Sex Differences in Sand Lizard Telomere Inheritance: Paternal Epigenetic Effects Increases Telomere Heritability and Offspring Survival

Abstract

BackgroundTo date, the only estimate of the heritability of telomere length in wild populations comes from humans. Thus, there is a need for analysis of natural populations with respect to how telomeres evolve.Methodology/Principal FindingsHere, we show that telomere length is heritable in free-ranging sand lizards, Lacerta agilis. More importantly, heritability estimates analysed within, and contrasted between, the sexes are markedly different; son-sire heritability is much higher relative to daughter-dam heritability. We assess the effect of paternal age on Telomere Length (TL) and show that in this species, paternal age at conception is the best predictor of TL in sons. Neither paternal age per se at blood sampling for telomere screening, nor corresponding age in sons impact TL in sons. Processes maintaining telomere length are also associated with negative fitness effects, most notably by increasing the risk of cancer and show variation across different categories of individuals (e.g. males vs. females). We therefore tested whether TL influences offspring survival in their first year of life. Indeed such effects were present and independent of sex-biased offspring mortality and offspring malformations.Conclusions/SignificanceTL show differences in sex-specific heritability with implications for differences between the sexes with respect to ongoing telomere selection. Paternal age influences the length of telomeres in sons and longer telomeres enhance offspring survival.

Heritability of telomere length in the Zebra Finch

“…Broer et al 2013), Kakapos (Horn et al 2011) and King Penguins (Reichert et al 2014), telomere length has a stronger maternal than paternal inheritance; however, in Sand Lizards (Olsson et al 2011), stronger paternal inheritance was found, although CI overlapped (Table 1). In contrast, we found no evidence for a difference between maternal and paternal effects in our study (Tables 4, 5).…”

On being the right size: increased body size is associated with reduced telomere length under natural conditions

“…Body size has been shown to be heritable in house sparrows [52,53], heritability of body size is well documented in avian literature [54,55]. Significant heritability of telomere lengths has so far been demonstrated non-human species such as sand lizard (Lacerta agilis) [56], collared flycatcher (Ficedula albicollis), kakapo (Strigops habroptilus) [57,58], king penguins (Aptenodytes patagonicus) [59] and the great reed warbler (Acrocephalus arundinaceus) [60]. Heritability of telomere length has also been found in humans [61][62][63].…”

Maternal telomere length inheritance in the king penguin

“…Studies in humans reported heritability estimates of telomere length between 0.44 and 0.78 (Slagboom et al, 1994;Njajou et al, 2007) and of 0.52-1.23 in other vertebrates such as the sand lizards (Lacerta agilis), with an interesting difference in sexspecific heritability (Olsson et al, 2011;see Table 1). However, these estimations were carried out mainly using mid-parent-offspring regressions (or comparisons between relatives) that may yield high heritability values (Conner and Hartl, 2004).…”

“…Most of these studies support paternal inheritance of telomere length (Nordfjäll et al, 2005(Nordfjäll et al, , 2009Njajou et al, 2007), further revealing that paternal age is a strong determinant of offspring telomere length (Unryn et al, 2005;De Meyer et al, 2007;Kimura et al, 2008;Eisenberg, 2011). Interestingly, in non-human species contrasting results reveal either bi-parental inheritance patterns, for example, male inheritance in lizards (Olsson et al, 2011) or maternal inheritance in birds (females being ZW; Horn et al, 2011). These studies report highly variable heritability estimates ranging from 0.18 to 41.…”