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Multiple hybridization events and repeated evolution of homoeologue expression bias in parthenogenetic, polyploid New Zealand stick insects
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  • Seung-Sub Choi,
  • Ann Mc Cartney,
  • Duckchul Park,
  • Hester Roberts,
  • Talia Brav-Cubitt,
  • Caroline Mitchell,
  • Thomas Buckley
Seung-Sub Choi
University of Auckland
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Ann Mc Cartney
Landcare Research New Zealand Auckland
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Duckchul Park
Landcare Research New Zealand Auckland
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Hester Roberts
Landcare Research New Zealand Auckland
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Talia Brav-Cubitt
Landcare Research New Zealand Auckland
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Caroline Mitchell
Landcare Research New Zealand
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Thomas Buckley
Landcare Research New Zealand Auckland

Corresponding Author:buckleyt@landcareresearch.co.nz

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Abstract

During hybrid speciation, homoeologues combine in a single genome. Homoeologue expression bias (HEB) occurs when one homoeologue has higher gene expression than another. HEB has been well characterized in plants but rarely investigated in animals, especially invertebrates. Consequently, we have little idea as to the role that HEB plays in allopolyploid invertebrate genomes. If HEB is constrained by features of the parental genomes, then we predict repeated evolution of similar HEB patterns among hybrid genomes formed from the same parental lineages. To address this, we reconstructed the history of hybridization between the New Zealand stick insect genera Acanthoxyla and Clitarchus using a high-quality genome assembly from Clitarchus hookeri to call variants and phase alleles. These analyses revealed the formation of three independent diploid and triploid hybrid lineages between these genera. RNA sequencing revealed a similar magnitude and direction of HEB among these hybrid lineages, and we observed that many enriched functions and pathways were also shared among lineages, consistent with repeated evolution due to parental genome constraints. In most lineages, a slight majority of the genes involved in mitochondrial function showed HEB towards the maternal homoeologues, consistent with only weak effects of mitonuclear incompatibility. We also observed a proteasome functional enrichment in most lineages and hypothesize this may result from the need to maintain proteostasis in hybrid genomes. Reference bias was a pervasive problem, and we caution against relying on HEB estimates from a single parental reference genome.
31 Oct 2023Submitted to Molecular Ecology
31 Oct 2023Submission Checks Completed
31 Oct 2023Assigned to Editor
31 Oct 2023Review(s) Completed, Editorial Evaluation Pending
04 Mar 20241st Revision Received
04 Mar 2024Submission Checks Completed
04 Mar 2024Assigned to Editor
04 Mar 2024Review(s) Completed, Editorial Evaluation Pending
17 Apr 2024Editorial Decision: Accept