Patterns of hybridization and cryptic introgression among one- and four-needled pinyon pines.
Cryptic introgression
genomics
hybridization
needle number
pines
pinyon resin canals
Journal
Annals of botany
ISSN: 1095-8290
Titre abrégé: Ann Bot
Pays: England
ID NLM: 0372347
Informations de publication
Date de publication:
13 08 2020
13 08 2020
Historique:
received:
12
12
2019
accepted:
27
03
2020
pubmed:
31
3
2020
medline:
3
10
2020
entrez:
31
3
2020
Statut:
ppublish
Résumé
Pinyon pine hybridization is widely acknowledged, but the frequency of and contributors to such interspecific mating remain largely unstudied. Pinus quadrifolia has three to four needles per fascicle, suggesting that it is a result of hybridization between the five-needled P. juarezensis and the single-needled P. monophylla. In this study we address the taxonomic validity of P. juarezensis, the hybrid origin of P. quadrifolia and the presence of hybridization and intermediate morphology as a result of interspecific hybridization in this complex. We address these questions by combining a genomic and morphological approach. We generated 1868 single nucleotide polymorphisms (SNPs) to detect genetic clusters using principal co-ordinates analyis, discriminant analysis of principal components, fastSTRUCTURE and ADMIXTURE analyses, and performed a morphological analysis of the leaves. We found that the five-needled pinyons did not differ genetically from the four-needled P. quadrifolia, reducing the status of P. juarezensis to P. quadrifolia. We also found no evidence that P. quadrifolia is of hybrid origin from P. juarezensis × P. monophylla but is instead a genetically distinct species with natural needle number variation that has yet to be explained. Hybridization does occur in this complex, but mostly between P. quadrifolia and P. californiarum, and less commonly between P. quadrifolia and P. monophylla. Interestingly, some hybrid derivatives were detected between both single-needled taxa, P. monophylla and P. californiarum, a hybrid combination that has not yet been proposed. Hybrids have intermediate morphology when they have similar genetic contributions from both parental species; however, when one parent contributes more, hybrid derivatives resemble the parent with higher genetic contribution, resulting in cryptic introgression. Our detailed sampling across the distribution of this complex allows us to describe the patterns of hybridization among these taxa, resolves an ancient taxonomic conflict and provides insights into the challenges of exclusively using morphological traits when identifying these taxa with cryptic hybridization and variable morphology.
Sections du résumé
BACKGROUND AND AIMS
Pinyon pine hybridization is widely acknowledged, but the frequency of and contributors to such interspecific mating remain largely unstudied. Pinus quadrifolia has three to four needles per fascicle, suggesting that it is a result of hybridization between the five-needled P. juarezensis and the single-needled P. monophylla. In this study we address the taxonomic validity of P. juarezensis, the hybrid origin of P. quadrifolia and the presence of hybridization and intermediate morphology as a result of interspecific hybridization in this complex.
METHODS
We address these questions by combining a genomic and morphological approach. We generated 1868 single nucleotide polymorphisms (SNPs) to detect genetic clusters using principal co-ordinates analyis, discriminant analysis of principal components, fastSTRUCTURE and ADMIXTURE analyses, and performed a morphological analysis of the leaves.
KEY RESULTS
We found that the five-needled pinyons did not differ genetically from the four-needled P. quadrifolia, reducing the status of P. juarezensis to P. quadrifolia. We also found no evidence that P. quadrifolia is of hybrid origin from P. juarezensis × P. monophylla but is instead a genetically distinct species with natural needle number variation that has yet to be explained. Hybridization does occur in this complex, but mostly between P. quadrifolia and P. californiarum, and less commonly between P. quadrifolia and P. monophylla. Interestingly, some hybrid derivatives were detected between both single-needled taxa, P. monophylla and P. californiarum, a hybrid combination that has not yet been proposed. Hybrids have intermediate morphology when they have similar genetic contributions from both parental species; however, when one parent contributes more, hybrid derivatives resemble the parent with higher genetic contribution, resulting in cryptic introgression.
CONCLUSIONS
Our detailed sampling across the distribution of this complex allows us to describe the patterns of hybridization among these taxa, resolves an ancient taxonomic conflict and provides insights into the challenges of exclusively using morphological traits when identifying these taxa with cryptic hybridization and variable morphology.
Identifiants
pubmed: 32222765
pii: 5813433
doi: 10.1093/aob/mcaa045
pmc: PMC7424738
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Research Support, U.S. Gov't, Non-P.H.S.
Langues
eng
Sous-ensembles de citation
IM
Pagination
401-411Informations de copyright
© The Author(s) 2020. Published by Oxford University Press on behalf of the Annals of Botany Company.
Références
R Soc Open Sci. 2017 Jul 19;4(7):161061
pubmed: 28791133
PeerJ. 2016 Oct 27;4:e2593
pubmed: 27812407
J Biogeogr. 2008 Feb;35(2):257-269
pubmed: 21188300
BMC Evol Biol. 2012 Jan 20;12:8
pubmed: 22264329
Heredity (Edinb). 2012 Mar;108(3):179-89
pubmed: 21897439
Mol Phylogenet Evol. 2010 Apr;55(1):168-177
pubmed: 19945537
Heredity (Edinb). 2018 Aug;121(2):126-141
pubmed: 29632325
BMC Genet. 2010 Oct 15;11:94
pubmed: 20950446
Genetics. 2014 Jun;197(2):573-89
pubmed: 24700103
Am J Bot. 2010 May;97(5):846-55
pubmed: 21622450
Mol Phylogenet Evol. 2001 Dec;21(3):449-67
pubmed: 11741386
Mol Biol Evol. 2017 Jun 1;34(6):1363-1377
pubmed: 28333233
Nucleic Acids Res. 2001 Feb 15;29(4):E25
pubmed: 11160945
Mol Ecol. 2018 Dec;27(23):4820-4838
pubmed: 30071141
Genetics. 2002 Mar;160(3):1217-29
pubmed: 11901135
Mol Phylogenet Evol. 2009 Aug;52(2):498-511
pubmed: 19249377
Annu Rev Plant Biol. 2009;60:561-88
pubmed: 19575590
Evol Appl. 2019 Apr 29;13(1):195-209
pubmed: 31892952
Mol Ecol. 2003 Nov;12(11):3013-25
pubmed: 14629382
Mol Phylogenet Evol. 2013 Dec;69(3):940-9
pubmed: 23831459
AoB Plants. 2017 Nov 25;10(1):plx061
pubmed: 29308124
PLoS One. 2013 May 28;8(5):e64062
pubmed: 23724020
Evolution. 2014 Nov;68(11):3120-33
pubmed: 25065387
Mol Ecol Resour. 2017 Jan;17(1):27-32
pubmed: 26850166
Oecologia. 1995 Jan;101(1):29-36
pubmed: 28306972
Bioinformatics. 2008 Jun 1;24(11):1403-5
pubmed: 18397895
Proc Natl Acad Sci U S A. 2004 Jun 29;101(26):9915-20
pubmed: 15192146
Mol Ecol. 2018 Mar;27(5):1245-1260
pubmed: 29411444
Ann Bot. 2008 Feb;101(3):403-19
pubmed: 18089582
Genetics. 2000 Jun;155(2):945-59
pubmed: 10835412
Genome Res. 2009 Sep;19(9):1655-64
pubmed: 19648217
J Evol Biol. 2013 Feb;26(2):229-46
pubmed: 23323997
Mol Ecol Resour. 2018 May;18(3):691-699
pubmed: 29266847
Science. 2007 Aug 17;317(5840):910-4
pubmed: 17702935
Mol Phylogenet Evol. 2017 Mar;108:70-87
pubmed: 28185948