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

Whole-genome duplications (WGDs) have occurred multiple times during animal evolution, including in lineages leading to vertebrates, teleosts, horseshoe crabs, and arachnopulmonates. These dramatic events initially produce a wealth of new genetic material, generally followed by extensive gene loss....

Full description

Bibliographic Details
Main Authors: Harper, A, Baudouin Gonzalez, L, Schönauer, A, Janssen, R, Seiter, M, Holzem, M, Arif, S, McGregor, AP, Sumner-Rooney, L
Format: Journal article
Language:English
Published: Genetics Society of America 2021
_version_ 1826313541211127808
author Harper, A
Baudouin Gonzalez, L
Schönauer, A
Janssen, R
Seiter, M
Holzem, M
Arif, S
McGregor, AP
Sumner-Rooney, L
author_facet Harper, A
Baudouin Gonzalez, L
Schönauer, A
Janssen, R
Seiter, M
Holzem, M
Arif, S
McGregor, AP
Sumner-Rooney, L
author_sort Harper, A
collection OXFORD
description Whole-genome duplications (WGDs) have occurred multiple times during animal evolution, including in lineages leading to vertebrates, teleosts, horseshoe crabs, and arachnopulmonates. These dramatic events initially produce a wealth of new genetic material, generally followed by extensive gene loss. It appears, however, that developmental genes such as homeobox genes, signaling pathway components and microRNAs are frequently retained as duplicates (so-called ohnologs) following WGD. These not only provide the best evidence for WGD, but an opportunity to study its evolutionary consequences. Although these genes are well studied in the context of vertebrate WGD, similar comparisons across the extant arachnopulmonate orders are patchy. We sequenced embryonic transcriptomes from two spider species and two amblypygid species and surveyed three important gene families, Hox, Wnt, and frizzled, across these and 12 existing transcriptomic and genomic resources for chelicerates. We report extensive retention of putative ohnologs, further supporting the ancestral arachnopulmonate WGD. We also found evidence of consistent evolutionary trajectories in Hox and Wnt gene repertoires across three of the six arachnopulmonate orders, with interorder variation in the retention of specific paralogs. We identified variation between major clades in spiders and are better able to reconstruct the chronology of gene duplications and losses in spiders, amblypygids, and scorpions. These insights shed light on the evolution of the developmental toolkit in arachnopulmonates, highlight the importance of the comparative approach within lineages, and provide substantial new transcriptomic data for future study.
first_indexed 2024-09-25T04:16:14Z
format Journal article
id oxford-uuid:e888a5c4-3c12-4f89-a8d9-77ecec22eaf5
institution University of Oxford
language English
last_indexed 2024-09-25T04:16:14Z
publishDate 2021
publisher Genetics Society of America
record_format dspace
spelling oxford-uuid:e888a5c4-3c12-4f89-a8d9-77ecec22eaf52024-07-20T14:01:51ZWidespread retention of ohnologs in key developmental gene families following whole-genome duplication in arachnopulmonatesJournal articlehttp://purl.org/coar/resource_type/c_dcae04bcuuid:e888a5c4-3c12-4f89-a8d9-77ecec22eaf5EnglishJisc Publications RouterGenetics Society of America2021Harper, ABaudouin Gonzalez, LSchönauer, AJanssen, RSeiter, MHolzem, MArif, SMcGregor, APSumner-Rooney, LWhole-genome duplications (WGDs) have occurred multiple times during animal evolution, including in lineages leading to vertebrates, teleosts, horseshoe crabs, and arachnopulmonates. These dramatic events initially produce a wealth of new genetic material, generally followed by extensive gene loss. It appears, however, that developmental genes such as homeobox genes, signaling pathway components and microRNAs are frequently retained as duplicates (so-called ohnologs) following WGD. These not only provide the best evidence for WGD, but an opportunity to study its evolutionary consequences. Although these genes are well studied in the context of vertebrate WGD, similar comparisons across the extant arachnopulmonate orders are patchy. We sequenced embryonic transcriptomes from two spider species and two amblypygid species and surveyed three important gene families, Hox, Wnt, and frizzled, across these and 12 existing transcriptomic and genomic resources for chelicerates. We report extensive retention of putative ohnologs, further supporting the ancestral arachnopulmonate WGD. We also found evidence of consistent evolutionary trajectories in Hox and Wnt gene repertoires across three of the six arachnopulmonate orders, with interorder variation in the retention of specific paralogs. We identified variation between major clades in spiders and are better able to reconstruct the chronology of gene duplications and losses in spiders, amblypygids, and scorpions. These insights shed light on the evolution of the developmental toolkit in arachnopulmonates, highlight the importance of the comparative approach within lineages, and provide substantial new transcriptomic data for future study.
spellingShingle Harper, A
Baudouin Gonzalez, L
Schönauer, A
Janssen, R
Seiter, M
Holzem, M
Arif, S
McGregor, AP
Sumner-Rooney, L
Widespread retention of ohnologs in key developmental gene families following whole-genome duplication in arachnopulmonates
title Widespread retention of ohnologs in key developmental gene families following whole-genome duplication in arachnopulmonates
title_full Widespread retention of ohnologs in key developmental gene families following whole-genome duplication in arachnopulmonates
title_fullStr Widespread retention of ohnologs in key developmental gene families following whole-genome duplication in arachnopulmonates
title_full_unstemmed Widespread retention of ohnologs in key developmental gene families following whole-genome duplication in arachnopulmonates
title_short Widespread retention of ohnologs in key developmental gene families following whole-genome duplication in arachnopulmonates
title_sort widespread retention of ohnologs in key developmental gene families following whole genome duplication in arachnopulmonates
work_keys_str_mv AT harpera widespreadretentionofohnologsinkeydevelopmentalgenefamiliesfollowingwholegenomeduplicationinarachnopulmonates
AT baudouingonzalezl widespreadretentionofohnologsinkeydevelopmentalgenefamiliesfollowingwholegenomeduplicationinarachnopulmonates
AT schonauera widespreadretentionofohnologsinkeydevelopmentalgenefamiliesfollowingwholegenomeduplicationinarachnopulmonates
AT janssenr widespreadretentionofohnologsinkeydevelopmentalgenefamiliesfollowingwholegenomeduplicationinarachnopulmonates
AT seiterm widespreadretentionofohnologsinkeydevelopmentalgenefamiliesfollowingwholegenomeduplicationinarachnopulmonates
AT holzemm widespreadretentionofohnologsinkeydevelopmentalgenefamiliesfollowingwholegenomeduplicationinarachnopulmonates
AT arifs widespreadretentionofohnologsinkeydevelopmentalgenefamiliesfollowingwholegenomeduplicationinarachnopulmonates
AT mcgregorap widespreadretentionofohnologsinkeydevelopmentalgenefamiliesfollowingwholegenomeduplicationinarachnopulmonates
AT sumnerrooneyl widespreadretentionofohnologsinkeydevelopmentalgenefamiliesfollowingwholegenomeduplicationinarachnopulmonates