Rear‐edge daylily populations show legacies of habitat fragmentation due to the Holocene climate warming

Aims Quaternary climate changes dramatically affected species' distributions and thus impacted genetic diversity patterns, particularly for rear‐edge populations. Empirical studies have shown the southernmost (rear‐edge), fragmented populations of Japanese woody plants can harbour high genetic...

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Veröffentlicht in:Journal of biogeography 2023-03, Vol.50 (3), p.551-563
Hauptverfasser: Masuda, Kazutoshi, Setoguchi, Hiroaki, Nagasawa, Koki, Ishihara, Masae Iwamoto, Sawa, Kazuhiro, Horie, Kenji, Tsuboi, Hayato, Fukumoto, Shigeru, Tango, Tsuguoki, Sakaguchi, Shota
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container_end_page 563
container_issue 3
container_start_page 551
container_title Journal of biogeography
container_volume 50
creator Masuda, Kazutoshi
Setoguchi, Hiroaki
Nagasawa, Koki
Ishihara, Masae Iwamoto
Sawa, Kazuhiro
Horie, Kenji
Tsuboi, Hayato
Fukumoto, Shigeru
Tango, Tsuguoki
Sakaguchi, Shota
description Aims Quaternary climate changes dramatically affected species' distributions and thus impacted genetic diversity patterns, particularly for rear‐edge populations. Empirical studies have shown the southernmost (rear‐edge), fragmented populations of Japanese woody plants can harbour high genetic diversity owing to their origin in southern glacial refugia. The effect of Holocene climate warming on rear‐edge populations has, however, rarely been demonstrated. We assessed whether the genetic structure of populations of temperate plants in Japan can be interpreted to show legacies of both icy (Last Glacial Maximum, LGM) and warm (Holocene) climates. Location Japanese Archipelago. Taxon Hemerocallis middendorffii (Asphodelaceae). Methods Population genetic profiles of 737 individuals from 41 populations were analysed to examine population structure and past population demography, using 12 EST‐SSR markers. Present and past suitable habitat areas during the LGM and the Holocene climatic optimum were estimated by ecological niche modelling (ENM). Reconstructed palaeodistribution was combined with population genetics to statistically predict population demographics in relation to past climate changes. Results Genetic analysis of the 41 populations revealed 6 regional population groups. Four groups widely dominating the northern–central ranges harboured high genetic diversity, whereas genetic divergence within the groups was low. In contrast, the two groups at the southwestern edge were geographically and genetically isolated, and they showed the lowest genetic diversity. The estimated palaeodistributions showed a decrease in the suitable range during the Holocene in comparison with that at the LGM, and only habitat suitability in the Holocene was able to predict the genetic diversity across the range. Main conclusions Populations at the centre of the current distribution harbour high genetic diversity because they remained stable during both cold and warm periods. However, habitat fragmentation and population decline in relation to climate warming during the Holocene resulted in genetic isolation and impoverishment of the rear‐edge populations.
doi_str_mv 10.1111/jbi.14552
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Empirical studies have shown the southernmost (rear‐edge), fragmented populations of Japanese woody plants can harbour high genetic diversity owing to their origin in southern glacial refugia. The effect of Holocene climate warming on rear‐edge populations has, however, rarely been demonstrated. We assessed whether the genetic structure of populations of temperate plants in Japan can be interpreted to show legacies of both icy (Last Glacial Maximum, LGM) and warm (Holocene) climates. Location Japanese Archipelago. Taxon Hemerocallis middendorffii (Asphodelaceae). Methods Population genetic profiles of 737 individuals from 41 populations were analysed to examine population structure and past population demography, using 12 EST‐SSR markers. Present and past suitable habitat areas during the LGM and the Holocene climatic optimum were estimated by ecological niche modelling (ENM). Reconstructed palaeodistribution was combined with population genetics to statistically predict population demographics in relation to past climate changes. Results Genetic analysis of the 41 populations revealed 6 regional population groups. Four groups widely dominating the northern–central ranges harboured high genetic diversity, whereas genetic divergence within the groups was low. In contrast, the two groups at the southwestern edge were geographically and genetically isolated, and they showed the lowest genetic diversity. The estimated palaeodistributions showed a decrease in the suitable range during the Holocene in comparison with that at the LGM, and only habitat suitability in the Holocene was able to predict the genetic diversity across the range. Main conclusions Populations at the centre of the current distribution harbour high genetic diversity because they remained stable during both cold and warm periods. However, habitat fragmentation and population decline in relation to climate warming during the Holocene resulted in genetic isolation and impoverishment of the rear‐edge populations.</description><identifier>ISSN: 0305-0270</identifier><identifier>EISSN: 1365-2699</identifier><identifier>DOI: 10.1111/jbi.14552</identifier><language>eng</language><publisher>Oxford: Wiley Subscription Services, Inc</publisher><subject>Archipelagoes ; Asphodelaceae ; Climate ; Climate change ; Current distribution ; Demographics ; Demography ; Divergence ; Ecological niches ; Empirical analysis ; EST‐SSR ; Fragmentation ; Genetic analysis ; Genetic divergence ; Genetic diversity ; Genetic isolation ; Genetic structure ; Genetics ; Global warming ; Habitat fragmentation ; Habitats ; Holocene ; Phylogeography ; Population ; Population (statistical) ; Population decline ; Population genetics ; Population structure ; Population studies ; Quaternary ; Refugia ; Woody plants</subject><ispartof>Journal of biogeography, 2023-03, Vol.50 (3), p.551-563</ispartof><rights>2022 John Wiley &amp; Sons Ltd.</rights><rights>Copyright © 2023 John Wiley &amp; Sons Ltd</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3632-41cae0d0fd9863ff5f18a1ebff57bdbe92bb8d84f7e1307039bdb15258740943</citedby><cites>FETCH-LOGICAL-c3632-41cae0d0fd9863ff5f18a1ebff57bdbe92bb8d84f7e1307039bdb15258740943</cites><orcidid>0000-0002-4304-0219 ; 0000-0002-8365-7766 ; 0000-0002-6180-1747 ; 0000-0003-0808-7502 ; 0000-0001-9966-9967</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%2Fjbi.14552$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fjbi.14552$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,27901,27902,45550,45551</link.rule.ids></links><search><creatorcontrib>Masuda, Kazutoshi</creatorcontrib><creatorcontrib>Setoguchi, Hiroaki</creatorcontrib><creatorcontrib>Nagasawa, Koki</creatorcontrib><creatorcontrib>Ishihara, Masae Iwamoto</creatorcontrib><creatorcontrib>Sawa, Kazuhiro</creatorcontrib><creatorcontrib>Horie, Kenji</creatorcontrib><creatorcontrib>Tsuboi, Hayato</creatorcontrib><creatorcontrib>Fukumoto, Shigeru</creatorcontrib><creatorcontrib>Tango, Tsuguoki</creatorcontrib><creatorcontrib>Sakaguchi, Shota</creatorcontrib><title>Rear‐edge daylily populations show legacies of habitat fragmentation due to the Holocene climate warming</title><title>Journal of biogeography</title><description>Aims Quaternary climate changes dramatically affected species' distributions and thus impacted genetic diversity patterns, particularly for rear‐edge populations. Empirical studies have shown the southernmost (rear‐edge), fragmented populations of Japanese woody plants can harbour high genetic diversity owing to their origin in southern glacial refugia. The effect of Holocene climate warming on rear‐edge populations has, however, rarely been demonstrated. We assessed whether the genetic structure of populations of temperate plants in Japan can be interpreted to show legacies of both icy (Last Glacial Maximum, LGM) and warm (Holocene) climates. Location Japanese Archipelago. Taxon Hemerocallis middendorffii (Asphodelaceae). Methods Population genetic profiles of 737 individuals from 41 populations were analysed to examine population structure and past population demography, using 12 EST‐SSR markers. Present and past suitable habitat areas during the LGM and the Holocene climatic optimum were estimated by ecological niche modelling (ENM). Reconstructed palaeodistribution was combined with population genetics to statistically predict population demographics in relation to past climate changes. Results Genetic analysis of the 41 populations revealed 6 regional population groups. Four groups widely dominating the northern–central ranges harboured high genetic diversity, whereas genetic divergence within the groups was low. In contrast, the two groups at the southwestern edge were geographically and genetically isolated, and they showed the lowest genetic diversity. The estimated palaeodistributions showed a decrease in the suitable range during the Holocene in comparison with that at the LGM, and only habitat suitability in the Holocene was able to predict the genetic diversity across the range. Main conclusions Populations at the centre of the current distribution harbour high genetic diversity because they remained stable during both cold and warm periods. 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Setoguchi, Hiroaki ; Nagasawa, Koki ; Ishihara, Masae Iwamoto ; Sawa, Kazuhiro ; Horie, Kenji ; Tsuboi, Hayato ; Fukumoto, Shigeru ; Tango, Tsuguoki ; Sakaguchi, Shota</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3632-41cae0d0fd9863ff5f18a1ebff57bdbe92bb8d84f7e1307039bdb15258740943</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Archipelagoes</topic><topic>Asphodelaceae</topic><topic>Climate</topic><topic>Climate change</topic><topic>Current distribution</topic><topic>Demographics</topic><topic>Demography</topic><topic>Divergence</topic><topic>Ecological niches</topic><topic>Empirical analysis</topic><topic>EST‐SSR</topic><topic>Fragmentation</topic><topic>Genetic analysis</topic><topic>Genetic divergence</topic><topic>Genetic diversity</topic><topic>Genetic isolation</topic><topic>Genetic structure</topic><topic>Genetics</topic><topic>Global warming</topic><topic>Habitat fragmentation</topic><topic>Habitats</topic><topic>Holocene</topic><topic>Phylogeography</topic><topic>Population</topic><topic>Population (statistical)</topic><topic>Population decline</topic><topic>Population genetics</topic><topic>Population structure</topic><topic>Population studies</topic><topic>Quaternary</topic><topic>Refugia</topic><topic>Woody plants</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Masuda, Kazutoshi</creatorcontrib><creatorcontrib>Setoguchi, Hiroaki</creatorcontrib><creatorcontrib>Nagasawa, Koki</creatorcontrib><creatorcontrib>Ishihara, Masae Iwamoto</creatorcontrib><creatorcontrib>Sawa, Kazuhiro</creatorcontrib><creatorcontrib>Horie, Kenji</creatorcontrib><creatorcontrib>Tsuboi, Hayato</creatorcontrib><creatorcontrib>Fukumoto, Shigeru</creatorcontrib><creatorcontrib>Tango, Tsuguoki</creatorcontrib><creatorcontrib>Sakaguchi, Shota</creatorcontrib><collection>CrossRef</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Journal of biogeography</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Masuda, Kazutoshi</au><au>Setoguchi, Hiroaki</au><au>Nagasawa, Koki</au><au>Ishihara, Masae Iwamoto</au><au>Sawa, Kazuhiro</au><au>Horie, Kenji</au><au>Tsuboi, Hayato</au><au>Fukumoto, Shigeru</au><au>Tango, Tsuguoki</au><au>Sakaguchi, Shota</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Rear‐edge daylily populations show legacies of habitat fragmentation due to the Holocene climate warming</atitle><jtitle>Journal of biogeography</jtitle><date>2023-03</date><risdate>2023</risdate><volume>50</volume><issue>3</issue><spage>551</spage><epage>563</epage><pages>551-563</pages><issn>0305-0270</issn><eissn>1365-2699</eissn><abstract>Aims Quaternary climate changes dramatically affected species' distributions and thus impacted genetic diversity patterns, particularly for rear‐edge populations. Empirical studies have shown the southernmost (rear‐edge), fragmented populations of Japanese woody plants can harbour high genetic diversity owing to their origin in southern glacial refugia. The effect of Holocene climate warming on rear‐edge populations has, however, rarely been demonstrated. We assessed whether the genetic structure of populations of temperate plants in Japan can be interpreted to show legacies of both icy (Last Glacial Maximum, LGM) and warm (Holocene) climates. Location Japanese Archipelago. Taxon Hemerocallis middendorffii (Asphodelaceae). Methods Population genetic profiles of 737 individuals from 41 populations were analysed to examine population structure and past population demography, using 12 EST‐SSR markers. Present and past suitable habitat areas during the LGM and the Holocene climatic optimum were estimated by ecological niche modelling (ENM). Reconstructed palaeodistribution was combined with population genetics to statistically predict population demographics in relation to past climate changes. Results Genetic analysis of the 41 populations revealed 6 regional population groups. Four groups widely dominating the northern–central ranges harboured high genetic diversity, whereas genetic divergence within the groups was low. In contrast, the two groups at the southwestern edge were geographically and genetically isolated, and they showed the lowest genetic diversity. The estimated palaeodistributions showed a decrease in the suitable range during the Holocene in comparison with that at the LGM, and only habitat suitability in the Holocene was able to predict the genetic diversity across the range. Main conclusions Populations at the centre of the current distribution harbour high genetic diversity because they remained stable during both cold and warm periods. However, habitat fragmentation and population decline in relation to climate warming during the Holocene resulted in genetic isolation and impoverishment of the rear‐edge populations.</abstract><cop>Oxford</cop><pub>Wiley Subscription Services, Inc</pub><doi>10.1111/jbi.14552</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-4304-0219</orcidid><orcidid>https://orcid.org/0000-0002-8365-7766</orcidid><orcidid>https://orcid.org/0000-0002-6180-1747</orcidid><orcidid>https://orcid.org/0000-0003-0808-7502</orcidid><orcidid>https://orcid.org/0000-0001-9966-9967</orcidid></addata></record>
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source Wiley Online Library Journals Frontfile Complete
subjects Archipelagoes
Asphodelaceae
Climate
Climate change
Current distribution
Demographics
Demography
Divergence
Ecological niches
Empirical analysis
EST‐SSR
Fragmentation
Genetic analysis
Genetic divergence
Genetic diversity
Genetic isolation
Genetic structure
Genetics
Global warming
Habitat fragmentation
Habitats
Holocene
Phylogeography
Population
Population (statistical)
Population decline
Population genetics
Population structure
Population studies
Quaternary
Refugia
Woody plants
title Rear‐edge daylily populations show legacies of habitat fragmentation due to the Holocene climate warming
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