Sexual transfer of the steroid hormone 20E induces the postmating switch in Anopheles gambiae

Significance Anopheles gambiae females are the principal vectors of malaria, a disease that kills more than 600,000 people every year. Current control methods using insecticides to kill mosquitoes are threatened by the spread of resistance in natural populations. A promising alternative control stra...

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Veröffentlicht in:Proceedings of the National Academy of Sciences - PNAS 2014-11, Vol.111 (46), p.16353-16358
Hauptverfasser: Gabrieli, Paolo, Kakani, Evdoxia G., Mitchell, Sara N., Mameli, Enzo, Want, Elizabeth J., Anton, Ainhoa Mariezcurrena, Serrao, Aurelio, Baldini, Francesco, Catteruccia, Flaminia
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container_end_page 16358
container_issue 46
container_start_page 16353
container_title Proceedings of the National Academy of Sciences - PNAS
container_volume 111
creator Gabrieli, Paolo
Kakani, Evdoxia G.
Mitchell, Sara N.
Mameli, Enzo
Want, Elizabeth J.
Anton, Ainhoa Mariezcurrena
Serrao, Aurelio
Baldini, Francesco
Catteruccia, Flaminia
description Significance Anopheles gambiae females are the principal vectors of malaria, a disease that kills more than 600,000 people every year. Current control methods using insecticides to kill mosquitoes are threatened by the spread of resistance in natural populations. A promising alternative control strategy is based on interfering with mosquito reproduction to reduce the number of malaria-transmitting females. Here we show that a male hormone transferred to the female during sex induces large changes in female behavior. These changes, defined as the postmating switch, include a physical incapacity for fertilization by additional males and the ability to lay mature eggs. Tampering with the function of this hormone generates unprecedented opportunities to reduce the reproductive success of Anopheles mosquitoes and impact malaria transmission. Female insects generally mate multiple times during their lives. A notable exception is the female malaria mosquito Anopheles gambiae , which after sex loses her susceptibility to further copulation. Sex in this species also renders females competent to lay eggs developed after blood feeding. Despite intense research efforts, the identity of the molecular triggers that cause the postmating switch in females, inducing a permanent refractoriness to further mating and triggering egg-laying, remains elusive. Here we show that the male-transferred steroid hormone 20-hydroxyecdysone (20E) is a key regulator of monandry and oviposition in An . gambiae . When sexual transfer of 20E is impaired by partial inactivation of the hormone and inhibition of its biosynthesis in males, oviposition and refractoriness to further mating in the female are strongly reduced. Conversely, mimicking sexual delivery by injecting 20E into virgin females switches them to an artificial mated status, triggering egg-laying and reducing susceptibility to copulation. Sexual transfer of 20E appears to incapacitate females physically from receiving seminal fluids by a second male. Comparative analysis of microarray data from females after mating and after 20E treatment indicates that 20E-regulated molecular pathways likely are implicated in the postmating switch, including cytoskeleton and musculature-associated genes that may render the atrium impenetrable to additional mates. By revealing signals and pathways shaping key processes in the An . gambiae reproductive biology, our data offer new opportunities for the control of natural populations of malaria vect
doi_str_mv 10.1073/pnas.1410488111
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Current control methods using insecticides to kill mosquitoes are threatened by the spread of resistance in natural populations. A promising alternative control strategy is based on interfering with mosquito reproduction to reduce the number of malaria-transmitting females. Here we show that a male hormone transferred to the female during sex induces large changes in female behavior. These changes, defined as the postmating switch, include a physical incapacity for fertilization by additional males and the ability to lay mature eggs. Tampering with the function of this hormone generates unprecedented opportunities to reduce the reproductive success of Anopheles mosquitoes and impact malaria transmission. Female insects generally mate multiple times during their lives. A notable exception is the female malaria mosquito Anopheles gambiae , which after sex loses her susceptibility to further copulation. Sex in this species also renders females competent to lay eggs developed after blood feeding. Despite intense research efforts, the identity of the molecular triggers that cause the postmating switch in females, inducing a permanent refractoriness to further mating and triggering egg-laying, remains elusive. Here we show that the male-transferred steroid hormone 20-hydroxyecdysone (20E) is a key regulator of monandry and oviposition in An . gambiae . When sexual transfer of 20E is impaired by partial inactivation of the hormone and inhibition of its biosynthesis in males, oviposition and refractoriness to further mating in the female are strongly reduced. Conversely, mimicking sexual delivery by injecting 20E into virgin females switches them to an artificial mated status, triggering egg-laying and reducing susceptibility to copulation. Sexual transfer of 20E appears to incapacitate females physically from receiving seminal fluids by a second male. Comparative analysis of microarray data from females after mating and after 20E treatment indicates that 20E-regulated molecular pathways likely are implicated in the postmating switch, including cytoskeleton and musculature-associated genes that may render the atrium impenetrable to additional mates. 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Current control methods using insecticides to kill mosquitoes are threatened by the spread of resistance in natural populations. A promising alternative control strategy is based on interfering with mosquito reproduction to reduce the number of malaria-transmitting females. Here we show that a male hormone transferred to the female during sex induces large changes in female behavior. These changes, defined as the postmating switch, include a physical incapacity for fertilization by additional males and the ability to lay mature eggs. Tampering with the function of this hormone generates unprecedented opportunities to reduce the reproductive success of Anopheles mosquitoes and impact malaria transmission. Female insects generally mate multiple times during their lives. A notable exception is the female malaria mosquito Anopheles gambiae , which after sex loses her susceptibility to further copulation. Sex in this species also renders females competent to lay eggs developed after blood feeding. Despite intense research efforts, the identity of the molecular triggers that cause the postmating switch in females, inducing a permanent refractoriness to further mating and triggering egg-laying, remains elusive. Here we show that the male-transferred steroid hormone 20-hydroxyecdysone (20E) is a key regulator of monandry and oviposition in An . gambiae . When sexual transfer of 20E is impaired by partial inactivation of the hormone and inhibition of its biosynthesis in males, oviposition and refractoriness to further mating in the female are strongly reduced. Conversely, mimicking sexual delivery by injecting 20E into virgin females switches them to an artificial mated status, triggering egg-laying and reducing susceptibility to copulation. Sexual transfer of 20E appears to incapacitate females physically from receiving seminal fluids by a second male. Comparative analysis of microarray data from females after mating and after 20E treatment indicates that 20E-regulated molecular pathways likely are implicated in the postmating switch, including cytoskeleton and musculature-associated genes that may render the atrium impenetrable to additional mates. 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Current control methods using insecticides to kill mosquitoes are threatened by the spread of resistance in natural populations. A promising alternative control strategy is based on interfering with mosquito reproduction to reduce the number of malaria-transmitting females. Here we show that a male hormone transferred to the female during sex induces large changes in female behavior. These changes, defined as the postmating switch, include a physical incapacity for fertilization by additional males and the ability to lay mature eggs. Tampering with the function of this hormone generates unprecedented opportunities to reduce the reproductive success of Anopheles mosquitoes and impact malaria transmission. Female insects generally mate multiple times during their lives. A notable exception is the female malaria mosquito Anopheles gambiae , which after sex loses her susceptibility to further copulation. Sex in this species also renders females competent to lay eggs developed after blood feeding. Despite intense research efforts, the identity of the molecular triggers that cause the postmating switch in females, inducing a permanent refractoriness to further mating and triggering egg-laying, remains elusive. Here we show that the male-transferred steroid hormone 20-hydroxyecdysone (20E) is a key regulator of monandry and oviposition in An . gambiae . When sexual transfer of 20E is impaired by partial inactivation of the hormone and inhibition of its biosynthesis in males, oviposition and refractoriness to further mating in the female are strongly reduced. Conversely, mimicking sexual delivery by injecting 20E into virgin females switches them to an artificial mated status, triggering egg-laying and reducing susceptibility to copulation. Sexual transfer of 20E appears to incapacitate females physically from receiving seminal fluids by a second male. Comparative analysis of microarray data from females after mating and after 20E treatment indicates that 20E-regulated molecular pathways likely are implicated in the postmating switch, including cytoskeleton and musculature-associated genes that may render the atrium impenetrable to additional mates. By revealing signals and pathways shaping key processes in the An . gambiae reproductive biology, our data offer new opportunities for the control of natural populations of malaria vectors.</abstract><cop>United States</cop><pub>National Academy of Sciences</pub><pmid>25368171</pmid><doi>10.1073/pnas.1410488111</doi><tpages>6</tpages><oa>free_for_read</oa></addata></record>
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subjects Animal reproduction
Animals
Anopheles - physiology
Anopheles gambiae
Atriums
Biological Sciences
Biosynthesis
Comparative analysis
Copulation
Cytoskeleton
Drosophila
Ecdysterone - pharmacology
Ecdysterone - physiology
Female
Female animals
Gene Expression Profiling
Gene expression regulation
Genes
Genes, Insect
Hormones
Injections
Insect Vectors - physiology
Malaria - transmission
Male
Male animals
Mating behavior
Mosquitos
Oligonucleotide Array Sequence Analysis
Ova
Oviposition
Oviposition - physiology
Sexual Behavior, Animal - physiology
Steroids
Time Factors
Transcription, Genetic
title Sexual transfer of the steroid hormone 20E induces the postmating switch in Anopheles gambiae
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