Pacific Populations, Metabolic Disease and ‘Just‐So Stories’: A Critique of the ‘Thrifty Genotype’ Hypothesis in Oceania

Pacific populations have long been observed to suffer a high burden of metabolic disease, including obesity, type 2 diabetes and gout. The ‘Thrifty Genotype’ hypothesis has frequently been used to explain this high prevalence of disease. Here, the ‘Thrifty Genotype’ hypothesis and the evolutionary background of Pacific populations are examined. We question its relevance not only in the Pacific region but more generally. Not only has the hypothesis not been explicitly tested, but most archaeological and anthropological data from the Pacific fundamentally do not support its application.

[1]  M. Stoneking,et al.  Recent developments in the genetic history of East Asia and Oceania. , 2014, Current opinion in genetics & development.

[2]  Y. Teo,et al.  Can Evidence from Genome-Wide Association Studies and Positive Natural Selection Surveys Be Used to Evaluate the Thrifty Gene Hypothesis in East Asians? , 2014, PloS one.

[3]  I. Goodwin,et al.  Climate windows for Polynesian voyaging to New Zealand and Easter Island , 2014, Proceedings of the National Academy of Sciences.

[4]  L. Beil.  Ancient genes, modern meals: Poking holes in the thrifty gene hypothesis , 2014 .

[5]  S. Bedford,et al.  Scurvy in a tropical paradise? Evaluating the possibility of infant and adult vitamin C deficiency in the Lapita skeletal sample of Teouma, Vanuatu, Pacific islands. , 2014, International journal of paleopathology.

[6]  E. Matisoo-Smith,et al.  Hyperuricaemia in the Pacific: why the elevated serum urate levels? , 2014, Rheumatology International.

[7]  Pardis C. Sabeti,et al.  Natural selection and infectious disease in human populations , 2014, Nature Reviews Genetics.

[8]  Haitao Wen,et al.  Inflammasomes and metabolic disorders: old genes in modern diseases. , 2014, Molecular cell.

[9]  R. Cox,et al.  On the evolutionary origins of obesity: a new hypothesis. , 2014, Endocrinology.

[10]  E. Ortlund,et al.  Evolutionary history and metabolic insights of ancient mammalian uricases , 2014, Proceedings of the National Academy of Sciences.

[11]  Luca Pagani,et al.  Revisiting the thrifty gene hypothesis via 65 loci associated with susceptibility to type 2 diabetes. , 2014, American journal of human genetics.

[12]  Kari Stefansson,et al.  Identification of low-frequency and rare sequence variants associated with elevated or reduced risk of type 2 diabetes , 2014, Nature Genetics.

[13]  S. Fitzpatrick,et al.  From west to east: Environmental influences on the rate and pathways of Polynesian colonization , 2014 .

[14]  J. Kuiaté,et al.  Distribution of CCR5-Delta32, CCR5 promoter 59029 A/G, CCR2-64I and SDF1-3’A genetic polymorphisms in HIV-1 infected and uninfected patients in the West Region of Cameroon , 2013, BMC Research Notes.

[15]  J. Speakman.  Evolutionary perspectives on the obesity epidemic: adaptive, maladaptive, and neutral viewpoints. , 2013, Annual review of nutrition.

[16]  A. Bashashati,et al.  DriverNet: uncovering the impact of somatic driver mutations on transcriptional networks in cancer , 2012, Genome Biology.

[17]  D. Burley,et al.  High Precision U/Th Dating of First Polynesian Settlement , 2012, PloS one.

[18]  K. Westerterp,et al.  A mathematical model of weight loss under total starvation: evidence against the thrifty-gene hypothesis , 2012, Disease Models & Mechanisms.

[19]  Itsik Pe'er,et al.  Implications for health and disease in the genetic signature of the Ashkenazi Jewish population , 2012, Genome Biology.

[20]  D. Weeks,et al.  Common Variants in FTO Are Not Significantly Associated with Obesity‐Related Phenotypes among Samoans of Polynesia , 2012, Annals of human genetics.

[21]  Yong Wang,et al.  An Aboriginal Australian Genome Reveals Separate Human Dispersals into Asia , 2011, Science.

[22]  Carey N Lumeng,et al.  Inflammatory links between obesity and metabolic disease. , 2011, The Journal of clinical investigation.

[23]  M. Spriggs.  Archaeology and the Austronesian expansion: where are we now? , 2011, Antiquity.

[24]  H. Buckley.  Epidemiology of Gout: Perspectives from the Past , 2011 .

[25]  M. Stoneking,et al.  Testing the thrifty gene hypothesis: the Gly482Ser variant in PPARGC1A is associated with BMI in Tongans , 2011, BMC Medical Genetics.

[26]  Carl P. Lipo,et al.  High-precision radiocarbon dating shows recent and rapid initial human colonization of East Polynesia , 2010, Proceedings of the National Academy of Sciences.

[27]  M. Stoneking,et al.  Demographic History of Oceania Inferred from Genome-wide Data , 2010, Current Biology.

[28]  Richard Fullagar,et al.  Human Adaptation and Plant Use in Highland New Guinea 49,000 to 44,000 Years Ago , 2010, Science.

[29]  R. Chaisson,et al.  Body mass index and risk of tuberculosis and death , 2010, AIDS.

[30]  J. Field,et al.  Paleoclimates and the emergence of fortifications in the tropical Pacific islands , 2010 .

[31]  T. Inaoka,et al.  The Q223R polymorphism in LEPR is associated with obesity in Pacific Islanders , 2010, Human Genetics.

[32]  M. Kayser.  The Human Genetic History of Oceania: Near and Remote Views of Dispersal , 2010, Current Biology.

[33]  D. Weeks,et al.  A tagging SNP in INSIG2 is associated with obesity-related phenotypes among Samoans , 2009, BMC Medical Genetics.

[34]  Rasmus Nielsen,et al.  Adaptionism—30 Years After Gould and Lewontin , 2009, Evolution; international journal of organic evolution.

[35]  A. Prentice,et al.  Type 2 diabetes, cardiovascular disease, and the evolutionary paradox of the polycystic ovary syndrome: A fertility first hypothesis , 2009, American journal of human biology : the official journal of the Human Biology Council.

[36]  M. McCarthy,et al.  Is the thrifty genotype hypothesis supported by evidence based on confirmed type 2 diabetes- and obesity-susceptibility variants? , 2009, Diabetologia.

[37]  J V Neel,et al.  The "thrifty genotype" in 1998. , 2009, Nutrition reviews.

[38]  D. Weeks,et al.  Susceptibility Loci for Adiposity Phenotypes on 8p, 9p, and 16q in American Samoa and Samoa , 2009, Obesity.

[39]  L. Plank,et al.  Body size, body composition and fat distribution: comparative analysis of European, Maori, Pacific Island and Asian Indian adults , 2009, British Journal of Nutrition.

[40]  Benjamin M. Neale,et al.  Genome-Wide Association Studies in an Isolated Founder Population from the Pacific Island of Kosrae , 2009, PLoS genetics.

[41]  W. Chung,et al.  Functional Consequences of the Human Leptin Receptor (LEPR) Q223R Transversion , 2009, Obesity.

[42]  J. Speakman.  Thrifty genes for obesity, an attractive but flawed idea, and an alternative perspective: the ‘drifty gene’ hypothesis , 2008, International Journal of Obesity.

[43]  Jonathan Scott Friedlaender,et al.  The Genetic Structure of Pacific Islanders , 2008, PLoS genetics.

[44]  T. Inaoka,et al.  FTO polymorphisms in oceanic populations , 2007, Journal of Human Genetics.

[45]  Fernando A. Villanea,et al.  Diet and the evolution of human amylase gene copy number variation , 2007, Nature Genetics.

[46]  H. Buckley.  Possible Gouty Arthritis in Lapita‐Associated Skeletons from Teouma, Efate Island, Central Vanuatu , 2007, Current Anthropology.

[47]  K. Collerson,et al.  Stone Adze Compositions and the Extent of Ancient Polynesian Voyaging and Trade , 2007, Science.

[48]  J. Speakman.  A nonadaptive scenario explaining the genetic predisposition to obesity: the "predation release" hypothesis. , 2007, Cell metabolism.

[49]  Beverley Balkau,et al.  Variation in FTO contributes to childhood obesity and severe adult obesity , 2007, Nature Genetics.

[50]  J. Gulcher,et al.  A variant in CDKAL1 influences insulin response and risk of type 2 diabetes , 2007, Nature Genetics.

[51]  M. Jarvelin,et al.  A Common Variant in the FTO Gene Is Associated with Body Mass Index and Predisposes to Childhood and Adult Obesity , 2007, Science.

[52]  Peter Nürnberg,et al.  Identification of a candidate genetic variant for the high prevalence of type II diabetes in Polynesians , 2007, European Journal of Human Genetics.

[53]  Michael J. Montoya,et al.  Racialized Genetics and the Study of Complex Diseases: The Thrifty Genotype Revisited , 2007, Perspectives in biology and medicine.

[54]  V. Mohan,et al.  Epidemiology of type 2 diabetes: Indian scenario. , 2007, The Indian journal of medical research.

[55]  J. Gulcher,et al.  Refining the impact of TCF7L2 gene variants on type 2 diabetes and adaptive evolution , 2007, Nature Genetics.

[56]  S. Bedford,et al.  The Teouma Lapita site and the early human settlement of the Pacific Islands , 2006, Antiquity.

[57]  P. Underhill,et al.  Melanesian and Asian origins of Polynesians: mtDNA and Y chromosome gradients across the Pacific. , 2006, Molecular biology and evolution.

[58]  J. Watson,et al.  Exploring the thrifty genotype's food-shortage assumptions: a cross-cultural comparison of ethnographic accounts of food security among foraging and agricultural societies. , 2006, American journal of physical anthropology.

[59]  J. Speakman.  Thrifty genes for obesity and the metabolic syndrome — time to call off the search? , 2006, Diabetes & vascular disease research.

[60]  H. Shin,et al.  Polymorphisms in the leptin receptor (LEPR)—putative association with obesity and T2DM , 2006, Journal of Human Genetics.

[61]  P. Stover.  Influence of human genetic variation on nutritional requirements. , 2006, The American journal of clinical nutrition.

[62]  Andrew M. Prentice,et al.  Early influences on human energy regulation: Thrifty genotypes and thrifty phenotypes , 2005, Physiology & Behavior.

[63]  D. Kwiatkowski.  How malaria has affected the human genome and what human genetics can teach us about malaria. , 2005, American journal of human genetics.

[64]  H. Whittle,et al.  Body Mass Index at Time of HIV Diagnosis: A Strong and Independent Predictor of Survival , 2004, Journal of acquired immune deficiency syndromes.

[65]  Pardis C Sabeti,et al.  Genetic signatures of strong recent positive selection at the lactase gene. , 2004, American journal of human genetics.

[66]  J. Diamond,et al.  The double puzzle of diabetes , 2003, Nature.

[67]  M. Sande.  Cardiovascular disease in sub-Saharan Africa: a disaster waiting to happen. , 2003 .

[68]  Pardis C Sabeti,et al.  Detecting recent positive selection in the human genome from haplotype structure , 2002, Nature.

[69]  M. Slatkin,et al.  Natural selection and resistance to HIV , 2001, Nature.

[70]  Claudio D. González,et al.  Obesity prevalence and trends in Latin‐American countries , 2001, Obesity reviews : an official journal of the International Association for the Study of Obesity.

[71]  H. Buckley.  Subadult health and disease in prehistoric Tonga, Polynesia. , 2000, American journal of physical anthropology.

[72]  M. Pigliucci,et al.  The fall and rise of Dr Pangloss: adaptationism and the Spandrels paper 20 years later. , 2000, Trends in ecology & evolution.

[73]  L. Plank,et al.  Body size and composition in Polynesians , 1999, International Journal of Obesity.

[74]  M. A. Crook,et al.  Is Type II diabetes mellitus a disease of the innate immune system? , 1998, Diabetologia.

[75]  P. Baker,et al.  Bergmann's rule and the thrifty genotype. , 1997, American journal of physical anthropology.

[76]  S. Gould,et al.  The exaptive excellence of spandrels as a term and prototype. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[77]  S. Cheer,et al.  The Non-Thrifty Genotype , 1996, Current Anthropology.

[78]  M. Allen.  The Prehistoric Exploration and Colonisation of the Pacific , 1994 .

[79]  K. O'dea,et al.  Diabetes in Australian Aborigines: impact of the western diet and life style , 1992, Journal of internal medicine.

[80]  C. Hales,et al.  Type 2 (non-insulin-dependent) diabetes mellitus: the thrifty phenotype hypothesis , 1992, Diabetologia.

[81]  R. Lewontin,et al.  Facts and the Factitious in Natural Sciences , 1991, Critical Inquiry.

[82]  H. King,et al.  The epidemiology and natural history of NIDDM--lessons from the South Pacific. , 1990, Diabetes/metabolism reviews.

[83]  P. Kirch,et al.  Human skeletal and dental remains from Lapita sites (1600-500 B.C.) in the Mussau Islands, Melanesia. , 1989, American journal of physical anthropology.

[84]  B. Childs.  Human Biology: An introduction to human evolution, variation, growth, and adaptability , 1988 .

[85]  L. Prior.  Epidemiology of Rheumatic disorders in the Pacific with particular emphasis on hyperuricaemia and gout. , 1981, Seminars in arthritis and rheumatism.

[86]  S. Gould,et al.  The spandrels of San Marco and the Panglossian paradigm: a critique of the adaptationist programme , 1979, Proceedings of the Royal Society of London. Series B. Biological Sciences.

[87]  C. E. Snow.  Early Hawaiians: An Initial Study of Skeletal Remains from Mokapu, Oahu , 1974 .

[88]  I. Prior,et al.  Hyperuricaemia, gout, and diabetic abnormality in Polynesian people. , 1966, Lancet.

[89]  J. Neel.  Diabetes mellitus: a "thrifty" genotype rendered detrimental by "progress"? , 1962, American journal of human genetics.

[90]  G. Irwin.  AGAINST, ACROSS AND DOWN THE WIND: A CASE FOR THE SYSTEMATIC EXPLORATION OF THE REMOTE PACIFIC ISLANDS , 2016 .

[91]  S. McGarvey.  THE THRIFTY GENE CONCEPT AND ADIPOSITY STUDIES IN BIOLOGICAL ANTHROPOLOGY , 2016 .

[92]  Gregory A. Nelson,et al.  Functional Consequences of , 2013 .

[93]  D. O’Rourke.  Causes and Consequences of Human Migration: Why do we migrate? A retrospective , 2012 .

[94]  Peter Wilberfoss.  Cold case: Cold induced vasodilation response, and the origins of Polynesian body morphology as an adaptation to a cold environment , 2012 .

[95]  D. Musher,et al.  The obesity paradox in community-acquired bacterial pneumonia. , 2011, International journal of infectious diseases : IJID : official publication of the International Society for Infectious Diseases.

[96]  E. Matisoo-Smith,et al.  Tamuarawai (EQS ): An Early Lapita Site on Emirau, New Ireland, PNG , 2010 .

[97]  H. Buckley,et al.  The People of Wairau Bar: a Re-examination , 2010 .

[98]  P. Raven,et al.  The age and origin of the Pacific islands : a geological overview , 2008 .

[99]  Susan E. Luczak,et al.  ALDH2, ADH1B, and ADH1C Genotypes in Asians: A Literature Review , 2007, Alcohol research & health : the journal of the National Institute on Alcohol Abuse and Alcoholism.

[100]  S. Fitzpatrick.  Archaeology's Contribution to Island Studies , 2007 .

[101]  H. Buckley.  Bioarchaeology of Southeast Asia: ‘The predators within’: investigating the relationship between malaria and health in the prehistoric Pacific Islands , 2006 .

[102]  Birgir Hrafnkelsson,et al.  An Icelandic example of the impact of population structure on association studies , 2005, Nature Genetics.

[103]  James H. Brown,et al.  The Physiological Ecology of Vertebrates: A View from Energetics , 2002 .

[104]  S. Bedford.  ON THE ROAD OF THE WINDS: AN ARCHAEOLOGICAL HISTORY OF THE PACIFIC ISLANDS BEFORE EUROPEAN CONTACT, by , 2001 .

[105]  P. Houghton.  People of the Great Ocean: Aspects of Human Biology of the Early Pacific , 1996 .

[106]  P. Houghton.  The adaptive significance of Polynesian body form. , 1990, Annals of human biology.

[107]  A. Goodman,et al.  Indications of Stress from Bone and Teeth. In: Paleopathology at the Origins of Agriculture , 1984 .

[108]  C. Viscoli,et al.  [Hereditary fructose intolerance]. , 1983, La Pediatria medica e chirurgica : Medical and surgical pediatrics.

[109]  W. Howells.  Early Hawaiians: An initial study of skeletal remains from Mokapu, Oahu. By Charles E. Snow. xi + 179 pp., figures, tables, bibliography, index. University Press of Kentucky, Lexington. 1974. $16.75 (cloth) , 1976 .

[110]  Te Rangi Hīroa.  Vikings of the sunrise , 1938 .