Life-history theory predicts that competition and trade-offs should arise between two processes if they depend on the allocation of the same limited resources. The ubiquity of predators imposes selection pressures on resource allocation and organismal physiology: it has been shown, for example, that acquiring a high level of body reserves, i.e. larger body mass, incurs costs in terms of reduced take-off speed and maneuverability when escaping predators (Krams, 2002, and references therein). However, animals must generally maintain high levels of energy reserves because they are supposed to serve as an ‘energetic buffer’ against the unpredictability of food access and death by starvation. Hence, regulation of body mass has been generally conceptualized as a trade-off between starvation risk and predation risk.
In a recent review paper, John Speakman (2018) proposed a novel hypothesis on the regulation of adiposity and body mass. Speakman agrees with the idea that the risk of predation selects for low adiposity. However, he concludes that evidence is generally missing to support the risk of starvation as a selective force against low adiposity. Speakman suggests that the risk of disease and the need to survive periods of pathogen-induced anorexia are the main forces selecting for high adiposity. Speakman provides evidence for pathogen-induced anorexia and shows that individuals carrying more fat have a better chance of survival when infected, which provides the basis for the obesity paradox (reviewed in Speakman, 2018).
Overall, we support the novel hypothesis proposed by Speakman. However, it is important to note that fat reserves consist not merely of fat. Adipose tissue is known to be the source of myriad signaling molecules affecting life-history decisions (Wells, 2009). While subcutaneous body fat is viewed as relatively harmless, abdominal or visceral fat is stored around the inner organs and is associated with non-infectious inflammation. Visceral fat contributes to metabolic diseases such as cardiovascular disease and type 2 diabetes as well as mental disorders such as depression (e.g. Rantala et al., 2018). Visceral fat increases the concentration of inflammatory cytokines, which provides a potential mechanistic link between visceral fat and systemic inflammation (Fontana et al., 2007). Thus, metabolism of subcutaneous and visceral fat produces different metabolites and visceral fat is generally considered to be harmful (Qiang et al., 2016).
Nevertheless, both subcutaneous and visceral fat can be used as energy sources during famine, which causes questions about the evolutionary role and functions of visceral fat. This is of crucial importance for the model suggested by Speakman. Interestingly, increasing body mass index (BMI) is associated with increasing body fat content; for any given BMI value, however, people in densely populated South Asian countries tend to have substantially more visceral fat than Europeans (Rush et al., 2004). South Asians have been historically exposed both to regular famines (Fagan, 1999) and to enduring heat stress that may contribute to the spread of infectious diseases (Dunn et al., 2010). Speakman admits that food shortage potentially compromises immune function, increasing susceptibility to disease. Importantly, chronic stress induced by population density and famine may down-regulate testosterone, which is associated with the accumulation of visceral fat (Björntorp, 1991). Therefore, local climate, pathogen prevalence, high density of people and regular famines might have favored increased visceral adiposity in South Asian populations as an adaptation against infections, especially gut-borne ones as suggested by Wells (2009).
We highlight that ecologists and physiologists have to distinguish between subcutaneous fat and visceral fat because the former may generally function as a source of energy while the latter not only accumulates energy for an organism but may also provide protection against parasitic worms, protozoans and bacteria. The mechanism by which visceral fat does this is through toxic compounds and/or by increasing general levels of oxidative stress. However, this may cause phenotypic and functional damage to self-tissue. We suggest that subcutaneous and visceral fat need to be viewed separately in Speakman's model.
