Social modulation of oogenesis and egg laying in Drosophila melanogaster
Being part of a group facilitates cooperation between group members but also creates competition for resources. This is a conundrum for gravid females, whose future offspring benefit from being in a group only if there are enough resources relative to group size. Females may therefore be expected to...
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Veröffentlicht in: | Current biology 2023-07, Vol.33 (14), p.2865-2877.e4 |
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creator | Bailly, Tiphaine P.M. Kohlmeier, Philip Etienne, Rampal S. Wertheim, Bregje Billeter, Jean-Christophe |
description | Being part of a group facilitates cooperation between group members but also creates competition for resources. This is a conundrum for gravid females, whose future offspring benefit from being in a group only if there are enough resources relative to group size. Females may therefore be expected to modulate reproductive output depending on social context. In the fruit fly Drosophila melanogaster, females actively attract conspecifics to lay eggs on the same resources, generating groups in which individuals may cooperate or compete. The genetic tractability of this species allows dissecting the mechanisms underlying physiological adaptation to social context. Here, we show that females produce eggs increasingly faster as group size increases. By laying eggs faster when grouped than when isolated, females reduce competition between offspring and increase offspring survival. In addition, grouped females lay eggs during the day, while isolated females lay them at night. We show that responses to the presence of others requires visual input and that flies from any sex, mating status, or species can trigger these responses. The mechanisms of this modulation of egg laying by group is connected to a lifting of the inhibition of light on oogenesis and egg laying, possibly mediated in part by an increase in juvenile hormone activity. Because modulation of reproduction by social context is a hallmark of animals with higher levels of sociality, our findings in a species considered solitary question the validity of this nomenclature and suggest a widespread and profound influence of social context on reproduction.
[Display omitted]
•Light inhibits egg laying in isolated, but not in grouped, females•Presence of other flies lifts light’s inhibition of oogenesis and ovulation•Females speed egg-laying onset in a group to ensure offspring survival•D. melanogaster’s reproduction is fundamentally influenced by social context
Bailly et al. show that being grouped induces fruit fly females to lay eggs through the day and night, while isolated females lay eggs at night. Females detect others via vision, which results in faster oogenesis during the day, likely mediated by juvenile hormone. Reproduction in fruit flies is thus fundamentally modulated by the presence of others. |
doi_str_mv | 10.1016/j.cub.2023.05.074 |
format | Article |
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[Display omitted]
•Light inhibits egg laying in isolated, but not in grouped, females•Presence of other flies lifts light’s inhibition of oogenesis and ovulation•Females speed egg-laying onset in a group to ensure offspring survival•D. melanogaster’s reproduction is fundamentally influenced by social context
Bailly et al. show that being grouped induces fruit fly females to lay eggs through the day and night, while isolated females lay eggs at night. Females detect others via vision, which results in faster oogenesis during the day, likely mediated by juvenile hormone. Reproduction in fruit flies is thus fundamentally modulated by the presence of others.</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2023.05.074</identifier><identifier>PMID: 37369209</identifier><language>eng</language><publisher>England: Elsevier Inc</publisher><subject>Drosophila melanogaster ; egg laying ; juvenile hormone ; light ; motion sensing ; oogenesis ; reproduction ; social environment ; sociality ; vision</subject><ispartof>Current biology, 2023-07, Vol.33 (14), p.2865-2877.e4</ispartof><rights>2023 Elsevier Inc.</rights><rights>Copyright © 2023 Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c348t-62bc659de1146edd18cbeb0a1c50923eed18fe40913682d211c562b7250fd3bf3</cites><orcidid>0000-0001-7796-4068</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.cub.2023.05.074$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37369209$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Bailly, Tiphaine P.M.</creatorcontrib><creatorcontrib>Kohlmeier, Philip</creatorcontrib><creatorcontrib>Etienne, Rampal S.</creatorcontrib><creatorcontrib>Wertheim, Bregje</creatorcontrib><creatorcontrib>Billeter, Jean-Christophe</creatorcontrib><title>Social modulation of oogenesis and egg laying in Drosophila melanogaster</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>Being part of a group facilitates cooperation between group members but also creates competition for resources. This is a conundrum for gravid females, whose future offspring benefit from being in a group only if there are enough resources relative to group size. Females may therefore be expected to modulate reproductive output depending on social context. In the fruit fly Drosophila melanogaster, females actively attract conspecifics to lay eggs on the same resources, generating groups in which individuals may cooperate or compete. The genetic tractability of this species allows dissecting the mechanisms underlying physiological adaptation to social context. Here, we show that females produce eggs increasingly faster as group size increases. By laying eggs faster when grouped than when isolated, females reduce competition between offspring and increase offspring survival. In addition, grouped females lay eggs during the day, while isolated females lay them at night. We show that responses to the presence of others requires visual input and that flies from any sex, mating status, or species can trigger these responses. The mechanisms of this modulation of egg laying by group is connected to a lifting of the inhibition of light on oogenesis and egg laying, possibly mediated in part by an increase in juvenile hormone activity. Because modulation of reproduction by social context is a hallmark of animals with higher levels of sociality, our findings in a species considered solitary question the validity of this nomenclature and suggest a widespread and profound influence of social context on reproduction.
[Display omitted]
•Light inhibits egg laying in isolated, but not in grouped, females•Presence of other flies lifts light’s inhibition of oogenesis and ovulation•Females speed egg-laying onset in a group to ensure offspring survival•D. melanogaster’s reproduction is fundamentally influenced by social context
Bailly et al. show that being grouped induces fruit fly females to lay eggs through the day and night, while isolated females lay eggs at night. Females detect others via vision, which results in faster oogenesis during the day, likely mediated by juvenile hormone. Reproduction in fruit flies is thus fundamentally modulated by the presence of others.</description><subject>Drosophila melanogaster</subject><subject>egg laying</subject><subject>juvenile hormone</subject><subject>light</subject><subject>motion sensing</subject><subject>oogenesis</subject><subject>reproduction</subject><subject>social environment</subject><subject>sociality</subject><subject>vision</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNp9kDFv2zAQhYkiRe24_QFZAo5ZpBxJiRLRKUjaOICBDm1ngiJPKg1JdEUpgP99adjNmOmAu_ce3n2E3DDIGTB5v8_t0uQcuMihzKEqPpA1qyuVQVGUV2QNSkKmas5X5DrGPQDjtZKfyEpUQioOak22P4P1pqdDcEtvZh9GGloaQocjRh-pGR3FrqO9Ofqxo36kT1OI4fDH94YO2JsxdCbOOH0mH1vTR_xymRvy-_u3X4_bbPfj-eXxYZdZUdRzJnljZakcMlZIdI7VtsEGDLMlKC4Q06bFAhQTsuaOs3RInoqX0DrRtGJD7s65hyn8XTDOevDRYp-aYFii5rUAWfFC1knKzlKbKscJW32Y_GCmo2agTwD1XieA-gRQQ6kTwOS5vcQvzYDuzfGfWBJ8PQswPfnqcdLRehwtOj-hnbUL_p34f1_GgNE</recordid><startdate>20230724</startdate><enddate>20230724</enddate><creator>Bailly, Tiphaine P.M.</creator><creator>Kohlmeier, Philip</creator><creator>Etienne, Rampal S.</creator><creator>Wertheim, Bregje</creator><creator>Billeter, Jean-Christophe</creator><general>Elsevier Inc</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0001-7796-4068</orcidid></search><sort><creationdate>20230724</creationdate><title>Social modulation of oogenesis and egg laying in Drosophila melanogaster</title><author>Bailly, Tiphaine P.M. ; Kohlmeier, Philip ; Etienne, Rampal S. ; Wertheim, Bregje ; Billeter, Jean-Christophe</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c348t-62bc659de1146edd18cbeb0a1c50923eed18fe40913682d211c562b7250fd3bf3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Drosophila melanogaster</topic><topic>egg laying</topic><topic>juvenile hormone</topic><topic>light</topic><topic>motion sensing</topic><topic>oogenesis</topic><topic>reproduction</topic><topic>social environment</topic><topic>sociality</topic><topic>vision</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Bailly, Tiphaine P.M.</creatorcontrib><creatorcontrib>Kohlmeier, Philip</creatorcontrib><creatorcontrib>Etienne, Rampal S.</creatorcontrib><creatorcontrib>Wertheim, Bregje</creatorcontrib><creatorcontrib>Billeter, Jean-Christophe</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Bailly, Tiphaine P.M.</au><au>Kohlmeier, Philip</au><au>Etienne, Rampal S.</au><au>Wertheim, Bregje</au><au>Billeter, Jean-Christophe</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Social modulation of oogenesis and egg laying in Drosophila melanogaster</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2023-07-24</date><risdate>2023</risdate><volume>33</volume><issue>14</issue><spage>2865</spage><epage>2877.e4</epage><pages>2865-2877.e4</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><abstract>Being part of a group facilitates cooperation between group members but also creates competition for resources. This is a conundrum for gravid females, whose future offspring benefit from being in a group only if there are enough resources relative to group size. Females may therefore be expected to modulate reproductive output depending on social context. In the fruit fly Drosophila melanogaster, females actively attract conspecifics to lay eggs on the same resources, generating groups in which individuals may cooperate or compete. The genetic tractability of this species allows dissecting the mechanisms underlying physiological adaptation to social context. Here, we show that females produce eggs increasingly faster as group size increases. By laying eggs faster when grouped than when isolated, females reduce competition between offspring and increase offspring survival. In addition, grouped females lay eggs during the day, while isolated females lay them at night. We show that responses to the presence of others requires visual input and that flies from any sex, mating status, or species can trigger these responses. The mechanisms of this modulation of egg laying by group is connected to a lifting of the inhibition of light on oogenesis and egg laying, possibly mediated in part by an increase in juvenile hormone activity. Because modulation of reproduction by social context is a hallmark of animals with higher levels of sociality, our findings in a species considered solitary question the validity of this nomenclature and suggest a widespread and profound influence of social context on reproduction.
[Display omitted]
•Light inhibits egg laying in isolated, but not in grouped, females•Presence of other flies lifts light’s inhibition of oogenesis and ovulation•Females speed egg-laying onset in a group to ensure offspring survival•D. melanogaster’s reproduction is fundamentally influenced by social context
Bailly et al. show that being grouped induces fruit fly females to lay eggs through the day and night, while isolated females lay eggs at night. Females detect others via vision, which results in faster oogenesis during the day, likely mediated by juvenile hormone. Reproduction in fruit flies is thus fundamentally modulated by the presence of others.</abstract><cop>England</cop><pub>Elsevier Inc</pub><pmid>37369209</pmid><doi>10.1016/j.cub.2023.05.074</doi><orcidid>https://orcid.org/0000-0001-7796-4068</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Drosophila melanogaster egg laying juvenile hormone light motion sensing oogenesis reproduction social environment sociality vision |
title | Social modulation of oogenesis and egg laying in Drosophila melanogaster |
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