Pollen dispersal and mating patterns determine resilience for a large-yet-fragmented population of Cariniana estrellensis
Forest fragmentation studies are now urgent due to increased rates of deforestation and forest fires worldwide. In South America, the bee-pollinated Cariniana estrellensis is one of the largest trees, and a paradigm for the health and sustainability of forest biomes. For a large-yet-fragmented popul...
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description | Forest fragmentation studies are now urgent due to increased rates of deforestation and forest fires worldwide. In South America, the bee-pollinated
Cariniana estrellensis
is one of the largest trees, and a paradigm for the health and sustainability of forest biomes. For a large-yet-fragmented population (four subpopulations) in the transition zone between Brazilian Savannah and Atlantic Forest, we carried out a study of pollen flow, mating system and spatial genetic structure using nine microsatellite loci. This revealed that the subpopulations are not reproductively isolated because of pollen flow from outside the study area (18.3%) and between subpopulations (16.1–31.3%). Pollen dispersal reached long distances (3.5 km), but mating occurred predominantly between larger-diameter trees located close to mother-trees. We found that
C. estrellensis
is self-compatible with reproduction mediated mainly by outcrossing (> 0.95), but matings were not random due to biparental inbreeding (tr: 0.048–0.124) and correlated-paternity (rp: 0.16–0.28), which was higher within (rpw: 0.524–0.95) than among fruits (rpa: 0.048–0.052). Inbreeding decreased from seedlings (0.088) to adults, indicating inbreeding depression between the seedling and adult stages. Subpopulations exhibited spatial genetic structure (50–200 m), revealing a pattern of genetic dispersion of isolation-by-distance. Seeds should be harvested from trees that are > 200 m apart for successful ex-situ conservation and populations should not be isolated by more than the maximum pollen-dispersion distance observed (3.5 km) for in-situ conservation. The findings are consistent with the maximum distance that bees can disperse pollen and thereby maintain genetic connectivity between populations and resilience to population fragmentation into forest remnants. |
doi_str_mv | 10.1007/s10592-023-01557-8 |
format | Article |
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Cariniana estrellensis
is one of the largest trees, and a paradigm for the health and sustainability of forest biomes. For a large-yet-fragmented population (four subpopulations) in the transition zone between Brazilian Savannah and Atlantic Forest, we carried out a study of pollen flow, mating system and spatial genetic structure using nine microsatellite loci. This revealed that the subpopulations are not reproductively isolated because of pollen flow from outside the study area (18.3%) and between subpopulations (16.1–31.3%). Pollen dispersal reached long distances (3.5 km), but mating occurred predominantly between larger-diameter trees located close to mother-trees. We found that
C. estrellensis
is self-compatible with reproduction mediated mainly by outcrossing (> 0.95), but matings were not random due to biparental inbreeding (tr: 0.048–0.124) and correlated-paternity (rp: 0.16–0.28), which was higher within (rpw: 0.524–0.95) than among fruits (rpa: 0.048–0.052). Inbreeding decreased from seedlings (0.088) to adults, indicating inbreeding depression between the seedling and adult stages. Subpopulations exhibited spatial genetic structure (50–200 m), revealing a pattern of genetic dispersion of isolation-by-distance. Seeds should be harvested from trees that are > 200 m apart for successful ex-situ conservation and populations should not be isolated by more than the maximum pollen-dispersion distance observed (3.5 km) for in-situ conservation. The findings are consistent with the maximum distance that bees can disperse pollen and thereby maintain genetic connectivity between populations and resilience to population fragmentation into forest remnants.</description><identifier>ISSN: 1566-0621</identifier><identifier>EISSN: 1572-9737</identifier><identifier>DOI: 10.1007/s10592-023-01557-8</identifier><language>eng</language><publisher>Dordrecht: Springer Netherlands</publisher><subject>Animal Genetics and Genomics ; Animal reproduction ; Bees ; Biodiversity ; Biomedical and Life Sciences ; Conservation ; Conservation Biology/Ecology ; Deforestation ; Dispersion ; Ecology ; Evolutionary Biology ; Forest fires ; Forests ; Fragmentation ; Genetic diversity ; Genetic structure ; Habitat fragmentation ; Inbreeding ; Inbreeding depression ; Life Sciences ; Mating ; Microsatellites ; Paternity ; Plant Genetics and Genomics ; Plant reproduction ; Pollen ; Population ; Population genetics ; Populations ; Reproductive isolation ; Research Article ; Resilience ; Seedlings ; Seeds ; Subpopulations ; Transition zone ; Trees</subject><ispartof>Conservation genetics, 2024-02, Vol.25 (1), p.117-132</ispartof><rights>The Author(s), under exclusive licence to Springer Nature B.V. 2023. Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c319t-a41173e98a1b6fa5559867564b0397a77f84929e2adffc11e815df6e9b934dc63</citedby><cites>FETCH-LOGICAL-c319t-a41173e98a1b6fa5559867564b0397a77f84929e2adffc11e815df6e9b934dc63</cites><orcidid>0000-0001-6797-9362 ; 0000-0001-6939-8430 ; 0000-0002-1076-9812 ; 0000-0003-1458-2454 ; 0000-0001-5928-4181 ; 0000-0003-0839-633X ; 0000-0003-2352-0941</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s10592-023-01557-8$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s10592-023-01557-8$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>315,782,786,27931,27932,41495,42564,51326</link.rule.ids></links><search><creatorcontrib>Kubota, Thaisa Y. K.</creatorcontrib><creatorcontrib>Hallsworth, John E.</creatorcontrib><creatorcontrib>da Silva, Alexandre M.</creatorcontrib><creatorcontrib>Moraes, Mario L. T.</creatorcontrib><creatorcontrib>Cambuim, Jose</creatorcontrib><creatorcontrib>Corseuil, Cláudia W.</creatorcontrib><creatorcontrib>Sebbenn, Alexandre M.</creatorcontrib><title>Pollen dispersal and mating patterns determine resilience for a large-yet-fragmented population of Cariniana estrellensis</title><title>Conservation genetics</title><addtitle>Conserv Genet</addtitle><description>Forest fragmentation studies are now urgent due to increased rates of deforestation and forest fires worldwide. In South America, the bee-pollinated
Cariniana estrellensis
is one of the largest trees, and a paradigm for the health and sustainability of forest biomes. For a large-yet-fragmented population (four subpopulations) in the transition zone between Brazilian Savannah and Atlantic Forest, we carried out a study of pollen flow, mating system and spatial genetic structure using nine microsatellite loci. This revealed that the subpopulations are not reproductively isolated because of pollen flow from outside the study area (18.3%) and between subpopulations (16.1–31.3%). Pollen dispersal reached long distances (3.5 km), but mating occurred predominantly between larger-diameter trees located close to mother-trees. We found that
C. estrellensis
is self-compatible with reproduction mediated mainly by outcrossing (> 0.95), but matings were not random due to biparental inbreeding (tr: 0.048–0.124) and correlated-paternity (rp: 0.16–0.28), which was higher within (rpw: 0.524–0.95) than among fruits (rpa: 0.048–0.052). Inbreeding decreased from seedlings (0.088) to adults, indicating inbreeding depression between the seedling and adult stages. Subpopulations exhibited spatial genetic structure (50–200 m), revealing a pattern of genetic dispersion of isolation-by-distance. Seeds should be harvested from trees that are > 200 m apart for successful ex-situ conservation and populations should not be isolated by more than the maximum pollen-dispersion distance observed (3.5 km) for in-situ conservation. The findings are consistent with the maximum distance that bees can disperse pollen and thereby maintain genetic connectivity between populations and resilience to population fragmentation into forest remnants.</description><subject>Animal Genetics and Genomics</subject><subject>Animal reproduction</subject><subject>Bees</subject><subject>Biodiversity</subject><subject>Biomedical and Life Sciences</subject><subject>Conservation</subject><subject>Conservation Biology/Ecology</subject><subject>Deforestation</subject><subject>Dispersion</subject><subject>Ecology</subject><subject>Evolutionary Biology</subject><subject>Forest fires</subject><subject>Forests</subject><subject>Fragmentation</subject><subject>Genetic diversity</subject><subject>Genetic structure</subject><subject>Habitat fragmentation</subject><subject>Inbreeding</subject><subject>Inbreeding depression</subject><subject>Life Sciences</subject><subject>Mating</subject><subject>Microsatellites</subject><subject>Paternity</subject><subject>Plant Genetics and Genomics</subject><subject>Plant reproduction</subject><subject>Pollen</subject><subject>Population</subject><subject>Population genetics</subject><subject>Populations</subject><subject>Reproductive isolation</subject><subject>Research Article</subject><subject>Resilience</subject><subject>Seedlings</subject><subject>Seeds</subject><subject>Subpopulations</subject><subject>Transition zone</subject><subject>Trees</subject><issn>1566-0621</issn><issn>1572-9737</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNp9kMtKxDAUhoMoqKMv4CrgOpqkTdIsZfAGA7rQdTjTnpQMbVqTzmLe3o4V3Ln6z-K_HD5CbgS_E5yb-yy4spJxWTAulDKsOiEXQhnJrCnM6fHWmnEtxTm5zHnHudDSiAtyeB-6DiNtQh4xZegoxIb2MIXY0hGmCVPMtMFZ-xCRJsyhCxhrpH5IFGgHqUV2wIn5BG2PccKGjsO47-aOIdLB0zWkEANEoJinhMe9HPIVOfPQZbz-1RX5fHr8WL-wzdvz6_phw-pC2IlBKYQp0FYgttqDUspW2ihdbnlhDRjjq9JKixIa72shsBKq8Rrt1hZlU-tiRW6X3jENX_v5A7cb9inOk05aya2WvFKzSy6uOg05J_RuTKGHdHCCuyNityB2M2L3g9hVc6hYQnk2xxbTX_U_qW_mkYD_</recordid><startdate>20240201</startdate><enddate>20240201</enddate><creator>Kubota, Thaisa Y. K.</creator><creator>Hallsworth, John E.</creator><creator>da Silva, Alexandre M.</creator><creator>Moraes, Mario L. 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K. ; Hallsworth, John E. ; da Silva, Alexandre M. ; Moraes, Mario L. 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K.</creatorcontrib><creatorcontrib>Hallsworth, John E.</creatorcontrib><creatorcontrib>da Silva, Alexandre M.</creatorcontrib><creatorcontrib>Moraes, Mario L. T.</creatorcontrib><creatorcontrib>Cambuim, Jose</creatorcontrib><creatorcontrib>Corseuil, Cláudia W.</creatorcontrib><creatorcontrib>Sebbenn, Alexandre M.</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>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><jtitle>Conservation genetics</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Kubota, Thaisa Y. K.</au><au>Hallsworth, John E.</au><au>da Silva, Alexandre M.</au><au>Moraes, Mario L. T.</au><au>Cambuim, Jose</au><au>Corseuil, Cláudia W.</au><au>Sebbenn, Alexandre M.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Pollen dispersal and mating patterns determine resilience for a large-yet-fragmented population of Cariniana estrellensis</atitle><jtitle>Conservation genetics</jtitle><stitle>Conserv Genet</stitle><date>2024-02-01</date><risdate>2024</risdate><volume>25</volume><issue>1</issue><spage>117</spage><epage>132</epage><pages>117-132</pages><issn>1566-0621</issn><eissn>1572-9737</eissn><abstract>Forest fragmentation studies are now urgent due to increased rates of deforestation and forest fires worldwide. In South America, the bee-pollinated
Cariniana estrellensis
is one of the largest trees, and a paradigm for the health and sustainability of forest biomes. For a large-yet-fragmented population (four subpopulations) in the transition zone between Brazilian Savannah and Atlantic Forest, we carried out a study of pollen flow, mating system and spatial genetic structure using nine microsatellite loci. This revealed that the subpopulations are not reproductively isolated because of pollen flow from outside the study area (18.3%) and between subpopulations (16.1–31.3%). Pollen dispersal reached long distances (3.5 km), but mating occurred predominantly between larger-diameter trees located close to mother-trees. We found that
C. estrellensis
is self-compatible with reproduction mediated mainly by outcrossing (> 0.95), but matings were not random due to biparental inbreeding (tr: 0.048–0.124) and correlated-paternity (rp: 0.16–0.28), which was higher within (rpw: 0.524–0.95) than among fruits (rpa: 0.048–0.052). Inbreeding decreased from seedlings (0.088) to adults, indicating inbreeding depression between the seedling and adult stages. Subpopulations exhibited spatial genetic structure (50–200 m), revealing a pattern of genetic dispersion of isolation-by-distance. Seeds should be harvested from trees that are > 200 m apart for successful ex-situ conservation and populations should not be isolated by more than the maximum pollen-dispersion distance observed (3.5 km) for in-situ conservation. The findings are consistent with the maximum distance that bees can disperse pollen and thereby maintain genetic connectivity between populations and resilience to population fragmentation into forest remnants.</abstract><cop>Dordrecht</cop><pub>Springer Netherlands</pub><doi>10.1007/s10592-023-01557-8</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0001-6797-9362</orcidid><orcidid>https://orcid.org/0000-0001-6939-8430</orcidid><orcidid>https://orcid.org/0000-0002-1076-9812</orcidid><orcidid>https://orcid.org/0000-0003-1458-2454</orcidid><orcidid>https://orcid.org/0000-0001-5928-4181</orcidid><orcidid>https://orcid.org/0000-0003-0839-633X</orcidid><orcidid>https://orcid.org/0000-0003-2352-0941</orcidid></addata></record> |
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subjects | Animal Genetics and Genomics Animal reproduction Bees Biodiversity Biomedical and Life Sciences Conservation Conservation Biology/Ecology Deforestation Dispersion Ecology Evolutionary Biology Forest fires Forests Fragmentation Genetic diversity Genetic structure Habitat fragmentation Inbreeding Inbreeding depression Life Sciences Mating Microsatellites Paternity Plant Genetics and Genomics Plant reproduction Pollen Population Population genetics Populations Reproductive isolation Research Article Resilience Seedlings Seeds Subpopulations Transition zone Trees |
title | Pollen dispersal and mating patterns determine resilience for a large-yet-fragmented population of Cariniana estrellensis |
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