Evolution of lactase persistence: an example of human niche construction

Abstract

Niche construction is the process by which organisms construct important components of their local environment in ways that introduce novel selection pressures. Lactase persistence is one of the clearest examples of niche construction in humans. Lactase is the enzyme responsible for the digestion of the milk sugar lactose and its production decreases after the weaning phase in most mammals, including most humans. Some humans, however, continue to produce lactase throughout adulthood, a trait known as lactase persistence. In European populations, a single mutation (-13910*T) explains the distribution of the phenotype, whereas several mutations are associated with it in Africa and the Middle East. Current estimates for the age of lactase persistence-associated alleles bracket those for the origins of animal domestication and the culturally transmitted practice of dairying. We report new data on the distribution of -13910*T and summarize genetic studies on the diversity of lactase persistence worldwide. We review relevant archaeological data and describe three simulation studies that have shed light on the evolution of this trait in Europe. These studies illustrate how genetic and archaeological information can be integrated to bring new insights to the origins and spread of lactase persistence. Finally, we discuss possible improvements to these models.

Figure 1.

Interpolated maps of the distribution of LP and the −13910*T allele in the ‘old world’. (a) LP phenotype distribution. Data points (dots) were taken from the literature (see text and [14] for details). (b) Distribution of the allele −13910*T, associated to LP. Dots represent sample data taken from a previous review [,–30]; crosses represent data for new locations not previously tested and diamonds correspond to locations where additional data have been added. Regularly updated frequency data are available at http://www.ucl.ac.uk//mace-lab/GLAD/ website.

Figure 2.

Arrival dates and approximate geographical expansions of defined Early Neolithic cultures from [61].

Figure 3.

Scenarios simulated in [18] and selection coefficients required to fit the observed estimates of LP frequencies (taken from [18]). Bars represent the 95% confidence interval of the selection coefficient estimated for the population and the central point is the MLE (maximum-likelihood estimate). Populations are ordered from the highest to the lowest latitude: Danish (Dan), Irish (Iri), German from Bremen (Bre), German from Berlin (Ber), English (Eng), Polish (Pol), Czech (Cze), German from Stuttgart (Stu), German from Munchen (Mun), Austrian (Aus), French from Nantes (Nan), Swiss (Swi), Slovenian (Slo), Italian from Brescia (Bre), French from Nice (Nic), Spanish from Santiago de Compostela (Com), Italian from Roma (Rom), Italian from Napoli (Nap), Sardinian (Sas), Spanish from Valencia (Val), Greek (Gre), Sicilian (Sic), Cypriot (Cyp), Lebanese (Leb) and Iranian (Ira) (doi:10.1371/journal.pone.0006369.g002). (a) Demic diffusion, gene–culture coevolution; (b) demic diffusion, calcium assimilation; (c) cultural diffusion, gene–culture coevolution; and (d) cultural diffusion, calcium assimilation.

Figure 4.

Approximate posterior density of region of origin for LP—dairying coevolution (taken from [105]). Points represent regression-adjusted latitude and longitude coordinates from simulations accepted at the 0.5% tolerance level. Shading was added using two-dimensional kernel density estimation (doi:10.1371/journal.pcbi.1000491.g003).