Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior?
Abstract Queen discrimination behavior in the fire ant Solenopsis invicta maintains its two types of societies: colonies with one (monogyne) or many (polygyne) queens, yet the underlying genetic mechanism is poorly understood. This behavior is controlled by two supergene alleles, SB and Sb, with ~60...
| Main Authors: | , , , , |
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| Format: | Article |
| Language: | English |
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Wiley
2019-11-01
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| Series: | Ecology and Evolution |
| Subjects: | |
| Online Access: | https://doi.org/10.1002/ece3.5748 |
| _version_ | 1818320973336674304 |
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| author | Viet‐Dai Dang Amir B. Cohanim Silvia Fontana Eyal Privman John Wang |
| author_facet | Viet‐Dai Dang Amir B. Cohanim Silvia Fontana Eyal Privman John Wang |
| author_sort | Viet‐Dai Dang |
| collection | DOAJ |
| description | Abstract Queen discrimination behavior in the fire ant Solenopsis invicta maintains its two types of societies: colonies with one (monogyne) or many (polygyne) queens, yet the underlying genetic mechanism is poorly understood. This behavior is controlled by two supergene alleles, SB and Sb, with ~600 genes. Polygyne workers, having either the SB/SB or SB/Sb genotype, accept additional SB/Sb queens into their colonies but kill SB/SB queens. In contrast, monogyne workers, all SB/SB, reject all additional queens regardless of genotype. Because the SB and Sb alleles have suppressed recombination, determining which genes within the supergene mediate this differential worker behavior is difficult. We hypothesized that the alternate worker genotypes sense queens differently because of the evolution of differential expression of key genes in their main sensory organ, the antennae. To identify such genes, we sequenced RNA from four replicates of pooled antennae from three classes of workers: monogyne SB/SB, polygyne SB/SB, and polygyne SB/Sb. We identified 81 differentially expressed protein‐coding genes with 13 encoding potential chemical metabolism or perception proteins. We focused on the two odorant perception genes: an odorant receptor SiOR463 and an odorant‐binding protein SiOBP12. We found that SiOR463 has been lost in the Sb genome. In contrast, SiOBP12 has an Sb‐specific duplication, SiOBP12b′, which is expressed in the SB/Sb worker antennae, while both paralogs are expressed in the body. Comparisons with another fire ant species revealed that SiOBP12b′ antennal expression is specific to S. invicta and suggests that queen discrimination may have evolved, in part, through expression neofunctionalization. |
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| id | doaj.art-4640db4493f447f4b4c7c4087cac988a |
| institution | Directory Open Access Journal |
| issn | 2045-7758 |
| language | English |
| last_indexed | 2024-12-13T10:33:31Z |
| publishDate | 2019-11-01 |
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| series | Ecology and Evolution |
| spelling | doaj.art-4640db4493f447f4b4c7c4087cac988a2022-12-21T23:50:47ZengWileyEcology and Evolution2045-77582019-11-01922127541276610.1002/ece3.5748Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior?Viet‐Dai Dang0Amir B. Cohanim1Silvia Fontana2Eyal Privman3John Wang4Biodiversity Research Center Academia Sinica Taipei TaiwanDepartment of Evolutionary and Environmental Biology Institute of Evolution University of Haifa Haifa IsraelBiodiversity Research Center Academia Sinica Taipei TaiwanDepartment of Evolutionary and Environmental Biology Institute of Evolution University of Haifa Haifa IsraelBiodiversity Research Center Academia Sinica Taipei TaiwanAbstract Queen discrimination behavior in the fire ant Solenopsis invicta maintains its two types of societies: colonies with one (monogyne) or many (polygyne) queens, yet the underlying genetic mechanism is poorly understood. This behavior is controlled by two supergene alleles, SB and Sb, with ~600 genes. Polygyne workers, having either the SB/SB or SB/Sb genotype, accept additional SB/Sb queens into their colonies but kill SB/SB queens. In contrast, monogyne workers, all SB/SB, reject all additional queens regardless of genotype. Because the SB and Sb alleles have suppressed recombination, determining which genes within the supergene mediate this differential worker behavior is difficult. We hypothesized that the alternate worker genotypes sense queens differently because of the evolution of differential expression of key genes in their main sensory organ, the antennae. To identify such genes, we sequenced RNA from four replicates of pooled antennae from three classes of workers: monogyne SB/SB, polygyne SB/SB, and polygyne SB/Sb. We identified 81 differentially expressed protein‐coding genes with 13 encoding potential chemical metabolism or perception proteins. We focused on the two odorant perception genes: an odorant receptor SiOR463 and an odorant‐binding protein SiOBP12. We found that SiOR463 has been lost in the Sb genome. In contrast, SiOBP12 has an Sb‐specific duplication, SiOBP12b′, which is expressed in the SB/Sb worker antennae, while both paralogs are expressed in the body. Comparisons with another fire ant species revealed that SiOBP12b′ antennal expression is specific to S. invicta and suggests that queen discrimination may have evolved, in part, through expression neofunctionalization.https://doi.org/10.1002/ece3.5748fire antneofunctionalizationodorant‐binding proteinRNA‐SeqSolenopsis invictaworker antennae |
| spellingShingle | Viet‐Dai Dang Amir B. Cohanim Silvia Fontana Eyal Privman John Wang Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior? Ecology and Evolution fire ant neofunctionalization odorant‐binding protein RNA‐Seq Solenopsis invicta worker antennae |
| title | Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior? |
| title_full | Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior? |
| title_fullStr | Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior? |
| title_full_unstemmed | Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior? |
| title_short | Has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior? |
| title_sort | has gene expression neofunctionalization in the fire ant antennae contributed to queen discrimination behavior |
| topic | fire ant neofunctionalization odorant‐binding protein RNA‐Seq Solenopsis invicta worker antennae |
| url | https://doi.org/10.1002/ece3.5748 |
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