Analysis of higher-primate phylogeny from transversion differences in nuclear and mitochondrial DNA by Lake's methods of evolutionary parsimony and operator metrics

In the companion paper (Holmquist et al. 1988), we concluded that there isno agreement on either the correct branching order or differential rates ofevolution among the higher primates, and we examined in depth why thisuncertainty in the evolutionary understanding of our closest livingrelatives persists. Recently, Lake developed two novel methods, based ongroup properties of transition and transversion operators, that (a) permit,in principle, objective resolution of problems of the above type and (b)attach a statistical significance level to the conclusions drawn. In thepresent paper, we develop formulas for using these two methods in tandemand apply them to study transversion differences in (1) nuclear DNA for a7-kb segment of the psi eta-globin locus and a 3-kb intergenic regionbetween the psi beta- and delta- globin loci and (2) mitochondrial DNA forthe 896-bp fragment of Brown et al. Although each of these nucleotidesequence regions has its characteristic tempo and mode of evolution, thenuclear and mitochondrial data together, comprising a total of 10,939 basepositions, support a Homo/Pan clade at the 97% confidence level. If wecalibrate the divergence point for humans and chimpanzees at 5 Myr,consideration of the transversion branch lengths for the combined nucleardata indicates that the gorilla lineage branched off 600,000- 900,000 yearsprior to that, although the 2 sigma sampling errors do not preclude eithera temporal trifurcation for the three species or a considerably moreancient branch point for the gorilla. To resolve the length of this centralbranch to a relative accuracy of 25% and 30% will require a factor of 16and nine times more data, respectively-- i.e., in excess of 100,000homologous nucleotides for each of the four primates. For the nucleargenes, heterogeneity in evolutionary rates between different parts of thegenome is mostly restricted to the human lineage for these two segments.The lineage leading to chimpanzees has evolved 0.4 (3-kb fragment) to 3.5(7-kb segment) times as rapidly as the lineage leading to humans, and thatleading to the gorilla has evolved approximately one-fifth to one-half asrapidly as that leading to chimpanzees. Thus, even local molecular clockscan "tick" badly. As significant is the fact that virtually contiguousparts of the genome tick at markedly different rates.(ABSTRACT TRUNCATED AT400 WORDS)