Why is individual reproduction in Drosophila flies stochastic?

Reproduction is essential in studying of aging and senescence in fruit flies as for the resources devoted to egg-laying are subtracted from the total resources of the organism and thus intensive reproduction shorten the life span of an individual. According to prevailing opinion, the stochastic nature of spatial and temporal distribution of external factors leads to randomness of reproductive patterns in fly populations in the wild. Environments are often not constant, but can vary stochastically. The amplitude of variability in environmental conditions influences organismal responses (Boyce et al., 2006; Boggs, 2009). It was believed that the random character of egg-laying can be studied with stochasticity of reproductive behavior (Markow, 1996). Nonetheless, the question of why real egg-laying patterns are stochastic was never asked until 2003 (Novoseltsev et al., 2003b). To analyze random individual reproductive patterns for the first time it was proposed that Drosophila females should be studied by a three-stage non-random approximation embracing the time interval from hatching to death. The analysis included maturation (when eggs are ripened in ovarioles), adult stage (when eggs are laid in a maximal rate), and the senescence stage, when energy shortages produce an exponential decrease of this rate. This means that the total “stochasticity” in reproductive process was reflected by a set of random parameters adjusted individually for each pattern. Five parameters were used—the moment of the first egg laid was t0, duration of constancy interval of egg-laying T, time constant of exponential tail τ, reproductive capacity RC, and life span LS (Novoseltsev et al., 2004). This three-stage approximation technique is the only one which produces the whole pattern description starting with an individual's hatching and ending at death. In this, it is different from the approximations related to various segments of the reproductive process. For example, in Muller et al. (2001) it is shown that individual reproduction experiences exponentially decline in advanced ages, and in Rauser et al. (2003) the assertion is expressed that eggs laying is not reduced to zero in the end of life, but stabilizes at some low level. Still, the description of individual reproductive patterns contains two types of stochasticity. Slow changes in reproduction, connected with age alterations, are reflected in the “skeleton” of the pattern, but also there exist fast, day-to-day variations in egg-laying, reflected in the tooth-like graph imposed on the three-stage skeleton. Here, we discuss a hypothesis about the mechanisms that lead to the emergence of the second type of the randomness in the pattern, and on this basis we construct the model of egg production in silico. Then this model is used to study heterogeneity in resource allocation and causes of death in fruit flies. The death of a fly usually occurs at advanced ages when reproductive process has been completed. This is a death caused by senescence. However, in the case of a large share of resource for reproduction and a lack of resources for somatic maintenance, death may occur earlier. In this case, the fly is still in the full swing of egg-laying and death from reproductive overload occurs.