Beneficial acclimation hypothesis

The Beneficial Acclimation Hypothesis is the physiological hypothesis that acclimating to a particular environment (particularly thermal) provides an organism with fitness advantages in that environment. First formally defined and tested by Armand M. Leroi, Albert Bennett, and Richard Lenski in 1994, it has however been a central assumption in historical physiological work that acclimation is adaptive. Further refined by Raymond B. Huey and David Berrigan under the strong inference approach, the hypothesis has been falsified as a general rule by a series of multiple hypotheses experiments.

History and Definition

While physiologists have traditionally assumed that acclimation is beneficial (or explicitly defined it as such), criticism of the adaptationist program by Stephen Jay Gould and Richard Lewontin led to a call for increased robustness in testing adaptationist hypotheses. The initial definition of the Beneficial Acclimation Hypothesis, as published in 1994 in the Proceedings of the National Academy of Sciences by Leroi et al., is that

“acclimation to a particular environment gives an organism a performance advantage in that environment over another organism that has not had the opportunity to acclimate to that particular environment.”

This definition was further reworked in an article in American Zoologist 1999 by Raymond B. Huey, David Berrigan, George W. Gilchrist, and Jon C. Herron. They determined that, following Platt’s strong inference approach, multiple competing hypotheses were needed to properly assess beneficial acclimation (see picture at right). These included:

1. Beneficial Acclimation. Acclimating to a particular environment confers fitness advantages in that environment.

2. Optimal Developmental Temperature. There is an ideal temperature to develop at so individuals reared at an optimal temperature compete better in all environments.

3. Colder (bigger) Is Better. In ectotherms, individuals reared in colder environments tend to develop to a larger body size. These individuals therefore have a fitness advantage in all environments.

4. Warmer (smaller) Is Better. The inverse of Colder Is Better. Smaller individuals have a fitness advantage.

5. Developmental Buffering. Development temperature does not affect adult fitness.

Experimental Tests

The majority of tests of the Beneficial Adaptation Hypothesis have, following Krogh’s Principle, centered on the model organisms Drosophila melanogaster and Escherichia coli. And more particularly, experimental tests have centered on easily-measured temperature adaptation (although other systems have been studied, see). Of the several experimental tests of the Beneficial Acclimation Hypothesis, the majority have rejected it being true in all cases.

Leroi et al.’s initial experiments, testing only the Beneficial Acclimation Hypothesis and not the subsequent hypotheses developed by Huey et al., were the first to address the issue. Colonies of E. coli were acclimated for seven generations in two different temperature conditions: 32 °C and 41.5 °C. Colonies were then competed against each other at those temperatures (see picture). He found that, agreeing with the Beneficial Acclimation Hypothesis, colonies acclimated at 32 °C competed better at 32 °C. However, at 41.5 °C, colonies acclimated at 32 °C competed better as well which lead to the authors rejecting the generality of beneficial acclimation.

Huey et al. examined four previously-conducted studies, applying the five competing hypotheses, and found that none of the results of the studies could be entirely explained by beneficial acclimation. Instead, a combination of hypotheses were required to explain the observed patterns of acclimation.