Basis for the gain and subsequent dilution of epidermal pigmentation during human evolution: The barrier and metabolic conservation hypotheses revisited.
The evolution of human skin pigmentation must address both the initial evolution of intense epidermal pigmentation in hominins, and its subsequent dilution in modern humans. While many authorities believe that epidermal pigmentation evolved to protect against either ultraviolet B (UV-B) irradiation-induced mutagenesis or folic acid photolysis, we hypothesize that pigmentation augmented the epidermal barriers by shifting the UV-B dose-response curve from toxic to beneficial. Whereas erythemogenic UV-B doses produce apoptosis and cell death, suberythemogenic doses benefit permeability and antimicrobial function. Heavily melanized melanocytes acidify the outer epidermis and emit paracrine signals that augment barrier competence. Modern humans, residing in the cooler, wetter climes of south-central Europe and Asia, initially retained substantial pigmentation. While their outdoor lifestyles still permitted sufficient cutaneous vitamin D3 (VD3) synthesis, their marginal nutritional status, coupled with cold-induced caloric needs, selected for moderate pigment reductions that diverted limited nutritional resources towards more urgent priorities (=metabolic conservation). The further pigment-dilution that evolved as humans reached north-central Europe (i.e., northern France, Germany), likely facilitated cutaneous VD3 synthesis, while also supporting ongoing, nutritional requirements. But at still higher European latitudes where little UV-B breaches the atmosphere (i.e., present-day UK, Scandinavia, Baltic States), pigment dilution alone could not suffice. There, other nonpigment-related mutations evolved to facilitate VD3 production; for example, in the epidermal protein, filaggrin, resulting in reduced levels of its distal metabolite, trans-urocanic acid, a potent UV-B chromophore. Thus, changes in human pigmentation reflect a complex interplay between latitude, climate, diet, lifestyle, and shifting metabolic priorities.
Department of Veterans Affairs Medical Center, Dermatology Service, University of California San Francisco, California. Eliasp@derm.ucsf.edu.|Department of Dermatology, Dermatology Service, University of California San Francisco, California. Eliasp@derm.ucsf.edu.
Peter M
PM
Elias
Department of Dermatology, University of California, San Francisco, California.|Department of Pediatrics, University of California, San Francisco, California.
Mary L
ML
Williams
D000328:Adult; D000885:Anthropology, Physical; D005075:Biological Evolution; D005260:Female; D000091344:Filaggrin Proteins; D005492:Folic Acid / Q000378:metabolism; D006801:Humans; D008297:Male; D008543:Melanins / Q000378:metabolism* / Q000502:physiology*; D008544:Melanocytes / Q000502:physiology; D012880:Skin Pigmentation / Q000502:physiology*; D014466:Ultraviolet Rays; D014807:Vitamin D / Q000378:metabolism
C000717249:FLG protein, human; D000091344:Filaggrin Proteins; D008543:Melanins; D014807:Vitamin D; D005492:Folic Acid
UV-B; barrier function; filaggrin; melanocytes; metabolic conservation; pH; pigmentation; urocanic acid; vitamin D