The beneficial acclimation hypothesis (BAH) is the

physiological Physiology (; ) is the scientific study of functions and mechanisms in a living system. As a sub-discipline of biology, physiology focuses on how organisms, organ systems, individual organs, cells, and biomolecules carry out the chemical ...

hypothesis A hypothesis (plural hypotheses) is a proposed explanation for a phenomenon. For a hypothesis to be a scientific hypothesis, the scientific method requires that one can test it. Scientists generally base scientific hypotheses on previous obse ...

that acclimating to a particular environment (usually thermal) provides an

organism In biology, an organism () is any living system that functions as an individual entity. All organisms are composed of cells (cell theory). Organisms are classified by taxonomy into groups such as multicellular animals, plants, and ...

with advantages in that environment. First formally tested by

Armand Marie Leroi Armand Marie Leroi (born 16 July 1964) is a New Zealand-born Dutch author, broadcaster, and professor of evolutionary developmental biology at Imperial College in London. He received the Guardian First Book Award in 2004 for his book ''Mutant ...

, Albert Bennett, and

Richard Lenski Richard Eimer Lenski (born August 13, 1956) is an American evolutionary biologist, a Hannah Distinguished Professor of Microbial Ecology at Michigan State University. He is a member of the National Academy of Sciences and a MacArthur fellow. ...

in 1994, it has however been a central assumption in historical physiological work that acclimation is

adaptive Adaptation, in biology, is the process or trait by which organisms or population better match their environment Adaptation may also refer to: Arts * Adaptation (arts), a transfer of a work of art from one medium to another ** Film adaptation, a ...

. Further refined by

Raymond B. Huey Raymond Brunson Huey (born 14 September 1944) is a biologist specializing in evolutionary physiology. He has taught at the University of Washington (UW), and he earned his Ph.D. in biology at Harvard University under E. E. Williams. He has recentl ...

and David Berrigan under the

strong inference In philosophy of science, strong inference is a model of scientific inquiry that emphasizes the need for alternative hypotheses, rather than a single hypothesis to avoid confirmation bias. The term "strong inference" was coined by John R. Pla ...

approach, the hypothesis has been

falsified Falsifiability is a standard of evaluation of scientific theories and hypotheses that was introduced by the philosopher of science Karl Popper in his book ''The Logic of Scientific Discovery'' (1934). He proposed it as the cornerstone of a sol ...

as a general rule by a series of multiple hypotheses experiments.

History and definition

Acclimation is a set of

responses that occurs during an individual's lifetime to chronic laboratory-induced environmental conditions (in contrast to

acclimatization Acclimatization or acclimatisation ( also called acclimation or acclimatation) is the process in which an individual organism adjusts to a change in its environment (such as a change in altitude, temperature, humidity, photoperiod, or pH), ...

). It is one component of

adaptation In biology, adaptation has three related meanings. Firstly, it is the dynamic evolutionary process of natural selection that fits organisms to their environment, enhancing their evolutionary fitness. Secondly, it is a state reached by the po ...

. While physiologists have traditionally assumed that acclimation is beneficial (or explicitly defined it as such), criticism of the adaptationist program by

Stephen Jay Gould Stephen Jay Gould (; September 10, 1941 – May 20, 2002) was an American paleontologist, evolutionary biologist, and historian of science. He was one of the most influential and widely read authors of popular science of his generation. Gould sp ...

and

Richard Lewontin Richard Charles Lewontin (March 29, 1929 – July 4, 2021) was an American evolutionary biologist, mathematician, geneticist, and social commentator. A leader in developing the mathematical basis of population genetics and evolutionary theory, h ...

led to a call for increased robustness in testing

adaptationist Adaptationism (also known as functionalism) is the Darwinian view that many physical and psychological traits of organisms are evolved adaptations. Pan-adaptationism is the strong form of this, deriving from the early 20th century modern synthesis ...

hypotheses.Gould, S.J and Lewontin, R.C. (1979). ''The Spandrels of San Marco and the Panglossian Paradigm: A Critique of the Adaptationist Programme.'' Proc. Roy. Soc. London B 205. pp. 581-598. The initial definition of the BAH, 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.Huey, R. B., Berrigan, D., Gilchrist, G.W. and Herron, J.C. (1999). ''Testing the Adaptive Significance of Acclimation: A Strong Inference Approach.'' Am. Zool. 39. pp. 323-336 They determined that, following Platt's

approach, multiple competing hypotheses were needed to properly assess beneficial acclimation. 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 An ectotherm (from the Greek () "outside" and () "heat") is an organism in which internal physiological sources of heat are of relatively small or of quite negligible importance in controlling body temperature.Davenport, John. Animal Life a ...
, 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 Krogh's principle states that "for such a large number of problems there will be some animal of choice, or a few such animals, on which it can be most conveniently studied." This concept is central to those disciplines of biology that rely on the c ...

, centered on the model organisms ''

Drosophila melanogaster ''Drosophila melanogaster'' is a species of fly (the taxonomic order Diptera) in the family Drosophilidae. The species is often referred to as the fruit fly or lesser fruit fly, or less commonly the "vinegar fly" or "pomace fly". Starting with Ch ...

'' and ''

Escherichia coli ''Escherichia coli'' (),Wells, J. C. (2000) Longman Pronunciation Dictionary. Harlow ngland Pearson Education Ltd. also known as ''E. coli'' (), is a Gram-negative, facultative anaerobic, rod-shaped, coliform bacterium of the genus ''Escher ...

''. More specifically, experimental tests have centered on easily measured temperature adaptation (although other systems have been studied; see Kristensen, T.N., Hoffmann, A. A., Overgaard, J., Sorensen, J.G., Hallas, R., and Loeschke, V. (2008). ''Costs and Benefits of Cold Acclimation in Field-Released Drosophila.'' PNAS. 105 (1). pp. 216-221.3.). Of the several experimental tests of the beneficial acclimation hypothesis, most have rejected it as a universal rule (see reviews Woods, H.A. and Harrison, J.F. (2002). ''Interpreting Rejections of the Beneficial Acclimation Hypothesis: When is Physiological Plasticity Adaptive?'' Evolution. 56(9). pp. 1863-1866.Wilson, R. S. and Franklin, C. E. (2002).'' Testing the Beneficial Acclimation Hypothesis.'' TREE. 17(2). pp. 66-70.). Initial experiments by Leroi ''et al.'', the first scientists to address this problem, tested only the beneficial acclimation hypothesis and not the subsequent hypotheses developed by Huey ''et al.'' 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. 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. This led to the authors' rejection of 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.

Why acclimation is not beneficial

While it seems intuitive that acclimation would provide benefits to individuals, the majority of empirical tests of the hypothesis have rejected its general application. Why then is acclimation not beneficial? H. Arthur Woods and Jon F. Harrison examined the possible reasons in a 2002 ''

Evolution Evolution is change in the heritable characteristics of biological populations over successive generations. These characteristics are the expressions of genes, which are passed on from parent to offspring during reproduction. Variation ...

'' paper. They suggested that:

1. The timescale of
adaptation In biology, adaptation has three related meanings. Firstly, it is the dynamic evolutionary process of natural selection that fits organisms to their environment, enhancing their evolutionary fitness. Secondly, it is a state reached by the po ...
is much longer than that of environmental variation.

2. Environmental cues for timing of adaptive acclimation are unreliable.

3. It may cost more to adapt than not to.

4.
Migration Migration, migratory, or migrate may refer to: Human migration * Human migration, physical movement by humans from one region to another ** International migration, when peoples cross state boundaries and stay in the host state for some minimum le ...
by adjacent populations may swamp out
genes In biology, the word gene (from , ; "...Wilhelm Johannsen coined the word gene to describe the Mendelian units of heredity..." meaning ''generation'' or ''birth'' or ''gender'') can have several different meanings. The Mendelian gene is a ba ...
for adaptive acclimation.

Criticism

In response to continuing rejections of the beneficial acclimation hypothesis, a number of common criticisms of experimental tests have been developed:

1. The majority of studies have actually been examining developmental acclimation. That is, rather than acclimating an adult individual and testing, they suggest that developmental switches triggered by particular temperatures result in a different mechanism of acclimation. More recently, it has been found that adult acclimation and developmental acclimation lead to support for different hypotheses.

2. Most studies have included stressful temperatures. Acclimation to those temperatures may decrease fitness in an individual.

3. Finally, a variety of traits are examined in these studies that may only be indirectly linked to fitness. For example, examining
longevity The word " longevity" is sometimes used as a synonym for "life expectancy" in demography. However, the term ''longevity'' is sometimes meant to refer only to especially long-lived members of a population, whereas ''life expectancy'' is always d ...
as a fitness measure in ''D. melanogaster'' may be irrelevant since
fertility Fertility is the capability to produce offspring through reproduction following the onset of sexual maturity. The fertility rate is the average number of children born by a female during her lifetime and is quantified demographically. Fertili ...
declines rapidly with age in this species.

Current state

The majority of studies have concluded the beneficial acclimation hypothesis is not true in all cases, and that alternate hypotheses should be tested. In addition to this, recent studies of the hypothesis have provided additional complications, such as trade-offs evident only in field environments and interactions with behavior and life history traits.Deere, J.A. and Chown, S.L. (2006). ''Testing the Beneficial Acclimation Hypothesis and Its Alternatives for Locomotor Performance.'' Am. Nat. 168(5)Marais, E. and Chown, S.L. (2008). ''Beneficial Acclimation and the Bogert Effect.'' Ecol. Lett. 11. pp. 1027:1036. The study of developmental and

phenotypic plasticity Phenotypic plasticity refers to some of the changes in an organism's behavior, morphology and physiology in response to a unique environment. Fundamental to the way in which organisms cope with environmental variation, phenotypic plasticity encompa ...

continues.

References