Although the primary function of mating is gamete transfer, male ejaculates contain numerous other substances that are produced by accessory glands and transferred to females during mating. Studies ...with several model organisms have shown that these substances can exert diverse behavioural and physiological effects on females, including altered longevity and reproductive output, yet a comprehensive synthesis across taxa is lacking. Here we use a meta-analytic approach to synthesize quantitatively extensive experimental work examining how male ejaculate quantity affects different components of female fitness. We summarize effect sizes for female fecundity (partial and lifetime) and longevity from 84 studies conducted on 70 arthropod species that yielded a total of 130 comparisons of female fecundity and 61 comparisons of female longevity. In response to greater amounts of ejaculate, arthropod females demonstrate enhanced fecundity (both partial and lifetime) but reduced longevity, particularly for Diptera and Lepidoptera. Across taxa, multiply mated females show particularly large fecundity increases compared to singly mated females, indicating that single matings do not maximize female fitness. This fecundity increase is balanced by a slight negative effect on lifespan, with females that received more ejaculate through polyandrous matings showing greater reductions in lifespan compared with females that have mated repeatedly with the same male. We found no significant effect size differences for either female fecundity or longevity between taxa that transfer sperm packaged into spermatophores compared to taxa that transfer ejaculates containing free sperm. Furthermore, females that received relatively larger or more spermatophores demonstrated greater lifetime fecundity, indicating that these seminal nuptial gifts provide females with a net fitness benefit. These results contribute to our understanding of the evolutionary origin and maintenance of non-sperm ejaculate components, and provide insight into female mate choice and optimal mating patterns.
The reproductive fitness of the Anopheles gambiae mosquito represents a promising target to prevent malaria transmission. The ecdysteroid hormone 20-hydroxyecdysone (20E), transferred from male to ...female during copulation, is key to An. gambiae reproductive success as it licenses females to oviposit eggs developed after blood feeding. Here we show that 20E-triggered oviposition in these mosquitoes is regulated by the stress- and immune-responsive c-Jun N-terminal kinase (JNK). The heads of mated females exhibit a transcriptional signature reminiscent of a JNK-dependent wounding response, while mating-or injection of virgins with exogenous 20E-selectively activates JNK in the same tissue. RNAi-mediated depletion of JNK pathway components inhibits oviposition in mated females, whereas JNK activation by silencing the JNK phosphatase puckered induces egg laying in virgins. Together, these data identify JNK as a potential conduit linking stress responses and reproductive success in the most important vector of malaria.
Postcopulatory sexual selection is recognized as a key driver of reproductive trait evolution, including the machinery required to produce endogenous nuptial gifts. Despite the importance of such ...gifts, the molecular composition of the non-gametic components of male ejaculates and their interactions with female reproductive tracts remain poorly understood. During mating, male Photinus fireflies transfer to females a spermatophore gift manufactured by multiple reproductive glands. Here we combined transcriptomics of both male and female reproductive glands with proteomics and metabolomics to better understand the synthesis, composition and fate of the spermatophore in the common Eastern firefly, Photinus pyralis. Our transcriptome of male glands revealed up-regulation of proteases that may enhance male fertilization success and activate female immune response. Using bottom-up proteomics we identified 208 functionally annotated proteins that males transfer to the female in their spermatophore. Targeted metabolomic analysis also provided the first evidence that Photinus nuptial gifts contain lucibufagin, a firefly defensive toxin. The reproductive tracts of female fireflies showed increased gene expression for several proteases that may be involved in egg production. This study offers new insights into the molecular composition of male spermatophores, and extends our understanding of how nuptial gifts may mediate postcopulatory interactions between the sexes.
Sexual dimorphism in adult Chinese fireflies. A. Male Aquatica ficta; B. Female A. ficta; C. Male Pyrocoelia pectoralis; D. Female P. pectoralis. These fireflies exhibit major differences in ...reproductive physiology and ecology. Display omitted
► We describe the time course of spermatophore transfer in Aquatica ficta. ► We describe the reproductive anatomy of Pyrocoelia pectoralis males and females. ► Female fecundity and hatching success increased with more matings in P. pectoralis. ► A single mating doubled female lifespan in A. ficta.
Many insect taxa show conspicuous sexual dimorphism in which females lack functional wings and are therefore incapable of flight. In fireflies, this loss of female flight is correlated with male production of spermatophore nuptial gifts, with species with flightless females also lacking gift production. In this study we further examined the relationship between sexual dimorphism and nuptial gifts by examining the reproductive ecology of two Asian fireflies, the sexually monomorphic Aquatica ficta (Luciolinae) and dimorphic Pyrocoelia pectoralis (Lampyrinae). We describe the reproductive anatomy of P. pectoralis males and females, and the time course of A. ficta spermatophore transfer. Through a series of mating experiments, we determined the effect of the number of matings on female fecundity, egg hatching success and female lifespan. The spermatophore-producing A. ficta was found to be monandrous, and female lifespan doubled as a result of that single mating. P. pectoralis was found to lack spermatophores but females were polyandrous and fecundity and egg hatching success both increased with additional matings. These results contradict patterns known from North American firefly species and provide insight into the role of male-derived substances in mating systems.
The beetle family Lampyridae (fireflies) encompasses ~100 genera worldwide with considerable diversity in life histories and signaling modes. Some lampyrid males use reproductive accessory glands to ...produce spermatophores, which have been shown to increase female lifetime fecundity. Sexual dimorphism in the form of neotenic and flightless females is also common in this family. A major goal of this study was to test a hypothesized link between female flight ability and male spermatophore production. We examined macroevolutionary patterns to test for correlated evolution among different levels of female neoteny (and associated loss of flight ability), male accessory gland number (and associated spermatophore production), and sexual signaling mode. Trait reconstruction on a molecular phylogeny indicated that flying females and spermatophores were ancestral traits and that female neoteny increased monotonically and led to flightlessness within multiple lineages. In addition, male spermatophore production was lost multiple times. Our evolutionary trait analysis revealed significant correlations between increased female neoteny and male accessory gland number, as well as between flightlessness and spermatophore loss. In addition, female flightlessness was positively correlated with the use of glows as female sexual signal. Transition probability analysis supported an evolutionary sequence of female flightlessness evolving first, followed by loss of male spermatophores. These results contribute to understanding how spermatophores have evolved and how this important class of seminal nuptial gifts is linked to other traits, providing new insights into sexual selection and life-history evolution.
Molecular interactions between male and female factors during mating profoundly affect the reproductive behavior and physiology of female insects. In natural populations of the malaria mosquito ...Anopheles gambiae, blood-fed females direct nutritional resources towards oogenesis only when inseminated. Here we show that the mating-dependent pathway of egg development in these mosquitoes is regulated by the interaction between the steroid hormone 20-hydroxy-ecdysone (20E) transferred by males during copulation and a female Mating-Induced Stimulator of Oogenesis (MISO) protein. RNAi silencing of MISO abolishes the increase in oogenesis caused by mating in blood-fed females, causes a delay in oocyte development, and impairs the function of male-transferred 20E. Co-immunoprecipitation experiments show that MISO and 20E interact in the female reproductive tract. Moreover MISO expression after mating is induced by 20E via the Ecdysone Receptor, demonstrating a close cooperation between the two factors. Male-transferred 20E therefore acts as a mating signal that females translate into an increased investment in egg development via a MISO-dependent pathway. The identification of this male-female reproductive interaction offers novel opportunities for the control of mosquito populations that transmit malaria.
Many chemotherapeutic agents selectively target rapidly dividing cells, including cancer cells, by causing DNA damage that leads to genome instability and cell death. We used Drosophila melanogaster ...to study how mutations in key DNA repair genes affect an organism's response to chemotherapeutic drugs. In this study, we focused on camptothecin and its derivatives, topotecan and irinotecan, which are type I topoisomerase inhibitors that create DNA double-strand breaks in rapidly dividing cells. Here, we describe two polymorphisms in Drosophila Cyp6d2 that result in extreme sensitivity to camptothecin but not topotecan or irinotecan. We confirmed that the sensitivity was due to mutations in Cyp6d2 by rescuing the defect with a wild-type copy of Cyp6d2. In addition, we showed that combining a cyp6d2 mutation with mutations in Drosophila brca2 results in extreme sensitivity to camptothecin. Given the frequency of the Cyp6d2 polymorphisms in publcly available Drosophila stocks, our study demonstrates the need for caution when interpreting results from drug sensitivity screens in Drosophila and other model organisms. Furthermore, our findings illustrate how genetic background effects can be important when determining the efficacy of chemotherapeutic agents in various DNA repair mutants.
Sexual selection drives the evolution of diverse traits that can prove advantageous in reproduction. Because females often mate with multiple males, traditional premating processes such as female ...choice and male-male competition have counterparts both during and after mating in the form of cryptic female choice and sperm competition. Therefore, it is critical to expand our view of sexual selection. The goal of this research was to investigate how nuptial gifts in the form of spermatophores operate in sequential episodes of sexual selection in several species of beetle. Examining how nuptial gifts affect male and female fitness components can provide insight into male trait evolution, patterns of female choice and potential sexual conflict. The impact of receiving relatively different quantities of genital nuptial gifts on female fitness parameters across many arthropod taxa was examined using a meta-analysis. In response to greater amounts of nuptial gifts, females demonstrate enhanced fecundity but reduced longevity. In two studies, spermatophore size in Photinus fireflies is manipulated to evaluate the effect of variation in nuptial gift size on female fitness parameters and male reproductive success. One of these studies documents a significant effect on female post-mating lifespan of receiving a single large spermatophore relative to a single small spermatophore, but no significant effect on female reproductive output. In the other study, firefly males with larger spermatophores experienced dual benefits in terms of both higher mate acceptance and increased paternity share. Additionally, rigourous phylogenetic methods are utilized to demonstrate a link between female flight and male spermatophore production in worldwide firefly species, with loss of female flight leading to a loss of male spermatophore production. An evaluation of the use of close chemical contact cues, cuticular hydrocarbons, to mediate communication in diurnal and nocturnal fireflies was done with gas chromatography. This analysis revealed undetectable levels of these cues in nocturnal species. Finally, proteomics and mass spectrometry were used to identify the seminal fluid proteome of male spermatophores in Tribolium castanuem. The results of these studies contribute a number of novel and broadly applicable insights into the nature and evolution of nuptial gifts in animal species.
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