Heritability of hsp70 expression in the beetle Tenebrio molitor: Ontogenetic and environmental effects

Highlights

• Expression levels of HSP70 were higher in the variable environment.

• Additive genetic variance was higher in the variable environment and in adults.

• Almost all the genetic correlations across stages and environment were positive.

• The expression of additive genetic variation increases under adverse conditions.

• Our results suggest the evolvability for HSP70 expression might be restricted.

Abstract

Ectotherms constitute the vast majority of terrestrial biodiversity and are especially likely to be vulnerable to climate warming because their basic physiological functions such as locomotion, growth, and reproduction are strongly influenced by environmental temperature. An integrated view about the effects of global warming will be reached not just establishing how the increase in mean temperature impacts the natural populations but also establishing the effects of the increase in temperature variance. One of the molecular responses that are activated in a cell under a temperature stress is the heat shock protein response (HSP). Some studies that have detected consistent differences among thermal treatments and ontogenetic stages in HSP70 expression have assumed that these differences had a genetic basis and consequently expression would be heritable. We tested for changes in quantitative genetic parameters of HSP70 expression in a half-sib design where individuals of the beetle Tenebrio molitor were maintained in constant and varying thermal environments. We estimated heritability of HSP70 expression using a linear mixed modelling approach in different ontogenetic stages. Expression levels of HSP70 were consistently higher in the variable environment and heritability estimates were low to moderate. The results imply that within each ontogenetic stage additive genetic variance was higher in the variable environment and in adults compared with constant environment and larvae stage, respectively. We found that almost all the genetic correlations across ontogenetic stages and environment were positive. These suggest that directional selection for higher levels of expression in one environment will result in higher expression levels of HSP70 on the other environment for the same ontogenetic stage.

Introduction

The impact of current climate change on biodiversity has been widespread and has involved several types of responses from the molecular to the ecosystem level (Pörtner et al., 2006, Parmesan, 2006, Chown et al., 2010, Hoffmann and Sgrò, 2011). Important determinants of the biological responses to global warming will be the degree of warming itself (Helmuth et al., 2005), the physiological sensitivity of organisms to changes in the temperature (Calosi et al., 2008, Helmuth et al., 2005, Huey et al., 2012) and the effects of the increase in temperature variance and frequency of extreme events (see Seneviratne et al., 2006, Pertoldi and Bach, 2007, Bentz et al., 2010). In addition, it has been shown that the thermal performance of many organisms is proportional to the magnitude of temperature variation they experience (Addo-Bediako et al., 2002, Gilman et al., 2006, Angilletta, 2009) as suggested by Jensen’s inequality (Ruel and Ayres, 1999).

One of the molecular responses that is activated in a cell under temperature stress is the heat shock protein response (HSP), an event of genetic activation that occurs in the cells in response to abnormal, stressfully high or low temperatures (Rinehart et al., 2007). The genes that encode for Heat-Shock Proteins (HSPs) are highly conserved and have been found in every studied species (Feder and Hofmann, 1999, Yeh and Hsu, 2002). Among HSP families, the group within the 70-kilo Daltons size range (HSP 70) is the most extensively studied because of its well-known response to stresses (see reviews in Feder and Hofmann, 1999, Sanders, 1993 Halpin et al., 2002, Hofmann and Todgham, 2010). The expression of these proteins could explain differences not only in fitness but also in the geographical distribution of organisms (Sorte and Hofmann, 2005, Bernabò et al., 2011, Lyytinen et al., 2012). Several studies that have detected consistent differences among populations and/or thermal treatments in HSP70 expression have assumed that these differences had a genetic basis (Roberts and Feder, 2000; Somero, 2010; Tine et al., 2010, Lyytinen et al., 2012). Nevertheless, this assumption has a direct test only in Drosophila melanogaster (Krebs et al., 1998, Morgan and Mackay, 2006). Furthermore, it is known that the synthesis, degradation and replacement of these proteins represent an important energetic cost for the organisms (Hartl and Hayer-Hartl, 2002, Sørensen and Loeschcke, 2002). Therefore, trade-offs might be expected between different ontogenic stages if development occurs under different thermal stressful environments (see Krebs et al., 1998, Sørensen et al., 2003).

The speed of evolutionary change in a phenotypic trait is determined by two key components: the amount of additive genetic variance underlying the trait and the strength of selection acting on it. Many studies have shown that both selection and expression of genetic variance may depend on the environmental conditions the population experiences (Husby et al., 2011). It is important to realize that heritability (h²) may change under different environmental conditions either because of changes in additive genetic variance (V_A) or other variance components (e.g., permanent environmental variance (V_PE) or residual variance (V_R). However, changes in V_A are of particular interest because they indicate a change in the “evolvability”, or the potential to respond to selection of a trait. On the other hand, cross-environment genetic correlations have important implications for evolution, that is, a trait measured in two environments can be considered as genetically correlated traits (sensu Via and Lande, 1985).

Here, we evaluated whether HSP70 expression has a genetic basis and whether that expression is affected by the ontogenetic stage and thermal environment in which an insect develops. We used the yellow mealworm beetle Tenebrio molitor (Polyphaga, Tenebrionidae) as our study model, an insect with a complex life-cycle which is a world pest of stored grains and that can be easily captured in field and reared in the laboratory (Worden and Parker, 2001). T. molitor has been used previously in molecular and ecological research (Graham et al., 2000, Drnevich et al., 2000, Vainikka et al., 2006), however, we are not aware of any studies examining the evolutionary potential of physiology or life-history traits in this species. In particular, using a quantitative genetic design we evaluated the following questions. First, what is the heritability of HSP70 under different thermal environments and ontogenetic stages? As stress conditions increase the phenotypic differences between genotypes (Hoffman and Merilä, 1999), we should observe an increase of additive genetic variance (and of heritability) under such conditions. Second, we evaluated the potential evolutionary response of HSP70 expression across environments and ontogenetic stages by estimating the cross environment genetic correlation. As the magnitude of this correlation reflects the extent to which the same genes control HSP70 expression, we predict a positive association in each environment and ontogenetic stage.