Theoretical contributions, considerations and limitations

6.2.1. Carotenoids cue health

In understanding the evolutionary relevance of a preference for skin yellowness, the work contained in this thesis suggested that skin yellowness reflects more than carotenoid

108 consumption, and that skin colouration from carotenoids can act as a cue to the bearer’s health.

Findings from Chapter 5 showed that whilst skin yellowness reflected participants’ health in the prior eight weeks, it was not reliable in indicating current health status (or that of the prior week). This idea, that skin carotenoids do not reflect more immediate changes in ill health was supported by findings from Chapter 5 which showed no clear evidence of skin colour changes consistent with carotenoid loss. Chapter 5 was instrumental however in providing evidence that skin yellowness reflected plasma carotenoids at baseline. Findings from the two chapters together provide convincing evidence that lasting changes in carotenoid availability will be reflected in skin colour, reflecting health history of an individual on a scale of weeks to months.

Findings from Chapter 3 suggest that carotenoid colouration is more relevant to recent experiences than risk factors that are likely to affect future health outcomes. There was no evidence that carotenoid colouration reflected smoker status, body fat, alcohol consumption or exercise habits, but there was evidence of psychological stress in the prior week relating to skin yellowness. Together with findings from Chapter 4, showing symptoms of ill health in the prior two months relate to skin yellowness, this would suggest that there are direct evolutionary benefits to be gained from a preference for skin yellowness e.g. avoiding contagious illness today. Although it remains to be tested whether indirect benefits, in terms of selecting for good genes for health, are to be gained also.

6.2.2. Carotenoids and colour

Throughout this thesis, carotenoid content of skin was inferred from skin colour rather than measured directly. With respect to understanding the evolutionary significance of a

preference for yellowness, and whether it is linked to carotenoids (which was the aim of this thesis), the inference of carotenoids from colour measures is not a limitation. In fact, testing whether skin yellowness related to health was necessary to answer the question of whether skin carotenoids act as a cue to health beyond diet, because judgements of health are based upon the appearance of skin colour. Assessing skin colour in terms of CIE L* a* b* space allowed empirical measurements to be taken which directly relate to the visual appearance of skin colour. It is acknowledged that melanin and blood perfusion or oxygenation status can influence the yellow appearance of skin, but these pigments also contribute to changes in lightness and redness. Consequently, throughout the experimental work presented, any

109 associations found between health and skin yellowness were also explored with reference to these other colour axes. Doing so allowed an inference to be made that the variation in yellowness associated with health in Chapters 3 (stress) and 4 (health history), were most likely to be driven by variation in carotenoid content of skin. Chapter 5, was instrumental in demonstrating that variation in skin yellowness with illness is not always best explained by carotenoids. In Study 6, a drop in blood perfusion or oxygenation more adequately accounted for a drop in skin yellowness witnessed. Such a finding does not compromise the validity of carotenoids as a cue to health because with a shift in oxygenation status of blood, the skin also becomes darker and less red; the colour of blood status will therefore be visibly different from that of carotenoid status. Furthermore, the relationships between blood oxygenation, skin yellowness and health are all positive so contribute in the same direction towards an association between increased yellowness and increased perceived health. The knowledge that other chromophores contribute to skin yellowness, does not then threaten the

interpretation that variation in carotenoid content may act as a cue to health. What this acknowledgment does suggest though is that colour measurements will not be the most accurate way to determine carotenoid levels, and this will add limitations to some of the practical applications arising from the finding that skin carotenoid content is related to health status (see below, section 6.3)

6.2.3. Why are we not bright yellow?

If carotenoid colouration of human skin is a valid reflection of health status, and is deemed more attractive by others, it is reasonable to ask why we are not brightly coloured, as are carotenoid ornaments of many birds and fish.

Within evolutionary biology there is a distinction between cues and signals (as noted in the introductory chapter: 1.4). Cues are traits (such as skin colour) that are assessed during mate choice and influence the mating decision. If this trait is modified to serve a purpose of

communicating mate quality to others, it becomes a signal (Candolin, 2003). Often a trait will be exaggerated to a point where it becomes detrimental to survival but increases

attractiveness to the opposite sex. Bright feathers and fins for example will increase predation risk; and carotenoids displayed in feathers will become unavailable for physiological

functions, but bright ornaments will increase mating success and therefore there is an evolutionary pressure for them to continue to become brighter. Cues, meanwhile can be maintained due to other selection pressures, carotenoid colouration of human skin for

110 example will be maintained as a cue simply because consumption of carotenoids afford physiological benefits and excess carotenoids will passively colour the skin.

If carotenoid colouration had evolved as a signal to communicate health status we may expect variation in colour to be greatest in body locations most readily observable (e.g. the face). Here, as in other studies (Stahl et al., 1998; Alaluf, Heinrich, et al., 2002) we find greatest variation in yellowness at sweaty regions (e.g. palm and forehead). This would suggest carotenoid colour evolved simply as a potential cue that arose as a by-product of physiological processes.

Perceptual studies have demonstrated that there is a limit to the degree of yellowness which others find attractive or healthy in appearance. In interactive trials, when given the

opportunity to optimise apparent health by digitally altering skin colour; participants reliably add yellowness or carotenoid colour to stimuli, but they do not apply the maximum available colour (Stephen et al., 2011; Whitehead et al., 2013). There is a limit then to the positive relationship between skin yellowness and perceived health. This may be constrained by a negative selection pressure associated with a high degree of skin yellowness.

Jaundice is a yellowing of the skin, sclera and mucosa that occurs as with a build-up of bilirubin: a breakdown product of blood cells. Spectrophotometrically the colour of bilirubin is very similar to beta-carotene and in normal healthy individuals, bilirubin acts as an

endogenous antioxidant, serving a similar role as carotenoids in the maintenance of health (Neuzil & Stocker, 1994). At normal levels then, bilirubin is unlikely to compromise the validity of the relationship between skin yellowness and health. Jaundice present only when there are abnormally high levels of bilirubin and in adults can be a sign of serious health complications such as liver dysfunction, pancreatitis and biliary tract infection (Roche & Kobos, 2004). This association between very high levels of skin yellowness and serious health problems, could reasonably act as a negative selection pressure for ever increasing skin yellowness. This negative selection pressure would have prevented carotenoid colouration of human skin from evolving from a cue to a signal of health.

It is important to note that although participants will not maximise yellowness to optimise apparent health on interactive trials; in studies of natural images, a linear relationship does exist between skin yellowness and apparent health (Henderson et al., 2016; Scott et al., 2010; Stephen et al., 2012). Such studies are invariably conducted with stimuli of young healthy adults where examples of extreme yellowness associated with jaundice is not present. Given

111 that the studies within the present thesis were also restricted to young and healthy samples, the use of linear statistics throughout was deemed appropriate.