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Widespread retention of ohnologs in key developmental gene families following whole genome duplication in arachnopulmonates

Amber Harper, Luis Baudouin Gonzalez, Anna Schönauer, Michael Seiter, Michaela Holzem, Saad Arif, Alistair P. McGregor, Lauren Sumner-Rooney
doi: https://doi.org/10.1101/2020.07.10.177725
Amber Harper
1Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
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Luis Baudouin Gonzalez
1Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
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Anna Schönauer
1Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
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Michael Seiter
2Department of Evolutionary Biology, Unit Integrative Zoology, University of Vienna, Althanstrasse 14, 1090 Vienna, Austria
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Michaela Holzem
1Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
3Division of Signalling and Functional Genomics, German Cancer Research Centre (DKFZ), Heidelberg, Germany and Department of Cell and Molecular Biology, Medical Faculty Mannheim, Heidelberg University, Heidelberg, Germany
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Saad Arif
1Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
4Centre for Functional Genomics, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
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Alistair P. McGregor
1Department of Biological and Medical Sciences, Faculty of Health and Life Sciences, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
4Centre for Functional Genomics, Oxford Brookes University, Oxford, OX3 0BP, United Kingdom
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  • For correspondence: amcgregor@brookes.ac.uk lauren.sumner-rooney@oum.ox.ac.uk
Lauren Sumner-Rooney
5Oxford University Museum of Natural History, University of Oxford, Oxford OX1 3PW, United Kingdom
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  • For correspondence: amcgregor@brookes.ac.uk lauren.sumner-rooney@oum.ox.ac.uk
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Abstract

Whole genome duplications (WGD) have occurred multiple times in the evolution of animals, including in the lineages leading to vertebrates, teleosts, horseshoe crabs and arachnopulmonates. These dramatic genomic events initially produce a wealth of new genetic material, which is generally followed by extensive gene loss. It appears that developmental genes such as homeobox genes, signalling pathway components and microRNAs, however, tend to be more frequently retained in duplicate following WGD (ohnologs). These not only provide the best evidence for the occurrence of WGD, but an opportunity to study its evolutionary implications. Although these genes are relatively well studied in the context of vertebrate WGD, genomic and transcriptomic data for independent comparison in other groups are scarce, with patchy sampling of only two of the five extant arachnopulmonate orders. To improve our knowledge of developmental gene repertoires, and their evolution since the arachnopulmonate WGD, we sequenced embryonic transcriptomes from two additional spider species and two whip spider species and surveyed them for three important gene families: Hox, Wnt and frizzled. We report extensive retention of ohnologs in all four species, further supporting the arachnopulmonate WGD hypothesis. Thanks to improved sampling we were able to identify patterns of likely ohnolog retention and loss within spiders, including apparent differences between major clades. The two amblypygid species have larger ohnolog repertoires of these genes than both spiders and scorpions; including the first reported duplicated Wnt1/wg, the first Wnt10 recovered in an arachnid, and broad retention of frizzled genes. These insights shed light on the evolution of the enigmatic whip spiders, highlight the importance of the comparative approach within lineages, and provide substantial new transcriptomic data for future study.

Competing Interest Statement

The authors have declared no competing interest.

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Posted July 10, 2020.
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Widespread retention of ohnologs in key developmental gene families following whole genome duplication in arachnopulmonates
Amber Harper, Luis Baudouin Gonzalez, Anna Schönauer, Michael Seiter, Michaela Holzem, Saad Arif, Alistair P. McGregor, Lauren Sumner-Rooney
bioRxiv 2020.07.10.177725; doi: https://doi.org/10.1101/2020.07.10.177725
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Widespread retention of ohnologs in key developmental gene families following whole genome duplication in arachnopulmonates
Amber Harper, Luis Baudouin Gonzalez, Anna Schönauer, Michael Seiter, Michaela Holzem, Saad Arif, Alistair P. McGregor, Lauren Sumner-Rooney
bioRxiv 2020.07.10.177725; doi: https://doi.org/10.1101/2020.07.10.177725

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