doi: 10.1161/01.CIR.0000159348.91164.6F
(Circulation. 2005;111:e166.)
© 2005 American Heart Association, Inc.
Correspondence |
Letter Regarding Article by Khan et al, "Predictive Adaptive Responses to Maternal High-Fat Diet Prevent Endothelial Dysfunction but Not Hypertension in Adult Rat Offspring"
Department of Biology, IFM, University of Linköping, Linköping, Sweden, jordi{at}ifm.liu.se
Studying the consequences of a maternal high-fat diet in rats, Khan et al1 conclude that "predictive adaptive responses" prevent endothelial dysfunction and reduce heart rate in the offspring if they are raised on the same high-fat diet. The article, relevant as it is in understanding the mechanisms of fetal programming, fails when generalizing the responses observed as "predictive adaptations." The concept of adaptation itself has long been a matter of debate between evolutionary biologists and physiologists.2,3 Khan et al1 side with a conventional and well-accepted interpretation in which adaptive responses (or adaptations) are those that confer survival benefit to the fetus when facing an adverse uterine environment, namely poor prenatal nutrition. Khan et al1 go a step further, however, in identifying such adaptive responses as predictive of the future postnatal environment, implicitly indicating that the responses take place to confront and survive a postnatal nutritional hardship. Obviously, this is not the case; the fetus is only responsive to prevailing uterine conditions and cannot respond to possible future challenges. We consider the concept of "predictive adaptive response" to be flawed and therefore inappropriate because it obviates the need of a stimulus to trigger a response. The unfortunate term has parallels with the word "preadaptation," which implies that evolution is forward looking.4 Combining adaptive/adaptation with inappropriate prefixes or adjectives may erode the specific evolutionary or physiological meaning and at worst put a teleological spell on our thinking about the concepts. The predictive adaptive responses reported by Khan et al1 qualify well as a programming mechanism, as defined by Lucas5: "programming occurs when an early stimulus or insult, operating at a critical or sensitive period, results in a permanent or long-term change in the structure or function of the organism." For scientific discussion, the concepts of study need to be defined clearly. Thus, the introduction of new terminology requires proper formalization and general acceptance. We feel that "predictive adaptation" is not up to the challenge and should be avoided.
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- Khan I, Dekou V, Hanson M, Poston L, Taylor P. Predictive adaptive responses to maternal high-fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation. 2004; 110: 1097–1102.
[Abstract/Free Full Text]
- Reeve HK, Sherman PW. Adaptation and the goals of evolutionary research. Q Rev Biol. 1993; 68: 1–32.[CrossRef]
- Bennett AF. Adaptation and the evolution of physiological characters. In: Dantzler WH, ed. Handbook of Physiology. Section 13: Comparative Physiology. New York, NY: Oxford University Press; 1997: 3–16.
- Ghiselin MT. On semantic pitfalls of biological adaptation. Philos Sci. 1966; 33: 147–153.[CrossRef]
- Lucas A. Programming by early nutrition in man. In: The Childhood Environment and Adult Disease. Ciba Foundation Symposium 156. Chichester, UK: John Wiley & Sons; 1991: 38–55.
Response
Maternal and Fetal Research Unit, Division of Reproductive Health, Endocrinology, and Development, King’s College, London, UK
Centre for Developmental Origins of Adulthood Disease, Southampton University, Southampton, UK
Drs Altimiras and Milberg question our use of the term "predictive adaptive responses" in describing the developmental consequences of a maternal high-fat diet in rats in which offspring raised on a control diet developed endothelial dysfunction, whereas offspring raised on the maternal diet did not.1
We would like to point out that the concept of predictive adaptive responses has previously been formalized.2–5 Indeed, it is widely accepted in developmental biology that adaptive plastic responses during early development have consequences for function in later life. The correspondents confuse adaptations with adaptive responses. The former can only be deduced when shown to increase Darwinian fitness. Hence, the concept of predictive adaptive responses was proposed because the embryo or fetus cannot anticipate whether the response will be appropriate, let alone whether it could be a valuable adaptation for the species.
Of course the fetus cannot respond to future challenges, but it can use signals or cues (eg, nutritional, endocrine) from the mother and the placenta to change its phenotype. If this process turns out to be beneficial as a prediction of its later environment, then it will be retained by evolution. We stress that the prediction is not only in relation to a poor postnatal environment, as our study demonstrated,1 nor can it be seen as a fetal adaptation. This is particularly true when the response is induced by an epigenetic change in early development. The concept should not be confused with that of "preadaptation." The more formal exploration of the concept involves cues in addition to nutrition. It is an extension of the concept of "maternal effects," effects that are well rehearsed in evolutionary biology.
The predictive adaptive responses concept shares some similarities with "programming," a term coined by Jacob and Monod in 1961 that refers to the genetic program of growth. We prefer not to use the term programming because it seems too deterministic. New concepts and theories permit a synthesis of current data and ideas and also suggest testable hypotheses. This is the case for the predictive adaptive responses concept. Furthermore, its relevance to human medicine, especially in view of the consequences of nutritional and energy balance transitions occurring in many parts of the world, suggests avenues for public health interventions. For this reason alone, this concept cannot be ignored.
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References |
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TopReferencesReferences |
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- Khan IY, Dekou V, Hanson M, Poston L, Taylor PD. Predictive adaptive responses to maternal high fat diet prevent endothelial dysfunction but not hypertension in adult rat offspring. Circulation. 2004; 110: 1097–1102.
[Abstract/Free Full Text]
- Gluckman PD, Hanson MA. Living with the past: evolution, development, and patterns of disease. Science. 2004; 305: 1733–1736.
[Abstract/Free Full Text]
- Gluckman PD, Hanson MA. Developmental origins of disease paradigm: a mechanistic and evolutionary perspective. Pediatr Res. 2004; 56: 311–317.[Medline]
[Order article via Infotrieve]
- Gluckman PD, Hanson MA. The developmental origins of the metabolic syndrome. Trends Endocrinol Metab. 2004; 15: 183–187.[CrossRef][Medline]
[Order article via Infotrieve]
- Gluckman P, Hanson M. The Fetal Matrix: Evolution, Development and Disease. Cambridge, UK: Cambridge University Press; 2004.
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Circulation 2005 111: 1455.[Full Text]
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