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A combined approach to heat stress effect on male fertility in Nasonia vitripennis: from the physiological consequences on spermatogenesis to the reproductive adjustment of females mated with stressed males
In recent years, several studies have shown a decline in reproductive success in males in both humans and wildlife. Research on male fertility has largely focused on vertebrates, although invertebrates constitute the vast majority of terrestrial biodiversity. The reduction of their reproductive capa...
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| Published in: | PloS one 2015-03, Vol.10 (3), p.e0120656-e0120656 |
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| creator | Chirault, Marlène Lucas, Christophe Goubault, Marlène Chevrier, Claude Bressac, Christophe Lécureuil, Charlotte |
| description | In recent years, several studies have shown a decline in reproductive success in males in both humans and wildlife. Research on male fertility has largely focused on vertebrates, although invertebrates constitute the vast majority of terrestrial biodiversity. The reduction of their reproductive capacities due to environmental stresses can have strong negative ecological impacts, and also dramatic consequences on world food production if it affects the reproductive success of biological control agents, such as parasitic wasps used to control crop pests. Here Nasonia vitripennis, a parasitic wasp of various fly species, was studied to test the effects of 24h-heat stress applied during the first pupal stage on male fertility. Results showed that only primary spermatocytes were present at the first pupal stage in all cysts of the testes. Heat stress caused a delay in spermatogenesis during development and a significant decrease in sperm stock at emergence. Females mated with these heat-stressed males showed a reduce sperm count stored in their spermatheca. Females did not appear to distinguish heat-stressed from control males and did not remate more frequently to compensate for the lack of sperm transferred. As a result, females mated with heat-stressed males produced a suboptimal lifetime offspring sex ratio compared to those mated with control males. This could further impact the population dynamics of this species. N. vitripennis appears to be an interesting biological model to study the mechanisms of subfertility and its consequence on female reproductive strategies and provides new research perspectives in both invertebrates and vertebrates. |
| doi_str_mv | 10.1371/journal.pone.0120656 |
| format | article |
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Research on male fertility has largely focused on vertebrates, although invertebrates constitute the vast majority of terrestrial biodiversity. The reduction of their reproductive capacities due to environmental stresses can have strong negative ecological impacts, and also dramatic consequences on world food production if it affects the reproductive success of biological control agents, such as parasitic wasps used to control crop pests. Here Nasonia vitripennis, a parasitic wasp of various fly species, was studied to test the effects of 24h-heat stress applied during the first pupal stage on male fertility. Results showed that only primary spermatocytes were present at the first pupal stage in all cysts of the testes. Heat stress caused a delay in spermatogenesis during development and a significant decrease in sperm stock at emergence. Females mated with these heat-stressed males showed a reduce sperm count stored in their spermatheca. 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N. vitripennis appears to be an interesting biological model to study the mechanisms of subfertility and its consequence on female reproductive strategies and provides new research perspectives in both invertebrates and vertebrates.</description><identifier>ISSN: 1932-6203</identifier><identifier>EISSN: 1932-6203</identifier><identifier>DOI: 10.1371/journal.pone.0120656</identifier><identifier>PMID: 25807005</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Agricultural pests ; Analysis ; Animal biology ; Animal reproduction ; Animals ; Apis mellifera ; Bioclimatology ; Biodiversity ; Biological control ; Biological models (mathematics) ; Biological pest control ; Breeding success ; Cysts ; Development Biology ; Ecology, environment ; Eggs ; Environmental stress ; Female ; Females ; Fertility ; Fertility - physiology ; Food production ; Gametogenesis ; Gas Chromatography-Mass Spectrometry ; Gene expression ; Heat ; Heat stress ; Heat tolerance ; Hymenoptera ; Invertebrate Zoology ; Invertebrates ; Life Sciences ; Male ; Males ; Nasonia vitripennis ; Offspring ; Pest control ; Pests ; Pheromones ; Physiological effects ; Physiology ; Population dynamics ; Pteromalidae ; Pupa - growth & development ; Pupa - physiology ; Reproduction ; Reproductive Biology ; Sex Attractants - analysis ; Sex Ratio ; Sexual reproduction ; Sperm ; Sperm Count ; Spermatheca ; Spermatocytes ; Spermatogenesis ; Spermatogenesis - physiology ; Spermatozoa - physiology ; Stress, Psychological ; Temperature ; Terrestrial environments ; Testes ; Testis - pathology ; Vertebrates ; Wasps ; Wasps - growth & development ; Wasps - physiology ; Wildlife</subject><ispartof>PloS one, 2015-03, Vol.10 (3), p.e0120656-e0120656</ispartof><rights>COPYRIGHT 2015 Public Library of Science</rights><rights>2015 Chirault et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><rights>2015 Chirault et al 2015 Chirault et al</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c726t-cdb6decf475d37ac712285ea4abdb00bbaac38675ff2c71cdd700e26464f43c23</citedby><cites>FETCH-LOGICAL-c726t-cdb6decf475d37ac712285ea4abdb00bbaac38675ff2c71cdd700e26464f43c23</cites><orcidid>0000-0002-7339-9185 ; 0000-0003-2839-7583 ; 0000-0002-9452-7668 ; 0000-0001-7609-8970</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.proquest.com/docview/1666747973/fulltextPDF?pq-origsite=primo$$EPDF$$P50$$Gproquest$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.proquest.com/docview/1666747973?pq-origsite=primo$$EHTML$$P50$$Gproquest$$Hfree_for_read</linktohtml><link.rule.ids>230,314,727,780,784,885,25753,27924,27925,37012,37013,44590,53791,53793,75126</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25807005$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-02146269$$DView record in HAL$$Hfree_for_read</backlink></links><search><contributor>Volle, David H</contributor><creatorcontrib>Chirault, Marlène</creatorcontrib><creatorcontrib>Lucas, Christophe</creatorcontrib><creatorcontrib>Goubault, Marlène</creatorcontrib><creatorcontrib>Chevrier, Claude</creatorcontrib><creatorcontrib>Bressac, Christophe</creatorcontrib><creatorcontrib>Lécureuil, Charlotte</creatorcontrib><title>A combined approach to heat stress effect on male fertility in Nasonia vitripennis: from the physiological consequences on spermatogenesis to the reproductive adjustment of females mated with stressed males</title><title>PloS one</title><addtitle>PLoS One</addtitle><description>In recent years, several studies have shown a decline in reproductive success in males in both humans and wildlife. Research on male fertility has largely focused on vertebrates, although invertebrates constitute the vast majority of terrestrial biodiversity. The reduction of their reproductive capacities due to environmental stresses can have strong negative ecological impacts, and also dramatic consequences on world food production if it affects the reproductive success of biological control agents, such as parasitic wasps used to control crop pests. Here Nasonia vitripennis, a parasitic wasp of various fly species, was studied to test the effects of 24h-heat stress applied during the first pupal stage on male fertility. Results showed that only primary spermatocytes were present at the first pupal stage in all cysts of the testes. Heat stress caused a delay in spermatogenesis during development and a significant decrease in sperm stock at emergence. Females mated with these heat-stressed males showed a reduce sperm count stored in their spermatheca. Females did not appear to distinguish heat-stressed from control males and did not remate more frequently to compensate for the lack of sperm transferred. As a result, females mated with heat-stressed males produced a suboptimal lifetime offspring sex ratio compared to those mated with control males. This could further impact the population dynamics of this species. N. vitripennis appears to be an interesting biological model to study the mechanisms of subfertility and its consequence on female reproductive strategies and provides new research perspectives in both invertebrates and vertebrates.</description><subject>Agricultural pests</subject><subject>Analysis</subject><subject>Animal biology</subject><subject>Animal reproduction</subject><subject>Animals</subject><subject>Apis mellifera</subject><subject>Bioclimatology</subject><subject>Biodiversity</subject><subject>Biological control</subject><subject>Biological models (mathematics)</subject><subject>Biological pest control</subject><subject>Breeding success</subject><subject>Cysts</subject><subject>Development Biology</subject><subject>Ecology, environment</subject><subject>Eggs</subject><subject>Environmental stress</subject><subject>Female</subject><subject>Females</subject><subject>Fertility</subject><subject>Fertility - physiology</subject><subject>Food production</subject><subject>Gametogenesis</subject><subject>Gas Chromatography-Mass Spectrometry</subject><subject>Gene expression</subject><subject>Heat</subject><subject>Heat stress</subject><subject>Heat tolerance</subject><subject>Hymenoptera</subject><subject>Invertebrate Zoology</subject><subject>Invertebrates</subject><subject>Life Sciences</subject><subject>Male</subject><subject>Males</subject><subject>Nasonia vitripennis</subject><subject>Offspring</subject><subject>Pest control</subject><subject>Pests</subject><subject>Pheromones</subject><subject>Physiological effects</subject><subject>Physiology</subject><subject>Population dynamics</subject><subject>Pteromalidae</subject><subject>Pupa - growth & development</subject><subject>Pupa - physiology</subject><subject>Reproduction</subject><subject>Reproductive Biology</subject><subject>Sex Attractants - analysis</subject><subject>Sex Ratio</subject><subject>Sexual reproduction</subject><subject>Sperm</subject><subject>Sperm Count</subject><subject>Spermatheca</subject><subject>Spermatocytes</subject><subject>Spermatogenesis</subject><subject>Spermatogenesis - physiology</subject><subject>Spermatozoa - physiology</subject><subject>Stress, Psychological</subject><subject>Temperature</subject><subject>Terrestrial environments</subject><subject>Testes</subject><subject>Testis - pathology</subject><subject>Vertebrates</subject><subject>Wasps</subject><subject>Wasps - growth & development</subject><subject>Wasps - 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combined approach to heat stress effect on male fertility in Nasonia vitripennis: from the physiological consequences on spermatogenesis to the reproductive adjustment of females mated with stressed males</title><author>Chirault, Marlène ; Lucas, Christophe ; Goubault, Marlène ; Chevrier, Claude ; Bressac, Christophe ; Lécureuil, Charlotte</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c726t-cdb6decf475d37ac712285ea4abdb00bbaac38675ff2c71cdd700e26464f43c23</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Agricultural pests</topic><topic>Analysis</topic><topic>Animal biology</topic><topic>Animal reproduction</topic><topic>Animals</topic><topic>Apis mellifera</topic><topic>Bioclimatology</topic><topic>Biodiversity</topic><topic>Biological control</topic><topic>Biological models (mathematics)</topic><topic>Biological pest control</topic><topic>Breeding 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Christophe</au><au>Goubault, Marlène</au><au>Chevrier, Claude</au><au>Bressac, Christophe</au><au>Lécureuil, Charlotte</au><au>Volle, David H</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A combined approach to heat stress effect on male fertility in Nasonia vitripennis: from the physiological consequences on spermatogenesis to the reproductive adjustment of females mated with stressed males</atitle><jtitle>PloS one</jtitle><addtitle>PLoS One</addtitle><date>2015-03-25</date><risdate>2015</risdate><volume>10</volume><issue>3</issue><spage>e0120656</spage><epage>e0120656</epage><pages>e0120656-e0120656</pages><issn>1932-6203</issn><eissn>1932-6203</eissn><abstract>In recent years, several studies have shown a decline in reproductive success in males in both humans and wildlife. Research on male fertility has largely focused on vertebrates, although invertebrates constitute the vast majority of terrestrial biodiversity. The reduction of their reproductive capacities due to environmental stresses can have strong negative ecological impacts, and also dramatic consequences on world food production if it affects the reproductive success of biological control agents, such as parasitic wasps used to control crop pests. Here Nasonia vitripennis, a parasitic wasp of various fly species, was studied to test the effects of 24h-heat stress applied during the first pupal stage on male fertility. Results showed that only primary spermatocytes were present at the first pupal stage in all cysts of the testes. Heat stress caused a delay in spermatogenesis during development and a significant decrease in sperm stock at emergence. Females mated with these heat-stressed males showed a reduce sperm count stored in their spermatheca. Females did not appear to distinguish heat-stressed from control males and did not remate more frequently to compensate for the lack of sperm transferred. As a result, females mated with heat-stressed males produced a suboptimal lifetime offspring sex ratio compared to those mated with control males. This could further impact the population dynamics of this species. N. vitripennis appears to be an interesting biological model to study the mechanisms of subfertility and its consequence on female reproductive strategies and provides new research perspectives in both invertebrates and vertebrates.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>25807005</pmid><doi>10.1371/journal.pone.0120656</doi><orcidid>https://orcid.org/0000-0002-7339-9185</orcidid><orcidid>https://orcid.org/0000-0003-2839-7583</orcidid><orcidid>https://orcid.org/0000-0002-9452-7668</orcidid><orcidid>https://orcid.org/0000-0001-7609-8970</orcidid><oa>free_for_read</oa></addata></record> |
| fulltext | fulltext |
| identifier | ISSN: 1932-6203 |
| ispartof | PloS one, 2015-03, Vol.10 (3), p.e0120656-e0120656 |
| issn | 1932-6203 1932-6203 |
| language | eng |
| recordid | cdi_plos_journals_1666747973 |
| source | Publicly Available Content Database; PubMed Central |
| subjects | Agricultural pests Analysis Animal biology Animal reproduction Animals Apis mellifera Bioclimatology Biodiversity Biological control Biological models (mathematics) Biological pest control Breeding success Cysts Development Biology Ecology, environment Eggs Environmental stress Female Females Fertility Fertility - physiology Food production Gametogenesis Gas Chromatography-Mass Spectrometry Gene expression Heat Heat stress Heat tolerance Hymenoptera Invertebrate Zoology Invertebrates Life Sciences Male Males Nasonia vitripennis Offspring Pest control Pests Pheromones Physiological effects Physiology Population dynamics Pteromalidae Pupa - growth & development Pupa - physiology Reproduction Reproductive Biology Sex Attractants - analysis Sex Ratio Sexual reproduction Sperm Sperm Count Spermatheca Spermatocytes Spermatogenesis Spermatogenesis - physiology Spermatozoa - physiology Stress, Psychological Temperature Terrestrial environments Testes Testis - pathology Vertebrates Wasps Wasps - growth & development Wasps - physiology Wildlife |
| title | A combined approach to heat stress effect on male fertility in Nasonia vitripennis: from the physiological consequences on spermatogenesis to the reproductive adjustment of females mated with stressed males |
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