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Flower morphology as a predictor of pollination mode in a biotic to abiotic pollination continuum

Abstract Background and Aims Wind pollination has evolved repeatedly in flowering plants, yet the identification of a wind pollination syndrome as a set of integrated floral traits can be elusive. Thalictrum (Ranunculaceae) comprises temperate perennial herbs that have transitioned repeatedly from i...

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Published in:Annals of botany 2023-10, Vol.132 (1), p.61-76
Main Authors: Martínez-Gómez, Jesús, Park, Seongjun, Hartogs, Samantha R, Soza, Valerie L, Park, Seon Joo, Di Stilio, Verónica S
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container_title Annals of botany
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creator Martínez-Gómez, Jesús
Park, Seongjun
Hartogs, Samantha R
Soza, Valerie L
Park, Seon Joo
Di Stilio, Verónica S
description Abstract Background and Aims Wind pollination has evolved repeatedly in flowering plants, yet the identification of a wind pollination syndrome as a set of integrated floral traits can be elusive. Thalictrum (Ranunculaceae) comprises temperate perennial herbs that have transitioned repeatedly from insect to wind pollination while also exhibiting mixed pollination, providing an ideal system to test for evolutionary correlation between floral morphology and pollination mode in a biotic to abiotic continuum. Moreover, the lack of floral organ fusion across this genus allows testing for specialization to pollination vectors in the absence of this feature. Methods We expanded phylogenetic sampling in the genus from a previous study using six chloroplast loci, which allowed us to test whether species cluster into distinct pollination syndromes based on floral morphology. We then used multivariate analyses on floral traits followed by ancestral state reconstruction of the emerging flower morphotypes and determined whether these traits are evolutionarily correlated under a Bayesian framework with Brownian motion. Key Results Floral traits fell into five distinct clusters, which were reduced to three after considering phylogenetic relatedness and were largely consistent with flower morphotypes and associated pollination vectors. Multivariate evolutionary analyses found a positive correlation between the lengths of floral reproductive structures (styles, stigmas, filaments and anthers). Shorter reproductive structures tracked insect-pollinated species and clades in the phylogeny, whereas longer structures tracked wind-pollinated ones, consistent with selective pressures exerted by biotic vs. abiotic pollination vectors, respectively. Conclusions Although detectable suites of integrated floral traits across Thalictrum were correlated with wind or insect pollination at the extremes of the morphospace distribution, a presumed intermediate, mixed pollination mode morphospace was also detected. Thus, our data broadly support the existence of detectable flower morphotypes from convergent evolution underlying the evolution of pollination mode in Thalictrum, presumably via different paths from an ancestral mixed pollination state.
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Thalictrum (Ranunculaceae) comprises temperate perennial herbs that have transitioned repeatedly from insect to wind pollination while also exhibiting mixed pollination, providing an ideal system to test for evolutionary correlation between floral morphology and pollination mode in a biotic to abiotic continuum. Moreover, the lack of floral organ fusion across this genus allows testing for specialization to pollination vectors in the absence of this feature. Methods We expanded phylogenetic sampling in the genus from a previous study using six chloroplast loci, which allowed us to test whether species cluster into distinct pollination syndromes based on floral morphology. We then used multivariate analyses on floral traits followed by ancestral state reconstruction of the emerging flower morphotypes and determined whether these traits are evolutionarily correlated under a Bayesian framework with Brownian motion. Key Results Floral traits fell into five distinct clusters, which were reduced to three after considering phylogenetic relatedness and were largely consistent with flower morphotypes and associated pollination vectors. Multivariate evolutionary analyses found a positive correlation between the lengths of floral reproductive structures (styles, stigmas, filaments and anthers). Shorter reproductive structures tracked insect-pollinated species and clades in the phylogeny, whereas longer structures tracked wind-pollinated ones, consistent with selective pressures exerted by biotic vs. abiotic pollination vectors, respectively. Conclusions Although detectable suites of integrated floral traits across Thalictrum were correlated with wind or insect pollination at the extremes of the morphospace distribution, a presumed intermediate, mixed pollination mode morphospace was also detected. Thus, our data broadly support the existence of detectable flower morphotypes from convergent evolution underlying the evolution of pollination mode in Thalictrum, presumably via different paths from an ancestral mixed pollination state.</description><identifier>ISSN: 0305-7364</identifier><identifier>EISSN: 1095-8290</identifier><identifier>DOI: 10.1093/aob/mcad069</identifier><identifier>PMID: 37235981</identifier><language>eng</language><publisher>US: Oxford University Press</publisher><subject>Animals ; Bayes Theorem ; Flowers - anatomy &amp; histology ; Insecta ; Original : Part of a Focus Issue on Plant Reproductive Biology ; Phylogeny ; Pollination ; Reproduction ; Thalictrum</subject><ispartof>Annals of botany, 2023-10, Vol.132 (1), p.61-76</ispartof><rights>The Author(s) 2023. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com. 2023</rights><rights>The Author(s) 2023. Published by Oxford University Press on behalf of the Annals of Botany Company. All rights reserved. For permissions, please e-mail: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c376t-6085c819fa7c65a2e973aa799841252e30051d3b6c4988e165b83aa5ff0665973</citedby><cites>FETCH-LOGICAL-c376t-6085c819fa7c65a2e973aa799841252e30051d3b6c4988e165b83aa5ff0665973</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10550269/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC10550269/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/37235981$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Martínez-Gómez, Jesús</creatorcontrib><creatorcontrib>Park, Seongjun</creatorcontrib><creatorcontrib>Hartogs, Samantha R</creatorcontrib><creatorcontrib>Soza, Valerie L</creatorcontrib><creatorcontrib>Park, Seon Joo</creatorcontrib><creatorcontrib>Di Stilio, Verónica S</creatorcontrib><title>Flower morphology as a predictor of pollination mode in a biotic to abiotic pollination continuum</title><title>Annals of botany</title><addtitle>Ann Bot</addtitle><description>Abstract Background and Aims Wind pollination has evolved repeatedly in flowering plants, yet the identification of a wind pollination syndrome as a set of integrated floral traits can be elusive. Thalictrum (Ranunculaceae) comprises temperate perennial herbs that have transitioned repeatedly from insect to wind pollination while also exhibiting mixed pollination, providing an ideal system to test for evolutionary correlation between floral morphology and pollination mode in a biotic to abiotic continuum. Moreover, the lack of floral organ fusion across this genus allows testing for specialization to pollination vectors in the absence of this feature. Methods We expanded phylogenetic sampling in the genus from a previous study using six chloroplast loci, which allowed us to test whether species cluster into distinct pollination syndromes based on floral morphology. We then used multivariate analyses on floral traits followed by ancestral state reconstruction of the emerging flower morphotypes and determined whether these traits are evolutionarily correlated under a Bayesian framework with Brownian motion. Key Results Floral traits fell into five distinct clusters, which were reduced to three after considering phylogenetic relatedness and were largely consistent with flower morphotypes and associated pollination vectors. Multivariate evolutionary analyses found a positive correlation between the lengths of floral reproductive structures (styles, stigmas, filaments and anthers). Shorter reproductive structures tracked insect-pollinated species and clades in the phylogeny, whereas longer structures tracked wind-pollinated ones, consistent with selective pressures exerted by biotic vs. abiotic pollination vectors, respectively. Conclusions Although detectable suites of integrated floral traits across Thalictrum were correlated with wind or insect pollination at the extremes of the morphospace distribution, a presumed intermediate, mixed pollination mode morphospace was also detected. Thus, our data broadly support the existence of detectable flower morphotypes from convergent evolution underlying the evolution of pollination mode in Thalictrum, presumably via different paths from an ancestral mixed pollination state.</description><subject>Animals</subject><subject>Bayes Theorem</subject><subject>Flowers - anatomy &amp; histology</subject><subject>Insecta</subject><subject>Original : Part of a Focus Issue on Plant Reproductive Biology</subject><subject>Phylogeny</subject><subject>Pollination</subject><subject>Reproduction</subject><subject>Thalictrum</subject><issn>0305-7364</issn><issn>1095-8290</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><recordid>eNp90UFLBCEYBmCJoratU_fwFEFM6bg6eoqItoKFLnUWx3HKmJlv0pli_30uu8V26aTow6t8L0InlFxSotiVgfKqtaYiQu2gSTrimcwV2UUTwgjPCiZmB-gwxndCSC4U3UcHrMgZV5JOkJk38OUCbiH0b9DA6xKbiA3ug6u8HSBgqHEPTeM7M3joEqwc9l0ipYfBWzwANpvttrPQDb4bx_YI7dWmie54s07Ry_zu-fYhWzzdP97eLDLLCjFkgkhuJVW1KazgJneqYMYUSskZzXnuGCGcVqwUdqakdFTwUibA65oIwROeout1bj-Wraus64ZgGt0H35qw1GC8_nvT-Tf9Cp-aEs5Xg0kJ55uEAB-ji4NufbSuaUznYIw6l3maYMH46rGLNbUBYgyu_n2HEr1qRadW9KaVpE-3v_Zrf2pI4GwNYOz_TfoGoviXuw</recordid><startdate>20231004</startdate><enddate>20231004</enddate><creator>Martínez-Gómez, Jesús</creator><creator>Park, Seongjun</creator><creator>Hartogs, Samantha R</creator><creator>Soza, Valerie L</creator><creator>Park, Seon Joo</creator><creator>Di Stilio, Verónica S</creator><general>Oxford University Press</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20231004</creationdate><title>Flower morphology as a predictor of pollination mode in a biotic to abiotic pollination continuum</title><author>Martínez-Gómez, Jesús ; Park, Seongjun ; Hartogs, Samantha R ; Soza, Valerie L ; Park, Seon Joo ; Di Stilio, Verónica S</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c376t-6085c819fa7c65a2e973aa799841252e30051d3b6c4988e165b83aa5ff0665973</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Animals</topic><topic>Bayes Theorem</topic><topic>Flowers - anatomy &amp; histology</topic><topic>Insecta</topic><topic>Original : Part of a Focus Issue on Plant Reproductive Biology</topic><topic>Phylogeny</topic><topic>Pollination</topic><topic>Reproduction</topic><topic>Thalictrum</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Martínez-Gómez, Jesús</creatorcontrib><creatorcontrib>Park, Seongjun</creatorcontrib><creatorcontrib>Hartogs, Samantha R</creatorcontrib><creatorcontrib>Soza, Valerie L</creatorcontrib><creatorcontrib>Park, Seon Joo</creatorcontrib><creatorcontrib>Di Stilio, Verónica S</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Annals of botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Martínez-Gómez, Jesús</au><au>Park, Seongjun</au><au>Hartogs, Samantha R</au><au>Soza, Valerie L</au><au>Park, Seon Joo</au><au>Di Stilio, Verónica S</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Flower morphology as a predictor of pollination mode in a biotic to abiotic pollination continuum</atitle><jtitle>Annals of botany</jtitle><addtitle>Ann Bot</addtitle><date>2023-10-04</date><risdate>2023</risdate><volume>132</volume><issue>1</issue><spage>61</spage><epage>76</epage><pages>61-76</pages><issn>0305-7364</issn><eissn>1095-8290</eissn><abstract>Abstract Background and Aims Wind pollination has evolved repeatedly in flowering plants, yet the identification of a wind pollination syndrome as a set of integrated floral traits can be elusive. 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Key Results Floral traits fell into five distinct clusters, which were reduced to three after considering phylogenetic relatedness and were largely consistent with flower morphotypes and associated pollination vectors. Multivariate evolutionary analyses found a positive correlation between the lengths of floral reproductive structures (styles, stigmas, filaments and anthers). Shorter reproductive structures tracked insect-pollinated species and clades in the phylogeny, whereas longer structures tracked wind-pollinated ones, consistent with selective pressures exerted by biotic vs. abiotic pollination vectors, respectively. Conclusions Although detectable suites of integrated floral traits across Thalictrum were correlated with wind or insect pollination at the extremes of the morphospace distribution, a presumed intermediate, mixed pollination mode morphospace was also detected. 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subjects Animals
Bayes Theorem
Flowers - anatomy & histology
Insecta
Original : Part of a Focus Issue on Plant Reproductive Biology
Phylogeny
Pollination
Reproduction
Thalictrum
title Flower morphology as a predictor of pollination mode in a biotic to abiotic pollination continuum
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