Telomere length reveals cumulative individual and transgenerational inbreeding effects in a passerine bird

Abstract

Inbreeding results in more homozygous offspring that should suffer reduced fitness, but it can be difficult to quantify these costs for several reasons. First, inbreeding depression may vary with ecological or physiological stress and only be detectable over long time periods. Second, parental homozygosity may indirectly affect offspring fitness, thus confounding analyses that consider offspring homozygosity alone. Finally, measurement of inbreeding coefficients, survival and reproductive success may often be too crude to detect inbreeding costs in wild populations. Telomere length provides a more precise measure of somatic costs, predicts survival in many species and should reflect differences in somatic condition that result from varying ability to cope with environmental stressors. We studied relative telomere length in a wild population of Seychelles warblers (Acrocephalus sechellensis) to assess the lifelong relationship between individual homozygosity, which reflects genome‐wide inbreeding in this species, and telomere length. In juveniles, individual homozygosity was negatively associated with telomere length in poor seasons. In adults, individual homozygosity was consistently negatively related to telomere length, suggesting the accumulation of inbreeding depression during life. Maternal homozygosity also negatively predicted offspring telomere length. Our results show that somatic inbreeding costs are environmentally dependent at certain life stages but may accumulate throughout life.

Evidence of opposing fitness effects of parental heterozygosity and relatedness in a critically endangered marine turtle?

“…Correlations between maternal heterozygosity and reproductive metrics may therefore be difficult to detect in marine turtles without controlling for variance in rates of capital accumulation (Broderick et al ., ). However, with sufficient long‐term data, it might be possible to test the hypothesis that heterozygosity affects efficiency at accumulating energy capital, and thereby remigration frequency and reproductive success, or to use biomarkers of stress such as telomeres (Plot et al ., ; Bebbington et al ., ).…”

Evolutionary ecology of telomeres: a review

“…Another genetic factor that has been suggested to affect telomere length is inbreeding depression (e.g., with long telomeres and high somatic telomerase levels throughout the body). For example, Bebbington et al . analyzed molecular inbreeding data on Seychelles warblers ( A. sechellensis ) and showed that inbreeding negatively affects telomere length (using qPCR).…”

“…Blackburn, Greider, and Szostak won the Nobel Prize for telomere and telomerase research, there has been a monumental increase in the research output on the associations between telomeres and a broad range of biomedical health‐related and other biological phenomena. These areas range from cancer and disease research, oxidative stress biochemistry, assisted reproductive technologies, developmental biology, epigenetic control of telomere length, and in‐ and outbreeding genetics to life history evolution . In many cases, these phenomena are interpreted to be causally linked to telomere dynamics.…”

Individual variation in early‐life telomere length and survival in a wild mammal

“…Hence, studies of wild populations have informed understanding of how early‐life environments shape individual senescence patterns (Cooper & Kruuk, ; Lemaitre et al, ; Nussey, Froy, Lemaitre, Gaillard, & Austad, ). This understanding has been further improved by quantification of extrinsic effects through biomarkers that reflect ecological effects that are otherwise difficult to measure (Bebbington et al, ; Spurgin et al, ).…”