Male dominance rarely skews the frequency distribution of Y chromosome haplotypes in human populations

Abstract

A central tenet of evolutionary social science holds that behaviors, such as those associated with social dominance, produce fitness effects that are subject to cultural selection. However, evidence for such selection is inconclusive because it is based on short-term statistical associations between behavior and fertility. Here, we show that the evolutionary effects of dominance at the population level can be detected using noncoding regions of DNA. Highly variable polymorphisms on the nonrecombining portion of the Y chromosome can be used to trace lines of descent from a common male ancestor. Thus, it is possible to test for the persistence of differential fertility among patrilines. We examine haplotype distributions defined by 12 short tandem repeats in a sample of 1269 men from 41 Indonesian communities and test for departures from neutral mutation-drift equilibrium based on the Ewens sampling formula. Our tests reject the neutral model in only 5 communities. Analysis and simulations show that we have sufficient power to detect such departures under varying demographic conditions, including founder effects, bottlenecks, and migration, and at varying levels of social dominance. We conclude that patrilines seldom are dominant for more than a few generations, and thus traits or behaviors that are strictly paternally inherited are unlikely to be under strong cultural selection.

Fig. 1.

Population models. Colored dots represent individuals who have descendants in the final generation. Red dots represent dominant individuals who are more likely to reproduce. Pink dots represent nondominant individuals having a dominant ancestor. Blue dots represent nondominant individuals having no dominant ancestor. Dominant individuals in 1 generation are chosen at random from the offspring of dominant individuals in the previous generation. (See SI Text Population Models for more details.)

Fig. 2.

Example haplotype distributions. The height of column i is the number of individuals whose haplotype is represented i times in the sample (normalized by sample size). (A) An example of a community haplotype distribution that does not show evidence of departure from neutrality based on the exact test: Sumba/Mamboro. (B) An example of a community showing departure from neutrality based on the exact test: Sumba/Wanokaka. Although nonneutral cases often appear to have mass shifted to the right, it generally is not possible to determine the outcome of the exact test by inspection. Colors indicate Y chromosome haplogroup membership (C, F, K, M, O, or S). All 41 distributions and the color key are given in Fig. S1. Additional haplogroup information is in Table S5.

Fig. 3.

Probability of seeing 5 or fewer (of 41) nonneutral villages for a given power of the individual tests to detect departure from neutrality. If the power of the individual tests is 0.2, the probability of observing ≤5 is ≈0.2. If the power of the individual tests is > 0.3, then this probability is vanishingly small.

Fig. 4.

Effects of adding nonheritable reproductive skew to a simulated population of size n = 300. The first column shows simulation results for δ = 0.02, the second column for δ = 0.06. (A) Reduction of power. As p increases, the power to detect skew is reduced. However, the length of time lineages are dominant also decreases, nullifying any long-term evolutionary advantage of dominance. (B) N_e reduction. Effective population size remains depressed for all values of p, providing an additional way to assess the strength of both heritable and nonheritable skew. Estimates eventually exceed the actual population size because the estimator is biased upwards.