Mitochondrial DNA and the Y chromosome: parallels and paradoxes

Abstract

Both mitochondrial DNA (mtDNA) and the Y chromosome have been used extensively by molecular paleoanthropologists in attempts to reconstruct human lineages. Both are inherited in a haploid manner: mtDNA through the female and the Y through the male. For mtDNA, maternal inheritance is ensured by a species-specific mechanism of proteolysis of the sperm midpiece in early embryogenesis, based on ubiquitination of the mitochondria during spermiogenesis. Both genomes are thought to lack recombination and are thus liable to high rates of neutral mutation. For the human Y chromosome, it is now clear that there has been selection on genes controlling spermatogenesis, resulting in differential long-term reproductive success. This is corroborated from studies of genealogies and hunting–gathering societies, although these lack the rigour provided by the modern molecular markers of inheritance. Selection is made more complicated by a concentration of genes controlling secondary sexual characteristics on the X chromosome. Likewise, mtDNA affects the bioenergetics of gametogenesis and embryo development, as well as longevity, disease and the aging process. Both Y chromosome and mitochondrial haplotypes show significant associations with patterns of male infertility that could distort their use for phylogenetic reconstruction. Moreover, the molecular analysis of mtDNA is complicated by the presence of numerous nuclear mitochondrial pseudogenes (Numts) that can be erroneously amplified by molecular techniques such as PCR. This review examines some of these complex interactions and suggests that some of the more contentious issues in understanding human evolution may be resolved by considering the biology of these genetic markers.