Telomere length is highly heritable and independent of growth rate manipulated by temperature in field crickets

Abstract

Many organisms are capable of growing faster than they do. Restrained growth rate has functionally been explained by negative effects on lifespan of accelerated growth. However, the underlying mechanisms remain elusive. Telomere attrition has been proposed as a causal agent and has been studied in endothermic vertebrates. We established that telomeres exist as chromosomal-ends in a model insect, the field cricket, using terminal restriction fragment and Bal 31 methods. Telomeres comprised TTAGGn repeats of 38kb on average, more than four times longer than the telomeres of human infants. Bal 31 assays confirmed that telomeric repeats were located at the chromosome-ends. We tested whether rapid growth is achieved at the expense of telomere length by comparing crickets reared at 23°C with their siblings reared at 28°C, which grew three times faster. Surprisingly, neither temperature treatment nor age affected average telomere length. Concomitantly, the broad sense heritability of telomere length was remarkably high at ~100%. Despite high heritability, the evolvability (a mean standardized measure of genetic variance) was low relative to that of body mass. We discuss the different interpretations of these scaling methods in the context of telomere evolution. It is clear that some important features of vertebrate telomere biology are evident in an insect species dating back to the Triassic, but also that there are some striking differences. The apparent lack of an effect of growth rate and the total number of cell divisions on telomere length is puzzling, suggesting that telomere length could be actively maintained during the growth phase. Whether such maintenance of telomere length is adaptive remains elusive and requires further study investigating the links with fitness in the wild.

High heritability of telomere length, but low evolvability, and no significant heritability of telomere shortening in wild jackdaws

“…TL evolvability was also low in field crickets (Boonekamp et al, 2020a), which fits the expectations for a trait related to fitness (Houle et al 1992), where high selection pressures and trait canalisation are expected (Stearns, Kaiser, & Kawecki, 1995;Vedder, Verhulst, Bauch, & Bouwhuis, 2018). But more studies that provide coefficients of additive genetic variation for comparison among populations and taxa are required to gain a more comprehensive picture.…”

“…The evolutionary potential of a trait is dependent on the additive genetic variance, which scaled to the mean of the trait yields a metric known as the evolvability (Houle, 1992). We are aware of one study estimating the evolvability of TL, in an insect, which found evolvability to be low despite high heritability (Boonekamp et al, 2020a).…”

Associations between DNA methylation and telomere length during early life: insight from wild zebra finches (Taeniopygia guttata)

“…Temperature has been shown to effect within individual changes in DNAm (Sheldon et al, 2020) and telomere length (Stier et al 2020;Fitzpatrick et al 2019) however, it is unclear if temperature effects these DNA modifications comparably. The temperatures (average daily maximum of 27.6 o C) in our study may not have been 'stressful' enough to impact telomere dynamics, and indeed temperature has not affected telomere length in studies on other taxa (McLennan et al, 2018;Boonekamp et al, 2020).…”

Evidence for genetic isolation and local adaptation in the field cricket Gryllus campestris

“…Previous work (Boonekamp et al, 2020) identified significant heritability of growth rate, again using nymphs reared in sibling groups. In our growth rate study, nymphs were reared individually to eliminate environmental effects resulting from competition (including faster growing individuals potentially having to compete with faster growing siblings).…”

“…Lastly, we investigated whether in addition to the observed genetic variation in growth rate (G × Age), there was also evidence for genetic variation in the response to temperature (G × E) as such effects were reported in a similar experiment (Boonekamp et al, 2020). However, the bivariate model (with body mass at the two temperature conditions after 39 days of treatment as the response variables) yielded unreliable results due to singularities and/ or estimates that were highly dependent on initial starting values of the ASReml optimization procedures.…”