Artificial selection on chill-coma recovery time in Drosophila melanogaster: Direct and correlated responses to selection

Abstract

Artificial selection can be used to create populations with extreme phenotypic responses to environmental stressors. When artificial selection is applied to a single component of a stress response, this selection may result in correlated responses in other stress responses, a phenomenon called cross-tolerance, which is ultimately controlled by the genetic correlations among traits. We selected for extreme responses to cold tolerance by selecting for chill-coma recovery time from a single temperate population of Drosophila melanogaster. Chill-coma recovery time is a common metric of low, but non-lethal, cold temperature tolerance. Replicated divergent artificial selection was applied to a genetically variable base population for 31 generations, resulting in two cold resistant, two cold susceptible, and two unselected control lines. To quantify the relationship between selection on chill-coma recovery and other metrics of thermal performance, we also measured survivorship after acute cold exposure, survivorship after chronic cold exposure, survivorship after cold exposure following a pre-treatment period (rapid cold hardening), starvation tolerance, and heat tolerance. We find that chill-coma recovery time is heritable within this population and that there is an asymmetric response to increased and decreased chill-coma recovery time. Surprisingly, we found no cross-tolerances between selection on chill-coma recovery time and the other environmental stress response traits. These results suggest that although artificial selection has dramatically altered chill-coma recovery time, the correlated response to selection on other stress response phenotypes has been negligible. The lack of a correlated response suggests that chill-coma recovery time in these selection lines is likely genetically independent from measures of cold survivorship tested here.

Heat knockdown resistance and chill‐coma recovery as correlated responses to selection on mating success at high temperature in Drosophila buzzatii

“…In addition, selection for CCR had no correlated responses on KRHT in D. buzzatii (Bertoli, Scannapieco, Sambucetti, & Norry, ). Similar results of no trade‐off association in correlated selection responses were obtained for CCR and survival after heat stress in D. melanogaster (Gerken, Mackay, & Morgan, ; Mori & Kimura, ). Nevertheless, Drosophila and other insects can constantly adapt to their surrounding environment in the field, where heat resistance can be negatively correlated with cold resistance (Condon et al, ; Overgaard & Sørensen, ).…”

“…In addition, selection for CCR had no correlated responses on KRHT in D. buzzatii (Bertoli, Scannapieco, Sambucetti, & Norry, 2010). Similar results of no trade-off association in correlated selection responses were obtained for CCR and survival after heat stress in D. melanogaster (Gerken, Mackay, & Morgan, 2016;Mori & Kimura, 2008).…”

“…As mentioned above, QTL studies showed a trade‐off association between KRHT and CCR for one QTL in the middle of chromosome 2 in diverse mapping populations in D. melanogaster (Morgan & Mackay, ; Norry et al, , ). However, this trade‐off association was not apparent in experiments of artificial selection on either KRHT or CCR in D. buzzatii (Bertoli et al, ; Sambucetti et al, ; see Mori & Kimura, and Gerken et al, for similar results in D. melanogaster ). Dominant gene action in a pleiotropic allele at high frequency might partially mask correlated selection responses (Defays, Gomez Fernandez, & Norry, ).…”

Constraints, independence, and evolution of thermal plasticity: Probing genetic architecture of long- and short-term thermal acclimation

“…Flies were considered alive if they showed coordinated movement 24 h after exposure (12). Discriminating temperatures for acute cold stress were determined previously for a similar population of D. melanogaster from a scale of −5°to −8°C for flies reared at 18°C and 25°C (9,12,73,74). To calculate RCH for flies reared at 25°C (RCH at 25°C), flies were pretreated for 2 h at 4°C followed by cold exposure at −6°C for 1 h (i.e., RCH) or were moved directly from room temperature to −6°C for 1 h (i.e., acute survivorship) (73,75).…”

CRISPR-induced null alleles show that Frost protects Drosophila melanogaster reproduction after cold exposure

“…Therefore, we infer that the primary function of Fst is the preservation of post-cold-exposure reproductive capacity in female flies. The preservation of post-cold-exposure reproductive capacity is clearly a trait under selective pressure, and would explain the observation of Fst allele variation along a thermal cline (Hoffmann et al, 2012) and its presence on QTL associated with cold tolerance (Morgan and Mackay, 2006;Gerken et al, 2016).…”