Review of Jonathan CK Wells’s The EvolutionaryBiology of Human Body Fatness: Thrift and Control(Cambridge: Cambridge University Press, 2010)

Jack Baker

Published online: 9 November 2011# Springer Science+Business Media, LLC 2011

Keywords Adiposity . Human body fat . Evolutionary biology

In The Evolutionary Biology of Human Body Fatness: Thrift and Control, readers ofHuman Nature will find a highly readable account of contemporary bioanthropo-logical approaches to understanding the ecology and evolution of human adiposity.Although the book provides an admirably comprehensive review of the literature onhuman body fat variation, especially with respect to the developmental originsthereof (chapters 4 and 5), its main thesis is likely to be controversial among humanbiologists and paleoanthropologists alike. Wells establishes this thesis, that humanadipose tissue biology was as crucial to the origin of Homo sapiens as long-acceptedtraits such as large brains, bipedalism, or language/culture, early in the volume:

without substantial refinement of hominin adipose tissue biology, modernhumans would never have come to exist (p. xi).

and

human adipose tissue biology is as much a hallmark of our species as are othertraits long considered peculiarly human, such as bipedalism, large brain size,and complex social behavior (p. 14).

Paleoanthropologists in particular will likely be skeptical of the importance ofadipose tissue to human origins. To garner support for this intriguing idea, Wellsmust establish that specific aspects of human adipose tissue biology are uniquelyhuman, occur in response to specific aspects of the human evolutionary niche, and atleast plausibly increase the fitness of organisms bearing them within theseenvironments (Williams 1966). This review discusses how well Wells achieves

Hum Nat (2011) 22:439–443DOI 10.1007/s12110-011-9124-6

J. Baker (*)Geospatial and Population Studies and the Department of Anthropology, 1 University of NewMexico, MSC06 3510, Albuquerque, NM 87131, USAe-mail: kali@unm.edu

these goals from the point of view of an evolutionary ecologist with similar interestsin human growth, body composition, and evolution.

Wells adopts the four-cause framework of Niko Tinbergen early on, attempting tolink potentially unique aspects of human adipose tissue physiology to proximate(chapters 1–3), ultimate (chapters 5–7), developmental (chapters 4 and 5), andlineage-specific (chapters 8 and 9) factors. For Wells, two specific aspects of humanadiposity merit consideration as unique, derived traits that are intimately linked tohuman origins: (a) sexually dimorphic patterns of fat deposition and (b) an ability toadaptively modulate life-long adiposity patterns in response to early-life exposuresthrough the mechanism of developmental induction. Evidence is cited in an attemptto make plausible links between these characteristics and likely fitness-enhancements within an emerging human species faced with novel environmentalchallenges as they spread out of Africa and into novel terrestrial ecologies.

Wells’s argument that sexually dimorphic patterns of human fat storage areunique and functionally related to specific aspects of the ancestral human niche iscompelling. The storage of adipose tissue in specific anatomical depots is not uniqueto humans,1 but Wells reviews a number of important differences in how humansanatomically store and access body fat that suggest such unique adaptations. Humanmales are known to store relatively more fat abdominally (both intra-abdominallyand in subcutaneous truncal depots), whereas females of our species tend to store fatin the buttocks, hips, and thighs. These gluteofemoral fat cells are known tospecifically and nearly exclusively fund lactation (Rebuffe-Scrive et al. 1985), beinghighly resistant to hydrolysis for other purposes. This conservation of female fatstores to specifically fund lactation suggests the shaping force of natural selectionand resulting adaptive organization (Williams 1966). Wells provides an interestingand novel link between these observations and an ancestral human nichecharacterized by potentially significant risks of energetic shortfalls as Homo sapiensexpanded out of Africa. This niche expansion was most certainly characterized bynew challenges in obtaining resources, but it was also clearly replete with adaptiveopportunities upon which a nascent human species could capitalize. In this context,it is plausible to imagine specific advantages for individuals taking the strategy ofsetting aside a dedicated savings account stored specifically in the gluteofemoral fatdepots of human females, resistant to hydrolysis for purposes other than milkproduction, and aimed at subsidizing lactational dependency among offspring.

Hutchinson’s conception of the “niche” as a set of environments in which aspecific organism may maintain positive population growth (births exceed deaths;Hutchinson 1957) becomes immediately useful. As a trait that plausibly wouldincrease the niche space of Homo sapiens, sexual dimorphism in adipose tissuestorage meets all commonly accepted views of an adaptation (Williams 1966),suggesting a coordinated and likely fitness-enhancing response to a specific adaptivechallenge faced by early humans. Wells’s argument is interesting, non-trivial, andworthy of further consideration. It may yield testable hypotheses that can be falsifiedwith existing or collectable data, and making use of Wells’s suggestion to furtherexplore modeling based in microeconomic theory (such as game theory frameworks)will only further this line of inquiry (see Baker et al. 2008 for a similar view).

1 Many lizards, for example, store fat nearly exclusively in their tails.

440 Hum Nat (2011) 22:439–443

From a classic evolutionary point of view (Williams 1966), Wells’s assertion thatdevelopmental induction of adiposity variation is another unique and adaptive aspectof human adipose tissue biology appears much less certain. It is well-known thathuman body composition is sensitive to exposures early in life (see Wells’s chapters4 and 5, as well as Baker et al. 2008, 2009, 2010), but this plasticity is not unique tohumans. It has been observed in rats, pigs, and sheep (see Gluckman et al. 2007 forone example), making it unclear how such induction could be linked to novel aspectsof the human ancestral niche in the way that fat-patterning seems to be. Moreover,existing theory in evolutionary biology introduced by Levins (1962, 1968) andothers (Williams 1966) has suggested that when organisms are faced with a changingenvironment over either time or space, natural selection will favor allelic variantsthat do best on average across the range of environments experienced by theindividual organism. Such a situation presents no need for intragenerational adaptiveplasticity, and in fact, such a strategy could very well entail significant fitness costswhen environments shift over shorter time scales (Levins 1962, 1968; Williams 1966).Within human biology, a number of conceptual papers have also argued against theplausibility of maximizing fitness by tracking later environments based on early ones,for the same reasons (Jones 2005; Kuzawa 2005; Wells 2007). Such action maysimply constitute following an evolutionary red-herring in a long-lived iteroparousspecies such as humans. Last, in spite of the intriguing nature of the relationshipsWells so thoroughly describes, no study has yet linked such developmental effects topositive increases in lifetime reproductive success,2 and the results of previous effortsat establishing the adaptive plausibility of such shifts have been ambiguous at best(Baker et al. 2010). These conceptual and empirical findings would seem to suggestgreater caution in widespread acceptance of developmental induction of humanadiposity variation as an adaptation in the sense typically used by evolutionarybiologists (Williams 1966). Arguments for maternal mediation of environmentaltracking (Baker et al. 2009; Kuzawa 2005; Wells 2007) are intriguing, but it remains tobe seen whether such relationships reflect adaptation or susceptibility.

On this point, theoretical work by Williams (1966) provides an alternativeexplanation for the presence of developmental plasticity that has been littleappreciated within bioanthropology and may provide additional perspectives onthe developmental induction of adiposity reviewed by Wells. In his classicAdaptation and Natural Selection, Williams (1966:75–78) addressed the develop-mental origins of phenotypes within the adaptationist perspective in detail. He wasresponding to the work of Waddington (1956), who had argued for a significant rolefor what he called genetic assimilation in evolution by natural selection. Waddingtonis well-known for his induction of the bithorax phenotype in D. melanogasterthrough exposure of flies to ether in a controlled environment. The exposure to etherunveiled latent genetic variation that under these specific circumstances resulted inthe development of the bithorax phenotype as a “downstream” effect within a subsetof the laboratory population (Waddington 1956). Williams acknowledges theimportance of this observation in terms of the then-developing concept of the

2 Nor has the inverse—where failure to accomplish such shifts has led to potential fitness deficits—beenestablished.

Hum Nat (2011) 22:439–443 441

reaction norm, but he argues that these responses represent a susceptibility ratherthan an adaptation. As Williams cautions:

It is possible to confuse responses and susceptibilities because both conform toa pattern of cause-effect relationships involving organisms and their environ-ment. It is important that they not be confused because a response shows theunique biological property of adaptive organization, and susceptibility resultsfrom the absence or deficiency of this property (1966:76).

This key point is relevant for interpreting the literature on developmental origins ofadiposity variation in humans. In order to consider any particular instance of induction tobe an adaptive trait, further studies must discriminate between adaptation andsusceptibility associated with latent genetic variation. My point is not that theseresponses do not constitute adaptations; rather, I think that in agreement with Williamsthere should be clear substantiation that the response shows the hallmarks of adaptiveorganization rather than an assumption that all such relationships must reflect adaptationbased in historical natural selection. Although sexually dimorphic patterns of fat storageseem to display some of these hallmarks, I find myself much more skeptical thatdevelopmental induction of overall adiposity shows such hallmarks.

While the tenability of Wells’s thesis may appear mixed, the work should bepraised for its effort to refocus research on describing relationships between uniqueaspects of human physiology and broad patterns of human evolution. It will, nodoubt, encourage further consideration of developmental effects on adiposity froman adaptationist point of view. Furthermore, Wells’s book makes it abundantly clearthat evolutionary and ecological perspectives on adipose tissue and its relationship tohuman origins must move beyond simple metaphors of savings and risk to a morecomprehensive perspective that acknowledges the regulatory role of adipocytes inmanaging other complex aspects of metabolic, immune, and reproductive physiol-ogy. Curiously, to my knowledge it was another Wells, H. Gideon Wells (1940) whowas the first to call for a specific consideration of adipose tissue as an activelyfunctioning organ and a system subject to its own diseases. He found it curious that atissue comprising as much as 1/5 of the average human body should receive so littleattention, being treated as a static substance rather than a dynamic organ—a criticismthat skeletal biologists will no doubt find similar to previous misconceptions aboutthe nature of bone. These conceptual contributions will likely stand the test of timeand will certainly stimulate a renewed interest in, and further research on, theecology of body composition in humans. In this way, Wells’s book makes a welcomelink to recent developments in the physiological ecology in general, aimed atspecifically relating endocrine and metabolic variation to functional regulatory shiftsin life-history (Zera 2009). By stimulating further interest in the complex regulatoryendocrine networks that underlie life-history variation, Wells’s book makes awelcome contribution to human biology.

Building upon strengths of thorough and thoughtful literature review and a desireto link modern adipose tissue biology to our understanding of human evolution, thisbook will both inspire interest and suggest important new pathways of research forthe next generation of bioanthropologists.

442 Hum Nat (2011) 22:439–443

References

Baker, J., Hurtado, A. M., Pearson, O. M., & Jones, T. (2008). Evolutionary medicine in human obesity:developmental adaptive responses in human body composition. In W. Trevathan, E. O. Smith, & J.McKenna (Eds.), Evolutionary medicine and health: New perspectives (pp. 314–324). Oxford: OxfordUniversity Press.

Baker, J., Hurtado, A. M., Hill, K. R., Pearson, O., Jones, T., & Frey, M. (2009). Original research.Developmental plasticity in fat-patterning of Ache children in response to variation interbirthintervals: a preliminary test of the roles of external environment and maternal reproductive strategies.American Journal of Human Biology, 21, 77–83.

Baker, J., Workman, M., Bedrick, E., Frey, M., Hurtado, A. M., & Pearson, O. M. (2010). Brains vsbrawn: an empirical test of Barker’s brain sparing model. American Journal of Human Biology, 22,206–215.

Gluckman, P. D., Lillycrop, K. A., Vickers, M. H., et al. (2007) Metabolic plasticity during mammaliandevelopment is directionally dependent on early nutritional status. Proceedings of the NationalAcademy of Sciences (USA), 104, 12796–800. doi:10.1073_pnas.0705667104

Hutchinson, G. E. (1957). Concluding remarks. Cold Spring Harbor Symposia on Quantitative Biology,22, 415–427.

Jones, J. H. (2005). Fetal programming: adaptive life-history tactics or making the best of a bad start?American Journal of Human Biology, 17, 22–33.

Kuzawa, C. (2005). Fetal origins of developmental plasticity: are fetal cues reliable predictors of futurenutritional environments? American Journal of Human Biology, 17, 5–21.

Levins, R. C. (1962). Theory of fitness in a heterogeneous environment, I: The fitness set and adaptivefunction. American Naturalist, 96(891), 361–373.

Levins, R. C. (1968). Evolution in changing environments: Some theoretical explorations. Princeton, NJ:Princeton University Press.

Rebuffe-Scrive, M., Enk, L., & Crona, N. (1985). Fat cell metabolism in different regions in women:effect of menstrual cycle, pregnancy, and lactation. Journal of Clinical Investigations, 75, 1973–1976.

Waddington, C. H. (1956). Genetic assimilation of the bithorax phenotype. Evolution, 10, 1–13.Wells, H. G. (1940). Adipose tissue: a neglected subject. Journal of the American Medical Association,

114(22), 2177–2183.Wells, J. K. C. (2007). Flaws in the theory of predictive adaptive responses. Trends in Endocrinology and

Metabolism, 18, 331–337.Williams, G. C. (1966). Adaptation and natural selection. Princeton, NJ: Princeton University Press.Zera, A. J. (2009). Wing polymorphism in Gryllus (Orthoptera: Gryllidae): Proximate endocrine, energetic

and biochemical mechanisms underlying morph specialization for flight vs reproduction. In D. W.Whitman & T. N. Ananthakrishan (Eds.), Phenotypic plasticity of insects: Mechanisms andconsequences (pp. 609–654). New York: Science Publishers.

Jack Baker is a senior research scientist in the Geospatial and Population Studies program and adjunctassistant professor of anthropology at the University of New Mexico. His previous research has focusedon the effects of early-life exposures on human body composition from an evolutionary point of view andon methods in statistical demography.

Hum Nat (2011) 22:439–443 443