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Contrasting Evolutionary Trajectories Under Paternal Genome Elimination in Male and Female Citrus Mealybugs

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posted on 2025-07-31, 15:05 authored by Andrew J Mongue, Tamsin E Woodman, Hollie MarshallHollie Marshall, Arkadiy Garber, José C Franco, John P McCutcheon, Laura Ross
<p dir="ltr">Most studies of sex‐biased genes explore their evolution in familiar chromosomal sex determination systems, leaving the evolution of sex differences under alternative reproductive systems unknown. Here we explore the system of paternal genome elimination employed by mealybugs (Hemiptera: Pseudococcidae) which have no sex chromosomes. Instead, all chromosomes are autosomal and inherited in two copies, but sex is determined by the ploidy of expression. Females express both parental alleles, but males reliably silence their paternally inherited chromosomes, creating genome‐wide haploid expression in males and diploid expression in females. Additionally, sons do not express alleles directly inherited from their fathers, potentially disrupting the evolution of male‐benefiting traits. To understand how these dynamics impact molecular evolution, we generated sex‐specific RNAseq, a new gene annotation, and whole‐genome population sequencing of the citrus mealybug, Planococcus citri. We found that genes expressed primarily in females hold more variation and evolve more quickly than those expressed in males or both sexes. Conversely, we found more apparent adaptation in genes expressed mainly in males than in those expressed in females. Put together, in this paternal genome elimination system there is slower change on the male side but, by increasing selective scrutiny, an increase in the degree of adaptation in these genes. These results expand our understanding of evolution in a non‐Mendelian genetic system and the data we generated should prove useful for future research on this pest insect.</p>

Funding

The Evolutionary Dynamics of Genetic Conflict: the Origin, Maintenance and Loss of Paternal Genome Elimination.

Natural Environment Research Council

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Royal Society (RG160842)

History

Author affiliation

College of Life Sciences Genetics, Genome Biology & Cancer Sciences

Version

  • VoR (Version of Record)

Published in

Molecular Ecology

Volume

34

Pagination

e17826

Publisher

Wiley

issn

0962-1083

eissn

1365-294X

Copyright date

2025

Available date

2025-07-31

Spatial coverage

England

Language

en

Deposited by

Dr Hollie Marshall

Deposit date

2025-06-27

Data Access Statement

We have archived the data used for this project as follows. The genome assembly was previously published and can be accessed with the accession GCA_950023065.1 on NCBI. The gene annotation is hosted alongside analysis scripts at the following git repo: https://github.com/amongue/citriPopGen. Short-read population genetic sequences are found under the NCBI BioProject PRJNA1211521 and RNA sequencing under PRJNA1207926.

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