The evolution of postmenopausal longevity in human females has been the subject of debate. Specifically, there is disagreement about whether the evolution of the trait should be understood as an adaptive or a neutral process, and if the former, what the selective mechanism is. There are two main adaptive proposals to explain the evolution of postreproductive longevity: the grandmother and the mother hypotheses. The grandmother hypothesis proposes that postreproductive longevity evolved because it is selectively advantageous for females to stop reproducing and to help raise their grandchildren. The mother hypothesis states that postmenopausal longevity evolved because it is advantageous for women to cease reproduction and concentrate their resources and energy in raising the children already produced. In this article, we test the mother and the grandmother hypotheses with a historical data set from which we bootstrapped random samples of women from different families who lived from the 1500s to the 1900s in the central valley of Costa Rica. We also compute the heritability of longevity, which allows us to determine if genes involved in longevity are nearly fixed in this population. Here we show that although longevity positively affects a woman's fertility, it negatively affects her daughter's fertility; for this reason, the heritability of longevity is unexpectedly high. Our data provide strong grounds for questioning the universality of the grandmother hypothesis and for supporting the mother hypothesis as a likely explanation for the evolution of human postreproductive longevity.

Estimates of mutation rates for the noncoding hypervariable Region I (HVR-I) of mitochondrial DNA (mtDNA) vary widely, depending on whether they are inferred from phylogenies (assuming that molecular evolution is clock-like) or directly from pedigrees. All pedigree-based studies so far were conducted on populations of European origin. In this paper we analyzed 19 deep-rooting pedigrees in a population of mixed origin in Costa Rica. We calculated two estimates of the HVR-I mutation rate, one considering all apparent mutations, and one disregarding changes at sites known to be mutational hot spots and eliminating genealogy branches which might be suspected to include errors, or unrecognized adoptions along the female lines. At the end of this procedure, we still observed a mutation rate equal to 1.24 × 10−6, per site per year, i.e., at least three-fold as high as estimates derived from phylogenies. Our results confirm that mutation rates observed in pedigrees are much higher than estimated assuming a neutral model of long-term HVRI evolution. We argue that, until the cause of these discrepancies will be fully understood, both lower estimates (i.e., those derived from phylogenetic comparisons) and higher, direct estimates such as those obtained in this study, should be considered when modeling evolutionary and demographic processes.

Previous work compared frequency of longevity-associated polymorphisms (LAPS) in long-lived individuals and in controls from the general population (primarily in Europe and Japan), suggesting the polymorphisms are responsible for unusual longevity. However, individuals from the general population are not the control group for long-lived subjects because both were born in different periods. We report results of a project which collected mtDNA from living subjects in Costa Rica, and traced back their maternal genealogy. Since mtDNA does not recombine and its probability of mutation is low, we can assume that the maternal ancestors had the same mtDNA of their descendants. We compared the longevity of individuals with LAPS with the longevity of controls born in the same time period. We did not confirm previous associations for several markers, but found that the 5178A mutation in haplogroup D is associated with decreased longevity, whereas the 150T mutation is associated with increased longevity. These associations however, are not significant for all time periods under study. While our data confirm that mtDNA make up affects longevity, they also indicate that the time period in which a person was born had a much greater impact on longevity than presence or absence of a marker.

Although LAPS significantly affect longevity, such differential longevity does not result in differential lifetime reproductive success. From an evolutionary perspective, these longevity-associated polymorphisms do not affect the carriers' Darwinian fitness.

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