Reproductive and post‐reproductive life history of wild‐caughtDrosophila melanogasterunder laboratory conditions

Abstract

The life history of the fruit fly (Drosophila melanogaster) is well understood, but fitness components are rarely measured by following single individuals over their lifetime, thereby limiting insights into lifetime reproductive success, reproductive senescence and post-reproductive lifespan. Moreover, most studies have examined long-established laboratory strains rather than freshly caught individuals and may thus be confounded by adaptation to laboratory culture, inbreeding or mutation accumulation. Here, we have followed the life histories of individual females from three recently caught, non-laboratory-adapted wild populations of D. melanogaster. Populations varied in a number of life-history traits, including ovariole number, fecundity, hatchability and lifespan. To describe individual patterns of age-specific fecundity, we developed a new model that allowed us to distinguish four phases during a female's life: a phase of reproductive maturation, followed by a period of linear and then exponential decline in fecundity and, finally, a post-ovipository period. Individual females exhibited clear-cut fecundity peaks, which contrasts with previous analyses, and post-peak levels of fecundity declined independently of how long females lived. Notably, females had a pronounced post-reproductive lifespan, which on average made up 40% of total lifespan. Post-reproductive lifespan did not differ among populations and was not correlated with reproductive fitness components, supporting the hypothesis that this period is a highly variable, random 'add-on' at the end of reproductive life rather than a correlate of selection on reproductive fitness. Most life-history traits were positively correlated, a pattern that might be due to genotype by environment interactions when wild flies are brought into a novel laboratory environment but that is unlikely explained by inbreeding or positive mutational covariance caused by mutation accumulation.

The song of the old mother: Reproductive senescence in female drosophila

“…In these populations, a steady decline in fecundity was observed from 4 d-35 d pe followed by an exponential decline in fertility. 15 Genetic variation among populations was also documented for the duration of some reproductive phases including the time to peak fertility, and the timing and rate of the exponential decline in fertility, but not the rate of gradual decline in fertility. 15 The mechanisms underlying this fecundity decline include age-related changes in oogenesis and responses to the male seminal protein sex peptide (SP).…”

“…With regular exposure to males, daily fecundity changes with age. It rapidly increases peaking at >60 eggs/day (range of 65-104 eggs/day in different genetic backgrounds) around 4-7 d pe followed by a progressive decline with fecundity levels half of peak levels 22 d-28 d pe and resulting in either infertility by 50 d pe 14,15,27,58,59 or a fecundity plateau. 60,61 Changes in fecundity over time have recently been modeled with more precision using 3 different recently wild-caught populations.…”

“…The degree to which maternal age affects these life stages varies. 16 Embryonic viability (often measured as percentage of eggs hatching) is high (>80%) when females are <7 d pe and decreases by 9-65% as females age (>23 d pe) ( [14][15][16]59,74,81 , although only 59 controls for male age). This developmental stage best predicts overall offspring viability.…”

“…2,[5][6][7] However, many laboratory studies characterizing female reproductive physiology or testing hypotheses related to sexual selection focus only on young females in their reproductive prime (e.g., [8][9][10][11][12][13] ) and/or allow both male and female age to increase concurrently. [14][15][16] Since male reproductive physiology also changes with increasing age, 17,18 controlling for male age in experiments helps distinguish the effects of female age, male age, and their interactions, on phenomena associated with reproductive senescence.…”

Insulin signalling underlies both plasticity and divergence of a reproductive trait inDrosophila

“…Several lines of evidence suggest that ovariole number is adaptive. First, ovariole number is a strong determinant of reproductive capacity, and thus is positively correlated to female fecundity and fitness [10][11][12][13]. Second, ovariole number is heritable and lineage-specific.…”