Genetic constraints for thermal coadaptation in Drosophila subobscura

Abstract

Background: Behaviour has been traditionally viewed as a driver of subsequent evolution because behavioural adjustments expose organisms to novel environments, which may result in a correlated evolution on other traits. In Drosophila subobscura, thermal preference and heat tolerance are linked to chromosomal inversion polymorphisms that show parallel latitudinal clines worldwide, such that "cold-climate" ("warm-climate") chromosome arrangements collectively favour a coherent response to colder (warmer) settings as flies carrying them prefer colder (warmer) conditions and have lower (higher) knock out temperatures. Yet, it is not clear whether a genetic correlation between thermal preference and heat tolerance can partially underlie such response.

Results: We have analyzed the genetic basis of thermal preference and heat tolerance using isochromosomal lines in D. subobscura. Chromosome arrangements on the O chromosome were known to have a biometrical effect on thermal preference in a laboratory temperature gradient, and also harbour several genes involved in the heat shock response; in particular, the genes Hsp68 and Hsp70. Our results corroborate that arrangements on chromosome O affect adult thermal preference in a laboratory temperature gradient, with cold-climate Ost carriers displaying a lower thermal preference than their warm-climate O3+4 and O3+4+8 counterparts. However, these chromosome arrangements did not have any effect on adult heat tolerance and, hence, we putatively discard a genetic covariance between both traits arising from linkage disequilibrium between genes affecting thermal preference and candidate genes for heat shock resistance. Nonetheless, a possible association of juvenile thermal preference and heat resistance warrants further analysis.

Conclusions: Thermal preference and heat tolerance in the isochromosomal lines of D. subobscura appear to be genetically independent, which might potentially prevent a coherent response of behaviour and physiology (i.e., coadaptation) to thermal selection. If this pattern is general to all chromosomes, then any correlation between thermal preference and heat resistance across latitudinal gradients would likely reflect a pattern of correlated selection rather than genetic correlation.

Figure 1

Latitudinal cline of O_st gene arrangement and schematic of chromosome O in Drosophila subobscura. (a) Lines in the Palaearctic region connect places at which O_st depicts similar frequencies, and show a clear northwest-southwest cline (O₃₊₄ shows an opposite cline). (b) Approximate location of genes Hsp68 and Hsp70 on chromosome O. The three gene arrangements used in the experiment are labelled on the right side of the schematic representation, with the centromere placed on the left (solid circle) and the telomere on the right. O₃₊₄ consists of two overlapping inversions, and O₃₊₄₊₈ of three.

Figure 2

Inbreeding and temperature effects on thermal preference. Homokaryotipic averages for T_p (in °C with 95% confidence intervals) in inbred (left panels) and outbred (right panels) crosses according to sex and developmental temperature.

Figure 3

Inbreeding and temperature effects on knock out temperature. Homokaryotipic averages for T_ko (in °C with 95% confidence intervals) in inbred (left panels) and outbred (right panels) crosses according to sex and developmental temperature.

Figure 4

Karyotypic values in the additive-dominance scale. Deviation values for thermal preference (T_p) and knockout temperature (T_ko) were measured after pooling arrangements O₃₊₄ and O₃₊₄₊₈ into a single class (${\text{O}}_{3+4}^{\ast }$), and the coordinate point (0, 0) was taken as the midparent (i.e., the average of T_p and T_ko for the two karyotypes O_st/O_st and ${\text{O}}_{3+4}^{*}/{\text{O}}_{3+4}^{*}$). Females (upper panel) and males (lower panel) are plotted separately because the interaction karyotype × sex was statistically significant for T_ko (Table 4). In the original scale the (0, 0) point corresponds to an average T_p of 18.31°C for females and 17.91°C for males, and an average T_ko of 33.58°C for females and 32.61°C for males. Open squares give the values for all six karyotypes to appreciate their dispersion from the midparent, as well as their dispersion from the pooled ${\text{O}}_{\text{st}}/{\text{O}}_{3+4}^{*}$ and ${\text{O}}_{3+4}^{*}/{\text{O}}_{3+4}^{*}$ karyotypes (black circles). Statistical significance for additive ($a_{T_{\text{p}}}\text{,}{a}_{T_{\text{ko}}}$) and dominance ($d_{T_{\text{p}}}\text{,}{d}_{T_{\text{ko}}}$) effects are given in Tables 3 and 4. Note also that the phenotypic ($r_{T_{\text{p}}\cdot T_{\text{ko}}}=-0.030$) and genetic (r_k = -0.068, r_p = -0.130; see Methods) correlations were non-significantly different from zero (see text for details).