Doubts about complex speciation between humans and chimpanzees

Abstract

Two patterns from large-scale DNA sequence data have been put forward as evidence that speciation between humans and chimpanzees was complex, involving hybridization and strong selection. First, divergence between humans and chimpanzees varies considerably across the autosomes. Second, divergence between humans and chimpanzees (but not gorillas) is markedly lower on the X chromosome. Here, we describe how simple speciation and neutral molecular evolution explain both patterns. In particular, the wide range in autosomal divergence is consistent with stochastic variation in coalescence times in the ancestral population; and the lower human-chimpanzee divergence on the X chromosome is consistent with species differences in the strength of male-biased mutation caused by differences in mating system. We also highlight two further patterns of divergence that are problematic for the complex speciation model. Our conclusions raise doubts about complex speciation between humans and chimpanzees.

Figure 1

Complex speciation between humans and chimpanzees. After an initial separation 5–7 Mya, the two lineages subsequently formed a third hybrid population. Strong selection against hybrid incompatibilities eliminated nearly the entire X chromosome from the hybrid population. In the case shown, the X chromosome from the ancestral chimpanzee lineage and autosomes mostly from a now extinct ancestral hominin lineage survived in the human descendants of the hybrid population. (The divergence data cannot distinguish if humans or chimpanzees descended from the hybrid population, but humans are arbitrarily shown as the descendants here, as in Ref. [1].) Under this scenario, the human-chimpanzee divergence time at autosomal loci is t_A (red), whereas that for X chromosome loci is t_X (blue).

Figure 2

Divergence times vary among loci under simple speciation. The time separating two DNA sequences sampled from different species is the sum of the species split time (t₂) and the time to coalescence in the ancestral population (t₁). The divergence histories of two unlinked loci, L₁ and L₂, are shown. Both loci have the same species split time (t₂) but different times to coalescence (t_1,L1 and t_1,L2, respectively), causing interlocus variation in divergence time.

Figure 3

Correlation between the intensities of sperm competition in hominoid mating systems and lineage-specific strengths of male-biased mutation (α). For gorilla, human and chimpanzee lineages, α ± 95% confidence intervals from the HCGM analysis (four-fold human diversity correction for ancestral polymorphism; Table 2) are plotted against relative testis mass.