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First evidence of gonadal hybrid dysgenesis in Chagas disease vectors (Hemiptera, Triatominae): gonad atrophy prevents events of interspecific gene flow and introgression

BACKGROUND: Hybridization events between Triatoma spp. have been observed under both natural and laboratory conditions. The ability to produce hybrids can influence different aspects of the parent species, and may even result in events of introgression, speciation and extinction. Hybrid sterility is...

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Autores principales: Azevedo, Luísa Martins Sensato, Cesaretto, Natália Regina, de Oliveira, Jader, Ravazi, Amanda, dos Reis, Yago Visinho, Tadini, Samanta Cristina Antoniassi Fernandes, da Silva Masarin, Isabella, Borsatto, Kelly Cristine, Galvão, Cleber, da Rosa, João Aristeu, de Azeredo-Oliveira, Maria Tercília Vilela, Alevi, Kaio Cesar Chaboli
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10604409/
https://www.ncbi.nlm.nih.gov/pubmed/37891624
http://dx.doi.org/10.1186/s13071-023-06006-6
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author Azevedo, Luísa Martins Sensato
Cesaretto, Natália Regina
de Oliveira, Jader
Ravazi, Amanda
dos Reis, Yago Visinho
Tadini, Samanta Cristina Antoniassi Fernandes
da Silva Masarin, Isabella
Borsatto, Kelly Cristine
Galvão, Cleber
da Rosa, João Aristeu
de Azeredo-Oliveira, Maria Tercília Vilela
Alevi, Kaio Cesar Chaboli
author_facet Azevedo, Luísa Martins Sensato
Cesaretto, Natália Regina
de Oliveira, Jader
Ravazi, Amanda
dos Reis, Yago Visinho
Tadini, Samanta Cristina Antoniassi Fernandes
da Silva Masarin, Isabella
Borsatto, Kelly Cristine
Galvão, Cleber
da Rosa, João Aristeu
de Azeredo-Oliveira, Maria Tercília Vilela
Alevi, Kaio Cesar Chaboli
author_sort Azevedo, Luísa Martins Sensato
collection PubMed
description BACKGROUND: Hybridization events between Triatoma spp. have been observed under both natural and laboratory conditions. The ability to produce hybrids can influence different aspects of the parent species, and may even result in events of introgression, speciation and extinction. Hybrid sterility is caused by unviable gametes (due to errors in chromosomal pairing [meiosis]) or by gonadal dysgenesis (GD). All of the triatomine hybrids analyzed so far have not presented GD. We describe here for the first time GD events in triatomine hybrids and highlight these taxonomic and evolutionary implications of these events. METHODS: Reciprocal experimental crosses were performed between Triatoma longipennis and Triatoma mopan. Intercrosses were also performed between the hybrids, and backcrosses were performed between the hybrids and the parent species. In addition, morphological and cytological analyzes were performed on the atrophied gonads of the hybrids. RESULTS: Hybrids were obtained only for the crosses T. mopan♀ × T. longipennis♂. Intercrosses and backcrosses did not result in offspring. Morphological analyses of the male gonads of the hybrids confirmed that the phenomenon that resulted in sterility of the hybrid was bilateral GD (the gonads of the hybrids were completely atrophied). Cytological analyses of the testes of the hybrids also confirmed GD, with no germ cells observed (only somatic cells, which make up the peritoneal sheath). CONCLUSIONS: The observations made during this study allowed us to characterize, for the first time, GD in triatomines and demonstrated that gametogenesis does not occur in atrophied gonads. The characterization of GD in male hybrids resulting from the crossing of T. mopan♀ × T. longipennis♂ highlights the importance of evaluating both the morphology and the cytology of the gonads to confirm which event resulted in the sterility of the hybrid: GD (which results in no gamete production) or meiotic errors (which results in non-viable gametes). GRAPHICAL ABSTRACT: [Image: see text]
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spelling pubmed-106044092023-10-28 First evidence of gonadal hybrid dysgenesis in Chagas disease vectors (Hemiptera, Triatominae): gonad atrophy prevents events of interspecific gene flow and introgression Azevedo, Luísa Martins Sensato Cesaretto, Natália Regina de Oliveira, Jader Ravazi, Amanda dos Reis, Yago Visinho Tadini, Samanta Cristina Antoniassi Fernandes da Silva Masarin, Isabella Borsatto, Kelly Cristine Galvão, Cleber da Rosa, João Aristeu de Azeredo-Oliveira, Maria Tercília Vilela Alevi, Kaio Cesar Chaboli Parasit Vectors Research BACKGROUND: Hybridization events between Triatoma spp. have been observed under both natural and laboratory conditions. The ability to produce hybrids can influence different aspects of the parent species, and may even result in events of introgression, speciation and extinction. Hybrid sterility is caused by unviable gametes (due to errors in chromosomal pairing [meiosis]) or by gonadal dysgenesis (GD). All of the triatomine hybrids analyzed so far have not presented GD. We describe here for the first time GD events in triatomine hybrids and highlight these taxonomic and evolutionary implications of these events. METHODS: Reciprocal experimental crosses were performed between Triatoma longipennis and Triatoma mopan. Intercrosses were also performed between the hybrids, and backcrosses were performed between the hybrids and the parent species. In addition, morphological and cytological analyzes were performed on the atrophied gonads of the hybrids. RESULTS: Hybrids were obtained only for the crosses T. mopan♀ × T. longipennis♂. Intercrosses and backcrosses did not result in offspring. Morphological analyses of the male gonads of the hybrids confirmed that the phenomenon that resulted in sterility of the hybrid was bilateral GD (the gonads of the hybrids were completely atrophied). Cytological analyses of the testes of the hybrids also confirmed GD, with no germ cells observed (only somatic cells, which make up the peritoneal sheath). CONCLUSIONS: The observations made during this study allowed us to characterize, for the first time, GD in triatomines and demonstrated that gametogenesis does not occur in atrophied gonads. The characterization of GD in male hybrids resulting from the crossing of T. mopan♀ × T. longipennis♂ highlights the importance of evaluating both the morphology and the cytology of the gonads to confirm which event resulted in the sterility of the hybrid: GD (which results in no gamete production) or meiotic errors (which results in non-viable gametes). GRAPHICAL ABSTRACT: [Image: see text] BioMed Central 2023-10-27 /pmc/articles/PMC10604409/ /pubmed/37891624 http://dx.doi.org/10.1186/s13071-023-06006-6 Text en © The Author(s) 2023 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) . The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/ (https://creativecommons.org/publicdomain/zero/1.0/) ) applies to the data made available in this article, unless otherwise stated in a credit line to the data.
spellingShingle Research
Azevedo, Luísa Martins Sensato
Cesaretto, Natália Regina
de Oliveira, Jader
Ravazi, Amanda
dos Reis, Yago Visinho
Tadini, Samanta Cristina Antoniassi Fernandes
da Silva Masarin, Isabella
Borsatto, Kelly Cristine
Galvão, Cleber
da Rosa, João Aristeu
de Azeredo-Oliveira, Maria Tercília Vilela
Alevi, Kaio Cesar Chaboli
First evidence of gonadal hybrid dysgenesis in Chagas disease vectors (Hemiptera, Triatominae): gonad atrophy prevents events of interspecific gene flow and introgression
title First evidence of gonadal hybrid dysgenesis in Chagas disease vectors (Hemiptera, Triatominae): gonad atrophy prevents events of interspecific gene flow and introgression
title_full First evidence of gonadal hybrid dysgenesis in Chagas disease vectors (Hemiptera, Triatominae): gonad atrophy prevents events of interspecific gene flow and introgression
title_fullStr First evidence of gonadal hybrid dysgenesis in Chagas disease vectors (Hemiptera, Triatominae): gonad atrophy prevents events of interspecific gene flow and introgression
title_full_unstemmed First evidence of gonadal hybrid dysgenesis in Chagas disease vectors (Hemiptera, Triatominae): gonad atrophy prevents events of interspecific gene flow and introgression
title_short First evidence of gonadal hybrid dysgenesis in Chagas disease vectors (Hemiptera, Triatominae): gonad atrophy prevents events of interspecific gene flow and introgression
title_sort first evidence of gonadal hybrid dysgenesis in chagas disease vectors (hemiptera, triatominae): gonad atrophy prevents events of interspecific gene flow and introgression
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10604409/
https://www.ncbi.nlm.nih.gov/pubmed/37891624
http://dx.doi.org/10.1186/s13071-023-06006-6
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