Diversity, genetic structure, and population genomics of the tropical tree Centrolobium tomentosum in remnant and restored Atlantic forests
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The rapid pace of deforestation and fragmentation that took place in the Brazilian Atlantic Forest and other global hotspots for biodiversity conservation has motivated ecosystem restoration efforts. The genetic viability of restored tree populations and their potential to conserve genetic diversity remains, however, unclear. Here, we assessed the genetic viability and potential to conserve the genetic diversity of restored populations of Centrolobium tomentosum, a native legume tree, in the Brazilian Atlantic Forest, based on a genotyping by sequencing (GBS). We have successfully generated a total of 2877 single nucleotide polymorphism (SNP) markers across the whole C. tomentosum genome. Surprisingly, restoration sites presented overall higher levels of genetic diversity compared to natural remnant areas and negative inbreeding coefficient (FIS), mainly in juveniles’ trees from newer restored areas, indicating an excess of heterozygotes probably due to the founding event. The most likely number of genetic clusters found was two (K = 2), suggesting that diverse seed sources were used to produce seedlings for restoration. Clear signs of gene flow from restored to natural remnants areas had also been detected when diversity values of adults and juveniles were contrasted. Even though we did not find any clear relation of the genetic diversity and landscape composition, the low percentage of forest and high levels of fragmentation are likely reducing patch connectivity in some areas. LOSITAN detected 88 SNP outliers under positive selection, but analysis with Bayescan failed to support this evidence. In conclusion, our post hoc evaluation of restored tree populations indicated that the old restored area is stable and new areas have great potential to contribute to conserving genetic diversity and increasing the chances of the natural populations to persist over time.
KeywordsActive restoration Conservation genetics Ecological restoration Landscape genetics Forest restoration Restoration plantations
We want to FAPESP (Industry) for the postdoc assistantships: CMM (FAPESP; Grant #2011/50296-8), EMGC (FAPESP; Grant #2017/02393-0), doctorate: KDS (FAPESP; Grant #2015/06349-0), EAS (FAPESP; Grant #2015/15536-9), and PSB (FAPESP; Grant #2014/01364-9). MIZ and PHSB thank the National Council for Scientific and Technological Development of Brazil (CNPq; Grant #310446/2015-5, CNPq; Grant #304817/2015-5).
This study was fully funded by the São Paulo Research Foundation (FAPESP, Portuguese: Fundação de Amparo à Pesquisa do Estado de São Paulo) and The Brazilian National Council for Scientific and Technological Development (CNPq, Portuguese: Conselho Nacional de Desenvolvimento Científico e Tecnológico). Sponsors have no role in the study design, data collection, and data analysis, or manuscript preparation.
Compliance with ethical standards
Conflict of interest
The authors declare that they have no conflict of interest. Mention of trade names is solely for specific details of the conducted research and does not imply endorsement or recommendation by CNPq, FAPESP, or the authors.
- Bertacchi MIF, Amazonas NT, Brancalion PHS, Brondani GE, de Oliveira ACS, de Pascoa MAR, Rodrigues RR (2016) Establishment of tree seedlings in the understory of restoration plantations: natural regeneration and enrichment plantings. Restor Ecol 24:100–108. https://doi.org/10.1111/rec.12290 CrossRefGoogle Scholar
- Brancalion PHS, Schweizer D, Gaudare U, Mangueira JR, Lamonato F, Farah FT, Nave AG, Rodrigues RR (2016) Balancing economic costs and ecological outcomes of passive and active restoration in agricultural landscapes: the case of Brazil. Biotropica 48:856–867. https://doi.org/10.1111/btp.12383 CrossRefGoogle Scholar
- Doyle JJ, Doyle JL (1987) A rapid DNA isolation procedure for small quantities of fresh leaf tissue. Phytochem Bull 19:11–15Google Scholar
- Frankham R (1996) Relationship of Genetic Variation to Population Size in Wildlife. Conserv Biol 10:1500–1508. https://doi.org/10.1046/j.1523-1739.1996.10061500.x CrossRefGoogle Scholar
- Guirao AC, Filho JT (2011) Preservação de um fragmento florestal urbano—Estudo de caso: a ARIE Mata de Santa Genebra, Campinas-SP. GEUSP: Espaço e Tempo, São Paulo 29:147–158Google Scholar
- McGarigal K, Cushman SA, Neel MC, Ene E (2012) FRAGSTATS v4: Spatial Pattern Analysis Program for Categorical and Continuous Maps. Univ. Massachusettes, Amherst. https://www.umass.edu/landeco/research/fragstats/fragstats.html
- Novello M, Viana JPG, Alves-Pereira A, de Aguiar Silvestre E, Nunes HF, Pinheiro JB, Brancalion PHS, Zucchi MI (2018) Genetic conservation of a threatened Neotropical palm through community-management of fruits in agroforests and second-growth forests. For Ecol Manage 407:200–209. https://doi.org/10.1016/j.foreco.2017.06.059 CrossRefGoogle Scholar
- Raeymaekers JAM, Konijnendijk N, Larmuseau MHD, Hellemans B, Meester L, Volckaert FAM (2013) A gene with major phenotypic effects as a target for selection vs. homogenizing gene flow. Mol Ecol 23:161–181Google Scholar
- REFLORA (2019) Brazilian Plants: historic rescue and virtual herbarium for knowledge and conservation of the Brazilian flora. In: REFLORA. http://reflora.jbrj.gov.br. Accessed 14 April 2019
- Sansevero JBB, Prieto PV, de Moraes LFD, Rodrigues PJFP (2011) Natural regeneration in plantations of native trees in lowland Brazilian Atlantic forest: community structure, diversity, and dispersal syndromes. Restor Ecol 19:79–389. https://doi.org/10.1111/j.1526-100X.2009.00556.x CrossRefGoogle Scholar
- Schwarcz KD (2014) Genetic feasibility of forest restorations: genetic diversity and structure in Myroxylon peruiferum L.f. Doctoral dissertation, University of CampinasGoogle Scholar
- Schwarcz KD, Silvestre EA, de Campos JB, Sujii PS, Grando C, Macrini CMT, de Souza AP, Pinheiro JB, Brancalion PHS, Rodrigues RR, Zucchi MI (2018) Shelter from the storm: restored populations of the neotropical tree Myroxylon peruiferum are as genetically diverse as those from conserved remnants. For Ecol Manage 410:95–103. https://doi.org/10.1016/j.foreco.2017.12.037 CrossRefGoogle Scholar
- Shannon CE, Weaver W (1949) The mathematical theory of communication. University of Illinois Press, IllinoisGoogle Scholar
- Silva CC (2013) Potential of natives species to produce timber in forest restoration plantings. Master thesis, University of São Paulo-ESALQGoogle Scholar
- Silvestre EDA, Schwarcz KD, Grando C, De Campos JB, Sujii PS, Tambarussi EV, Macrini CMT, Pinheiro JB, Brancalion PHS, Zucchi MI (2018) Mating system and effective population size of the overexploited neotropical tree (Myroxylon peruiferum L.f.) and their impact on seedling production. J Hered 109:264–271. https://doi.org/10.1093/jhered/esx096 CrossRefPubMedGoogle Scholar
- Sujii PS (2016) Genetic diversity, structure and mating system of Centrolobium tomentosum Guillem. Doctoral dissertation, University of CampinasGoogle Scholar
- Viana JPG, Siqueira MVBM, Araujo FL, Grando C, Sujii PS, De Aguiar Silvestre E, Novello M, Pinheiro JB, Cavallari MM, Brancalion PHS, Rodrigues RR, De Souza AP, Catchen J, Zucchi MI (2018) Genomic diversity is similar between Atlantic Forest restorations and natural remnants for the native tree Casearia sylvestris Sw. PLoS ONE 13:e0192165. https://doi.org/10.1371/journal.pone.0192165 CrossRefGoogle Scholar
- Zucchi MI, Sujii PS, Mori GM, Viana JPG, Grando C, Silvestre EA, Schwarcz KD, Macrini CM, Bajay MM, Araújo FL, Siqueira MVBM, Alves-Pereira A, Souza AP, Pinheiro JB, Rodrigues RR, Brancalion PHS (2017) Genetic diversity of reintroduced tree populations in restoration plantations of the Brazilian Atlantic Forest. Restor Ecol 26:694–701. https://doi.org/10.1111/rec.12620 CrossRefGoogle Scholar