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.
Anopheles mosquitoes have transmitted Plasmodium parasites for millions of years, yet it remains unclear whether they suffer fitness costs to infection. Here we report that the fecundity of virgin ...and mated females of two important vectors-Anopheles gambiae and Anopheles stephensi-is not affected by infection with Plasmodium falciparum, demonstrating that these human malaria parasites do not inflict this reproductive cost on their natural mosquito hosts. Additionally, parasite development is not impacted by mating status. However, in field studies using different P. falciparum isolates in Anopheles coluzzii, we find that Mating-Induced Stimulator of Oogenesis (MISO), a female reproductive gene strongly induced after mating by the sexual transfer of the steroid hormone 20-hydroxyecdysone (20E), protects females from incurring fecundity costs to infection. MISO-silenced females produce fewer eggs as they become increasingly infected with P. falciparum, while parasite development is not impacted by this gene silencing. Interestingly, previous work had shown that sexual transfer of 20E has specifically evolved in Cellia species of the Anopheles genus, driving the co-adaptation of MISO. Our data therefore suggest that evolution of male-female sexual interactions may have promoted Anopheles tolerance to P. falciparum infection in the Cellia subgenus, which comprises the most important malaria vectors.
Background The piglet is the only model to investigate the immunogenic relationship between Cryptosporidium hominis and C. parvum, the species responsible for diarrhea in humans. Despite being ...indistinguishable antigenically, and high genetic homology between them, they are only moderately cross protective after an active infection. Methodology/Principal findings Here we examined the degree of passive protection conferred to piglets suckling sows immunized during pregnancy with C. parvum. After birth suckling piglets were challenged orally with either C. parvum or C. hominis at age 5 days. Animals challenged with C. parvum had significant reduction of infection rate, while piglets challenged with C. hominis showed no reduction despite high C. parvum serum and colostrum IgG and IgA antibody. Conclusions/Significance We add these data to earlier studies where we described that infection derived immunity provides partial cross-protection. Together, it appears that for full protection, vaccines against human cryptosporidiosis must contain antigenic elements derived from both species.
The availability of genome sequences from 16 anopheline species provides unprecedented opportunities to study the evolution of reproductive traits relevant for malaria transmission. In Anopheles ...gambiae, a likely candidate for sexual selection is male 20-hydroxyecdysone (20E). Sexual transfer of this steroid hormone as part of a mating plug dramatically changes female physiological processes intimately tied to vectorial capacity. By combining phenotypic studies with ancestral state reconstructions and phylogenetic analyses, we show that mating plug transfer and male 20E synthesis are both derived characters that have coevolved in anophelines, driving the adaptation of a female 20E-interacting protein that promotes oogenesis via mechanisms also favoring Plasmodium survival. Our data reveal coevolutionary dynamics of reproductive traits between the sexes likely to have shaped the ability of anophelines to transmit malaria.
Environmental lead contamination negatively impacts human, animal, and ecosystem health, yet there is a lack of research in this area that incorporates a One Health framework – examining co-exposures ...among species through their shared environment. The purpose of this study was to integrate human and animal data with public soil lead levels to better understand lead exposure patterns across species in an urban US city. Over 200 soil samples were collected, analyzed for lead, and mapped in combination with other risk factors pulled from the literature to identify areas of highest risk. Human socio-demographic data, dog, and house sparrow density data were mapped to investigate the association between these variables and soil lead levels. Geospatial analysis software was used to visualize the geospatial distribution of soil lead levels and known risk factors for environmental lead contamination, and a block group risk score was calculated and mapped. Associations between human and animal-associated variables and soil lead levels and block risk scores were assessed using Spearman's correlations. Positive, statistically significant associations were found between soil lead levels and higher population density, higher education levels, and higher median household income. Areas with higher soil lead levels and lead exposure risk scores were associated with greater dog density and greater house sparrow density. This study fills an important knowledge gap on the risk of environmental lead exposure to humans, domestic animals, and wildlife.
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•Environmental lead similarly threatens human, domestic and wild urban inhabitants.•Environmental lead exposure is a prime field for One Health assessment.•There is a need to expand our understanding of ecosystem health threats.•Public soil lead levels sometimes exceeded state and federal thresholds for healthy soil.•Soil as an exposure source for humans and animals is underassessed.
Anopheles coluzzii females, important malaria vectors in Africa, mate only once in their lifetime. Mating occurs in aerial swarms with a high male-to-female ratio, where traits underlying male mating ...success are largely unknown. Here, we investigated whether cuticular hydrocarbons (CHCs) influence mating success in natural mating swarms in Burkina Faso. As insecticides are widely used in this area for malaria control, we also determined whether CHCs affect insecticide resistance levels. We find that mated males have higher CHC abundance than unmated controls, suggesting CHCs could be determinants of mating success. Additionally, mated males have higher insecticide resistance under pyrethroid challenge, and we show a link between resistance intensity and CHC abundance. Taken together, our results suggest that CHC abundance may be subject to sexual selection in addition to selection by insecticide pressure. This has implications for insecticide resistance management, as these traits may be sustained in the population due to their benefits in mating even in the absence of insecticides.
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.
Transmission of malaria parasites occurs when a female Anopheles mosquito feeds on an infected host to acquire nutrients for egg development. How parasites are affected by oogenetic processes, ...principally orchestrated by the steroid hormone 20-hydroxyecdysone (20E), remains largely unknown. Here we show that Plasmodium falciparum development is intimately but not competitively linked to processes shaping Anopheles gambiae reproduction. We unveil a 20E-mediated positive correlation between egg and oocyst numbers; impairing oogenesis by multiple 20E manipulations decreases parasite intensities. These manipulations, however, accelerate Plasmodium growth rates, allowing sporozoites to become infectious sooner. Parasites exploit mosquito lipids for faster growth, but they do so without further affecting egg development. These results suggest that P. falciparum has adopted a non-competitive evolutionary strategy of resource exploitation to optimize transmission while minimizing fitness costs to its mosquito vector. Our findings have profound implications for currently proposed control strategies aimed at suppressing mosquito populations.
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•Human malaria parasites interact non-competitively with their mosquito vectors•Mosquito hormone signaling co-regulates egg and parasite development•Parasites use host lipids for their growth via a mosquito lipid transporter•Parasites respond to mosquito metabolism with consequences for vector control
The development of the malaria-causing parasite Plasmodium falciparum depends on its ability to exploit the sexual cycle of its mosquito host in a non-competitive manner.
Anopheles gambiae and An. coluzzii, the two most important malaria vectors in sub-Saharan Africa, are recently radiated sibling species that are reproductively isolated even in areas of sympatry. In ...females from these species, sexual transfer of male accessory gland products, including the steroid hormone 20-hydroxyecdysone (20E), induces vast behavioral, physiological, and transcriptional changes that profoundly shape their post-mating ecology, and that may have contributed to the insurgence of post-mating, prezygotic reproductive barriers. As these barriers can be detected by studying transcriptional changes induced by mating, we set out to analyze the post-mating response of An. gambiae and An. coluzzii females captured in natural mating swarms in Burkina Faso. While the molecular pathways shaping short- and long-term mating-induced changes are largely conserved in females from the two species, we unravel significant inter-specific differences that suggest divergent regulation of key reproductive processes such as egg development, processing of seminal secretion, and mating behavior, that may have played a role in reproductive isolation. Interestingly, a number of these changes occur in genes previously shown to be regulated by the sexual transfer of 20E and may be due to divergent utilization of this steroid hormone in the two species.
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Many chemotherapeutic agents selectively target rapidly dividing cells, including cancer cells, by causing DNA damage that leads to genome instability and cell death. We utilize ...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. Additionally, 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 publicly 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.
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