Sequencing Y chromosomes resolves discrepancy in time to common ancestor of males versus females

Abstract

The Y chromosome and the mitochondrial genome have been used to estimate when the common patrilineal and matrilineal ancestors of humans lived. We sequenced the genomes of 69 males from nine populations, including two in which we find basal branches of the Y-chromosome tree. We identify ancient phylogenetic structure within African haplogroups and resolve a long-standing ambiguity deep within the tree. Applying equivalent methodologies to the Y chromosome and the mitochondrial genome, we estimate the time to the most recent common ancestor (T(MRCA)) of the Y chromosome to be 120 to 156 thousand years and the mitochondrial genome T(MRCA) to be 99 to 148 thousand years. Our findings suggest that, contrary to previous claims, male lineages do not coalesce significantly more recently than female lineages.

Fig. 1. Callability mask for the Y chromosome

Exponentially-weighted moving averages of read depth (blue line) and the proportion of reads mapping ambiguously (MQ0 ratio; violet line) versus physical position. Regions with values outside the envelopes defined by the dashed lines (depth) or dotted lines (MQ0) were flagged (blue and violet boxes) and merged for exclusion (gray boxes). The complement (black boxes) defines the regions within which reliable genotype calls can be made. Below, a scatter plot indicates the positions of all observed SNVs. Those incompatible with the inferred phylogenetic tree (red) are uniformly distributed. The X-degenerate regions yield quality sequence data, ampliconic sequences tend to fail both filters, and mapping quality is poor in the X-transposed region.

Fig. 2. Y chromosome phylogeny inferred from genomic sequencing

This tree recapitulates the previously known topology of the Y chromosome phylogeny; however, branch lengths are now free of ascertainment bias. Branches are drawn proportional to the number of derived SNVs. Internal branches are labeled with defining ISOGG variants inferred to have arisen on the branch. Leaves are colored by major haplogroup cluster and labeled with the most derived mutation observed and the population from which the individual was drawn. Previously uncharacterized structure within African hgB2 is indicated in orange. (Inset) Resolution of a polytomy was possible through the identification of a variant for which hgG retains the ancestral allele, whereas hgH and hgIJK share the derived allele.

Fig. 3. Similarity of T_MRCA does not imply equivalent N_e of males and females

The T_MRCA for a given locus is drawn from a predata (i.e., prior) distribution that is a function of N_e, generation time, sample size, and demographic history. Consider the distribution of possible T_MRCA's for a set of 100 uniparental chromosomes. Although the Mbuti mtDNA N_e is twice as large as that of the Baka Y chromosome, the corresponding predata T_MRCA distributions overlap considerably.