Positive Selection on a Regulatory Insertion-Deletion Polymorphism in FADS2 Influences Apparent Endogenous Synthesis of Arachidonic Acid

Mol Biol Evol. 2016 Jul;33(7):1726-39. doi: 10.1093/molbev/msw049. Epub 2016 Mar 29.

Abstract

Long chain polyunsaturated fatty acids (LCPUFA) are bioactive components of membrane phospholipids and serve as substrates for signaling molecules. LCPUFA can be obtained directly from animal foods or synthesized endogenously from 18 carbon precursors via the FADS2 coded enzyme. Vegans rely almost exclusively on endogenous synthesis to generate LCPUFA and we hypothesized that an adaptive genetic polymorphism would confer advantage. The rs66698963 polymorphism, a 22-bp insertion-deletion within FADS2, is associated with basal FADS1 expression, and coordinated induction of FADS1 and FADS2 in vitro. Here, we determined rs66698963 genotype frequencies from 234 individuals of a primarily vegetarian Indian population and 311 individuals from the US. A much higher I/I genotype frequency was found in Indians (68%) than in the US (18%). Analysis using 1000 Genomes Project data confirmed our observation, revealing a global I/I genotype of 70% in South Asians, 53% in Africans, 29% in East Asians, and 17% in Europeans. Tests based on population divergence, site frequency spectrum, and long-range haplotype consistently point to positive selection encompassing rs66698963 in South Asian, African, and some East Asian populations. Basal plasma phospholipid arachidonic acid (ARA) status was 8% greater in I/I compared with D/D individuals. The biochemical pathway product-precursor difference, ARA minus linoleic acid, was 31% and 13% greater for I/I and I/D compared with D/D, respectively. This study is consistent with previous in vitro data suggesting that the insertion allele enhances n-6 LCPUFA synthesis and may confer an adaptive advantage in South Asians because of the traditional plant-based diet practice.

Keywords: arachidonic acid; fatty acid desaturases; indel (insertion–deletion); long chain polyunsaturated fatty acids; population divergence.; positive selection.

MeSH terms

  • Adult
  • Alleles
  • Arachidonic Acid / biosynthesis*
  • Arachidonic Acid / genetics
  • Arachidonic Acid / metabolism
  • Databases, Nucleic Acid
  • Delta-5 Fatty Acid Desaturase
  • Fatty Acid Desaturases / genetics*
  • Fatty Acid Desaturases / metabolism
  • Fatty Acids, Unsaturated / genetics
  • Fatty Acids, Unsaturated / metabolism
  • Female
  • Gene Frequency / genetics
  • Genetic Variation
  • Haplotypes
  • Humans
  • INDEL Mutation
  • Male
  • Phospholipids / genetics
  • Phospholipids / metabolism
  • Polymorphism, Single Nucleotide
  • Selection, Genetic*
  • Young Adult

Substances

  • Delta-5 Fatty Acid Desaturase
  • Fatty Acids, Unsaturated
  • Phospholipids
  • Arachidonic Acid
  • Fatty Acid Desaturases
  • FADS1 protein, human
  • FADS2 protein, human