ABSTRACT
Telomeres are highly conserved regions of DNA that protect the ends of linear chromosomes. The loss of telomeres can signal an irreversible change to a cell's state, including cellular senescence. Senescent cells no longer divide and can damage nearby healthy cells, thus potentially placing them at the crossroads of cancer and ageing. While the epidemiology, cellular and molecular biology of telomeres are well studied, a newer field exploring telomere biology in the context of ecology and evolution is just emerging. With work to date focusing on how telomere shortening relates to individual mortality, less is known about how telomeres relate to ageing rates across species. Here, we investigated telomere length in cross-sectional samples from 19 bird species to determine how rates of telomere loss relate to interspecific variation in maximum lifespan. We found that bird species with longer lifespans lose fewer telomeric repeats each year compared with species with shorter lifespans. In addition, phylogenetic analysis revealed that the rate of telomere loss is evolutionarily conserved within bird families. This suggests that the physiological causes of telomere shortening, or the ability to maintain telomeres, are features that may be responsible for, or co-evolved with, different lifespans observed across species.This article is part of the theme issue 'Understanding diversity in telomere dynamics'.
Subject(s)
Aging/physiology , Birds/physiology , Longevity/physiology , Telomere Shortening/physiology , Telomere/physiology , Aging/genetics , Animals , Biological Variation, Population , Birds/genetics , Cellular Senescence , Cross-Sectional Studies , Female , Longevity/genetics , Male , Phylogeny , Telomere/genetics , Telomere Shortening/geneticsABSTRACT
Common and roseate terns are migratory piscivorous seabirds with major breeding colonies within feeding range of the polychlorinated biphenyl (PCB)-contaminated New Bedford Harbor (NBH, MA, USA) Superfund site. Our longitudinal study shows that before PCB discharges into NBH ceased (late 1970s), tern eggs had very high but variable PCB concentrations. However, egg concentrations of PCBs as well as DDE (1,1-bis(p-chlorophenyl)-2,2-dichloroethene), the degradation product of the ubiquitous global contaminant DDT (1,1,1-trichloro-2,2-bis(p-chlorophenyl) ethane), have since declined. Rate constants for temporal decline of PCB congeners in tern eggs varied inversely with log10KOW (n-octanol-water partition coefficient), shifting egg congener patterns away from those characterizing NBH sediment. To estimate the toxic effects on tern eggs of PCB dioxin-like congener (DLC) exposures, we extrapolated published laboratory data on common terns to roseate terns by characterizing genetic and functional similarities in species aryl hydrocarbon receptors (AHRs), which mediate DLC sensitivity. Our assessment of contaminant risks suggests that terns breeding near NBH were exposed historically to toxic levels of PCBs and DDE; however, acute effects on tern egg development have become less likely since the 1970s. Our approach demonstrates how comparative genetics at target loci can effectively increase the range of inference for chemical risk assessments from tested to untested and untestable species.
Subject(s)
Charadriiformes/metabolism , Polychlorinated Biphenyls , Animals , Dichlorodiphenyl Dichloroethylene , Massachusetts , Water Pollutants, ChemicalABSTRACT
Post-natal growth is an important life-history trait and can be a sensitive indicator of ecological stress. For over 50 years, monotonic (never-decreasing) growth has been viewed as the predominant trajectory of post-natal mass change in most animal species, notably among birds. However, prevailing analytical approaches and energetic constraints may limit detection of non-monotonic (or multiphasic), determinate growth patterns, such as mass recession in birds (weight loss prior to fledging, preceded by overshooting adult mass), which is currently believed to be restricted to few taxa. Energetic surplus and shortfall are widespread conditions that can directly influence the degree of mass overshooting and recession. Thus, we hypothesize that in many species, prevailing energetic constraints force mass change away from a fundamental non-monotonic trajectory to instead follow a monotonic curve. We observed highly non-monotonic, mass change trajectories (overshooting adult mass by up to almost 20%) among common tern Sterna hirundo chicks, a well-studied species long-established as growing monotonically. We quantified the prevalence and magnitude of non-monotonic mass change prior to fledging for 313 common tern chicks that successfully fledged from two discrete populations in multiple years. We used a new approach for analysing non-monotonic curves to examine differences in mass change trajectories between populations under contrasting abiotic (freshwater vs. saltwater) and biotic stresses (low rates of food provisioning). Some degree of mass recession occurred in 73% of all study chicks. Overshooting adult mass followed by extensive mass recession was most prevalent at our freshwater colony, being detected among 34-38% of chicks annually. Non-monotonic trajectories were less marked in populations experiencing ecological stress and among lower quality individuals. Chicks that were provisioned at higher rates were more likely to both overshoot adult mass and experience subsequent mass recession. Our results in common terns provide strong support for the hypothesis that non-monotonic trajectories are the fundamental pattern of mass change but are constrained to be monotonic under energetic shortfall. This justifies future tests of the generality of this hypothesis across a broad range of taxa. We also demonstrate a recent analytical tool that prevents routine fitting of monotonic curves without prior investigation of non-monotonic trends.
Subject(s)
Charadriiformes/physiology , Energy Intake , Animals , Charadriiformes/growth & development , Massachusetts , Models, Biological , Ontario , SeasonsABSTRACT
The recent trend for journals to require open access to primary data included in publications has been embraced by many biologists, but has caused apprehension amongst researchers engaged in long-term ecological and evolutionary studies. A worldwide survey of 73 principal investigators (Pls) with long-term studies revealed positive attitudes towards sharing data with the agreement or involvement of the PI, and 93% of PIs have historically shared data. Only 8% were in favor of uncontrolled, open access to primary data while 63% expressed serious concern. We present here their viewpoint on an issue that can have non-trivial scientific consequences. We discuss potential costs of public data archiving and provide possible solutions to meet the needs of journals and researchers.
Subject(s)
Information Dissemination/ethics , Information Dissemination/methods , Open Access Publishing/ethics , Surveys and Questionnaires , Biological Evolution , Ecology , Longitudinal Studies , Open Access Publishing/economics , Periodicals as TopicABSTRACT
In June and July 1995, 98 breeding common terns (Sterna hirundo) were captured, weighed, and bled as a part of ongoing research on the population health and reproductive biology of this species of special concern. Packed cell volume, total and differential white blood cell counts, and blood smears were obtained. Blood smears from 75 terns were examined. No hemoparasites were found. There were some significant differences among hematologic parameters in birds from different islands, and between birds nesting earlier versus later in the season, but there were no significant differences associated with body mass, sex, or age. The absence of hemoparasites in the blood smears of these terns is noteworthy, especially because other studies of seabirds (including Charadriiformes) have revealed low prevalences of hematozoa.
Subject(s)
Bird Diseases/epidemiology , Charadriiformes/blood , Parasitemia/veterinary , Animals , Bird Diseases/blood , Bird Diseases/parasitology , Blood Cell Count/veterinary , Breeding , Erythrocytes/parasitology , Female , Hematologic Tests/veterinary , Male , Massachusetts/epidemiology , Parasitemia/epidemiology , Population SurveillanceABSTRACT
In response to stressors, most vertebrates elevate secretion of glucocorticoids (CORT) to produce a 'stress response' that enhances survival, but simultaneously inhibits reproduction. Circumstances in which the value of current reproduction is high relative to the value of future reproduction and survival, often lead to suppression of the stress response thus ensuring that critical resources are not diverted away from reproduction. Consistent with this expectation, we have previously reported that the magnitude of the stress response (maximum levels of CORT) declines with age in breeding adults of a long-lived seabird, the common tern (Sterna hirundo). While age-related changes in the stress response may be common in vertebrates, the mechanisms that underlie them are poorly understood. The glucocorticoid stress response is regulated by the hypothalamic-pituitary-adrenal (HPA) axis, and one mechanism that may contribute to an age-related decline in the stress response is changes in adrenal capacity (adrenal sensitivity to ACTH and/or an ability to secrete CORT in response to ACTH). To test this hypothesis, we captured and injected 92 known-aged adult common terns (Sterna hirundo) ranging in age from 3 to 29 years with either a control saline or an experimental adrenocorticotropin (ACTH) solution and measured the effects on stress-induced CORT after 30 min of restraint. In both treatment groups, stress-induced CORT significantly declined with age, suggesting that a decrease in adrenal capacity contributes to a reduction in the stress response in older adults.
Subject(s)
Adrenal Glands/growth & development , Adrenal Glands/physiopathology , Aging/physiology , Charadriiformes/physiology , Stress, Psychological/physiopathology , Adrenal Glands/drug effects , Adrenocorticotropic Hormone/pharmacology , Animals , Female , Hydrocortisone/blood , Hypothalamus/metabolism , Male , Pituitary Gland/metabolism , Restraint, PhysicalABSTRACT
Telomerase is an enzyme capable of elongating telomeres, the caps at the ends of chromosomes associated with aging, lifespan and survival. We investigated tissue-level variation in telomerase across different ages in four bird species that vary widely in their life history. Telomerase activity in bone marrow may be associated with the rate of erythrocyte telomere shortening; birds with lower rates of telomere shortening and longer lifespans have higher bone marrow telomerase activity throughout life. Telomerase activity in all of the species appears to be tightly correlated with the proliferative potential of specific organs, and it is also highest in the hatchling age-class, when the proliferative demands of most organs are the highest. This study offers an alternative view to the commonly held hypothesis that telomerase activity is down-regulated in all post-mitotic somatic tissues in long-lived organisms as a tumor-protective mechanism. This highlights the need for more comparative analyses of telomerase, lifespan and the incidence of tumor formation.
Subject(s)
Life Expectancy , Songbirds/growth & development , Songbirds/physiology , Telomerase/metabolism , Animals , Bone Marrow/growth & development , Bone Marrow/physiology , Female , Male , Organ Specificity , Ovary/growth & development , Testis/growth & development , Tissue DistributionABSTRACT
In many taxa, reproductive performance increases throughout the lifespan and this may occur in part because older adults invest more in reproduction. The mechanisms that facilitate an increase in reproductive performance with age, however, are poorly understood. In response to stressors, vertebrates release glucocorticoids, which enhance survival but concurrently shift investment away from reproduction. Consequently, when the value of current reproduction is high relative to the value of future reproduction and survival, as it is in older adults, life history theory predicts that the stress response should be suppressed. In this study, we tested the hypothesis that older parents would respond less strongly to a stressor in a natural, breeding population of common terns (Sterna hirundo). Common terns are long-lived seabirds and reproductive performance is known to increase throughout the lifespan of this species. As predicted, the maximum level of glucocorticoids released in response to handling stress decreased significantly with age. We suggest that suppression of the stress response may be an important physiological mechanism that facilitates an increase in reproductive performance with age.
Subject(s)
Charadriiformes/physiology , Glucocorticoids/metabolism , Reproduction/physiology , Stress, Physiological/metabolism , Age Factors , Animals , Charadriiformes/metabolism , MassachusettsABSTRACT
The evolution of longevity requires a low risk of mortality from extrinsic factors, relative to intrinsic factors, so that individuals that differentially invest in physiological self-maintenance and minimize their annual reproductive costs will maximize lifetime fitness through a prolonged reproductive lifespan. The trade-off between reproductive effort and self-maintenance, as measured by immune function, has been well documented in short-lived birds, but is difficult to demonstrate in long-lived birds. To assess self-maintenance in a long-lived seabird, we measured serum protein levels, including immunoglobulin G (IgG = IgY), in 30 breeding pairs of common terns (Sterna hirundo) and their first-hatched (A) chicks. Most parents were of known age from banding as hatchlings; our sample was selected to contrast young breeders (6-9 years) with very old birds (17-23 years). Body-mass of the parents declined by 5% during the chick-rearing period, while serum protein levels were stable. Serum IgG levels were higher in parents of offspring with faster growth rates, while IgG levels were lower in parents whose broods were reduced by starvation. A-chicks in broods of two had higher IgG levels than singleton chicks. Albumin levels were not related to reproductive performance. Thus, despite adequate statistical power, we could find no evidence for a trade-off between reproduction and self-maintenance in common terns, even in old age. The results are consistent with life-history predictions for long-lived vertebrates, in which selection favors sustained self-maintenance across the reproductive lifespan. The positive relationships between IgG levels and reproductive performance indicate that IgG can be used as an index of parental "quality."
Subject(s)
Aging/blood , Breeding , Charadriiformes/physiology , Immunoglobulin G/blood , Reproduction/immunology , Animals , Body Mass Index , Environmental Exposure , Female , Hemagglutination Tests , Male , Nesting Behavior , Population Dynamics , Serum Albumin/analysisABSTRACT
The Common Tern (Sterno hirundo) is a long-lived colonial nesting seabird. Previous studies have shown that chick growth and fledging success vary with age of the parental pair and with laying date, with older parents and those nesting earlier being more successful. This study investigated the dependence of breeding performance and one aspect of behavior, defense against conspecifics, on age and laying date. Nest defense behavior was evaluated by recording individual responses to a mirror placed 20 cm from the nest, simulating an unfamiliar intruder within the territory. Most study birds were of known age (3-21 years) from banding as chicks; they were divided into three groups: ≥12, 8-11 and ≤seven years. Responses to the mirror were examined during incubation and at the time of hatching. Older birds nested earlier than younger birds. Chicks reared by older parents gained mass more quickly and survived better than chicks of younger parents. Using a composite score reflecting both the intensity and duration of aggressive responses to the mirror, older birds responded more strongly than younger birds during incubation, but responses were similar at the time of hatching. Older birds reduced their aggressive responses between incubation and hatching, while younger birds increased their responses. We suggest that this contributes to the greater success of older birds, because younger birds expend more time and energy on territorial defense at a time when they need to feed chicks. Our findings are consistent with previous studies and show that Common Tern colonies are finely structured by age and laying date; older and earlier-nesting birds are superior to younger and later birds on several measures of performance. This study suggests that finely-tuned nest defense behavior is one component of the superior performance of old birds.
Subject(s)
Animal Welfare/ethics , Animals, Domestic , Animals, Wild , Research Design , Agriculture , Animal Care Committees , Animal Population Groups , Animals , HumansABSTRACT
Cellular senescence caused by telomere shortening has been suggested as one potential causal agent of aging. In some tissues, telomeres are maintained by telomerase; however, telomerase promotes tumor formation, suggesting a trade-off between aging and cancer. We predicted that telomerase activity should vary directly with life span. We determined telomerase activity in bone marrow in cross-sectional samples from two short-lived bird species and two long-lived bird species. The two short-lived species had high telomerase activity as hatchlings but showed a sharp downregulation in both the young and old adults, whereas the two long-lived species had relatively high telomerase activity in bone marrow that did not decrease with age. In zebra finches, the age-related change in telomerase activity varied in different tissues. Telomerase activity increased late in life in skeletal muscle, liver, and gonad, but not in blood or bone marrow.
Subject(s)
Aging , Longevity , Telomerase/biosynthesis , Telomere/ultrastructure , Animals , Birds , Bone Marrow Cells/metabolism , Songbirds , Species Specificity , Time Factors , Tissue DistributionABSTRACT
We know very little about physiological constraints on the evolution of life-history traits in general, and, in particular, about physiological and molecular adjustments that accompany the evolution of variation in lifespan. Identifying mechanisms that underlie adaptive variation in lifespan should provide insight into the evolution of trade-offs between lifespan and other life-history traits. Telomeres, the DNA caps at the ends of linear chromosomes, usually shorten as animals age, but whether telomere rate of change is associated with lifespan is unknown. We measured telomere length in erythrocytes from five bird species with markedly different lifespans. Species with shorter lifespans lost more telomeric repeats with age than species with longer lifespans. A similar correlation is seen in mammals. Furthermore, telomeres did not shorten with age in Leach's storm-petrels, an extremely long-lived bird, but actually lengthened. This novel finding suggests that regulation of telomere length is associated not only with cellular replicative lifespan, but also with organismal lifespan, and that very long-lived organisms have escaped entirely any telomeric constraint on cellular replicative lifespan.
Subject(s)
Birds/genetics , Birds/physiology , Longevity/genetics , Longevity/physiology , Mammals/physiology , Telomere/physiology , Aging/genetics , Aging/physiology , Animals , Erythrocytes/cytology , Erythrocytes/metabolism , Mammals/genetics , Species Specificity , Telomere/geneticsABSTRACT
Field biologists often work with animals for which there are no prior history. A marker of an animal's age would offer insight into how age and experience affect reproductive success and other life history parameters. We previously reported that length of telomere restriction fragments shorten predictably with age in the captive zebra finch (Taeniopygia guttata). This paper reports that telomeres can also be used to gain knowledge on the age structure of wild, long-lived common terns (Sterna hirundo). Although ages cannot be determined precisely from telomere lengths alone, birds can be classified into broad age-classes. This technique can provide useful information about the age of individuals in cases where their previous histories are unknown.
Subject(s)
Aging/physiology , Animals, Wild/physiology , Birds/physiology , Telomere/ultrastructure , Animals , Calibration , Erythrocytes/physiology , Image Processing, Computer-Assisted , Microscopy, ElectronABSTRACT
Common terns (Sterna hirundo) and roseate terns (Sterna dougallii) breed on Bird Island, Massachusetts, USA, near a Superfund site highly contaminated with polychlorinated biphenyls (PCBs). Observations of skewed sex ratios and female-female pairings among endangered roseate terns (Nisbet and Hatch (1999) Ibis 141, 307) suggested the possibility of contaminant-related endocrine disruption in these birds and prompted investigation of common terns as a surrogate species. In 1993 and 1994, 60-90% of pipping male common tern embryos sampled exhibited ovarian cortical tissue in their testes (ovotestes) (Nisbet et al. (1996) Bull. Environ. Contam. Toxicol. 57, 895; Hart et al. (1998) Mar. Environ. Res. 46, 174). To examine the possible impact of ovotestes on the reproductive capabilities of common terns, we examined gonadal histology in common tern prefledglings (approximately 21 days old) collected from Bird Island in 1995. As a measure of embryonic contaminant exposure, contaminants were measured in a subset of eggs collected from the same nests as the prefledglings. Concentrations of total PCBs in these eggs ranged from 14.4 to 546 microg/g lipid. No evidence of ovotesticular development was observed in any of the 19 male prefledglings examined. Some gonadal irregularities were observed, including small nodules of testicular tissue within the epithelial capsule of the testes, but these were judged not likely to affect testicular function. There was no relationship between any observed irregularities and levels of contaminants present in the matched eggs. The results suggest that the ovotestes that occur in 60-90% of pipping common tern embryos from this site become fully regressed by approximately 21 days posthatch. Our data from this and previous studies are consistent with the idea that ovotestes occur naturally in some individual common terns at hatching, although the frequency of occurrence may be enhanced by exposure to chlorinated organic contaminants such as PCBs. In either case, we suggest that the presence of ovotestes in common tern embryos from PCB-contaminated sites such as Bird Island does not lead to permanent alterations in gonadal histology that would be expected to impair reproductive function.