Evolutionary drivers of reproductive fitness in two endangered forest trees

Summary Population genetics theory predicts a relationship between fitness, genetic diversity (H0) and effective population size (Ne), which is often tested through heterozygosity‐fitness correlations (HFCs). We tested whether population and individual fertility and heterozygosity are correlated in...

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Veröffentlicht in:The New phytologist 2024-11, Vol.244 (3), p.1086-1100
Hauptverfasser: Mendoza‐Maya, Eduardo, Giles‐Pérez, Gustavo Ibrahim, Vargas‐Hernández, J. Jesús, Sáenz‐Romero, Cuauhtémoc, Martínez‐Trujillo, Miguel, Angeles Beltrán‐Nambo, María, Hernández‐Díaz, José Ciro, Prieto‐Ruíz, José Ángel, Jaramillo‐Correa, Juan P., Wehenkel, Christian
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container_end_page 1100
container_issue 3
container_start_page 1086
container_title The New phytologist
container_volume 244
creator Mendoza‐Maya, Eduardo
Giles‐Pérez, Gustavo Ibrahim
Vargas‐Hernández, J. Jesús
Sáenz‐Romero, Cuauhtémoc
Martínez‐Trujillo, Miguel
Angeles Beltrán‐Nambo, María
Hernández‐Díaz, José Ciro
Prieto‐Ruíz, José Ángel
Jaramillo‐Correa, Juan P.
Wehenkel, Christian
description Summary Population genetics theory predicts a relationship between fitness, genetic diversity (H0) and effective population size (Ne), which is often tested through heterozygosity‐fitness correlations (HFCs). We tested whether population and individual fertility and heterozygosity are correlated in two endangered Mexican spruces (Picea martinezii and Picea mexicana) by combining genomic, demographic and reproductive data (seed development and germination traits). For both species, there was a positive correlation between population size and seed development traits, but not germination rate. Individual genome‐wide heterozygosity and seed traits were only correlated in P. martinezii (general‐effects HFC), and none of the candidate single nucleotide polymorphisms (SNPs) associated with individual fertility showed heterozygote advantage in any species (no local‐effects HFC). We observed a single and recent (c. 30 thousand years ago (ka)) population decline for P. martinezii; the collapse of P. mexicana occurred in two phases separated by a long period of stability (c. 800 ka). Recruitment always contributed more to total population census than adult trees in P. mexicana, while this was only the case in the largest populations of P. martinezii. Equating fitness to either H0 or Ne, as traditionally proposed in conservation biology, might not always be adequate, as species‐specific evolutionary factors can decouple the expected correlation between these parameters.
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Jesús ; Sáenz‐Romero, Cuauhtémoc ; Martínez‐Trujillo, Miguel ; Angeles Beltrán‐Nambo, María ; Hernández‐Díaz, José Ciro ; Prieto‐Ruíz, José Ángel ; Jaramillo‐Correa, Juan P. ; Wehenkel, Christian</creator><creatorcontrib>Mendoza‐Maya, Eduardo ; Giles‐Pérez, Gustavo Ibrahim ; Vargas‐Hernández, J. Jesús ; Sáenz‐Romero, Cuauhtémoc ; Martínez‐Trujillo, Miguel ; Angeles Beltrán‐Nambo, María ; Hernández‐Díaz, José Ciro ; Prieto‐Ruíz, José Ángel ; Jaramillo‐Correa, Juan P. ; Wehenkel, Christian</creatorcontrib><description>Summary Population genetics theory predicts a relationship between fitness, genetic diversity (H0) and effective population size (Ne), which is often tested through heterozygosity‐fitness correlations (HFCs). We tested whether population and individual fertility and heterozygosity are correlated in two endangered Mexican spruces (Picea martinezii and Picea mexicana) by combining genomic, demographic and reproductive data (seed development and germination traits). For both species, there was a positive correlation between population size and seed development traits, but not germination rate. Individual genome‐wide heterozygosity and seed traits were only correlated in P. martinezii (general‐effects HFC), and none of the candidate single nucleotide polymorphisms (SNPs) associated with individual fertility showed heterozygote advantage in any species (no local‐effects HFC). We observed a single and recent (c. 30 thousand years ago (ka)) population decline for P. martinezii; the collapse of P. mexicana occurred in two phases separated by a long period of stability (c. 800 ka). Recruitment always contributed more to total population census than adult trees in P. mexicana, while this was only the case in the largest populations of P. martinezii. Equating fitness to either H0 or Ne, as traditionally proposed in conservation biology, might not always be adequate, as species‐specific evolutionary factors can decouple the expected correlation between these parameters.</description><identifier>ISSN: 0028-646X</identifier><identifier>ISSN: 1469-8137</identifier><identifier>EISSN: 1469-8137</identifier><identifier>DOI: 10.1111/nph.20073</identifier><identifier>PMID: 39187985</identifier><language>eng</language><publisher>England: Wiley Subscription Services, Inc</publisher><subject>adults ; Biological Evolution ; Conservation biology ; conservation genomics ; Correlation ; effective population size ; Endangered plants ; Endangered Species ; Evolution ; extinction vortex ; Fertility ; Fitness ; Forests ; Genetic diversity ; Genetic Fitness ; Genetic Variation ; Genetics ; Genomes ; genomics ; Germination ; Germination - genetics ; heterozygosity ; heterozygosity‐fitness correlations (HFCs) ; Heterozygote ; Heterozygote advantage ; Hydrofluorocarbons ; Nucleotides ; Picea ; Picea - genetics ; Picea - growth &amp; development ; Picea - physiology ; Picea martinezii ; Picea mexicana ; Polymorphism, Single Nucleotide - genetics ; Population decline ; Population Density ; population dynamics ; Population genetics ; Population number ; Reproduction - genetics ; Reproductive fitness ; seed development ; Seeds - genetics ; Seeds - growth &amp; development ; Seeds - physiology ; Single-nucleotide polymorphism ; species ; Trees ; Trees - genetics ; Trees - physiology ; Wildlife conservation ; wildlife management</subject><ispartof>The New phytologist, 2024-11, Vol.244 (3), p.1086-1100</ispartof><rights>2024 The Author(s). © 2024 New Phytologist Foundation.</rights><rights>2024 The Author(s). New Phytologist © 2024 New Phytologist Foundation.</rights><rights>2024. This article is published under http://creativecommons.org/licenses/by-nc/4.0/ (the “License”). Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c3113-9f632aee6532cb472c4bd3390cbbc03727f95ca242f75db359d2db35cb43e8433</cites><orcidid>0000-0001-7617-913X ; 0000-0001-7422-4953 ; 0000-0002-6523-6618 ; 0000-0001-8482-6253 ; 0000-0002-2954-535X ; 0000-0002-8945-3959 ; 0000-0003-2240-5933 ; 0000-0002-2341-5458 ; 0000-0003-3739-4835 ; 0000-0002-3284-422X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fnph.20073$$EPDF$$P50$$Gwiley$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fnph.20073$$EHTML$$P50$$Gwiley$$Hfree_for_read</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/39187985$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Mendoza‐Maya, Eduardo</creatorcontrib><creatorcontrib>Giles‐Pérez, Gustavo Ibrahim</creatorcontrib><creatorcontrib>Vargas‐Hernández, J. Jesús</creatorcontrib><creatorcontrib>Sáenz‐Romero, Cuauhtémoc</creatorcontrib><creatorcontrib>Martínez‐Trujillo, Miguel</creatorcontrib><creatorcontrib>Angeles Beltrán‐Nambo, María</creatorcontrib><creatorcontrib>Hernández‐Díaz, José Ciro</creatorcontrib><creatorcontrib>Prieto‐Ruíz, José Ángel</creatorcontrib><creatorcontrib>Jaramillo‐Correa, Juan P.</creatorcontrib><creatorcontrib>Wehenkel, Christian</creatorcontrib><title>Evolutionary drivers of reproductive fitness in two endangered forest trees</title><title>The New phytologist</title><addtitle>New Phytol</addtitle><description>Summary Population genetics theory predicts a relationship between fitness, genetic diversity (H0) and effective population size (Ne), which is often tested through heterozygosity‐fitness correlations (HFCs). We tested whether population and individual fertility and heterozygosity are correlated in two endangered Mexican spruces (Picea martinezii and Picea mexicana) by combining genomic, demographic and reproductive data (seed development and germination traits). For both species, there was a positive correlation between population size and seed development traits, but not germination rate. Individual genome‐wide heterozygosity and seed traits were only correlated in P. martinezii (general‐effects HFC), and none of the candidate single nucleotide polymorphisms (SNPs) associated with individual fertility showed heterozygote advantage in any species (no local‐effects HFC). We observed a single and recent (c. 30 thousand years ago (ka)) population decline for P. martinezii; the collapse of P. mexicana occurred in two phases separated by a long period of stability (c. 800 ka). Recruitment always contributed more to total population census than adult trees in P. mexicana, while this was only the case in the largest populations of P. martinezii. Equating fitness to either H0 or Ne, as traditionally proposed in conservation biology, might not always be adequate, as species‐specific evolutionary factors can decouple the expected correlation between these parameters.</description><subject>adults</subject><subject>Biological Evolution</subject><subject>Conservation biology</subject><subject>conservation genomics</subject><subject>Correlation</subject><subject>effective population size</subject><subject>Endangered plants</subject><subject>Endangered Species</subject><subject>Evolution</subject><subject>extinction vortex</subject><subject>Fertility</subject><subject>Fitness</subject><subject>Forests</subject><subject>Genetic diversity</subject><subject>Genetic Fitness</subject><subject>Genetic Variation</subject><subject>Genetics</subject><subject>Genomes</subject><subject>genomics</subject><subject>Germination</subject><subject>Germination - genetics</subject><subject>heterozygosity</subject><subject>heterozygosity‐fitness correlations (HFCs)</subject><subject>Heterozygote</subject><subject>Heterozygote advantage</subject><subject>Hydrofluorocarbons</subject><subject>Nucleotides</subject><subject>Picea</subject><subject>Picea - genetics</subject><subject>Picea - growth &amp; development</subject><subject>Picea - physiology</subject><subject>Picea martinezii</subject><subject>Picea mexicana</subject><subject>Polymorphism, Single Nucleotide - genetics</subject><subject>Population decline</subject><subject>Population Density</subject><subject>population dynamics</subject><subject>Population genetics</subject><subject>Population number</subject><subject>Reproduction - genetics</subject><subject>Reproductive fitness</subject><subject>seed development</subject><subject>Seeds - genetics</subject><subject>Seeds - growth &amp; development</subject><subject>Seeds - physiology</subject><subject>Single-nucleotide polymorphism</subject><subject>species</subject><subject>Trees</subject><subject>Trees - genetics</subject><subject>Trees - physiology</subject><subject>Wildlife conservation</subject><subject>wildlife management</subject><issn>0028-646X</issn><issn>1469-8137</issn><issn>1469-8137</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>24P</sourceid><sourceid>EIF</sourceid><recordid>eNqFkcFKxDAURYMozji68Ack4EYX1SQvbZqliDqiqAsFd6VNX7TSacakVfx7M87oQhCzeRAOJ3n3ErLL2RGP57ibPx8JxhSskTGXmU5yDmqdjBkTeZLJ7HFEtkJ4YYzpNBObZASa50rn6Zhcnb25dugb15X-g9a-eUMfqLPU49y7ejB9vKG26TsMgTYd7d8dxa4uuyf0WFPrPIae9h4xbJMNW7YBd1ZzQh7Oz-5Pp8n17cXl6cl1YoBzSLTNQJSIWQrCVFIJI6saQDNTVYaBEsrq1JRCCqvSuoJU12IxIguYS4AJOVh64w9fh_h8MWuCwbYtO3RDKICnkGeM8ex_lGklNUgpIrr_C31xg-_iIlHIBSyCVZE6XFLGuxA82mLum1nMruCsWJRRxDKKrzIiu7cyDtUM6x_yO_0IHC-B96bFj79Nxc3ddKn8BDb9kr8</recordid><startdate>202411</startdate><enddate>202411</enddate><creator>Mendoza‐Maya, Eduardo</creator><creator>Giles‐Pérez, Gustavo Ibrahim</creator><creator>Vargas‐Hernández, J. 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Recruitment always contributed more to total population census than adult trees in P. mexicana, while this was only the case in the largest populations of P. martinezii. 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subjects adults
Biological Evolution
Conservation biology
conservation genomics
Correlation
effective population size
Endangered plants
Endangered Species
Evolution
extinction vortex
Fertility
Fitness
Forests
Genetic diversity
Genetic Fitness
Genetic Variation
Genetics
Genomes
genomics
Germination
Germination - genetics
heterozygosity
heterozygosity‐fitness correlations (HFCs)
Heterozygote
Heterozygote advantage
Hydrofluorocarbons
Nucleotides
Picea
Picea - genetics
Picea - growth & development
Picea - physiology
Picea martinezii
Picea mexicana
Polymorphism, Single Nucleotide - genetics
Population decline
Population Density
population dynamics
Population genetics
Population number
Reproduction - genetics
Reproductive fitness
seed development
Seeds - genetics
Seeds - growth & development
Seeds - physiology
Single-nucleotide polymorphism
species
Trees
Trees - genetics
Trees - physiology
Wildlife conservation
wildlife management
title Evolutionary drivers of reproductive fitness in two endangered forest trees
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