Advanced maternal age has negative multigenerational impacts during Drosophila melanogaster embryogenesis.

Increasing maternal age is commonly accompanied by decreased fitness in offspring. In Drosophila melanogaster, maternal senescence negatively affects multiple facets of offspring phenotype and fitness. These maternal effects are particularly large on embryonic viability. Identifying which embryonic stages are disrupted can indicate mechanisms of maternal effect senescence. Some maternal effects can also carry-over to subsequent generations. We examined potential multi- and transgenerational effects maternal senescence on embryonic development in two laboratory strains of D. melanogaster. We categorized the developmental stages of embryos from every combination of old and young mother, grandmother and great grandmother. We then modelled embryonic survival across the stages and compared these models among the multigenerational maternal age groups in order to identify which developmental processes were most sensitive to the effects of maternal effect senescence. Maternal effect senescence has negative multigenerational effects on multiple embryonic stages, indicating that maternal provisioning and, possibly epigenetics, but not mutation accumulation, contribute to decreased offspring survival. This study shows the large, early and multi-faceted nature of maternal effects senescence in an insect population.

Transgenerational effects of maternal and grandmaternal age on offspring viability and performance in Drosophila melanogaster.

In non-social insects, fitness is determined by relative lifetime fertility. Fertility generally declines with age as a part of senescence. For females, senescence has profound effects on fitness by decreasing viability and fertility as well as those of her offspring. However, important aspects of these maternal effects, including the cause(s) of reduced offspring performance and carry-over effects of maternal age, are poorly understood. Drosophila melanogaster is a useful system for examining potential transgenerational effects of increasing maternal age, because of their use as a model system for studying the physiology and genetic architecture of both reproduction and senescence. To test the hypothesis that female senescence has transgenerational effects on offspring viability and development, we measured the effects of maternal age on offspring survival over two generations and under two larval densities in two laboratory strains of flies (Oregon-R and Canton-S). Transgenerational effects of maternal age influence embryonic viability and embryonic to adult viability in both strains. However, the generation causing the effects, and the magnitude and direction of those effects differed by genotype. The effects of maternal age on embryonic to adult viability when larvae are stressed was also genotype-specific. Maternal effects involve provisioning: older females produced smaller eggs and larger offspring. These results show that maternal age has profound, complex, and multigenerational consequences on several components of offspring fitness and traits. This study contributes to a body of work demonstrating that female age is an important condition affecting phenotypic variation and viability across multiple generations.

The song of the old mother: reproductive senescence in female drosophila.

Among animals with multiple reproductive episodes, changes in adult condition over time can have profound effects on lifetime reproductive fitness and offspring performance. The changes in condition associated with senescence can be particularly acute for females who support reproductive processes from oogenesis through fertilization. The pomace fly Drosophila melanogaster is a well-established model system for exploring the physiology of reproduction and senescence. In this review, we describe how increasing maternal age in Drosophila affects reproductive fitness and offspring performance as well as the genetic foundation of these effects. Describing the processes underlying female reproductive senescence helps us understand diverse phenomena including population demographics, condition-dependent selection, sexual conflict, and transgenerational effects of maternal condition on offspring fitness. Understanding the genetic basis of reproductive senescence clarifies the nature of life-history trade-offs as well as potential ways to augment and/or limit female fertility in a variety of organisms.

Oh, the places they'll go: Female sperm storage and sperm precedence in Drosophila melanogaster.

Among most animals with internal fertilization, females store sperm in specific regions of their reproductive tract for later use. Sperm storage enables prolonged fertility, physical and temporal separation of mating from fertilization and, when females mate with multiple males, opportunities for differential use of the various males' sperm. Thus, stored sperm move within the female reproductive tract as well as to several potential fates - fertilization, displacement by other sperm or ejection by the female. Drosophila melanogaster is a leading model system for elucidating both the mechanisms and evolutionary consequences of female sperm storage and differential male fertilization success. The prominence of Drosophila is due, in part, to the ability to examine processes influencing sperm movement and fate at several biological levels, from molecules to organ systems. In this review, we describe male and female factors, as well as their interactions, involved in female sperm storage and differential male fertilization success.

A requirement for the neuromodulators octopamine and tyramine in Drosophila melanogaster female sperm storage.

Female sperm storage is common among organisms with internal fertilization. It is important for extended fertility and, in cases of multiple mating, for sperm competition. The physiological mechanisms by which females store and manage stored sperm are poorly understood. Here, we report that the biogenic amines tyramine (TA) and octopamine (OA) in Drosophila melanogaster females play essential roles in sperm storage. D. melanogaster females store sperm in two types of organs, a single seminal receptacle and a pair of spermathecae. We examined sperm storage parameters in females mutant in enzymes required for the biochemical synthesis of tyrosine to TA and TA to OA, respectively. Postmating uterine conformational changes, which are associated with sperm entry and accumulation into storage, were unaffected by the absence of either TA or OA. However, sperm release from storage requires both TA and OA; sperm were retained in storage in both types of mutant females at significantly higher levels than in control flies. Absence of OA inhibited sperm depletion only from the seminal receptacle, whereas absence of both OA and TA perturbed sperm depletion from both storage organ types. We find innervation of the seminal receptacle and spermathecae by octopaminergic-tyraminergic neurons. These findings identify a distinct role for TA and OA in reproduction, regulating the release of sperm from storage, and suggest a mechanism by which Drosophila females actively regulate the release of stored sperm.

Sex peptide is required for the efficient release of stored sperm in mated Drosophila females.

The Drosophila seminal fluid protein (SFP) sex peptide (SP) elicits numerous post-mating responses, including increased egg laying and decreased sexual receptivity, in the mated female. Unlike other SFPs, which are detectable in mated females for only a few hours post mating, SP is maintained-and its effects are sustained-for several days. The persistence of SP in the mated female's reproductive tract is thought to be a consequence of its binding to, and gradual release from, sperm in storage, which maintains SP's ability to act within the female reproductive tract. Recent studies have shown that several other SFPs, acting in a network, are needed for SP's localization to sperm and are necessary for the efficient release of sperm from storage. This result suggested an additional new role for SP modulating the release of sperm from storage. We tested for this possibility by examining sperm storage parameters in mated females that did not receive SP. We found that while sperm accumulation into storage was unaffected, sperm depletion from storage sites was significantly decreased (or impaired) in the absence of SP. Mates of males expressing a modified SP that is unable to be released from sperm showed a similar phenotype, indicating that release of sperm-bound SP is a necessary component of normal sperm depletion. Additionally, SP null males were more successful in a sperm competitive environment when they were first to mate, which is likely a consequence of higher retention of their sperm due to defective sperm release. Our findings illustrate a direct role for SP in the release of sperm from storage.

Hold on: females modulate sperm depletion from storage sites in the fly Drosophila melanogaster.

Among many species of insects, females gain fitness benefits by producing numerous offspring. Yet actions related to producing numerous offspring such as mating with multiple males, producing oocytes and placing offspring in sub-optimal environments incur costs. Females can decrease the magnitude of these costs by retaining gametes when suitable oviposition sites are absent. We used the pomace fly, Drosophila melanogaster, to explore how the availability of fresh feeding/oviposition medium influenced female fitness via changes in offspring survivorship and the modulation of gamete release. Availability of fresh medium affected the absolute number and temporal production of offspring. This outcome was attributable to both decreased larval survival under crowded conditions and to female modulation of gamete release. Direct examination of the number of sperm retained among the different female storage organs revealed that females 'hold on' to sperm, retaining more sperm in storage, disproportionately within the spermathecae, when exposed infrequently to fresh medium. Despite this retention, females with lower rates of storage depletion exhibited decreased sperm use efficiency shortly after mating. This study provides direct evidence that females influence the rate of sperm depletion from specific storage sites in a way that can affect both female and male fitness. The possible adaptive significance of selective gamete utilization by female Drosophila includes lowering costs associated with frequent remating and larval overcrowding when oviposition sites are limiting, as well as potentially influencing paternity when females store sperm from multiple males.

Emergence of sperm from female storage sites has egg-influenced and egg-independent phases in Drosophila melanogaster.

The coordinated introduction of sperm and eggs is a prerequisite of high fertilization efficiency. In Drosophila melanogaster, as in most internally fertilizing animals, mated females store sperm prior to fertilization. Yet the regulation of sperm exit from these storage sites is poorly understood. To test one likely factor that could coordinate gamete availability, we quantified sperm exit from storage in three types of female: genetically matched females that were normal or eggless, and an additional wild-type control. Long-term depletion of sperm stores in normal females and eggless females occurs at similar rates. However, soon after mating, egg presence appears to accelerate the transition from one storage stage to the next. Since male ejaculate components and female factors contribute to sperm depletion, opportunities exist for both cooperation and conflict between the sexes in sperm storage dynamics.

An early role for the Drosophila melanogaster male seminal protein Acp36DE in female sperm storage.

Female sperm storage is an essential component of reproduction in many animals. In insects, female sperm storage affects fecundity, sperm competition/preference and receptivity to re-mating. Female sperm storage consists of several stages, including sperm entry into the sperm storage organs (SSOs), maintenance within the SSOs and exit from the SSOs. The Drosophila melanogaster male seminal protein Acp36DE is essential for female sperm storage. Acp36DE associates with sperm and localizes to specific regions of the female reproductive tract, including the SSOs. We determined the stage of sperm storage at which Acp36DE acts by comparing the timing of initial sperm entry into storage as well as the rates of sperm accumulation and release from the SSOs in the presence or absence of Acp36DE. Acp36DE accelerates sperm accumulation into storage but does not mediate the entry of the first sperm into storage. This finding also demonstrates that the initial stage of sperm storage consists of multiple steps. Acp36DE enters the SSOs before sperm, and its residence within the SSOs does not require sperm. We propose that once sperm storage has initiated, Acp36DE acts as a guidance factor helping subsequent sperm move into storage, a corral concentrating sperm around the SSO entrances and/or a trigger for responses within the female that accelerate storage of sperm.

The developments between gametogenesis and fertilization: ovulation and female sperm storage in Drosophila melanogaster.

In animals with internal fertilization, ovulation and female sperm storage are essential steps in reproduction. While these events are often required for successful fertilization, they remain poorly understood at the developmental and molecular levels in many species. Ovulation involves the regulated release of oocytes from the ovary. Female sperm storage consists of the movement of sperm into, maintenance within, and release from specific regions of the female reproductive tract. Both ovulation and sperm storage elicit important changes in gametes: in oocytes, ovulation can trigger changes in the egg envelopes and the resumption of meiosis; for sperm, storage is a step in their transition from being "movers" to "fertilizers." Ovulation and sperm storage both consist of timed and directed cell movements within a morphologically and chemically complex environment (the female reproductive tract), culminating with gamete fusion. We review the processes of ovulation and sperm storage for Drosophila melanogaster, whose requirements for gamete maturation and sperm storage as well as powerful molecular genetics make it an excellent model organism for study of these processes. Within the female D. melanogaster, both processes are triggered by male factors during and after mating, including sperm and seminal fluid proteins. Therefore, an interplay of male and female factors coordinates the gametes for fertilization.