Genomic patterns of divergence in the early and late steps of speciation of the deep-sea vent thermophilic worms of the genus Alvinella.
Divergence
Ecological species
Genome architecture
Habitat specialization
Hydrothermal vents
Selection
Speciation
Journal
BMC ecology and evolution
ISSN: 2730-7182
Titre abrégé: BMC Ecol Evol
Pays: England
ID NLM: 101775613
Informations de publication
Date de publication:
03 09 2022
03 09 2022
Historique:
received:
28
02
2022
accepted:
05
08
2022
entrez:
3
9
2022
pubmed:
4
9
2022
medline:
9
9
2022
Statut:
epublish
Résumé
The transient and fragmented nature of the deep-sea hydrothermal environment made of ridge subduction, plate collision and the emergence of new rifts is currently acting to separate of vent populations, promoting local adaptation and contributing to bursts of speciation and species specialization. The tube-dwelling worms Alvinella pompejana called the Pompeii worm and its sister species A. caudata live syntopically on the hottest part of deep-sea hydrothermal chimneys along the East Pacific Rise. They are exposed to extreme thermal and chemical gradients, which vary greatly in space and time, and thus represent ideal candidates for understanding the evolutionary mechanisms at play in the vent fauna evolution. We explored genomic patterns of divergence in the early and late stages of speciation of these emblematic worms using transcriptome assemblies and the first draft genome to better understand the relative role of geographic isolation and habitat preference in their genome evolution. Analyses were conducted on allopatric populations of Alvinella pompejana (early stage of separation) and between A. pompejana and its syntopic species Alvinella caudata (late stage of speciation). We first identified divergent genomic regions and targets of selection as well as their position in the genome over collections of orthologous genes and, then, described the speciation dynamics by documenting the annotation of the most divergent and/or positively selected genes involved in the isolation process. Gene mapping clearly indicated that divergent genes associated with the early stage of speciation, although accounting for nearly 30% of genes, are highly scattered in the genome without any island of divergence and not involved in gamete recognition or mito-nuclear incompatibilities. By contrast, genomes of A. pompejana and A. caudata are clearly separated with nearly all genes (96%) exhibiting high divergence. This congealing effect however seems to be linked to habitat specialization and still allows positive selection on genes involved in gamete recognition, as a possible long-duration process of species reinforcement. Our analyses highlight the non-negligible role of natural selection on both the early and late stages of speciation in the iconic thermophilic worms living on the walls of deep-sea hydrothermal chimneys. They shed light on the evolution of gene divergence during the process of speciation and species specialization over a very long period of time.
Sections du résumé
BACKGROUND
The transient and fragmented nature of the deep-sea hydrothermal environment made of ridge subduction, plate collision and the emergence of new rifts is currently acting to separate of vent populations, promoting local adaptation and contributing to bursts of speciation and species specialization. The tube-dwelling worms Alvinella pompejana called the Pompeii worm and its sister species A. caudata live syntopically on the hottest part of deep-sea hydrothermal chimneys along the East Pacific Rise. They are exposed to extreme thermal and chemical gradients, which vary greatly in space and time, and thus represent ideal candidates for understanding the evolutionary mechanisms at play in the vent fauna evolution.
RESULTS
We explored genomic patterns of divergence in the early and late stages of speciation of these emblematic worms using transcriptome assemblies and the first draft genome to better understand the relative role of geographic isolation and habitat preference in their genome evolution. Analyses were conducted on allopatric populations of Alvinella pompejana (early stage of separation) and between A. pompejana and its syntopic species Alvinella caudata (late stage of speciation). We first identified divergent genomic regions and targets of selection as well as their position in the genome over collections of orthologous genes and, then, described the speciation dynamics by documenting the annotation of the most divergent and/or positively selected genes involved in the isolation process. Gene mapping clearly indicated that divergent genes associated with the early stage of speciation, although accounting for nearly 30% of genes, are highly scattered in the genome without any island of divergence and not involved in gamete recognition or mito-nuclear incompatibilities. By contrast, genomes of A. pompejana and A. caudata are clearly separated with nearly all genes (96%) exhibiting high divergence. This congealing effect however seems to be linked to habitat specialization and still allows positive selection on genes involved in gamete recognition, as a possible long-duration process of species reinforcement.
CONCLUSION
Our analyses highlight the non-negligible role of natural selection on both the early and late stages of speciation in the iconic thermophilic worms living on the walls of deep-sea hydrothermal chimneys. They shed light on the evolution of gene divergence during the process of speciation and species specialization over a very long period of time.
Identifiants
pubmed: 36057769
doi: 10.1186/s12862-022-02057-y
pii: 10.1186/s12862-022-02057-y
pmc: PMC9441076
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
106Informations de copyright
© 2022. The Author(s).
Références
Nat Rev Genet. 2002 Feb;3(2):137-44
pubmed: 11836507
J Mol Biol. 1991 Sep 5;221(1):209-23
pubmed: 1920405
Physiology (Bethesda). 2012 Dec;27(6):362-9
pubmed: 23223630
Biotechnol Lett. 2012 May;34(5):813-22
pubmed: 22212490
Mol Ecol. 2003 Nov;12(11):3185-90
pubmed: 14629398
Nature. 2004 Apr 1;428(6982):493-521
pubmed: 15057822
Biol Bull. 1990 Dec;179(3):366-373
pubmed: 29314955
Genetics. 2017 Nov;207(3):825-842
pubmed: 29097397
Proc Natl Acad Sci U S A. 2005 May 3;102 Suppl 1:6522-6
pubmed: 15851676
Sci Rep. 2017 May 3;7(1):1454
pubmed: 28469247
Nat Rev Genet. 2017 Feb;18(2):87-100
pubmed: 27840429
Evolution. 2010 Jun;64(6):1729-47
pubmed: 20624183
Genome Biol Evol. 2017 Feb 1;9(2):279-296
pubmed: 28082607
Nat Commun. 2018 Jun 28;9(1):2518
pubmed: 29955054
Evolution. 2001 Jun;55(6):1085-94
pubmed: 11475044
Mol Ecol. 2001 Dec;10(12):2819-31
pubmed: 11903895
Mol Ecol. 2014 Aug;23(16):4074-88
pubmed: 24724861
Proc Natl Acad Sci U S A. 2018 Oct 23;115(43):11006-11011
pubmed: 30297406
Mol Ecol. 2014 Jul;23(13):3133-57
pubmed: 24845075
Mol Ecol. 2009 Feb;18(3):375-402
pubmed: 19143936
PLoS Biol. 2005 Sep;3(9):e285
pubmed: 16076241
Am Nat. 2018 Jul;192(1):10-22
pubmed: 29897805
Am Nat. 2007 Feb;169(2):151-62
pubmed: 17211800
Mol Biol Evol. 2013 Dec;30(12):2723-4
pubmed: 24105918
Mol Ecol. 2017 Jan;26(2):554-570
pubmed: 27864910
BMC Evol Biol. 2010 Jul 22;10:220
pubmed: 20663123
Nat Rev Genet. 2014 Mar;15(3):176-92
pubmed: 24535286
Trends Genet. 2012 Jul;28(7):342-50
pubmed: 22520730
Mol Ecol. 2008 Oct;17(19):4334-45
pubmed: 18986504
Mol Biol Evol. 2002 Dec;19(12):2142-9
pubmed: 12446806
Nat Rev Genet. 2010 Mar;11(3):175-80
pubmed: 20051985
BMC Genomics. 2012 Mar 22;13:107
pubmed: 22439654
Science. 2002 Feb 15;295(5558):1253-7
pubmed: 11847331
Appl Environ Microbiol. 1997 Mar;63(3):1124-30
pubmed: 16535543
Mol Biol Evol. 2007 Aug;24(8):1586-91
pubmed: 17483113
BMC Evol Biol. 2016 Oct 28;16(1):235
pubmed: 27793079
Environ Microbiol Rep. 2022 Apr;14(2):299-307
pubmed: 35170217
Genom Data. 2015 Jul 15;5:352-9
pubmed: 26484285
Mol Ecol. 2009 Sep;18(18):3903-17
pubmed: 19709370
J Hered. 1997 Jul-Aug;88(4):285-93
pubmed: 9262010
J Mol Biol. 2000 Sep 29;302(4):811-20
pubmed: 10993725
BMC Genomics. 2010 Nov 16;11:634
pubmed: 21080938
Evolution. 2017 May;71(5):1366-1380
pubmed: 28272742
Mol Ecol. 2014 Aug;23(16):3938-40
pubmed: 25088551
BMC Evol Biol. 2013 Jan 24;13:21
pubmed: 23347448
J Hered. 2014;105 Suppl 1:810-20
pubmed: 25149256
Evol Appl. 2020 May 01;13(6):1320-1334
pubmed: 32684961
PLoS One. 2013 Dec 02;8(12):e81555
pubmed: 24312557
J Evol Biol. 2017 Aug;30(8):1478-1481
pubmed: 28786194
Nature. 1977 May 19;267(5608):275-6
pubmed: 865622
Mol Biol Evol. 2007 Feb;24(2):374-81
pubmed: 17101719
Evolution. 2009 Feb;63(2):418-31
pubmed: 19215292
PLoS One. 2009 Aug 03;4(8):e6485
pubmed: 19649261
Evolution. 1999 Aug;53(4):1128-1142
pubmed: 28565536
Mol Ecol. 2004 Sep;13(9):2603-15
pubmed: 15315674
Cold Spring Harb Protoc. 2009 Nov;2009(11):pdb.prot5319
pubmed: 20150058
PLoS Biol. 2016 Dec 27;14(12):e2000234
pubmed: 28027292