In a recent paper, I suggested that the supposed ‘predation–starvation’ trade-off model for the regulation of body fat has rather scant evidence to support the ‘starvation’ side of the trade-off. Instead of starvation risk, I suggested that a likely evolutionary factor driving up levels of stored fat is the risk of infectious disease, and the need to survive through periods of pathogen-induced anorexia (Speakman, 2018). I am glad that in their recent correspondence Krams et al. (2018) state that ‘Overall we support the novel hypothesis proposed by Speakman’. They then go on to highlight a potentially important distinction that my paper did not address: the lack of functional equivalence of different fat depots.
It is well established that in humans, and other animals, white adipose tissue is distributed in different depots. A distinction is often made between visceral fat, located around the viscera and vital organs, and subcutaneous fat, which is located outside the peritoneum. In terms of their role as stores of energy, these different depots are functionally equal, and in my ‘predation–disease’ trade-off model, as well as the earlier predation–starvation models (McNamara and Houston, 1990), no distinction was made between these stores. Krams et al. (2018) suggest this is a mistake and that these depots are not functionally equivalent in terms of their consequences. Visceral fat in particular is regarded as a major contributor to metabolic diseases, such as type 2 diabetes and cardiovascular disease, while subcutaneous fat is considered to be relatively benign.
This raises the interesting question of why individuals would ever choose (evolutionarily) to store fat viscerally if it has these disadvantageous consequences. This is an interesting question. Krams et al. (2018) point out that at any given body fatness, South Asians store more fat viscerally than Caucasians (Europeans). They suggest this is because such populations have high population densities leading to chronic stress, have historically been exposed to regular famines and have high levels of infectious disease. Together, they suggest these factors may have favoured greater visceral adiposity because it provides a defence against ‘parasitic worms, protozoans and bacteria’ through the production of ‘toxic compounds and/or by increasing general levels of oxidative stress’. These statements are not referenced, but appear to originate in Wells (2009), which is cited elsewhere in their paper.
While there is possibly a difference between Caucasian and South Asian populations in exposure to pathogens, there is little evidence to support the suggestion that these populations have historically endured greater levels of famine than populations in Europe (see Speakman, 2006). In addition, until recently (post-agricultural revolution), populations of humans were universally quite small, so stress caused by high population density also seems an unlikely evolutionarily important factor.
An additional (or alternative) factor to pathogen exposure driving the difference in the distribution patterns of fat storage between South Asians and Caucasians may be the ambient temperatures they experience (Pond, 1992). As I noted in my disease–predation trade-off paper (Speakman, 2018), fat serves not only as a store of energy: by virtue of its low water content, fat also has a lower thermal conductivity than lean tissue (Cohen, 1977). Hence, if distributed subcutaneously, it provides a barrier to heat loss. This function of the subcutaneous fat layer in cetaceans (or blubber) has been known for many decades. For example, in the novel Moby Dick, written in 1851, Herman Melville wrote ‘For the whale is indeed wrapped up in his blubber as in a real blanket… It is by reason of this cosy blanketing, that the whale is enabled to keep himself comfortable in all weathers, in all seas, times, and tides’. In humans, subcutaneous fat seems to play a similar role. Individuals with greater adiposity cool down more slowly when immersed in cool water, and do not need to elevate their metabolic rate as much to defend this slower cooling rate. However, a thick insulative layer of fat that retards heat loss in the cold may restrict the capacity to lose heat in hot conditions. As the capacity for heat dissipation may be an important limiting factor in endotherms (Speakman and Krol, 2010), a thick layer of subcutaneous fat may be a disadvantage in many circumstances. It has been suggested that the distribution of fat stores in tropical animals may reflect these heat dissipation issues (Pond, 1992). Humans living in the tropics may also redistribute their fat stores away from the subcutaneous fat, and into visceral fat depots to facilitate heat loss. This would also then explain why visceral obesity is an issue not only in South Asian countries but also across India, the Middle East and North Africa.
Overall there are probably adaptive reasons explaining the distribution of body fat in humans, and in modern societies, where humans live long enough to develop metabolic disorders, these differences may have important downstream consequences for differential susceptibility to metabolic disease. This is a valid question and Krams et al. (2018) are correct in highlighting it. However, as they admit, as regards energy storage, the subcutaneous and visceral stores are functionally equivalent, and hence the distribution issue is separate from the question of regulation of the total amount of fat to be stored, which was the primary question addressed in my previous paper (Speakman, 2018). This separation is emphasized by the fact the single nucleotide polymorphisms (SNPs) that are linked to fat storage level (body mass index: e.g. Locke et al., 2015) occur in a largely non-overlapping set of genes to those SNPs associated with fat distribution (waist to hip ratio: e.g. Held et al., 2010).
