Drosophila melanogaster is a convenient model organism for studying factors that affect lifespan (LS) and other life history traits. In this work, we tested flies from different laboratory lines, including those subjected to artificial selection for late reproduction, and showed that evolutionary changes in LS can be associated not only with changes in the gene pool of the experimental Drosophila line. Contrary to expectations, the genetic contribution to the increase in LS of flies selected for late reproduction appears to be relatively small. It is difficult to assess it separately, as it is masked by the influence of other factors, primarily the symbiotic microbiota. Our results are consistent with the assumption that differences in LS between Drosophila lines kept under different conditions can be largely determined by the components of their microbiota. The selection of Drosophila for late reproduction (as well as other environmental influences) can affect the LS of flies indirectly through changes in the microbiota, as well as directly, that is, through evolutionary changes in the gene pool of the experimental fly population. This example illustrates the “hologenomic theory of evolution,” showing that in some cases it is more correct to consider a holobiont, that is, a complex that includes a macroorganism and its associated microbiota as a unit of selection, and not an individual organism.

The spatiotemporal variability of environmental conditions is assumed to have a strong impact on the course of microevolution processes, including the efficiency of adaptation to unfavourable conditions and the probability of ecological specialization or, conversely, generalization (the acquisition of multipurpose adaptations). The experimentаl research on these effects is still at the initial stage, and the temporal, rather than spatial, heterogeneity of the environment is analyzed in most studies. We performed an evolution experiment that involved the adaptation of Drosophila melanogaster lines to two unfavourable media: a high-salt (S) medium and a starch-based (St) medium of low nutritional value. Some of the experimental lines had access to one of the two unfavourable media only (homogeneous environment), whereas the others had access to both media and could choose between them (heterogeneous environment). The control lines were reared on a normal laboratory medium (N) that provided favourable conditions for the species. The degree of adaptation of lines obtained on the S, St, and N media was assessed after one and a half years of adaptation. The reproduction efficiency (the amount of adult progeny derived from a pair of parents within a specified time interval), adult lifespan, oviposition rate, and ageing-related changes in the former were assessed. Flies reared in a heterogeneous environment were superior to those reared in a homogeneous one with regard to most adaptation parameters on all three media. The results agree with the hypothesis concerning the promotion of generalization and more efficient adaptation to unfavourable conditions upon spatial heterogeneity of the environment. The obtained data do not support the hypothesis of antagonistic pleiotropy, which leads to “evolutionary trade-offs” and a lower competitiveness of generalists than that of specialists under stable conditions.

The dynamics of aging is often described by survival curves that show the proportion of individuals surviving to a given age. The shape of the survival curve reflects the dependence of mortality on age, and it varies greatly for different organisms. In a recently published paper, Stroustrup and coauthors ((2016) Nature, {vn530}, 103–107) showed that many factors affecting the lifespan of Caenorhabditis elegans do not change the shape of the survival curve, but only stretch or compress it in time. Apparently, this means that aging is a programmed process whose trajectory is difficult to change, although it is possible to speed it up or slow it down. More research is needed to clarify whether the “rule of temporal scaling” is applicable to other organisms. A good indicator of temporal scaling is the coefficient of lifespan variation: similar values of this coefficient for two samples indicate similar shape of the survival curves. Preliminary results of experiments on adaptation of Drosophila melanogaster to unfavorable food show that temporal scalability of survival curves is sometimes present in more complex organisms, although this is not a universal rule. Both evolutionary and environmental changes sometimes affect only the average lifespan without changing the coefficient of variation (in this case, temporal scaling is present), but often both parameters (i.e. both scale and shape of the survival curve) change simultaneously. In addition to the relative stability of the coefficient of variation, another possible argument in favor of genetic determination of the aging process is relatively low variability of the time of death, which is sometimes of the same order of magnitude as the variability of timing of other ontogenetic events, such as the onset of sexual maturation.

Experimental adaptation of Drosophila melanogaster to nutrient-deficient starch-based (S) medium resulted in lifespan shortening, increased early-life fecundity, accelerated reproductive aging, and sexually dimorphic survival curves. The direction of all these evolutionary changes coincides with the direction of phenotypic plasticity observed in non-adapted flies cultured on S medium. High adult mortality rate caused by unfavorable growth medium apparently was the main factor of selection during the evolutionary experiment. The results are partially compatible with Williams’ hypothesis, which states that increased mortality rate should result in relaxed selection against mutations that decrease fitness late in life, and thus promote the evolution of shorter lifespan and earlier reproduction. However, our results do not confirm Williams’ prediction that the sex with higher mortality rate should undergo more rapid aging: lifespan shortening by S medium is more pronounced in naive males than females, but it was female lifespan that decreased more in the course of adaptation. These data, as well as the results of testing of F1 hybrids between adapted and control lineages, are compatible with the idea that the genetic basis of longevity is different in the two sexes, and that evolutionary response to increased mortality rate depends on the degree to which the mortality is selective. Selective mortality can result in the development of longer (rather than shorter) lifespan in the course of evolution. The results also imply that antagonistic pleiotropy of alleles, which increase early-life fecundity at the cost of accelerated aging, played an important role in the evolutionary changes of females in the experimental lineage, while accumulation of deleterious mutations with late-life effects due to drift was more important in the evolution of male traits.