TELOMERE SHORTENING IN A LONG-LIVED MARINE BIRD: CROSS-SECTIONAL ANALYSIS AND TEST OF AN AGING TOOL

Auk, The, Jul 2006 by Juola, Frans A, Haussmann, Mark F, Dearborn, Donald C, Vleck, Carol M

ABSTRACT.-

A correlation between length of telomere restriction fragments (TRFs) and age has recently been demonstrated in several bird species. Comparisons of different-aged individuals within a population have shown that TRFs typically shorten with age and that this shortening continues throughout the life span of the species. In addition, it has been shown that telomere rate-of-change (TROC) correlates tightly with life span across several bird species. Previous studies of long-lived birds, however, have shown exceptions to these trends, demonstrating no declines in TRF length in adults in some cases and increases in TRF length with age in other cases. Here, we report known ages of individuals from a colony of Great Frigatebirds (Fregata minor) based on recaptures of leg-banded birds, including two individuals that were at least 44 years of age, the oldest Great Frigatebirds ever reported. Using a previously developed molecular technique, we report a predictable, nonlinear decline of TRF length with age in this population. Telomere restriction fragments decline more rapidly early in life but continue to shorten throughout the life span examined. The rate of decline in TRF for this species does not fit the tight correlation previously reported between TROC and life span in other species. Finally, we tested the ability to estimate age and age structure of breeding females on the basis of the calibration of TRF length and individuals of known age. Because of the slow telomere-attrition rate and the variability observed in TRF lengths at given ages, estimations of age of individuals and of estimated age structure of breeding birds in this population are not particularly reliable.

Received 29 May 2004, accepted 3 October 2005.

Key words: age structure, aging, Fregata minor, Great Frigatebird, life span, telomere.

Encogimiento del Telomero en un Ave Marina Longeva: Análisis de Secciones Cruzadas y Evaluación de una Herramienta de Envejecimiento

RESUMEN.-Recientemente se ha demostrado una correlación entre el largo de los fragmentas de restricción de los telómeros (FRT) y la edad en varias especies de aves. Las comparaciones de individuos de edades diferentes de una población han mostrado que los FRT típicamente se acortan con la edad y que este encogimiento continúa a lo largo de la vida de estas especies. De modo adicional, se ha demostrado que la tasa de cambio del telómero (TCT) se correlaciona fuertemente con la longevidad en varias especies de aves. Sin embargo, estudios previos de aves longevas han mostrado excepciones a estas tendencias, demostrando la falta de disminuciones en el largo de los FRT de los adultos en algunos casos e incrementos en el largo de los FRT con la edad en otros casos. Aquí, documentamos datos sobre edades conocidas de individuos de una colonia de Fregata minor basados en recapturas de aves anilladas en las piernas, incluyendo dos individuos de por lo menos 44 años de edad, el individuo conocido más viejo de F. minor. Usando una técnica molecular previamente desarrollada, reportamos una disminución no lineal predecible del largo de los FRT con la edad en esta población. Los FRT disminuyeron más rápidamente temprano en la vida pero continuaron acortándose a lo largo del període de vida examinado. La tasa de disminución en los FRT para esta especie no concuerda con la estrecha correlación reportada anteriormente entre la TCT y el período de vida de otras especies. Finalmente, evaluamos la capacidad de estimar la edad y la estructura de edades de las hembras reproductivas basándose en la calibración del largo de los FRT y en individuos de edad conocida. Debido a la lenta tasa de desgaste del telómero y a la variabilidad observada en los largos de los FRT a determinadas edades, las estimaciones de la edad de los individuos y de la estructura de edades estimada a partir de las aves reproductivas en esta población no son particularmente confiables.

TELOMERES ARE PROTEIN-DNA complexes that cap the ends of linear eukaryotic chromosomes (Blackburn 1991, Zakian 1995). They serve a variety of functions, including providing chromosomal stability (Watson 1972, Prowse and Greider 1995), aiding in the replication process (Meyne et al. 1989), inhibiting rearrangements and fusions of broken chromosomes (McClintock 1941, Smogorzewska et al. 2002), and aiding in chromosome segregation (Kirk et al. 1997, Hande et al. 1999). The highly conserved repeated telomere sequence TTAGGG is present in at least 91 vertebrate species tested from a variety of classes, including bony fishes, reptiles, amphibians, birds, and mammals (Meyne et al. 1989). By nature of the linear DNA replication process, DNA polymerase is unable to complete the replication of the 3' end of DNA strands. Therefore, during each replication cycle of a cell, some telomeric repeats are left as single-stranded ends that are eventually lost to breakage or degradation by exonucleases (Watson 1972). Cultured human cells have a finite proliferative capacity, reaching a replication limit after a certain number of cell divisions (Hayflick and Moorhead 1961, Vaziri et al. 1994, Aikata et al. 2000). This limit is correlated with a critical telomere-length threshold. Therefore, cellular senescence may be regulated by a molecular clock, specifically, the gradual decrease in telomeres that occurs during each cellular replication (Olovnikov 1973). In rare cases, telomere length may be maintained or even lengthened through the activity of the ribonucleoprotein telomerase (Greider and Blackburn 1985).