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Are asymmetric inheritance systems an evolutionary trap? Transitions in the mechanism of paternal genome loss in the scale insect family Eriococcidae

Haplodiploidy and paternal genome elimination (PGE) are examples of asymmetric inheritance, where males transmit only maternally inherited chromosomes to their offspring. Under haplodiploidy, this results from males being haploid, whereas under PGE, males inherit but subsequently exclude paternally...

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Autores principales: Hodson, Christina N, Toon, Alicia, Cook, Lyn G, Ross, Laura
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Oxford University Press 2023
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10324942/
https://www.ncbi.nlm.nih.gov/pubmed/37183508
http://dx.doi.org/10.1093/genetics/iyad090
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author Hodson, Christina N
Toon, Alicia
Cook, Lyn G
Ross, Laura
author_facet Hodson, Christina N
Toon, Alicia
Cook, Lyn G
Ross, Laura
author_sort Hodson, Christina N
collection PubMed
description Haplodiploidy and paternal genome elimination (PGE) are examples of asymmetric inheritance, where males transmit only maternally inherited chromosomes to their offspring. Under haplodiploidy, this results from males being haploid, whereas under PGE, males inherit but subsequently exclude paternally inherited chromosomes from sperm. Their evolution involves changes in the mechanisms of meiosis and sex determination and sometimes also dosage compensation. As a result, these systems are thought to be an evolutionary trap, meaning that once asymmetric chromosome transmission evolves, it is difficult to transition back to typical Mendelian transmission. We assess whether there is evidence for this idea in the scale insect family Eriococcidae, a lineage with PGE and the only clade with a suggestion that asymmetric inheritance has transitioned back to Mendelian inheritance. We conduct a cytological survey of 13 eriococcid species, and a cytological, genetic, and gene expression analysis of species in the genus Cystococcus, to investigate whether there is evidence for species in this family evolving Mendelian chromosome transmission. Although we find that all species we examined exhibit PGE, the mechanism is extremely variable within Eriococcidae. Within Cystococcus, in fact, we uncover a previously undiscovered type of PGE in scale insects that acts exclusively in meiosis, where paternally inherited chromosomes in males are present, uncondensed, and expressed in somatic cells but eliminated prior to meiosis. Broadly, we fail to find evidence for a reversion from PGE to Mendelian inheritance in Eriococcidae, supporting the idea that asymmetric inheritance systems such as PGE may be an evolutionary trap.
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spelling pubmed-103249422023-07-07 Are asymmetric inheritance systems an evolutionary trap? Transitions in the mechanism of paternal genome loss in the scale insect family Eriococcidae Hodson, Christina N Toon, Alicia Cook, Lyn G Ross, Laura Genetics Investigation Haplodiploidy and paternal genome elimination (PGE) are examples of asymmetric inheritance, where males transmit only maternally inherited chromosomes to their offspring. Under haplodiploidy, this results from males being haploid, whereas under PGE, males inherit but subsequently exclude paternally inherited chromosomes from sperm. Their evolution involves changes in the mechanisms of meiosis and sex determination and sometimes also dosage compensation. As a result, these systems are thought to be an evolutionary trap, meaning that once asymmetric chromosome transmission evolves, it is difficult to transition back to typical Mendelian transmission. We assess whether there is evidence for this idea in the scale insect family Eriococcidae, a lineage with PGE and the only clade with a suggestion that asymmetric inheritance has transitioned back to Mendelian inheritance. We conduct a cytological survey of 13 eriococcid species, and a cytological, genetic, and gene expression analysis of species in the genus Cystococcus, to investigate whether there is evidence for species in this family evolving Mendelian chromosome transmission. Although we find that all species we examined exhibit PGE, the mechanism is extremely variable within Eriococcidae. Within Cystococcus, in fact, we uncover a previously undiscovered type of PGE in scale insects that acts exclusively in meiosis, where paternally inherited chromosomes in males are present, uncondensed, and expressed in somatic cells but eliminated prior to meiosis. Broadly, we fail to find evidence for a reversion from PGE to Mendelian inheritance in Eriococcidae, supporting the idea that asymmetric inheritance systems such as PGE may be an evolutionary trap. Oxford University Press 2023-05-15 /pmc/articles/PMC10324942/ /pubmed/37183508 http://dx.doi.org/10.1093/genetics/iyad090 Text en © The Author(s) 2023. Published by Oxford University Press on behalf of The Genetics Society of America. https://creativecommons.org/licenses/by/4.0/This is an Open Access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/), which permits unrestricted reuse, distribution, and reproduction in any medium, provided the original work is properly cited.
spellingShingle Investigation
Hodson, Christina N
Toon, Alicia
Cook, Lyn G
Ross, Laura
Are asymmetric inheritance systems an evolutionary trap? Transitions in the mechanism of paternal genome loss in the scale insect family Eriococcidae
title Are asymmetric inheritance systems an evolutionary trap? Transitions in the mechanism of paternal genome loss in the scale insect family Eriococcidae
title_full Are asymmetric inheritance systems an evolutionary trap? Transitions in the mechanism of paternal genome loss in the scale insect family Eriococcidae
title_fullStr Are asymmetric inheritance systems an evolutionary trap? Transitions in the mechanism of paternal genome loss in the scale insect family Eriococcidae
title_full_unstemmed Are asymmetric inheritance systems an evolutionary trap? Transitions in the mechanism of paternal genome loss in the scale insect family Eriococcidae
title_short Are asymmetric inheritance systems an evolutionary trap? Transitions in the mechanism of paternal genome loss in the scale insect family Eriococcidae
title_sort are asymmetric inheritance systems an evolutionary trap? transitions in the mechanism of paternal genome loss in the scale insect family eriococcidae
topic Investigation
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10324942/
https://www.ncbi.nlm.nih.gov/pubmed/37183508
http://dx.doi.org/10.1093/genetics/iyad090
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