Latitudinal and cold-tolerance variation associate with DNA repeat-number variation in the hsr-omega RNA gene of Drosophila melanogaster

Abstract

An 8-bp deletion in the hsr-omega heat-stress gene of Drosophila melanogaster has previously been associated with latitude, and with heat tolerance that decreases with latitude. Here we report a second polymorphic site, at the 3'-end of hsr-omega, at which multiple alleles segregate in natural populations for copy number of a approximately 280 bp tandem repeat. On each of 3 consecutive years (2000, 2001 and 2002) among populations sampled along the Australian eastern coast, repeat number was negatively associated with latitude. Neither altitudinal association was detected in 2002 when five high-altitude sites were included, nor was a robust association detected with local temperature or rainfall measures. Although in a large number of family lines, derived from a population located centrally in the latitudinal transect, no association between hsr-omega repeat number and heat tolerance occurred, a negative association of repeat number with cold tolerance was detected. As cold tolerance also exhibits latitudinal clines we examined a set of cold-tolerant populations derived by selection and found both reduced repeat number and low constitutive levels of the omega-n repeat-bearing transcript. In a sample from the central population, linkage disequilibrium was measured between repeat number and linked markers that also cline latitudinally. However, such disequilibrium could not account for the cline in repeat number or tolerance associations. Finally, during adult recovery from cold exposure a large increase occurred in tissue levels of the omega-c transcript. Together these data suggest that a latitudinal cline in hsr-omega repeat number influences cold-tolerance variation in this species.