An experimental test of evolutionary trade-offs during temperature adaptation

Abstract

We used experimental evolution to test directly the important and commonplace evolutionary hypothesis that adaptation, increased fitness within the selective environment, is accompanied by trade-off, a loss of fitness in other nonselective environments. Specifically, we determined whether trade-offs at high temperature generally and necessarily accompany genetic adaptation to low temperature. We measured the relative fitness increment of 24 lineages of the bacterium Escherichia coli evolved for 2,000 generations at 20 degrees C and the relative fitness decrement of these lines at 40 degrees C. Trade-offs at the higher temperature were examined for their generality, universality, quantitative relationship, and historical contingency. Considering all 24 lines as a group, a significant decline in fitness was found at 40 degrees C (mean decline = 9.4%), indicating the generality of the trade-off effect. However, in a lineage-by-lineage analysis, only 15 of 24 showed a significant trade-off, and one lineage increased fitness at high temperature. Thus, although general, trade-offs were not universal. Furthermore, there was no quantitative association between the magnitude of adaptive fitness increment at 20 degrees C and fitness decline at 40 degrees C, and no effect of lineages' historical thermal environment on either their improvement at 20 degrees C or the extent of their trade-off at high temperature. We do not yet know the underlying mechanisms responsible for the trade-off, but they are sufficiently prevalent to drive a general effect. However, approximately one-third of the experimental lineages achieved low-temperature adaptation without detectable high-temperature trade-offs; therefore, it cannot be necessary that every change conferring benefit in cold environments has a negative effect on function in warmer environments.

Fig. 1.

Phylogeny and nomenclature of the experimental lineages of E. coli used in this study. The ancestral organism (Anc) was obtained from a lineage that evolved under defined laboratory conditions at 37°C for 2,000 generations. A clone was sampled and cultured in six replicate populations that evolved in each of four thermal environments: 32°C, 37°C, or 42°C, or a daily alteration between 32°C and 42°C. After 2,000 generations, a clone was isolated from each lineage and propagated for another 2,000 generations at 20°C. Note that each of the 20°C selected lineages are equally related to Anc (separated by 4,000 generations) and are equally distant from each other (separated by 8,000 generations).

Fig. 2.

Correlation between change in fitness measured at 20°C and at 40°C after experimental evolution at 20°C. Although 20 of 24 points lie in the quadrant associated with an evolutionary trade-off (fitness gain at 20°C and loss at 40°C), the correlation between them is not significant (r = 0.006, n = 24, P > 0.50).