Can female Drosophila melanogaster lay eggs without males?

Can female Drosophila melanogaster lay eggs without males?

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Can female Drosophila melanogaster lay egg without males?

I maintain our lab stock but find a line that seems to have all females (or all males). The flies have been in the vial for two weeks, but I don't see any eggs hatching or become larva.

Yes, I regularly have to collect female virgins (12500 of them in the last week). They will lay eggs especially when there is extra yeast available. It is actually a good way to check virginity (in case a fly hatched early and was already mature, or a male made it through sorting etc.) - put some extra yeast grains in the vial when you collect them, leave them for a few days and then check for larvae, if they are not virgins there will be eggs and larvae, if they are virgins there will only be eggs!

Very old females (such as those in vials that have not been flipped for a long time) will often lay unfertilized eggs in the absence of males. This happens to me occasionally when I am collecting virgins and then forget about them for a while.

Carnivory in the larvae of Drosophila melanogaster and other Drosophila species

Drosophila melanogaster is widely used as a model organism for biological investigations, and food is a major aspect of its ecology and evolutionary biology. Previous studies have shown that this insect can use fruits, yeasts and insect carcasses as its food sources. In this study, we demonstrate that this species is an omnivore, that its larvae can exploit not only fruits and yeast but also foods of animal origin (FAOs), and that larvae consume adult carcasses regularly. FAO-fed larvae develop into adulthood within a normal developmental time frame without the help of microbes. Yeast foods are better for Drosophila development than are foods of plant origin (FPOs) or FAO because in yeast foods, more eggs complete their life cycle, and the body size of emerged flies is much greater. Flies can use a mixture of yeast-FAO, which significantly boosts female fertility. Larvae digest FAOs externally. Larval D. virilis, D. hydei, and D. simulans are also omnivorous and demonstrate the same feeding habits as larval D. melanogaster. These findings prompt us to reconsider previous conclusions about the original adaptations of D. melanogaster and other Drosophila species and have direct implications for diet-related studies using Drosophila as a model organism.

Materials and methods

Fly strains

Flies (Drosophila melanogaster Meig) were raised on standard yeast-glucose media at 25°C and a 12 h:12 h L:D cycle. Female flies were collected within 6 h of eclosion to ensure virginity. Males were collected 24-48 h after eclosion. All experiments were conducted on flies that were 3-6 days post eclosion. Males from three genotypes(Neubaum and Wolfner, 1999b)were used to test the effects of Acp36DE on sperm storage: (1) Acp36DE 1 /Df(2L)H20 males, which transfer normal quantities of sperm and seminal fluids but no Acp36DE, (2) Acp36DE 1 /CyO control males and (3) Acp36DE + /Df(2L)H20 control males. Two different lines were used as controls for the genetic background of the Acp36DE-deficient males: Acp36DE 1 /CyO controlled for the background of the mutagenized line, and Acp36DE + /Df(2L)H20 controlled for the background of the deficiency line as well as for effects of loci other than Acp36DE uncovered by the deficiency (see Neubaum and Wolfner, 1999b for additional details). Spermless males (sons of Canton S males × bw sp tud 1 females Boswell and Mahowald, 1985)were produced as in Bertram et al.(1996). A transgene possessing the coding sequences for green fluorescent protein (GFP) driven by the sperm-specific don juan (dj) promoter(Santel et al., 1997) inserted on the X chromosome (strain provided by B. Wakimoto) was crossed into the Df(2L)H20/CyO strain. This allowed us to generate Acp36DE-deficient or control males, as above, whose GFP-labeled sperm could be visualized within the female reproductive tract. When crossed into the Acp36DE 1 or Acp36DE + background, males produced GFP-labeled sperm and were either deficient or wild-type, respectively, for Acp36DE. Wild-type females were either Oregon R or Canton S, as stated. We saw no significant difference between the two types of females in the number of sperm stored 6 h after mating(t16=0.53, P=0.61). Because these females have a similar sperm storage pattern, using them in separate experiments should not affect the observed trends.

Timing of sperm storage in females

Effects of Acp36DE on sperm storage were examined by counting sperm stored within female SSOs (seminal receptacles and spermathecae) at various times after the start of mating. Virgin Oregon R females were individually paired with an Acp36DE 1 /Df(2L)H20 or Acp36DE 1 /CyO male in a vial containing food. At 0.3, 0.5,0.7, 1, 2, 6, 10, 24, 48 or 72 h after the beginning of mating, the female was removed and processed for sperm counts as described in Neubaum and Wolfner(1999b). Blindly coded slides of individual female SSOs were examined for the presence of orcein-stained sperm at 100× magnification using a compound microscope with transmitted light (Zeiss Axioskop). Each sample was counted twice. Variation among repeated counts of the same sample was, on average, 8% of the sample mean,indicating consistency among individual sample counts (N=241 samples).

In separate experiments designed to compare the initial timing of Acp36DE entry with sperm entry into the SSOs, matings between Canton S females and males (N=23) were interrupted 10 min after the start of copulation,and sperm storage was quantified as described above.

The significance of differences in mean number of sperm stored both at different times and between females mated to males with or without Acp36DE was tested using a two-factor analysis of variance (ANOVA). Linear contrasts were performed as planned comparisons to examine increases in sperm storage within 6 h of the start of mating for each type of male(Neter et al., 1996). A least-square means contrast tested the null hypothesis that a linear combination of group parameters (corresponding to each time point examined)was equal to zero. The means and s.e.m. s used were calculated from the time effect in the ANOVA analysis. t-tests were used to determine at which times mean female sperm storage differed depending on the presence of Acp36DE. The depletion of sperm from female storage for each type of male(time points after 6 h) was modeled using regression analysis, and a t-test of the slope coefficients (b) tested whether the slopes were homogeneous. All sperm counts were transformed [√(value + 1)] to meet the assumptions of parametric statistical tests, but untransformed data are used in figures. Statistical analysis was performed using StatView software or JMP (both SAS Inc., Cary, NC, USA).

Acp36DE presence and persistence in the SSOs

Wild-type (Canton S) females were mated to wild-type (Canton S) or spermless (tudor-progeny see Materials and methods) males. Pairs were then separated to prevent remating. At 0.17, 0.33, 1, 10 and 48 h after the start of mating, females were dissected in Yamamoto's saline(Stewart et al., 1994). Triplicate samples of 30 seminal receptacles and spermathecae per treatment and time point were placed separately into 10 μl of protease-inhibiting buffer (Monsma and Wolfner,1988), homogenized, processed and analyzed by western blotting as in Bertram et al. (1996).

Visualizing sperm storage in real time

Effects of Acp36DE on sperm entry into the seminal receptacle and their motility therein were examined by visualizing GFP-labeled sperm stored within females that had mated to males with or without Acp36DE. Copulations were interrupted at either 0.25 h or 0.33 h after the start of mating, and females were immediately placed on ice. A female's entire reproductive tract was removed as a unit and mounted in 4% methyl cellulose (Sigma, St Louis, MO,USA) in Yamamoto's saline. Optical sections of reproductive tracts were imaged at 40× (Zeiss Axiovert 10) then reassembled for analysis (BioRad MRC 600). Only those samples in which sperm were observed in the uterus(indicating sperm transfer) were included in the analysis. The presence and orientation of sperm within the seminal receptacle was observed and the association between sperm presence in the seminal receptacle and male genotype was tested using a χ 2 test of independence(Sokal and Rohlf, 1995).

A changing mating signal may initiate speciation in populations of Drosophila mojavensis

Male and female of Drosophila mojavensis wrigleyi during mating. In this subspecies, males advertise their presence by discharging a droplet of anal secretions in the vicinity of females. The droplet contains a sex pheromone that enhances female receptivity. Credit: Benjamin Fabian, Max Planck Institute for Chemical Ecology

When choosing a mate, females of different subspecies of Drosophila mojavensis recognize the right mating partners either mainly by their song or by their smell. This was discovered by researchers at the Max Planck Institute for Chemical Ecology and their international collaboration partners, as a new study reports.

A specific male sex pheromone is only produced by males from two of the four subspecies, and is crucial for the mate choice of the corresponding females. Females from the subspecies in which the males no longer produce this pheromone are also able to perceive the chemical messenger, but for them, the specific mating song is more important for the choice of the right males than their smell. New species apparently evolve when the chemical mating signal is altered, and when, in turn, the signal is reinterpreted by the opposite sex in the context of other signals, such as the courtship song. The study is published in Science Advances.

Four subspecies of the desert-dwelling fly Drosophila mojavensis are known in the U.S. and Mexico. They only evolved about 250,000 years ago, which is a relatively short period from an evolutionary perspective. An investigation of these subspecies is therefore an opportunity for scientists to follow evolutionary events and the incipient speciation. The four subspecies are found in geographically isolated regions. While the two northern subspecies specialized on the fruits of cactus species in the Mojave Desert or on the Californian island of Santa Catalina, the two southern subspecies use cacti in the Sonora Desert and in the Mexican part of California as their food and breeding substrate.

Of particular interest is the different mating behavior of the four Drosophila mojavensis subspecies. In their natural environment, males usually choose a site close to their brood substrate and attract females to this location. By conducting chemical analyses and neurobiological experiments, the research team was able to identify the chemical signals involved in courtship and mating and understand their function.

The loss of a pheromone can be an isolating mechanism

Although the subspecies have only been separated for a relatively short evolutionary time scale, the scientists discovered a pheromone only produced by the males in the two northern subspecies, whereas the males of the southern species do not produce it.

"Females of the northern subspecies prefer males that produce this odor and thus avoid mating with males of the southern subspecies," said Markus Knaden, senior author of the study. Surprisingly, the females of the southern subspecies were also able to detect this pheromone, but selected the right males anyway, even if the pheromone of their northern relatives had been applied to their male conspecifics. They apparently ignored the scent and attached greater importance to the courtship song specific to their subspecies when choosing a mate. For females of the northern subspecies, on the other hand, the male courtship song was far less important than the right scent when choosing a mate.

The video shows a male and female Drosophila mojavensis sonorensis fly copulating. The courtship song of the male is produced by vibrations of the wings. In this subspecies, females give the male song a higher priority than the presence of a pheromone when choosing a partner. Credit: Mohammed Khallaf and Ibrahim Alali, Max Planck Institute for Chemical Ecology

All four subspecies of Drosophila mojavensis use an additional sex pheromone as a mating signal. The researchers were able to show that this chemical compound is not perceived as an olfactory signal, but rather via gustatory cells on the foreleg of the flies. Interestingly, this pheromone, which is transferred from a male to a female during mating, acts like an anti-aphrodisiac on other males and prevents mated females from mating again before laying their eggs. By transmitting this pheromone during mating, a male can thus ensure his paternity.

The olfactory receptor responsible for female responses to sex pheromones identified using CRISPR-Cas9

In addition to chemical analyses and behavioral experiments, the scientists investigated which areas of the fly brain respond to the pheromones during mating. "The CRISPR-Cas9 technology allowed us to identify and even silence the olfactory channels that underlie the sexual behaviors in Drosophila mojavensis. This enabled us to solve the longstanding mystery of the isolation barriers responsible for the evolution of the four Drosophila mojavensis subspecies," says Mohammed Khallaf, the study's lead author.

The researchers observed that an activation of the olfactory receptor Or65a induces female receptivity in a subspecies of D. mojavensis. Interestingly, the same receptor also exists in the well-studied model species Drosophila melanogaster, where it has the opposite effect. However, in D. melanogaster, Or65a mediates that mated females are less attracted to the sex pheromone of other males.

The evolution of sex pheromones still holds many mysteries. A new odor signal produced by one sex must also be perceived and correctly interpreted by the other. In the case of the two southern subspecies of Drosophila mojavensis, one sex pheromone was lost in the course of evolution, while another mating signal, the courtship song of the males, was given a higher priority.

"We are currently identifying potential pheromones from a large number of flies. In order to gain a better understanding of pheromone evolution as a whole, we need to look more closely at other cases where either novel pheromones show up or where tiny chemical changes in closely related species might result in speciation events," says Bill Hansson, head of the Department of Evolutionary Neuroethology, explaining the further research plans.

Despite the complexity of changes in the production, detection and interpretation of mating signals, which do not always occur in a coordinated manner during the evolution of new species, one thing is certain: Females always find the right males, namely those of their own (sub)species. Whether they fall for a male scent or succumb to the charm of a song: it seems to be an advantage to weigh up all available clues thoroughly.


Direct costs

Females experiencing continuous exposure to males had an average lifetime fecundity that was 15.6% lower than that of females experiencing only minimal exposure to males (Fig. 3, F1,190 = 18.63, P < 0.0001, 2-way anova , factors = treatment [minimal vs. continuous exposure to males] and experimental block [1 vs. 2]). We estimate the 95% lower-bound (based on 10 000 bootstraps of the percentage ratio: 100*[−1]) of this percentage to be −10.0%, so we can be highly confident that persistent male courtship and re-mating reduced a female's fitness by at least one tenth of her lifetime reproductive output. A significant reduction in female lifetime fecundity due to interactions with males remained when we analysed only females that did not re-mate (11.7%, F1,136 = 6.89, P < 0.001, 2-way anova , factors = treatment [minimal vs. continuous exposure to males] and experimental block [1 vs. 2]), indicating that male behaviour alone harmed females. Last, the smaller assay of the direct effect of males on female fecundity during the oviposition stage of the life cycle (which was not included in our measure of male harm to females in adult competition vials) indicated that the presence of males at this time further reduced female fecundity (fecundity of females with males present was 8.84% lower than when males were absent, paired-test, t4 = 3.948, P = 0.02). As a result, our estimate of male harm to nonvirgin females, which was measured in the adult competition vials, is a conservative metric of total male harm.

Mean lifetime fecundity of females with minimal vs. continuous exposure to males.

Indirect benefits

The point estimates of the fitness of sons from primary and secondary males were not statistically different (Fig. 4, F1,116 = 0.66, NS, 2-way anova , factors = treatment [sons from primary vs. secondary sires] and experimental block [1, 2 or 3]) with the average number of grand-offspring (±SE) from sons derived through primary and secondary sires equaling 15.99 ± 0.636 and 15.22 ± 0.655, respectively. There was, however, a significant noncrossing interaction (P = 0.031) between blocks (1, 2 or 3) and treatment (sons from first vs. secondary sires), so we also analysed the data on a replicate by replicate basis and found that in none of the three replicates was there a statistically significant difference in the fitness of sons from first and secondary sires.

Mean grand-offspring production through sons produced from primary vs. secondary males that had mated their mothers.

Our lack of a finding of higher reproductive success of sons obtained from secondary sires may reflect lack of statistical power. Past studies of the LHM base population have shown there to be additive genetic variance for the lifetime reproductive success of adult males ( Chippindale et al., 2001 ), so some degree of indirect benefits via the sexy sons route would seem feasible despite the fact that our point estimate is less than zero (mean offspring from secondary-sire's sons – means offspring from primary-sire's sons = 15.22–15.99 = −0.77 ± 0.913). To address this issue we constructed a 95% upper bound for the percentage advantage in fitness of sons from secondary compared to primary sires (based on 10 000 bootstraps of the percentage ratio: 100*[−1]). This upper limit of the indirect benefits obtained by females through sexy sons was a 6.13% increase in grand-offspring production. Our estimate of indirect benefits to females is necessarily higher than the true value experienced on a per capita basis because our assay measured indirect benefits obtained by re-mated females and all females do not re-mate. Put another way, all females suffer the behavioural costs of interacting with males but only re-mated females obtain the potentially offsetting advantage of indirect benefits via sexy sons.


Like most invasive pests, SWD is a problematic insect in the United States. Its broad host range and lack of native predators make it a threat to fruit growers throughout the country. Organic control options are limited, but this article documents current research efforts and outlines various ways that growers can limit SWD presence and infestation on their land. This includes choosing crops whose fruiting phenology does not match up with SWD presence in their area, wise use of organically-approved sprays and attract-and-kill devices, employing plastic or fabric mulch to inhibit the development of infested fruit that has fallen on the canopy floor, and using exclusion tunnels to create a physical barrier between the crops and SWD in the field. Even more innovative research is being conducted on organic SWD control, so check the Organic Management of Spotted Wing Drosophila website for updates!

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Drosophila Development and Reproduction

One of the many reasons that make Drosophila an extremely valuable organism is that the molecular, cellular, and genetic foundations of development are highly conserved between flies and higher eukaryotes such as humans. Drosophila progress through several developmental stages in a process known as the life cycle and each stage provides a unique platform for developmental research. This video introduces each stage of the Drosophila life cycle and details the physical characteristics and major developmental events that occur during each stage. Next, the video discusses the genetic regulation of pattern formation, which is important for establishing the body plan of the organism and specifying individual tissues and organs. In addition, this video gives an overview of Drosophila reproduction, and how to use the reproductive characteristics of Drosophila to set up a genetic cross. Finally, we discuss examples of how the principles of Drosophila development and reproduction can be applied to research. These applications include RNA interference, behavioral assays of mating behaviors, and live imaging techniques that allow us to visualize development as a dynamic process. Overall, this video highlights the importance of understanding development and reproduction in Drosophila, and how this knowledge can be used to understand development in other organisms.


Drosophila melanogaster, are widely used as a model organism in the study development and reproduction. Drosophila progress through several developmental stages in a process known as the life cycle and each stage provides a unique platform for developmental research. In this video, we will present the basics of Drosophila development and reproduction, including how to set up a genetic cross and discuss how this research can be applied to understand processes ranging from wound healing to behavior.

First, let&rsquos discuss the Drosophila life cycle. Drosophila progress through 4 main stages of development: embryo, larva, pupa, and adult.

The embryo is a fertilized egg that is about 0.5 mm long and oval shaped. Immediately after fertilization, the embryo undergoes rapid mitotic division without growth. The zygotic nucleus undergoes nine rounds of nuclear division, but does not undergo cytokinesis, forming a multi-nucleate cell called a syncytial blastoderm. Since all the nuclei in the syncytial blastoderm share a common cytoplasm, proteins can diffuse freely, forming morphogen gradients, which are important for establishing the body plan and patterning of individual organs and tissues in the fly. After the 10th nuclear division, the nuclei migrate to the periphery of the syncytial blastoderm . Following the 13th round of nuclear division, which occurs approximately 3 hours after fertilization, the 6000 nuclei in the syncytial blastoderm become individualized forming the cellular blastoderm . The cellular blastoderm contains a monolayer of cells and is transformed into a complex multi-layered structure, in a process known as gastrulation. During gastrulation, cell shape changes drive invaginations of the monolayer, ultimately creating the endoderm, mesoderm, and ectoderm germ layers. The endoderm gives rise to the gut, the mesoderm gives rise to the muscles and heart, and the ectoderm gives rise to the epidermis and central nervous system. After 24 hours, embryos hatch as larvae.

Larvae are white with worm-like segmented bodies. They crawl around in wet food eating constantly, leading to rapid growth. Larvae progress through three stages: the first instar for 24 hours, second instar for another 24 hours, and third instar for 48 hours. Molting occurs between each stage. When ready for pupation, third instar larvae leave their food source and attach to a firm surface, such as the side of a vial.

Pupa are immobile and are initially soft and white but eventually harden and turn brown. Over a period of four days, larval tissues degenerate and adult tissues form. Eclosion marks the end of the pupal stage and the flies emerge as adults.

8 hours after eclosion, the adults become sexually receptive and begin to mate, starting the life cycle all over again.

The complete life cycle takes about 10 days at 25 °C, but it can be affected by temperature. For example, at 18 °C the life cycle is about 19 days and at 29 °C, the life cycle is only 7 days.

Throughout development, careful genetic regulation of pattern formation establishes the body plan and specifies individual tissues and organs. Importantly, the establishment of the anterior-posterior axis defines the head to tail orientation of the organism, and is regulated by several groups of genes.

First, maternal effect genes are supplied in the oocyte and inherited from the female. They are important in the syncytial blastoderm for initially establishing the anterior and posterior of the embryo. In particular, the bicoid gene defines the anterior of the embryo including the head and thorax, while the nanos gene defines the posterior, including the abdomen.

Second, the segmentation genes, which are regulated by maternal effect genes, include the gap genes and pair rule genes. Gap genes establish a segmented body plan along the anterior-posterior axis by broadly subdividing the embryo. Pair rule genes are expressed in a striped pattern perpendicular to anterior-posterior axis, further dividing the embryo into smaller segments. Then the segment polarity genes, such as engrailed begin to establish cell fates within each segment.

Lastly, homeotic genes are responsible for defining particular anatomical structures, such as wings and legs. Interestingly, the order of the genes on the chromosome reflect how they are expressed along the anterior-posterior axis.

Drosophila are extremely fertile organisms that can produce thousands of progeny in a lifetime. Females lay hundreds of eggs per day and continue to fertilize eggs well after mating has occurred.

Drosophila are also sexually dimorphic organisms meaning that the females are phenotypically distinct from males. In particular, males are smaller than females and have darkly colored external genitalia, as well as more black pigment on their lower abdomens. Males also have a patch of bristles on their forelegs called sex combs used to latch onto the female during copulation. These distinct phenotypic differences make it very easy to distinguish males from females, which is particularly useful when setting up a genetic cross.

Setting up a cross with Drosophila is a useful technique for studying genetics. So let&rsquos get started!

The first step to setting up a cross is to collect virgin females of the desired genotype, so that you can control exactly which male with whom she will mate. Drosophila are unable to mate during the first 8 hours after eclosion, so collecting very young adults guarantees virginity. To collect newly eclosed females, clear the vial into the morgue to get rid of all adults. Every 3-4 hours, check the vial for newly eclosed adults, and collect the females in a new vial without any males until ready for use. Virgin females are identified by their very light body color and a dark spot on their abdomen, known as the meconium.

When ready to begin the cross, combine 4-6 males with 4-6 virgin females of your desired genotypes in a dated food vial, and store at 25° C and 60% humidity. After 3-4 days, larvae will be present and the parents should be transferred to a new vial, preventing the parents from mating with the progeny. After approximately 10 days, new offspring will emerge and their phenotypes can be examined.

One tool that Drosophila researchers use are balancer chromosomes that prevent genetic recombination and contain genetic markers such as curly wings, which are useful in determining the correct genotype of a fly. If you wanted flies that are heterozygous for two different mutations, you can cross a stock with mutation #1 over the balancer chromosome CyO, to a second stock with mutation #2 also balanced over CyO. Any progeny that emerge without curly wings are heterozygous for both mutations.

Another commonly used tool in Drosophila research is the UAS-GAL4 system, which allows researchers to express or knockdown a gene in a specific tissue. GAL4 is a yeast transcription factor that is driven by a tissue specific promoter and UAS is the Upstream Activating sequence, which controls the expression of the gene of interest . When you cross a fly with a tissue specific GAL4 transgene to a fly with a UAS transgene with your gene of interest directly downstream, the GAL4 protein binds the UAS and drives expression of your desired gene. For example, UAS-GFP crossed to apterous-GAL4, which is specific for the wing discs in pupa, expresses GFP specifically in those cells.

There are many applications that can be used to study Drosophila development and reproduction. One application is behavioral analyses - specifically courtship behavior. During courtship, the male orients himself towards the female and follows her while tapping her with his forelegs. If the female is receptive, she allows the male to mount her. The male curls his abdomen and transfers seminal fluid into the female, a process known as copulation. The analyses of these behaviors of courtship in various mutants gives insight into the genetic control of behavior

Drosophila development is an extremely dynamic process that includes many cell movements and shape changes, which can be studied via live imaging. For example, dorsal closure during embryogenesis is when a gap in the epithelium is closed in a zipper-like manner involving the coordination of many cell types. Dorsal closure during development is often used as a model to study wound closure, which may have clinical implications.

A third application used to understand processes during Drosophila development is RNA interference, which knocks down the activity of individual genes and can be used in large scale reverse genetic screens. For example, dsRNA can be injected into embryos, and the impact of the gene knockdown on organ development, for example, can be assessed. Here, RNA interference revealed a gene important for fusion during tracheal development.

You&rsquove just watched JoVE&rsquos introduction to Drosophila melanogaster reproduction and development . In this video we reviewed: the Drosophila life cycle, including details about each stage of development. We also learned how to use the reproductive capabilities of Drosophila to study genetics and set up a cross. Finally, we learned how Drosophila development and reproduction are useful for understanding complex processes such as behavior, wound closure, and organ development.


We investigated how three aspects of male condition influenced the stimulation of post-mating female aggression. We found that old males stimulated less aggression in females, less time on the food cap, and were less likely to stimulate egg production. This effect of age was particularly strong for mates of old sexually active males, with females mated to Old-F males being the most similar to virgin females in all our behavioural and fecundity measures. Our results suggest that these differences in female behaviour due to male condition are likely predominantly driven by changes in Sfp quality, but that age and mating related changes in sperm numbers transferred to females also contribute.

4.1 Male age and mating history

Male age was the main aspect of male condition that affected how much female aggression was stimulated by mating. The quality of some Sfps decline with age, and quantity of sperm declines both with age and mating (Ruhmann et al., 2018 Sepil et al., 2020 ). These reductions come with major costs – in previous studies, old sexually active males fathered fewer offspring, were more likely to be infertile, were worse at suppressing female remating, and performed poorly in sperm competition (Koppik & Fricke, 2017 Koppik et al., 2018 Ruhmann et al., 2018 Sepil et al., 2020 Snoke & Promislow, 2003 ). Our results agree with previous work which indicates females can detect differences among male ejaculates and these differences influence the strength of their PMRs, including aggression (Bath et al., 2017 Bretman et al., 2010 Fricke et al., 2008 Guo & Reinhardt, 2020 Hopkins et al., 2019 Ruhmann et al., 2018 Sepil et al., 2020 ). Interestingly, different PMRs respond differently to aspects of male variation. While Old-F and Old-U males are both poor sperm competitors, Old-U males do not differ from young males in their reproductive output, fertility and ability to suppress female remating (Sepil et al., 2020 ). These differences are primarily due to differences in the ageing of sperm and seminal fluid proteins (Sfps). Sperm transfer declines in Old-F males, but not in Old-U males, but at least some Sfps undergo qualitative changes with age (Sepil et al., 2020 ). For post-mating female aggression, male age was the only significant factor, with both Old-U and Old-F males stimulating less aggression than young males, suggesting this age difference was potentially driven by a decline in Sfp quality (Sepil et al., 2020 ). However, females mated to Old-F males showed values closest to virgin females, suggesting a potential role for sperm quantity in determining their level of aggression as well.

Sperm is necessary for females to display a full increase in aggression after mating (Bath et al., 2017 ). It therefore seems likely that the significant reduction in the amount of sperm transferred to females by Old-F males is primarily responsible for the corresponding reduction in female aggression. Old-F males have previously been shown to transfer both fewer and lower quality sperm (Ruhmann et al., 2018 Sepil et al., 2020 ), but it is unclear whether it is sperm number, quality or both, which influence the degree to which mating induces female aggression. Future studies investigating whether it is overall sperm number, number of viable sperm or Sfp quality that stimulate this aggression would shed light on this matter, as well as the mechanism by which ejaculates stimulate aggression.

We show that post-mating female feeding duration can also be influenced by male age and mating history. Female nutrition has been closely linked to fitness in Drosophila and many other species (Chapman & Partridge, 1996 ). Male condition altered the amount of time females spent acquiring this nutrition, suggesting significant flow-on effects for female fitness. Mates of Old-F males spent the same amount of time on the food cap as virgins, while mates of Old-U males showed the full post-mating increase in feeding duration. These feeding results are consistent with findings that increased female feeding after mating is stimulated by sperm and possibly by Sfps (Carvalho et al., 2006 ). Feeding and aggression are often linked, with females displaying more aggression also spending more time on the food cap (Bath et al., 2017 , 2018 ). Our results from both experiments suggest that headbutt duration and food cap duration show similar patterns, with females that had been stimulated to spend more time fighting also spending more time on the food cap.

4.2 Male feeding status

How males alter their ejaculate in response to nutrient availability varies dramatically across species. Across both vertebrates and invertebrates, there is a common trend for seminal fluid and sperm quantity to decrease in response to nutrient limitation (Macartney et al., 2019 ). However, at the same time, there is also a trend in other species for males to increase their investment in ejaculate traits in response to limited nutrients (Mehlis et al., 2015 Perry & Rowe, 2010 ). Adult male D. melanogaster with less dietary yeast (a main source of protein) exhibit a reduced ability to prevent females from remating with rival males (a sperm and Sfp-mediated trait) (Fricke et al., 2008 ). As female aggression is stimulated by both sperm and Sfp transfer, we predicted that it would be a trait sensitive to differences between males in their adult feeding status. However, we found that although male adult feeding status influenced mating duration, it did not significantly alter female aggression or other PMRs, such as egg production. There was a suggestion that females mated to starved males spent slightly less time on the food cap than those mated to fed males, but this was not significant.

Starving males for 3 days may not have been a strong enough treatment to alter males’ ability to produce or transfer ejaculates in their first mating. However, a similar treatment where males were starved for 3 days before mating showed a significant reduction in the transfer of a PMR-inducing pheromone (cis-vaccenyl acetate) (Lebreton et al., 2014 ). We found that starved males mated for around 3 min less than fed males, which suggests a significant effect of starvation on a males' ability to perform mating behaviours. Mating duration has previously been shown not to correlate with sperm transfer in this species (Gilchrist & Partridge, 2000 Lüpold et al., 2011 ), but the relationship between mating duration and the transfer of seminal fluid proteins appears to be more complicated (Hopkins et al., 2019 Hopkins et al., 2019 Sepil et al., 2020 Sirot et al., 2011 Wigby et al., 2009 ). The differences in mating duration between fed and starved males may indicate differences in the size or amount of ejaculate males were transferring to females, though we found little evidence in the PMRs of females to support this supposition. Males raised in different developmental environments have been shown to transfer similar-sized ejaculates in their first matings despite differences in their ability to produce and replenish them afterwards (Wigby et al., 2016 ). Starved males may have transferred a larger proportion of their ejaculate reserves during their first mating but be unable to replenish them for a second mating, which we did not test in this experiment. Male feeding status may therefore only begin to influence female PMRs, including aggression, from the second mating onwards.

Whether increased female aggression after mating is adaptive for males or females has yet to be tested. Increasing aggression after mating may be an adaptive response by females as their nutritional needs shift to accommodate their increased investment in reproduction (Boggs, 1981 ). Acquiring more food, and particularly the more limited high-protein yeast, may require females to compete more vigorously with other females to access limited food resources. Variation in male ejaculate quality or quantity may indicate how much females should increase their overall investment in reproduction, and subsequently, in aggression—that is, a female mated to an old, sexually active male will receive less sperm and produce fewer offspring and therefore invest less in reproduction than a female mated to a young male. This comparative reduction in reproduction means the first female will require less food and therefore need to show less aggression. Conversely, variation in female aggression due to male ejaculates may not be adaptive but merely a by-product of the means of stimulation of aggression. A possible stimulation mechanism may be the female sperm storage organs filling with sperm. If the organs are filled with sperm, this triggers female aggression. If males transfer fewer sperm (such as old-F males), this will trigger less or no aggression in females, even if it would still benefit them to do so. Our results are more consistent with the second hypothesis as females mated to Old-F males were less likely to lay any eggs in our experiment (consistent with previous studies on these lines (Sepil et al., 2020 )), and showed less aggression. However, when they did lay eggs, they laid as many as all other mating treatments, suggesting it is the initial receipt of sperm that is related to the stimulation of aggression.

Potentially, females use mating as a cue to upregulate their aggression. This response may represent more of an ‘on–off’ switch with the receipt of male ejaculate components turning on the aggressive pathway, rather than females increasing their aggression in proportion to the amount of ejaculate they receive. One other post-mating response – ovipositor extrusion – has been suggested to follow a similar pattern, while other responses, such as oogenesis and reduction of receptivity, act more gradually and in a dose-dependent manner (Billeter & Wolfner, 2018 Rezával et al., 2012 ). The fact that females mated to Old-F males predominantly behaved like virgins in their post-mating aggressive behaviours, suggests that these females may not have received enough ejaculate to switch on this pathway. If they had shown an intermediate response, this would be more consistent with a dose-dependent effect. The idea of an ‘on–off’ switch is consistent with another study which found that different genotypes of males do not stimulate different levels of post-mating aggression in females, despite potential differences in their ejaculates (Bath et al., 2020 ).

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Keywords : oviposition preference, courtship, mating, fecundity, Drosophila melanogaster, menthol, choice

Citation: Abed-Vieillard D and Cortot J (2016) When Choice Makes Sense: Menthol Influence on Mating, Oviposition and Fecundity in Drosophila melanogaster. Front. Integr. Neurosci. 10:5. doi: 10.3389/fnint.2016.00005

Received: 26 October 2015 Accepted: 01 February 2016
Published: 22 February 2016.

Sylvia Anton, Institut National de la Recherche Agronomique, France
Claude Wicker-Thomas, Centre National de la Recherche Scientifique, France
Matthew Cobb, University of Manchester, UK

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