In vertebrates, one mechanism that may be important in this context is the highly conserved signaling factor insulin-like growth factor 1 (IGF-1), which is frequently positively related to postnatal growth and negatively related to longevity. To test this idea, we exposed captive Franklin's gulls (Leucophaeus pipixcan) to a physiologically relevant nutritional stressor by restricting food availability during postnatal development and examined the effects on growth, IGF-1, and two potential biomarkers of cellular and organismal aging (oxidative stress and telomeres). During food restriction, experimental chicks gained body mass more slowly and had lower IGF-1 levels than controls. Following food restriction, experimental chicks underwent compensatory growth, which was accompanied by an increase in IGF-1 levels. Interestingly, however, there were no significant effects of the experimental treatment or of variation in IGF-1 levels on oxidative stress or telomeres. These findings suggest that IGF-1 is responsive to changes in resource availability but is not associated with increased markers of cellular aging during development in this relatively long-lived species.

Is there an oxidative cost of acute stress? Characterization, implication of glucocorticoids and modulation by prior stress experience.

Acute rises in glucocorticoid hormones allow individuals to adaptively respond to environmental challenges but may also have negative consequences, including oxidative stress. While the effects of chronic glucocorticoid exposure on oxidative stress have been well characterized, those of acute stress or glucocorticoid exposure have mostly been overlooked. We examined the relationship between acute stress exposure, glucocorticoids and oxidative stress in Japanese quail (Coturnix japonica). We (i) characterized the pattern of oxidative stress during an acute stressor in two phenotypically distinct breeds; (ii) determined whether corticosterone ingestion, in the absence of acute stress, increased oxidative stress, which we call glucocorticoid-induced oxidative stress (GiOS); and (iii) explored how prior experience to stressful events affected GiOS. Both breeds exhibited an increase in oxidative stress in response to an acute stressor. Importantly, in the absence of acute stress, ingesting corticosterone caused an acute rise in plasma corticosterone and oxidative stress. Lastly, birds exposed to no previous acute stress or numerous stressful events had high levels of GiOS in response to acute stress, while birds with moderate prior exposure did not. Together, these findings suggest that an acute stress response results in GiOS, but prior experience to stressors may modulate that oxidative cost.

An assessment of the US endangered species act recovery plans: using physiology to support conservation.

Applying physiology to help solve conservation problems has become increasingly prominent. It is unclear, however, if the increased integration into the scientific community has translated into the application of physiological tools in conservation planning. We completed a review of the use of animal physiology in the US Fish and Wildlife Service (USFWS) and National Marine Fisheries Service (NMFS) Endangered Species Act (ESA) recovery plans released between 2005 and 2016. Over those 11 years, 135 of the 146 recovery plans mentioned physiology, with 56% including it as background information on the natural history of the species and not as part of the recovery process. Fish and bird species had the lowest proportion of recovery plans to include physiology beyond the description of the natural history. When considering multiple sub-disciplines of physiology, immunology and epidemiology were incorporated as part of the recovery process most often. Our review suggests a disconnect between available physiological tools and the potential role of physiology in developing conservation plans. We provide three suggestions to further guide conservation scientists, managers and physiologists to work synergistically to solve conservation problems: (1) the breadth of knowledge within a recovery plan writing team should be increased, for example, through increased training of federal scientists in new physiology methodologies and tools or the inclusion of authors in academia that have a background in physiology; (2) physiologists should make their research more available to conservation scientists and federal agencies by clearly linking their research to conservation and (3) communication should be enhanced between government conservation scientists and physiologists.

Telomere correlations during early life in a long-lived seabird.

Telomere dynamics in blood cells have been linked to aging in a variety of organisms. However, whether blood telomeres are correlated with telomeres in other parts of the body is not well known, especially during early life when telomere loss is expected to be most rapid. We investigated this question in Franklin's gulls (Leucophaeus pipixcan) by measuring telomere lengths in blood and several other tissues including: heart, liver, and skeletal muscle at the end of embryonic (n=31) and post-natal development (n=20). In late-stage embryos, blood telomeres were significantly positively correlated with heart and skeletal muscle, but not liver telomeres. However, at the end of post-natal development, there were no significant correlations among blood telomeres and telomeres in any other tissues. In late-stage embryos, heart telomeres were significantly longer than blood, liver, and skeletal muscle telomeres, but at the end of post-natal development telomere lengths did not significantly differ among tissues. These results suggest that blood telomere length is not necessarily indicative of other tissues at all stages of development and highlights the importance of understanding any functional consequences of tissue specific telomere dynamics in early life.

Timing of Breeding Determines Growth and Development in a Long-Distance Migratory Bird.

The timing of breeding can have significant consequences for adult and offspring fitness, yet our current hypotheses of seasonal timing focus on the parent perspective. When offspring survival is affected by timing of breeding, we expect to see offspring mechanisms to detect and respond to cues of seasonal timing. Avian embryos respond to photoperiod and seasonal cues during development and in this study we evaluate the influence of photoperiod and season on posthatching growth and development in Franklin's gull (Leucophaeus pipixcan). Early- and late-season chicks exposed to short and long photoperiods during development were reared under common garden conditions. Photoperiod had no effect on posthatching growth and development, but seasonal effects present in the egg (maternal egg effects or genetic) did influence posthatching growth and development. Late-season chicks grew body mass and primary flight feathers at faster rates than early-season chicks, which we hypothesize facilitates independence and readiness for migration. Growth rates are complex phenotypes and we propose a general growth model that incorporates delays in negative feedback systems regulating growth. We show that the timing of breeding programs intrinsic growth rates in offspring, which suggests that many of the metrics used to describe seasonal patterns of reproductive success may be biased.

Carotenoid supplementation and GnRH challenges influence female endocrine physiology, immune function, and egg-yolk characteristics in Japanese quail (Coturnix japonica).

Androgens and carotenoids circulating in plasma affect the physiology and behavior of vertebrates. Much is known about control mechanisms and functions of each of these substances, yet their interactive effects are not well understood. Here we examine possible additive, multiplicative, and interactive effects of testosterone and carotenoids on female endocrine physiology, immunocompetence, and investment in eggs by simultaneously manipulating levels of testosterone [via gonadotropin releasing hormone (GnRH) challenges] and carotenoids (via diet supplementation) in captive female Japanese quail (Coturnix japonica). Females were randomly assigned to one of four treatments: carotenoid supplementation, GnRH challenge, GnRH challenge + carotenoid supplementation, or control. Carotenoid supplementation significantly increased circulating plasma carotenoid levels and acquired immune system performance, but not innate immunity. GnRH challenges elevated circulating testosterone and carotenoid levels, and induced immunosuppression in females. However, females in the GnRH challenge + carotenoid supplementation treatment had higher cell-mediated immune responses than control females and similar responses to those of carotenoid-supplemented females. Hence, availability of carotenoids in female quail seemed to counteract immunosuppressive effects of GnRH challenges. Our results provide further evidence for synergistic effects of carotenoids and testosterone on endocrine physiology and immune function in female birds. Elevated plasma testosterone or carotenoids levels resulted in increased deposition of those compounds to eggs, respectively. Furthermore, because we found that concentrations of testosterone and carotenoids in yolks were correlated within each treatment group, differential deposition of hormones and carotenoids in eggs may not only respond to surrounding social and environmental conditions, but also to other components of the egg.

Beyond maternal effects in birds: responses of the embryo to the environment.

Embryonic growth and development are impacted by environmental conditions. In avian systems, parents tightly control these environments through provisioning of nutrients to the egg and through incubation. Parents can influence embryonic development through egg size, eggshell conductance, hormones, or other substances deposited in eggs and through the onset and temperature of incubation. In addition to these parental influences, evidence suggests that avian embryos are able to perceive and actively respond to their environment during incubation and adjust their own development. Evolution of embryos' responses to developmental environments in birds can be understood in the context of parent-offspring conflicts. When parental investments favor future reproduction over current reproduction, current offspring pay fitness costs, which result in strong selection for offspring that can respond to developmental environments independent of their parents. Here, we review literature indicating that avian embryos actively respond to maternally derived components of the egg, vocalizations, and differences in day length, and we explore these responses in the context of three situations where the consequence of these environments to the fitnesses of offspring and parents differ: the degree of synchrony in hatching, the deposition of hormones in yolks, and seasonal timing of breeding. However, the adaptive significance of responses of embryos to developmental environments arising from parent-offspring conflict has not been adequately explored in birds.

Egg yolk environment differentially influences physiological and morphological development of broiler and layer chicken embryos.

Maternal effects are important in epigenetic determination of offspring phenotypes during all life stages. In the chicken (Gallus gallus domesticus), transgenerational transfer of egg yolk factors may set the stage for morphological and physiological phenotypic differences observed among breeds. To investigate the effect of breed-specific yolk composition on embryonic broiler and layer chicken phenotypes, we employed an ex ovo, xenobiotic technique that allowed the transfer of broiler and layer chicken embryos from their natural yolks to novel yolk environments. Embryonic day two broiler embryos developing on broiler yolk culture medium (YCM) had significantly higher heart rates than layer embryos developing on layer YCM (176±7 beats min(-1) and 147±7 beats min(-1), respectively). Broiler embryos developing on layer YCM exhibited heart rates typical of layer embryos developing normally on layer YCM. However, layer embryo heart rates were not affected by development on broiler YCM. Unlike O(2) consumption, development rate and body mass of embryos were significantly affected by exposure to different yolk types, with both broiler and layer embryos displaying traits that reflected yolk source rather than embryo genotype. Analysis of hormone concentrations of broiler and layer egg yolks revealed that testosterone concentrations were higher in broiler yolk (4.63±2.02 pg mg(-1) vs 3.32±1.92 pg mg(-1)), whereas triiodothyronine concentrations were higher in layer yolk (1.05±0.18 pg mg(-1) vs 0.46±0.22 pg mg(-1)). Thus, a complex synergistic effect of breed-specific genotype and yolk environment exists early in chicken development, with yolk thyroid hormone and yolk testosterone as potential mediators of the physiological and morphological effects.

Maternal effects increase within-family variation in offspring survival.

Maternal effects are environmental components of phenotypes that complicate relationships between natural selection and evolution because they often affect phenotypes and fitness simultaneously. We studied the effects of egg size variation on juvenile survival in a population of American coots (Fulica americana). We experimentally evaluated egg size variation at three levels: across the population, within natal nests, and within foster nests. Natal nests accounted for the most variation in population egg size. Within clutches, early-laid eggs were larger than later-laid eggs, with the exception of first-laid eggs, which were small. In the fostering experiment, posthatching survival was most strongly related to egg size relative to natal siblings and natal hatching order and less so to egg size within foster nests. These effects on survival were found even though young from natal nests were neither raised together nor raised by genetic parents. These results indicate that females allocate resources unequally among offspring such that offspring from larger, early-laid eggs have higher survival than offspring from smaller, later-laid eggs, regardless of their size relative to foster siblings or to mean population egg size. These results suggest that egg size variation can be maintained through selection on maternal investment strategies and not on egg size per se.

Effects of egg size on Double-crested Cormorant (Phalacrocorax auritus) egg composition and hatchling phenotype.

Maternal investment of yolk and albumen in avian eggs varies with egg mass and contributes to variation in hatchling mass. Here we use the natural variation in mass and composition of Double-crested Cormorant (Phalacrocorax auritus) eggs to examine consequences of variation in yolk and albumen mass on hatchling phenotype. The Double-crested Cormorant, a large bird with altricial young, lays eggs ranging in mass from 40 to 60 g and containing an average of 82% albumen and 18% yolk. Variation in Cormorant egg mass arises primarily from variation in the amount of albumen and water in the eggs; yolk mass remains relatively constant, contributing only 10% to egg mass variation. Likewise, variation in hatchling mass correlates positively with albumen mass and albumen solids contribute to hatchling dry mass. Thus, variation in Cormorant egg mass is primarily the result of variation in the amount of egg albumen, which contributes most to variation in hatchling mass. Similarities in egg composition of altricial birds, along with data presented here, suggest that variation in hatchling mass of all altricial birds may depend most on the amount of egg albumen, unlike species with precocial young that hatch from eggs with substantially more yolk.

Functional significance of variation in egg-yolk androgens in the American coot.

Maternally derived hormones in cleidoic eggs have been implicated in mediating growth, behavior, and social interactions among offspring. Given these widespread and significant effects, hormonal investments have the potential to greatly influence fitness of offspring. Intraspecific variation can exist at three levels (within individual eggs, among eggs within clutches, and among eggs from different females), each of which has different implications for offspring. We characterized all three levels of variation in maternally derived androgens (testosterone and androstenedione) present in yolks of American coot eggs. We found no variation in testosterone levels within eggs which suggests that embryos are exposed to constant androgen levels during development, and that field-based yolk biopsies are an appropriate way to sample eggs for this species. Within clutches, early-laid eggs had higher androgen levels than late-laid eggs, and this pattern may exacerbate negative effects of hatching asynchrony on chicks from late-hatching eggs if androgens provide chicks with a behavioral or growth advantage over chicks from eggs with lower androgen levels. American coots lay large clutches, and unequal resource allocation among offspring may be the optimal strategy for females with access to limited resources. Most of the variation in androgen levels occurred among eggs from different females. Females nesting on ponds with two other pairs laid eggs with significantly higher androgen levels than females living on ponds with fewer pairs. This suggests that increased territory defense behaviors influence the levels of androgens allocated to eggs and may be one mechanism underlying density-dependent effects on reproduction.