Toward the Development of the Trojan Female Technique in Pest Insects: Male‐Specific Influence of Mitochondrial Haplotype on Reproductive Output in the Seed Beetle Acanthoscelides obtectus
ABSTRACT Biocontrol techniques that impair reproductive capacity of insect pests provide opportunities to control the dynamics of their populations while minimizing collateral damage to non‐target species and the environment. The Trojan Female Technique, or TFT, is a method of the trans‐generational...
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Wiley
2024-12-01
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| Series: | Evolutionary Applications |
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| Online Access: | https://doi.org/10.1111/eva.70065 |
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| author | Lea Vlajnić Uroš Savković Jelena Jović Sanja Budečević Biljana Stojković Mirko Đorđević |
| author_facet | Lea Vlajnić Uroš Savković Jelena Jović Sanja Budečević Biljana Stojković Mirko Đorđević |
| author_sort | Lea Vlajnić |
| collection | DOAJ |
| description | ABSTRACT Biocontrol techniques that impair reproductive capacity of insect pests provide opportunities to control the dynamics of their populations while minimizing collateral damage to non‐target species and the environment. The Trojan Female Technique, or TFT, is a method of the trans‐generational fertility‐based population control through the release of females that carry mitochondrial DNA mutations that negatively affect male, but not female, reproductive output. TFT is based on the evolutionary hypothesis that, due to maternal inheritance of mitochondria, mutations which are beneficial or neutral in females but harmful in males can accumulate in the mitochondrial genome without selection acting against them. Although TFT has been theoretically substantiated, empirical work to date has focused only on Drosophila melanogaster populations, while the existence of male‐biased mutations and the TFT approach in economically important pest species remain unexplored. Here, we examined the sex‐specific effects of three distinct and naturally occurring mitochondrial haplotypes (MG1a, MG1d, and MG3b) on several reproductive and life history traits in the seed beetle Acanthoscelides obtectus. Our results revealed that males harboring the MG3b mitotype exhibited lower early fecundity and fertility, while there were no effects on females or longevity in either sex. Our experiments provide support for the existence of the mitochondrial variant that specifically impairs male reproductive output in pest insects. These results can be harnessed to further develop TFT as a novel form of biocontrol with broad applicability to economic pests and disease vector insects. |
| format | Article |
| id | doaj-art-054c11130c4942fe8367cb886f87268a |
| institution | Kabale University |
| issn | 1752-4571 |
| language | English |
| publishDate | 2024-12-01 |
| publisher | Wiley |
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| series | Evolutionary Applications |
| spelling | doaj-art-054c11130c4942fe8367cb886f87268a2025-01-29T07:57:46ZengWileyEvolutionary Applications1752-45712024-12-011712n/an/a10.1111/eva.70065Toward the Development of the Trojan Female Technique in Pest Insects: Male‐Specific Influence of Mitochondrial Haplotype on Reproductive Output in the Seed Beetle Acanthoscelides obtectusLea Vlajnić0Uroš Savković1Jelena Jović2Sanja Budečević3Biljana Stojković4Mirko Đorđević5Faculty of Biology, Institute of Zoology University of Belgrade Belgrade SerbiaDepartment of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”‐National Institute of the Republic of Serbia University of Belgrade Belgrade SerbiaDepartment of Plant Pests Institute for Plant Protection and Environment Zemun SerbiaDepartment of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”‐National Institute of the Republic of Serbia University of Belgrade Belgrade SerbiaFaculty of Biology, Institute of Zoology University of Belgrade Belgrade SerbiaDepartment of Evolutionary Biology, Institute for Biological Research “Siniša Stanković”‐National Institute of the Republic of Serbia University of Belgrade Belgrade SerbiaABSTRACT Biocontrol techniques that impair reproductive capacity of insect pests provide opportunities to control the dynamics of their populations while minimizing collateral damage to non‐target species and the environment. The Trojan Female Technique, or TFT, is a method of the trans‐generational fertility‐based population control through the release of females that carry mitochondrial DNA mutations that negatively affect male, but not female, reproductive output. TFT is based on the evolutionary hypothesis that, due to maternal inheritance of mitochondria, mutations which are beneficial or neutral in females but harmful in males can accumulate in the mitochondrial genome without selection acting against them. Although TFT has been theoretically substantiated, empirical work to date has focused only on Drosophila melanogaster populations, while the existence of male‐biased mutations and the TFT approach in economically important pest species remain unexplored. Here, we examined the sex‐specific effects of three distinct and naturally occurring mitochondrial haplotypes (MG1a, MG1d, and MG3b) on several reproductive and life history traits in the seed beetle Acanthoscelides obtectus. Our results revealed that males harboring the MG3b mitotype exhibited lower early fecundity and fertility, while there were no effects on females or longevity in either sex. Our experiments provide support for the existence of the mitochondrial variant that specifically impairs male reproductive output in pest insects. These results can be harnessed to further develop TFT as a novel form of biocontrol with broad applicability to economic pests and disease vector insects.https://doi.org/10.1111/eva.70065longevitymale infertilitymitonuclear interactionsMother's Cursepest controlsex‐specific effects |
| spellingShingle | Lea Vlajnić Uroš Savković Jelena Jović Sanja Budečević Biljana Stojković Mirko Đorđević Toward the Development of the Trojan Female Technique in Pest Insects: Male‐Specific Influence of Mitochondrial Haplotype on Reproductive Output in the Seed Beetle Acanthoscelides obtectus Evolutionary Applications longevity male infertility mitonuclear interactions Mother's Curse pest control sex‐specific effects |
| title | Toward the Development of the Trojan Female Technique in Pest Insects: Male‐Specific Influence of Mitochondrial Haplotype on Reproductive Output in the Seed Beetle Acanthoscelides obtectus |
| title_full | Toward the Development of the Trojan Female Technique in Pest Insects: Male‐Specific Influence of Mitochondrial Haplotype on Reproductive Output in the Seed Beetle Acanthoscelides obtectus |
| title_fullStr | Toward the Development of the Trojan Female Technique in Pest Insects: Male‐Specific Influence of Mitochondrial Haplotype on Reproductive Output in the Seed Beetle Acanthoscelides obtectus |
| title_full_unstemmed | Toward the Development of the Trojan Female Technique in Pest Insects: Male‐Specific Influence of Mitochondrial Haplotype on Reproductive Output in the Seed Beetle Acanthoscelides obtectus |
| title_short | Toward the Development of the Trojan Female Technique in Pest Insects: Male‐Specific Influence of Mitochondrial Haplotype on Reproductive Output in the Seed Beetle Acanthoscelides obtectus |
| title_sort | toward the development of the trojan female technique in pest insects male specific influence of mitochondrial haplotype on reproductive output in the seed beetle acanthoscelides obtectus |
| topic | longevity male infertility mitonuclear interactions Mother's Curse pest control sex‐specific effects |
| url | https://doi.org/10.1111/eva.70065 |
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