A life history perspective on skin cancer and the evolution of skin pigmentation

Abstract

The ancestral state of human skin pigmentation evolved in response to high ultraviolet radiation (UVR) stress. Some argue that pigmentation evolved to limit folate photolysis, therein limiting neural tube defects. Pigmentation also protects against sunburn which decreases the efficiency of sweating and potentiates skin infection. Pigmentation increases the efficacy of skin as a barrier to infection. Skin cancer has been rejected or minimized as a selective pressure because it is believed to have little or no effect on mortality during reproductive years. This argument ignores evidence of human longevity as a derived life history trait and the adaptive value of investment in offspring and kin, particularly during the post-reproductive lifespan. Opponents argue that lifespan in prehistoric hunter-gatherers was too short to be relevant to the evolution of skin pigmentation. This argument is flawed in that it relies on estimates of longevity at birth rather than adolescence. When appropriate estimates are used, it is clear that human longevity has a deep evolutionary history. We use a life history perspective to demonstrate the value of skin pigmentation as an adaptation to skin cancer with the following points: UVR exposure increases dysregulation of gene expression in skin cells leading to immortal cell lines; cutaneous malignant melanoma (CMM) affects individuals throughout reproductive years; and lifespan was longer than has previously been acknowledged, providing the opportunity for kin selection. This hypothesis is not at odds with the folate or barrier hypotheses. We stress that the evolution of skin pigmentation is complex and is an ongoing process.

UV‐associated decline in systemic folate: implications for human nutrigenetics, health, and evolutionary processes

“…Globally, the report indicates that the T allele is at relatively low frequency in Africa and S Asia compared to Europe, Asia, and the Americas. This tends to support the above hypothesized model linking latitude/UV, folate and MTHFR genotype (Yafei et al, 2012) The precise molecular mechanisms involved in this evolutionary model remain unclear, but one area of future study should focus on whether the potentially greater amount of labile folate in TT individuals is being routed to repair UV-damage, and whether such a mechanism could fit this evolutionary hypothesis, an area where opinion is likely to be divided (Osborne & Hames, 2014). Figure 3 integrates these ideas, including the present observations, into a simplified model.…”

Absence of evidence or evidence of absence? A discussion on paleoepidemiology of neoplasms with contributions from two Portuguese human skeletal reference collections (19th–20th century)

“…Lieverse et al (2014) and Chamberlain (2006: 53) note that there is "no clear historical evidence that maximum lifespan was reduced in earlier historical times". Moreover, research in modern hunter-gatherers suggests that "longevity has a deep human history" (Osborne and Hames, 2014). As such, one might expect to encounter cancer cases in this group of individuals that, not so rarely, had longer longevity.…”

Telomere Length and the Cancer–Atherosclerosis Trade-Off

“…The idea that melanoma acted as an evolutionary selective force in ancestral humans has been challenged based on the assumption that the life span of ancestral humans was relatively short, and melanoma principally strikes individuals during the post-reproductive years [ 67 ]. However, this view does not consider that once surviving childhood, ancestral humans lived much longer than originally thought, and considerable evidence indicates that melanoma afflicts adults throughout the life course, including young adulthood [ 68 ]. One mechanism whereby individuals with light skin might have attenuated the risk of melanoma is by shortening their telomeres through polygenic adaptation, thereby explaining in part the shorter LTL in individuals of European ancestry than in sub-Saharan Africans [ 22 ].…”