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Polyploidy versus endosymbionts in obligately thelytokous thrips
BACKGROUND: Thelytoky, the parthenogenetic development of females, has independently evolved in several insect orders yet the study of its mechanisms has so far mostly focussed on haplodiploid Hymenoptera, while alternative mechanisms of thelytoky such as polyploidy are far less understood. In haplo...
Autores principales: | , , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
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BioMed Central
2015
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4349774/ https://www.ncbi.nlm.nih.gov/pubmed/25880387 http://dx.doi.org/10.1186/s12862-015-0304-6 |
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author | Nguyen, Duong T Spooner-Hart, Robert N Riegler, Markus |
author_facet | Nguyen, Duong T Spooner-Hart, Robert N Riegler, Markus |
author_sort | Nguyen, Duong T |
collection | PubMed |
description | BACKGROUND: Thelytoky, the parthenogenetic development of females, has independently evolved in several insect orders yet the study of its mechanisms has so far mostly focussed on haplodiploid Hymenoptera, while alternative mechanisms of thelytoky such as polyploidy are far less understood. In haplodiploid insects, thelytoky can be encoded in their genomes, or induced by maternally inherited bacteria such as Wolbachia or Cardinium. Microbially facilitated thelytoky usually results in complete homozygosity due to gamete duplication and can be reverted into arrhenotoky, the parthenogenetic development of males, through treatment with antibiotics. In contrast, genetically encoded thelytoky cannot be removed and may result in conservation of heterozygosity due to gamete fusion. We have probed the obligate thelytoky of the greenhouse thrips, Heliothrips haemorrhoidalis (Bouché), a significant cosmopolitan pest and a model species of thelytoky in the haplodiploid insect order Thysanoptera. Earlier studies suggested terminal fusion as a mechanism for thelytoky in this species, while another study reported presence of Wolbachia; later it was speculated that Wolbachia plays a role in this thrips’ thelytokous reproduction. RESULTS: By using PCR and sequence analysis, we demonstrated that global population samples of H. haemorrhoidalis were not infected with Wolbachia, Cardinium or any other known bacterial reproductive manipulators. Antibiotic treatment of this thrips did also not result in male production. Some individuals carried two different alleles in two nuclear loci, histone 3 and elongation factor 1 alpha, suggesting heterozygosity. However, the majority of individuals had three different alleles suggesting that they were polyploid. Genetic diversity across both nuclear loci was low in all populations, and absent from mitochondrial cytochrome oxidase I, indicating that this species had experienced genetic bottlenecks, perhaps due to its invasion biology or a switch to thelytoky. CONCLUSIONS: Geographically broad sampling and experimental manipulation revealed low genetic diversity, absence of Wolbachia but presence of three different alleles of nuclear loci in most analysed individuals of obligately thelytokous H. haemorrhoidalis. This suggests that polyploidy may be involved in the thelytokous reproduction of this thrips species, and polyploidy may be a contributing factor in the reproduction of Thysanoptera and other haplodiploid insect orders. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0304-6) contains supplementary material, which is available to authorized users. |
format | Online Article Text |
id | pubmed-4349774 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2015 |
publisher | BioMed Central |
record_format | MEDLINE/PubMed |
spelling | pubmed-43497742015-03-06 Polyploidy versus endosymbionts in obligately thelytokous thrips Nguyen, Duong T Spooner-Hart, Robert N Riegler, Markus BMC Evol Biol Research Article BACKGROUND: Thelytoky, the parthenogenetic development of females, has independently evolved in several insect orders yet the study of its mechanisms has so far mostly focussed on haplodiploid Hymenoptera, while alternative mechanisms of thelytoky such as polyploidy are far less understood. In haplodiploid insects, thelytoky can be encoded in their genomes, or induced by maternally inherited bacteria such as Wolbachia or Cardinium. Microbially facilitated thelytoky usually results in complete homozygosity due to gamete duplication and can be reverted into arrhenotoky, the parthenogenetic development of males, through treatment with antibiotics. In contrast, genetically encoded thelytoky cannot be removed and may result in conservation of heterozygosity due to gamete fusion. We have probed the obligate thelytoky of the greenhouse thrips, Heliothrips haemorrhoidalis (Bouché), a significant cosmopolitan pest and a model species of thelytoky in the haplodiploid insect order Thysanoptera. Earlier studies suggested terminal fusion as a mechanism for thelytoky in this species, while another study reported presence of Wolbachia; later it was speculated that Wolbachia plays a role in this thrips’ thelytokous reproduction. RESULTS: By using PCR and sequence analysis, we demonstrated that global population samples of H. haemorrhoidalis were not infected with Wolbachia, Cardinium or any other known bacterial reproductive manipulators. Antibiotic treatment of this thrips did also not result in male production. Some individuals carried two different alleles in two nuclear loci, histone 3 and elongation factor 1 alpha, suggesting heterozygosity. However, the majority of individuals had three different alleles suggesting that they were polyploid. Genetic diversity across both nuclear loci was low in all populations, and absent from mitochondrial cytochrome oxidase I, indicating that this species had experienced genetic bottlenecks, perhaps due to its invasion biology or a switch to thelytoky. CONCLUSIONS: Geographically broad sampling and experimental manipulation revealed low genetic diversity, absence of Wolbachia but presence of three different alleles of nuclear loci in most analysed individuals of obligately thelytokous H. haemorrhoidalis. This suggests that polyploidy may be involved in the thelytokous reproduction of this thrips species, and polyploidy may be a contributing factor in the reproduction of Thysanoptera and other haplodiploid insect orders. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12862-015-0304-6) contains supplementary material, which is available to authorized users. BioMed Central 2015-02-22 /pmc/articles/PMC4349774/ /pubmed/25880387 http://dx.doi.org/10.1186/s12862-015-0304-6 Text en © Nguyen et al.; licensee BioMed Central. 2015 This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly credited. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated. |
spellingShingle | Research Article Nguyen, Duong T Spooner-Hart, Robert N Riegler, Markus Polyploidy versus endosymbionts in obligately thelytokous thrips |
title | Polyploidy versus endosymbionts in obligately thelytokous thrips |
title_full | Polyploidy versus endosymbionts in obligately thelytokous thrips |
title_fullStr | Polyploidy versus endosymbionts in obligately thelytokous thrips |
title_full_unstemmed | Polyploidy versus endosymbionts in obligately thelytokous thrips |
title_short | Polyploidy versus endosymbionts in obligately thelytokous thrips |
title_sort | polyploidy versus endosymbionts in obligately thelytokous thrips |
topic | Research Article |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4349774/ https://www.ncbi.nlm.nih.gov/pubmed/25880387 http://dx.doi.org/10.1186/s12862-015-0304-6 |
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