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.

Keywords: Seychelles warbler; heterozygote advantage; inbreeding; lifetime fitness; telomere; trans-generational effects.

Figure 1

Relationship between standardized individual homozygosity (top row) or standardized maternal homozygosity (bottom row) and relative telomere length of juveniles born in years of high and low food availability, using raw data. In the left‐hand plots, food availability was split into a factor according to the median value for visual clarity, but was modelled as a continuous variable. Right‐hand plots display the conditional effect of homozygosity on RTL, across the range of food availability values. The value on the y‐axis indicates the direction of the homozygosity effect on RTL, given the value on the x‐axis. Bars represent 95% confidence limits.

Figure 2

Relationship between (a) standardized individual homozygosity and (b) standardized maternal homozygosity and relative telomere length in adult Seychelles warblers. Points represent raw data, lines represent fitted values (linear regression), and shading represents credible intervals.