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A male steroid controls female sexual behaviour in the malaria mosquito
Insects, unlike vertebrates, are widely believed to lack male-biased sex steroid hormones 1 . In the malaria mosquito Anopheles gambiae , the ecdysteroid 20-hydroxyecdysone (20E) appears to have evolved to both control egg development when synthesized by females 2 and to induce mating refractoriness...
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| Published in: | Nature (London) 2022-08, Vol.608 (7921), p.93-97 |
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| container_end_page | 97 |
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| container_title | Nature (London) |
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| creator | Peng, Duo Kakani, Evdoxia G. Mameli, Enzo Vidoudez, Charles Mitchell, Sara N. Merrihew, Gennifer E. MacCoss, Michael J. Adams, Kelsey Rinvee, Tasneem A. Shaw, W. Robert Catteruccia, Flaminia |
| description | Insects, unlike vertebrates, are widely believed to lack male-biased sex steroid hormones
1
. In the malaria mosquito
Anopheles gambiae
, the ecdysteroid 20-hydroxyecdysone (20E) appears to have evolved to both control egg development when synthesized by females
2
and to induce mating refractoriness when sexually transferred by males
3
. Because egg development and mating are essential reproductive traits, understanding how
Anopheles
females integrate these hormonal signals can spur the design of new malaria control programs. Here we reveal that these reproductive functions are regulated by distinct sex steroids through a sophisticated network of ecdysteroid-activating/inactivating enzymes. We identify a male-specific oxidized ecdysteroid, 3-dehydro-20E (3D20E), which safeguards paternity by turning off female sexual receptivity following its sexual transfer and activation by dephosphorylation. Notably, 3D20E transfer also induces expression of a reproductive gene that preserves egg development during
Plasmodium
infection, ensuring fitness of infected females. Female-derived 20E does not trigger sexual refractoriness but instead licenses oviposition in mated individuals once a 20E-inhibiting kinase is repressed. Identifying this male-specific insect steroid hormone and its roles in regulating female sexual receptivity, fertility and interactions with
Plasmodium
parasites suggests the possibility for reducing the reproductive success of malaria-transmitting mosquitoes.
The discovery of a male-specific sex hormone in the mosquito Anopheles gambiae may allow new strategies for the control of this notorious disease vector. |
| doi_str_mv | 10.1038/s41586-022-04908-6 |
| format | article |
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1
. In the malaria mosquito
Anopheles gambiae
, the ecdysteroid 20-hydroxyecdysone (20E) appears to have evolved to both control egg development when synthesized by females
2
and to induce mating refractoriness when sexually transferred by males
3
. Because egg development and mating are essential reproductive traits, understanding how
Anopheles
females integrate these hormonal signals can spur the design of new malaria control programs. Here we reveal that these reproductive functions are regulated by distinct sex steroids through a sophisticated network of ecdysteroid-activating/inactivating enzymes. We identify a male-specific oxidized ecdysteroid, 3-dehydro-20E (3D20E), which safeguards paternity by turning off female sexual receptivity following its sexual transfer and activation by dephosphorylation. Notably, 3D20E transfer also induces expression of a reproductive gene that preserves egg development during
Plasmodium
infection, ensuring fitness of infected females. Female-derived 20E does not trigger sexual refractoriness but instead licenses oviposition in mated individuals once a 20E-inhibiting kinase is repressed. Identifying this male-specific insect steroid hormone and its roles in regulating female sexual receptivity, fertility and interactions with
Plasmodium
parasites suggests the possibility for reducing the reproductive success of malaria-transmitting mosquitoes.
The discovery of a male-specific sex hormone in the mosquito Anopheles gambiae may allow new strategies for the control of this notorious disease vector.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/s41586-022-04908-6</identifier><identifier>PMID: 35794471</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>13/1 ; 13/89 ; 38 ; 38/22 ; 38/23 ; 38/39 ; 38/77 ; 42/44 ; 631/443/494 ; 631/45/776/1176 ; 631/601/1466 ; 82/16 ; 82/58 ; 82/80 ; 82/83 ; Animal reproduction ; Aquatic insects ; Breeding success ; Control programs ; Dephosphorylation ; Eggs ; Enzymes ; Females ; Fertility ; Gene expression ; Genes ; Hormones ; Humanities and Social Sciences ; Insects ; Kinases ; Malaria ; Males ; Mating ; Mosquitoes ; multidisciplinary ; Oviposition ; Parasites ; Paternity ; Phosphatase ; Physiology ; Plasmodium ; Reproduction ; Reproductive fitness ; Science ; Science (multidisciplinary) ; Sex ; Sexual behavior ; Sexual receptivity ; Steroid hormones ; Steroids ; Thermal resistance ; Vector-borne diseases ; Vertebrates</subject><ispartof>Nature (London), 2022-08, Vol.608 (7921), p.93-97</ispartof><rights>The Author(s) 2022</rights><rights>Copyright Nature Publishing Group Aug 4, 2022</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c451t-8cc9c8adeb73cc80ae530c53f251d9aee06f665846f2f4b506efc31e2aad43ac3</citedby><cites>FETCH-LOGICAL-c451t-8cc9c8adeb73cc80ae530c53f251d9aee06f665846f2f4b506efc31e2aad43ac3</cites><orcidid>0000-0002-0172-8090 ; 0000-0003-4903-0318 ; 0000-0002-1184-8360 ; 0000-0003-0953-7800 ; 0000-0003-3295-6683 ; 0000-0003-1853-0256 ; 0000-0002-2806-9718 ; 0000-0001-7540-8623</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27923,27924</link.rule.ids></links><search><creatorcontrib>Peng, Duo</creatorcontrib><creatorcontrib>Kakani, Evdoxia G.</creatorcontrib><creatorcontrib>Mameli, Enzo</creatorcontrib><creatorcontrib>Vidoudez, Charles</creatorcontrib><creatorcontrib>Mitchell, Sara N.</creatorcontrib><creatorcontrib>Merrihew, Gennifer E.</creatorcontrib><creatorcontrib>MacCoss, Michael J.</creatorcontrib><creatorcontrib>Adams, Kelsey</creatorcontrib><creatorcontrib>Rinvee, Tasneem A.</creatorcontrib><creatorcontrib>Shaw, W. Robert</creatorcontrib><creatorcontrib>Catteruccia, Flaminia</creatorcontrib><title>A male steroid controls female sexual behaviour in the malaria mosquito</title><title>Nature (London)</title><addtitle>Nature</addtitle><description>Insects, unlike vertebrates, are widely believed to lack male-biased sex steroid hormones
1
. In the malaria mosquito
Anopheles gambiae
, the ecdysteroid 20-hydroxyecdysone (20E) appears to have evolved to both control egg development when synthesized by females
2
and to induce mating refractoriness when sexually transferred by males
3
. Because egg development and mating are essential reproductive traits, understanding how
Anopheles
females integrate these hormonal signals can spur the design of new malaria control programs. Here we reveal that these reproductive functions are regulated by distinct sex steroids through a sophisticated network of ecdysteroid-activating/inactivating enzymes. We identify a male-specific oxidized ecdysteroid, 3-dehydro-20E (3D20E), which safeguards paternity by turning off female sexual receptivity following its sexual transfer and activation by dephosphorylation. Notably, 3D20E transfer also induces expression of a reproductive gene that preserves egg development during
Plasmodium
infection, ensuring fitness of infected females. Female-derived 20E does not trigger sexual refractoriness but instead licenses oviposition in mated individuals once a 20E-inhibiting kinase is repressed. Identifying this male-specific insect steroid hormone and its roles in regulating female sexual receptivity, fertility and interactions with
Plasmodium
parasites suggests the possibility for reducing the reproductive success of malaria-transmitting mosquitoes.
The discovery of a male-specific sex hormone in the mosquito Anopheles gambiae may allow new strategies for the control of this notorious disease vector.</description><subject>13/1</subject><subject>13/89</subject><subject>38</subject><subject>38/22</subject><subject>38/23</subject><subject>38/39</subject><subject>38/77</subject><subject>42/44</subject><subject>631/443/494</subject><subject>631/45/776/1176</subject><subject>631/601/1466</subject><subject>82/16</subject><subject>82/58</subject><subject>82/80</subject><subject>82/83</subject><subject>Animal reproduction</subject><subject>Aquatic insects</subject><subject>Breeding success</subject><subject>Control programs</subject><subject>Dephosphorylation</subject><subject>Eggs</subject><subject>Enzymes</subject><subject>Females</subject><subject>Fertility</subject><subject>Gene expression</subject><subject>Genes</subject><subject>Hormones</subject><subject>Humanities and Social Sciences</subject><subject>Insects</subject><subject>Kinases</subject><subject>Malaria</subject><subject>Males</subject><subject>Mating</subject><subject>Mosquitoes</subject><subject>multidisciplinary</subject><subject>Oviposition</subject><subject>Parasites</subject><subject>Paternity</subject><subject>Phosphatase</subject><subject>Physiology</subject><subject>Plasmodium</subject><subject>Reproduction</subject><subject>Reproductive fitness</subject><subject>Science</subject><subject>Science (multidisciplinary)</subject><subject>Sex</subject><subject>Sexual behavior</subject><subject>Sexual receptivity</subject><subject>Steroid hormones</subject><subject>Steroids</subject><subject>Thermal resistance</subject><subject>Vector-borne diseases</subject><subject>Vertebrates</subject><issn>0028-0836</issn><issn>1476-4687</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2022</creationdate><recordtype>article</recordtype><recordid>eNp9kUtLxTAQhYMoen38AVcFN26qk2fTjSDiCwQ3ug656dQbaRtNWtF_b7Si6MLVwMx3DjNzCNmncESB6-MkqNSqBMZKEDXoUq2RBRWVKoXS1TpZADBdguZqi2yn9AgAklZik2xxWdVCVHRBLk-L3nZYpBFj8E3hwjDG0KWixbmPr5PtiiWu7IsPUyz8UIwr_BDZ6G3Rh_Q8-THsko3Wdgn3vuoOub84vzu7Km9uL6_PTm9KJyQdS-1c7bRtcFlx5zRYlByc5C2TtKktIqhWKamFalkrlhIUto5TZNY2glvHd8jJ7Ps0LXtsHOZ1bWeeou9tfDPBevN7MviVeQgvpuaSyUpmg8MvgxieJ0yj6X1y2HV2wDAlw5RWIBUTdUYP_qCP-QNDPs-wKj-TMsZZpthMuRhSith-L0PBfORk5pxMzsl85mRUFvFZlDI8PGD8sf5H9Q5miJWg</recordid><startdate>20220804</startdate><enddate>20220804</enddate><creator>Peng, Duo</creator><creator>Kakani, Evdoxia G.</creator><creator>Mameli, Enzo</creator><creator>Vidoudez, Charles</creator><creator>Mitchell, Sara N.</creator><creator>Merrihew, Gennifer E.</creator><creator>MacCoss, Michael J.</creator><creator>Adams, Kelsey</creator><creator>Rinvee, Tasneem A.</creator><creator>Shaw, W. 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Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Peng, Duo</au><au>Kakani, Evdoxia G.</au><au>Mameli, Enzo</au><au>Vidoudez, Charles</au><au>Mitchell, Sara N.</au><au>Merrihew, Gennifer E.</au><au>MacCoss, Michael J.</au><au>Adams, Kelsey</au><au>Rinvee, Tasneem A.</au><au>Shaw, W. Robert</au><au>Catteruccia, Flaminia</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A male steroid controls female sexual behaviour in the malaria mosquito</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><date>2022-08-04</date><risdate>2022</risdate><volume>608</volume><issue>7921</issue><spage>93</spage><epage>97</epage><pages>93-97</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><abstract>Insects, unlike vertebrates, are widely believed to lack male-biased sex steroid hormones
1
. In the malaria mosquito
Anopheles gambiae
, the ecdysteroid 20-hydroxyecdysone (20E) appears to have evolved to both control egg development when synthesized by females
2
and to induce mating refractoriness when sexually transferred by males
3
. Because egg development and mating are essential reproductive traits, understanding how
Anopheles
females integrate these hormonal signals can spur the design of new malaria control programs. Here we reveal that these reproductive functions are regulated by distinct sex steroids through a sophisticated network of ecdysteroid-activating/inactivating enzymes. We identify a male-specific oxidized ecdysteroid, 3-dehydro-20E (3D20E), which safeguards paternity by turning off female sexual receptivity following its sexual transfer and activation by dephosphorylation. Notably, 3D20E transfer also induces expression of a reproductive gene that preserves egg development during
Plasmodium
infection, ensuring fitness of infected females. Female-derived 20E does not trigger sexual refractoriness but instead licenses oviposition in mated individuals once a 20E-inhibiting kinase is repressed. Identifying this male-specific insect steroid hormone and its roles in regulating female sexual receptivity, fertility and interactions with
Plasmodium
parasites suggests the possibility for reducing the reproductive success of malaria-transmitting mosquitoes.
The discovery of a male-specific sex hormone in the mosquito Anopheles gambiae may allow new strategies for the control of this notorious disease vector.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>35794471</pmid><doi>10.1038/s41586-022-04908-6</doi><tpages>5</tpages><orcidid>https://orcid.org/0000-0002-0172-8090</orcidid><orcidid>https://orcid.org/0000-0003-4903-0318</orcidid><orcidid>https://orcid.org/0000-0002-1184-8360</orcidid><orcidid>https://orcid.org/0000-0003-0953-7800</orcidid><orcidid>https://orcid.org/0000-0003-3295-6683</orcidid><orcidid>https://orcid.org/0000-0003-1853-0256</orcidid><orcidid>https://orcid.org/0000-0002-2806-9718</orcidid><orcidid>https://orcid.org/0000-0001-7540-8623</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 0028-0836 |
| ispartof | Nature (London), 2022-08, Vol.608 (7921), p.93-97 |
| issn | 0028-0836 1476-4687 |
| language | eng |
| recordid | cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_9352575 |
| source | Nature Journals Online |
| subjects | 13/1 13/89 38 38/22 38/23 38/39 38/77 42/44 631/443/494 631/45/776/1176 631/601/1466 82/16 82/58 82/80 82/83 Animal reproduction Aquatic insects Breeding success Control programs Dephosphorylation Eggs Enzymes Females Fertility Gene expression Genes Hormones Humanities and Social Sciences Insects Kinases Malaria Males Mating Mosquitoes multidisciplinary Oviposition Parasites Paternity Phosphatase Physiology Plasmodium Reproduction Reproductive fitness Science Science (multidisciplinary) Sex Sexual behavior Sexual receptivity Steroid hormones Steroids Thermal resistance Vector-borne diseases Vertebrates |
| title | A male steroid controls female sexual behaviour in the malaria mosquito |
| url | http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-01-08T15%3A03%3A42IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=A%20male%20steroid%20controls%20female%20sexual%20behaviour%20in%20the%20malaria%20mosquito&rft.jtitle=Nature%20(London)&rft.au=Peng,%20Duo&rft.date=2022-08-04&rft.volume=608&rft.issue=7921&rft.spage=93&rft.epage=97&rft.pages=93-97&rft.issn=0028-0836&rft.eissn=1476-4687&rft_id=info:doi/10.1038/s41586-022-04908-6&rft_dat=%3Cproquest_pubme%3E2686056249%3C/proquest_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c451t-8cc9c8adeb73cc80ae530c53f251d9aee06f665846f2f4b506efc31e2aad43ac3%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2700012232&rft_id=info:pmid/35794471&rfr_iscdi=true |