Evolution of increased early-life fecundity but faster reproductive senescence in Drosophila melanogaster females through adaptation to chronic live-yeast deprivation

Dietary restriction is a common ecological challenge that limits reproduction. Yet only a few studies have explored adaptation under chronic protein deprivation. We subjected four replicate laboratory-adapted populations (YLB) of Drosophila melanogaster to a complete deprivation of live-yeast to mimic diet restricted ecology. In this insect, live-yeast is a critical source of protein that strongly affect reproductive output, especially in females. Following 24 generations of experimental evolution, compared to their matched controls (BL), females from YLB populations showed increase in reproductive output early in life, both in presence and absence of live-yeast. The observed increase in reproductive output was not associated with any accommodating alteration in average egg size; and development time, pre-adult survivorship, and body mass at eclosion of the progeny. Interestingly, adult lifespan was also found to be unaffected. However, YLB females were found to have a significantly faster rate of reproductive senescence albeit without any change in a measure of lifetime reproductive output. Taken together, adaptation to LYD ecology shows that reproductive output can evolve without affecting lifespan, suggesting that widely observed reproduction-survival trade-off is not universal. Populations can optimize fitness by fine tuning the scheduling of reproduction even when lifetime reproductive output is constrained.

Male age alone predicts paternity success under sperm competition when effects of age and past mating effort are experimentally separated

Older males often perform poorly under post-copulatory sexual selection. It is unclear, however, whether reproductive senescence is because of male age itself or the accumulated costs of the higher lifetime mating effort that is usually associated with male age. To date, very few studies have accounted for mating history and sperm storage when testing the effect of male age on sperm traits, and none test how age and past mating history influence paternity success under sperm competition. Here, we experimentally manipulate male mating history to tease apart its effects from that of age on ejaculate traits and paternity in the mosquitofish, Gambusia holbrooki . We found that old, naive males had more sperm than old, experienced males, while the reverse was true for young males. By contrast, neither male age nor mating history affected sperm velocity. Finally, using artificial insemination to experimentally control the number of sperm per male, we found that old males sired significantly more offspring than young males independently of their mating history. Our results highlight that the general pattern of male reproductive senescence described in many taxa may often be affected by two naturally confounding factors, male mating history and sperm age, rather than male age itself.

Egg size variation in a long-lived polyandrous shorebird in the context of senescence and breeding phenology

Anisogamy is a central component of sex role evolution, however, the effect of female-female mating competition on egg size variation in polyandrous species is unclear. Moreover, egg size may also be shaped by age-dependent trade-offs between reproductive investments and somatic maintenance that are responsible for senescence. Here we investigate how mating behaviour and senescence are associated with egg size variation in female snowy plovers (Charadrius nivosus). Snowy plovers are long-lived shorebirds (longevity record: 20 years) that often produce several nests each year, with females either sequentially changing partners between breeding attempts or remaining monogamous between attempts. We examined how age, seasonality, body size, and mating behaviour relate to within- and between-female variation in egg volume using repeated measures collected over a 15-year period. We found no evidence of reproductive senescence in egg volume in snowy plover females. Rather, egg volume, polyandry, and re-nesting were strongly linked to breeding phenology: early breeding females had a higher likelihood of being polyandrous or replacing failed clutches, yet these individuals laid smaller eggs likely due to physiological limitations associated with the early season. Older individuals and local recruits secured the earliest breeding opportunities in the season suggesting that prior experience could give an edge in the female-female competition for mates. Larger females laid the largest eggs, as expected, but there was no relationship between body size and lay date - implying that size may not provide an advantage in female-female competition. Our findings highlight the existence of several direct and indirect constraints on female reproductive investment that likely shape individual variation in lifetime reproductive success. Future research investigating reproductive senescence of wild populations should consider mating system dynamics when examining variation in reproductive investment.

The impact of dietary protein:carbohydrate balance on lifespan and reproduction in Protaetia brevitarsis (Coleoptera: Scarabaeidae: Cetoniinae)

The establishment of efficient and sustainable production of industrially important insects necessitates the detailed knowledge of the optimal mixture of macronutrients required for maximising their performance and fitness. The white spotted flower chafer, Protaetia brevitarsis (Coleoptera: Scarabaeidae: Cetoniinae), is one of the most important edible insects in East Asia with high nutritional and medicinal value. Here, we report how the ratio of protein to digestible carbohydrate (P:C) in the diet influenced lifespan and reproductive performance in the adults of P. brevitarsis. Throughout their lifespan, beetles were fed ad libitum one of five diets with differing P:C ratio (0:1, 3:7, 1:1, 7:3, 1:0). Both lifespan and the number of eggs produced over the lifetime were maximised at the P:C ratio of 3:7 and declined as the ratio deviated away from this optimal P:C composition. Beetles fed a diet containing only protein (P:C 1:0) not only had the shortest lifespan but also exhibited substantially reduced lifetime egg production compared to those fed the other diets. However, the effects of dietary P:C ratio on daily egg production rate and egg hatchability were marginal. The number of eggs produced at each age stage peaked at the age of week 2 and then gradually declined with increasing age, showing the sign of reproductive senescence. Age-specific egg production was higher in beetles confined to three intermediate P:C ratios (3:7, 1:1, 7:3) than those confined to two extreme P:C ratios (0:1, 1:0) throughout their lifespan. The speed of age-related decrease in reproductive performance was the slowest at P:C 3:7. Our data have implications for optimising the production of this edible insect with emerging economic importance.

Targeted Downregulation of Estradiol Binding Na+/H+ Exchanger Nhx-2, Mimics Calorie Restriction, Extends Reproductive Longevity and Ameliorates Effects Associated With Alpha Synuclein Aggregation In C. Elegans

Setting in of reproductive senescence (RS) gives rise to several changes, making aged individuals susceptible to multiple disorders including neurodegenerative diseases, cardiovascular ailments and bone disorders amongst others. The present study, employing transgenic C. elegans that expresses ‘human’ alpha synuclein, endeavors to decipher the association of reproductive senescence with age-associated neurodegenerative diseases and behavioral ageing, under normal conditions and after being probed with estradiol. We carried out RNAi induced silencing of a subset of 22 genes that are known to delay RS, followed by studies on alpha-Synuclein aggregation and associated effects. These studies led us to functional characterization of the Na+/H+ exchanger; nhx-2, expressed exclusively in gut. We found that RNAi of nhx-2 not only ameliorates the effects associated with alpha-Synuclein aggregation, but it also attunes effects related to behavioral aging including that of reproductive health-span and neuroprotection via mimicking dietary restriction, as it alters food absorption from the gut. We further elucidated that these effects are Sir-2.1 driven as nhx-2 knock out did not delay reproductive senescence in knock down condition of sir-2.1. To substantiate our findings, we performed whole transcriptome analysis in nhx-2 mutant strain. Our data revealed differential expression of 61 out of 62 hallmark genes of CR described by GenDR, in knock out condition of nhx-2. As estradiol plays a central role in both reproductive health as well as neuronal health, we subjected worms to exogenous estradiol treatment and observed that it led to elevated levels of nhx-2. Studies on structural binding analysis demonstrated significant binding potential of estradiol receptor NHR-14 with nhx-2 gene and ChIP analysis revealed that estradiol treatment gives rise to enhanced NHX-2 levels through inducing the promoter specific histone H3 acetylation (H3K9) and lysine methylation (H3K4me3). These studies identify nhx-2 as an important modulator that extends reproductive longevity and ameliorates effects associated with alpha synuclein aggregation in C elegans.

Separating the effects of male age and past mating effort on paternity success under sperm competition

Older males often perform poorly under post-copulatory sexual selection. It is unclear, however, whether reproductive senescence is due to male age itself or the accumulated costs of the higher lifetime mating effort that is usually associated with male age. To date, very few studies have accounted for male mating history when testing for the effect of male age on sperm traits, and none test how age and past mating history influence paternity success under sperm competition. Here, we experimentally manipulate male mating history to tease apart its effects from that of age on ejaculate traits and paternity in the mosquitofish, Gambusia holbrooki. We found that old, naive males had more sperm than old, experienced males, while the reverse was true for young males. In contrast, neither male age nor mating history affected sperm velocity. Finally, using artificial insemination to experimentally control the number of sperm per male, we found that old males sired significantly more offspring than young males independent of their mating history. Our results highlight that the general pattern of male reproductive senescence described in many taxa may often be affected by two naturally confounding factors, male mating history and sperm age, rather than male age itself.

1,25-Dihydroxyvitamin D deficiency accelerates male reproductive senescence in aging mice and 1,25(OH)2D3 alleviates oxidative stress via NF-κB/SOD

Based on this studies, we propose that 1,25(OH)2D3 can delay male reproductive aging, and we also propose that 1,25(OH)2D3 regulates NF-κB to exert antioxidant effect. Therefore, by targeting a fundamental aging mechanism, 1,25(OH)2D3 may be an effective agent in maintaining fertility and postponing male reproductive senescence.

REPRODUCTIVE SENESCENCE IMPAIRS THE ENERGY METABOLISM OF HUMAN GRANULOSA CELLS

Female age is the single greatest factor influencing reproductive performance. It is widely known that mitochondrial dysfunction plays a key role in reproductive senescence. Ovarian bioenergetics includes a sophisticated metabolic synergism between oocytes and human mural granulosa cells (GCs), which is crucial for oocyte maturation during follicular growth. These cells are believed to be potential biomarkers of oocyte quality. It has been proposed that alterations in their energy metabolism could lead to infertility. We investigated if there is an age-related effect on the energy metabolism of human mural granulosa cells. We performed an observational prospective cohort and experimental study including 127 women that underwent in vitro fertilization cycles allocated to two groups: a control group comprising oocyte donors aged less than 35 years and a group of infertile women aged over 38 years. The bioenergetics of cumulus cells and purified mural GCs were determined from oxidative phosphorylation parameters, aerobic glycolysis and adenine nucleotide levels. We have found that human mural GCs and cumulus cells present a high glycolytic profile and that the follicular fluid is critical to sustain their energy metabolism. GCs from older women present lower mitochondrial respiration and glycolysis than those from young donors which is not accompanied by a lower respiratory capacity. The diminished energy metabolism leads to a decrease in the total cellular energy charge. We conclude that, as women age, mural granulosa cells exhibit a reduction in their energy metabolism that is likely to influence female reproductive potential.