PERSPECTIVE: THE EVOLUTIONARY BIOLOGY OF AGING, SEXUAL REPRODUCTION, AND DNA REPAIR

Three recent books on the evolutionary biology of aging and sexual reproduction are reviewed, with particular attention focused on the provocative suggestion by Bernstein and Bernstein (1991) that senescence and genetic recombination are related epiphenomena stemming from the universal challenge to life posed by DNA damages and the need for damage repair. Embellishments to these theories on aging and sex are presented that consider two relevant topics neglected or underemphasized in the previous treatments. The first concerns discussion of cytoplasmic genomes (such as mtDNA), which are transmitted asexually and therefore do not abide by the recombinational rules of nuclear genomes; the second considers the varying degrees of cellular and molecular autonomy which distinguish unicellular from multicellular organisms, germ cells from somatic cells, and sexual from asexual genomes. Building on the Bernsteins' suggestions, two routes to immortality for cell lineages appear to be available to life: an asexual strategy (exemplified by some bacteria), whereby cell proliferation outpaces the accumulation of DNA damages, thereby circumventing Muller's ratchet; and a sexual strategy (exemplified by germlines in multicellular organisms), whereby recombinational repair of DNA damages in conjunction with cell proliferation and gametic selection counter the accumulation of nuclear DNA damages. If true, then elements of both the recombinational strategy (nuclear DNA) and replacement strategy (cytoplasmic DNA) may operate simultaneously in the germ-cell lineages of higher organisms, producing at least some gametes that are purged of the DNA damages accumulated during the lifetime of the somatic parent. For multicellular organisms, production of functionally autonomous and genetically screened gametic cells is a necessary and sufficient condition for the continuance of life.