Abstract
Biodiversity is organized in three fundamental hierarchical levels in nature: diversity of genes within species, diversity of species in communities, and diversity of ecosystems. The analyses of the Species-Genetic Diversity Correlation (SGDC) are important for understanding the ecological and evolutionary mechanisms underlying the patterns of biodiversity in time and space and, at the same time, have contributed to the planning of the simultaneous conservation of these levels. Thus, SGDC can be important to establish a framework to evaluate diversity patterns and develop conservation programs in widely explored areas such as the Brazilian Cerrado, generating knowledge for species of great ecological and economic importance. An example is Stryphnodendron adstringens, a tree that occurs in the Brazilian Cerrado and has medicinal properties. In this study, SGDC analyses were applied to verify if there is a correlation between the genetic diversity of S. adstringens and the diversity of species of Stryphnodendron and other phylogenetically related genera. Ecological niche modeling procedures were used to estimate the occurrence area and species diversity of Stryphnodendron and related genera in the Brazilian Cerrado, which enabled the construction of maps of environmental suitability. The α-SGDC and β-SGDC correlations were calculated in two different situations, one using microsatellite genetic data and the other using chloroplastidal DNA (cpDNA) genetic data. The analyses revealed a significant negative relationship between the haplotypic diversity of S. adstringens and the diversity of species of Stryphnodendron and other genera. The negative α-SGDC detected is an indication that to develop a conservation plan for the set of species analyzed, it is necessary to combine conservation strategies that cover more than one level of biological diversity.
Similar content being viewed by others
References
Allouche O, Tsoar A, Kadmon R (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). J Appl Ecol 43:1223–1232. https://doi.org/10.1111/j.1365-2664.2006.01214.x
Antonovics J (1976) The input from population genetics: “The New Ecological Genetics.” Syst Bot 1:233–245. https://doi.org/10.2307/2418718
Barbosa ILBD, Oliveira HR, Terribile LC, Diniz-Filho JAF (2019) Geographical distribution of Stryphnodendron adstringens Mart. Coville (Fabaceae): modeling effects of climate change on past, present and future. Braz J Bot 42:53–61. https://doi.org/10.1007/s40415-019-00520-7
Blanchet S, Prunier JG, Paz-Vinas I et al (2020) A river runs through it: the causes, consequences, and management of intraspecific diversity in river networks. Evol Appl 13:1195–1213. https://doi.org/10.1111/eva.12941
Blum MJ, Bagley MJ, Walters DM et al (2012) Genetic diversity and species diversity of stream fishes covary across a land-use gradient. Oecologia 168:83–95. https://doi.org/10.1007/s00442-011-2078-x
Borcard D, Legendre P (2002) All-scale spatial analysis of ecological data by means of principal coordinates of neighbour matrices. Ecol Modell 153:51–68. https://doi.org/10.1016/S0304-3800(01)00501-4
Borges Filho HC, Felfili JM (2003) Avaliação dos níveis de extrativismo da casca de barbatimão [Stryphnodendron adstringens (Mart.) Coville] no Distrito Federal. Brasil Revista Árvore 27:735–745. https://doi.org/10.1590/S0100-67622003000500016
Borges LM, Inglis PW, Simon MF, Ribeiro PG, De Queiroz LP (2022) Misleading fruits: the non-monophyly of Pseudopiptadenia and Pityrocarpa supports generic re-circumscriptions and a new genus within mimosoid legumes. PhytoKeys 205:239–259. https://doi.org/10.3897/phytokeys.205.82275
Bowen BW (1999) Preserving genes, species, or ecosystems? Healing the fractured foundations of conservation policy. Mol Ecol 8:S5–S10. https://doi.org/10.1046/j.1365-294X.1999.00798.x
Braga RS (2019) Diversificação e radiação recente de Stryphnodendron adstringens (Leguminosae) no Cerrado: consequências genéticas frente às mudanças climáticas. Dissertation, Federal University of Goiás, Goiás
Chaves DA, Lemes SR, Araújo LA et al (2016) Avaliação da atividade angiogênica da solução aquosa do barbatimão (Stryphnodendron adstringens). Revista Brasileira De Plantas Medicinais 18:524–530. https://doi.org/10.1590/1983-084X/15_093
Cleary DFR, Fauvelot C, Genner MJ et al (2006) Parallel responses of species and genetic diversity to El Niño Southern Oscillation-induced environmental destruction. Ecol Lett 9:304–310. https://doi.org/10.1111/j.1461-0248.2005.00876.x
Colwell RK, Rangel TF (2009) Hutchinson’s duality: The once and future niche. Proc Natl Acad Sci 106:19651–19658. https://doi.org/10.1073/pnas.0901650106
Crutsinger GM, Collins MD, Fordyce JA et al (2006) Plant genotypic diversity predicts community structure and governs an ecosystem process. Science 313:966–968. https://doi.org/10.1126/science.1128326
de Marco P, Nóbrega CC (2018) Evaluating collinearity effects on species distribution models: an approach based on virtual species simulation. PLoS ONE 13:e0202403. https://doi.org/10.1371/journal.pone.0202403
de Siqueira MF, Peterson AT (2003) Consequences of global climate change for geographic distributions of cerrado tree species. Biota Neotrop 3:1–14. https://doi.org/10.1590/S1676-06032003000200005
Diniz-Filho JAF, Mauricio Bini L, Fernando Rangel T et al (2009a) Partitioning and mapping uncertainties in ensembles of forecasts of species turnover under climate change. Ecography 32:897–906. https://doi.org/10.1111/j.1600-0587.2009.06196.x
Diniz-Filho JAF, Melo DB, de Oliveira G et al (2012) Planning for optimal conservation of geographical genetic variability within species. Conserv Genet 13:1085–1093. https://doi.org/10.1007/s10592-012-0356-8
Diniz-Filho JAF, Nabout JC, de Telles MPC et al (2009b) A review of techniques for spatial modeling in geographical, conservation and landscape genetics. Genet Mol Biol 32:203–211. https://doi.org/10.1590/S1415-47572009000200001
Diniz-Filho JAF, Soares TN, Lima JS et al (2013) Mantel test in population genetics. Genet Mol Biol 36:475–485. https://doi.org/10.1590/S1415-47572013000400002
Felfili JM, da Silva-Junior MC, Dias BJ, Rezende AV (1999) Estudo fenológico de Stryphnodendron adstringens (Mart.) Coville no cerrado sensu stricto da Fazenda Água Limpa no Distrito Federal. Brasil Revista Brasileira De Botânica 22:83–90. https://doi.org/10.1590/S0100-84041999000100011
Flora e Funga (2022) Flora e Funga do Brasil. In: Jardim Botânico do Rio de Janeiro. https://floradobrasil.jbrj.gov.br/FB128461. Accessed 24 Aug 2022
Frankham R (2005a) Genetics and extinction. Biol Conserv 126:131–140. https://doi.org/10.1016/j.biocon.2005.05.002
Frankham R (2005b) Stress and adaptation in conservation genetics. J Evol Biol 18:750–755. https://doi.org/10.1111/j.1420-9101.2005.00885.x
Frankham R, Ballou JD, Ralls K et al (2017) Genetic management of fragmented animal and plant populations. Oxford University Press, Oxford
Frankham R, Ralls K (1998) Inbreeding leads to extinction. Nature 392:441–442. https://doi.org/10.1038/33022
Frey D, Arrigo N, Granereau G et al (2016) Parallel declines in species and genetic diversity driven by anthropogenic disturbance: a multispecies approach in a French Atlantic dune system. Evol Appl 9:479–488. https://doi.org/10.1111/eva.12351
Gonçalves AR (2020) Variabilidade genética e conservação de Stryphnodendron adstringens (Leguminosae). Dissertation, Federal University of Goiás, Goiás
Guisan A, Thuiller W, Zimmermann NE (2017) Habitat suitability and distribution models. Cambridge University Press, Cambridge
He T, Lamont BB, Krauss SL et al (2008) Covariation between intraspecific genetic diversity and species diversity within a plant functional group. J Ecol 96:956–961. https://doi.org/10.1111/j.1365-2745.2008.01402.x
Henriques BO, Corrêa O, Azevedo EPC et al (2016) In Vitro TNF-α inhibitory activity of Brazilian plants and anti-inflammatory effect of Stryphnodendron adstringens in an acute arthritis model. Evid Complement Altern Med 2016:1–15. https://doi.org/10.1155/2016/9872598
Hoban SM, Hauffe HC, Pérez-Espona S et al (2013) Bringing genetic diversity to the forefront of conservation policy and management. Conserv Genet Resour 5:593–598. https://doi.org/10.1007/s12686-013-9859-y
Kahilainen A, Puurtinen M, Kotiaho JS (2014) Conservation implications of species–genetic diversity correlations. Glob Ecol Conserv 2:315–323. https://doi.org/10.1016/j.gecco.2014.10.013
Klink C, Machado R (2005) A conservação do Cerrado brasileiro. In: Silva JMC (ed) 1st edn. Belo Horizonte, Brasil, pp 147–155
Laikre L, Allendorf FW, Aroner LC et al (2010) Neglect of genetic diversity in implementation of the convention on biological diversity. Conserv Biol 24:86–88. https://doi.org/10.1111/j.1523-1739.2009.01425.x
Lamy T, Jarne P, Laroche F et al (2013) Variation in habitat connectivity generates positive correlations between species and genetic diversity in a metacommunity. Mol Ecol 22:4445–4456. https://doi.org/10.1111/mec.12399
Lamy T, Laroche F, David P et al (2017) The contribution of species-genetic diversity correlations to the understanding of community assembly rules. Oikos 126:759–771. https://doi.org/10.1111/oik.03997
Lanfear R, Kokko H, Eyre-Walker A (2014) Population size and the rate of evolution. Trends Ecol Evol 29:33–41. https://doi.org/10.1016/j.tree.2013.09.009
Lima AG, Paula-Souza J, Ringelberg JJ et al (2022a) New segregates from the Neotropical genus Stryphnodendron (Leguminosae, Caesalpinioideae, mimosoid clade). PhytoKeys 205:203–237. https://doi.org/10.3897/phytokeys.205.82220
Lima AG, Souza VC, Paula-Souza J, Scalon VR (2020b) Stryphnodendron in Flora do Brasil 2020. In: Jardim Botânico do Rio de Janeiro. https://floradobrasil2020.jbrj.gov.br/FB19133. Accessed 25 Jan 2021
Lima NE, Lima-Ribeiro MS, Tinoco CF et al (2014) Phylogeography and ecological niche modelling, coupled with the fossil pollen record, unravel the demographic history of a Neotropical swamp palm through the Quaternary. J Biogeogr 41:673–686. https://doi.org/10.1111/jbi.12269
Lima AG, Paula-Souza J, Ringelberg JJ, Simon MF, Queiroz LP, Borges LM, Mansano VF, Souza VC, Scalon VR (2022b) New segregates from the Neotropical genus Stryphnodendron (Leguminosae, Caesalpinioideae, mimosoid clade). PhytoKeys 205:203–237
Lima-Ribeiro MS, Varela S, González-Hernández J et al (2015) EcoClimate: a database of climate data from multiple models for past, present, and future for macroecologists and biogeographers. Biodivers Inform. https://doi.org/10.17161/bi.v10i0.4955
Lino A, Ferreira E, Fonseca C et al (2021) Species–genetic diversity correlation in phyllostomid bats of the Bodoquena plateau, Brazil. Biodivers Conserv 30:403–429. https://doi.org/10.1007/s10531-020-02097-0
MacArthur RH, Wilson EO (1967) The theory of island biogeography, revised. Princeton University Press, New Jersey
Mace GM, Purvis A (2008) Evolutionary biology and practical conservation: bridging a widening gap. Mol Ecol 17:9–19. https://doi.org/10.1111/j.1365-294X.2007.03455.x
Marchesini A, Vernesi C, Battisti A, Ficetola GF (2018) Deciphering the drivers of negative species-genetic diversity correlation in Alpine amphibians. Mol Ecol 27:4916–4930. https://doi.org/10.1111/mec.14902
Mittermeier RA, Gil PR, Hoffmann M, Pilgrim J, Brooks T, Mittermeier CG, Lamoreux J, Fonseca GAB (2004) Hotspots revisited. Earth's biologically richest and most endangered terrestrial ecoregions. CEMEX Conservation Book Series
MMA M do MA (2009) Plano de Ação para Prevenção e Controle do Desmatamento e das Queimadas no Cerrado—PP Cerrado. http://combateaodesmatamento.mma.gov.br. Accessed 25 Jan 2021
Newman D, Pilson D (1997) Increased probability of extinction due to decreased genetic effective population size: experimental populations of Clarkia pulchella. Evolution 51:354–362. https://doi.org/10.1111/j.1558-5646.1997.tb02422.x
Nóbrega RLB, Ziembowicz T, Torres GN et al (2020) Ecosystem services of a functionally diverse riparian zone in the Amazon-Cerrado agricultural frontier. Glob Ecol Conserv 21:e00819. https://doi.org/10.1016/j.gecco.2019.e00819
Oksanen J, Blanchet FG, Kindt R et al (2022) Vegan: an R package for community ecologists. R Packag Vers 26–4:1–297
Ortiz PL, Arista M, Oliveira PE, Talavera S (2003) Pattern of flower and fruit production in Stryphnodendron adstringens, an andromonoecious legume tree of central Brazil. Plant Biol 5:592–599. https://doi.org/10.1055/s-2003-44720
Peterson AT, Soberón J, Pearson RG et al (2011) Ecological niches and geographic distributions (MPB-49). Princeton University Press, New Jersey
Pfeiffer VW, Ford BM, Housset J et al (2018) Partitioning genetic and species diversity refines our understanding of species–genetic diversity relationships. Ecol Evol 8:12351–12364. https://doi.org/10.1002/ece3.4530
Ponce-Reyes R, Clegg SM, Carvalho SB et al (2014) Geographical surrogates of genetic variation for selecting island populations for conservation. Divers Distrib 20:640–651. https://doi.org/10.1111/ddi.12195
Puşcaş M, Taberlet P, Choler P (2008) No positive correlation between species and genetic diversity in European alpine grasslands dominated by Carex curvula. Divers Distrib 14:852–861. https://doi.org/10.1111/j.1472-4642.2008.00489.x
R Core Team (2023) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. http://www.R-project.org/. Accessed 19 Aug 2020
Reisch C, Schmid C (2019) Species and genetic diversity are not congruent in fragmented dry grasslands. Ecol Evol 9:664–671. https://doi.org/10.1002/ece3.4791
Ribeiro-Neto JA, Tarôco BRP, dos Santos HB et al (2020) Using the plants of Brazilian Cerrado for wound healing: from traditional use to scientific approach. J Ethnopharmacol 260:112547. https://doi.org/10.1016/j.jep.2020.112547
Rousset F (1997) Genetic differentiation and estimation of gene flow from F-statistics under isolation by distance. Genetics 145:1219–1228. https://doi.org/10.1093/genetics/145.4.1219
Scariot A, Sousa-Silva JC, Felfili JM (2005) Cerrado: Ecologia, Biodiversidade e Conservação. Ministério do Meio Ambiente, Brasília
Simon MF, Pastore JFB, Souza AF et al (2016) Molecular phylogeny of stryphnodendron (mimosoideae, leguminosae) and generic delimitations in the piptadenia group. Int J Plant Sci 177:44–59. https://doi.org/10.1086/684077
Soberón J (2007) Grinnellian and Eltonian niches and geographic distributions of species. Ecol Lett 10:1115–1123. https://doi.org/10.1111/j.1461-0248.2007.01107.x
Soininen J, McDonald R, Hillebrand H (2007) The distance decay of similarity in ecological communities. Ecography 30:3–12. https://doi.org/10.1111/j.0906-7590.2007.04817.x
Sosa V, Loera I (2017) Influence of current climate, historical climate stability and topography on species richness and endemism in Mesoamerican geophyte plants. PeerJ 5:e3932. https://doi.org/10.7717/peerj.3932
Souza-Moreira T, Queiroz-Fernandes G, Pietro R (2018) Stryphnodendron species known as “Barbatimão”: a comprehensive report. Molecules 23:910. https://doi.org/10.3390/molecules23040910
Spielman D, Brook BW, Frankham R (2004) Most species are not driven to extinction before genetic factors impact them. Proc Natl Acad Sci 101:15261–15264. https://doi.org/10.1073/pnas.0403809101
Struebig MJ, Kingston T, Petit EJ et al (2011) Parallel declines in species and genetic diversity in tropical forest fragments. Ecol Lett 14:582–590. https://doi.org/10.1111/j.1461-0248.2011.01623.x
Taberlet P, Zimmermann NE, Englisch T et al (2012) Genetic diversity in widespread species is not congruent with species richness in alpine plant communities. Ecol Lett 15:1439–1448. https://doi.org/10.1111/ele.12004
Telles MPC, Dobrovolski R, Souza KS et al (2014) Disentangling landscape effects on population genetic structure of a Neotropical savanna tree. Natureza Conservação 12:65–70. https://doi.org/10.4322/natcon.2014.012
Vellend M (2003) Island biogeography of genes and species. Am Nat 162:358–365. https://doi.org/10.1086/377189
Vellend M (2005) Species diversity and genetic diversity: parallel processes and correlated patterns. Am Nat 166:199–215. https://doi.org/10.1086/431318
Vellend M (2004) Parallel effects of land-use history on species diversity and genetic diversity of forest herbs. Ecology 85:3043–3055. https://doi.org/10.1890/04-0435
Vellend M, Geber MA (2005) Connections between species diversity and genetic diversity. Ecol Lett 8:767–781. https://doi.org/10.1111/j.1461-0248.2005.00775.x
Vellend M, Lajoie G, Bourret A et al (2014) Drawing ecological inferences from coincident patterns of population- and community-level biodiversity. Mol Ecol 23:2890–2901. https://doi.org/10.1111/mec.12756
Walpole M, Almond REA, Besançon C et al (2009) Tracking progress toward the 2010 biodiversity target and beyond. Science 325:1503–1504. https://doi.org/10.1126/science.1175466
Wei X, Jiang M (2012) Contrasting relationships between species diversity and genetic diversity in natural and disturbed forest tree communities. New Phytol 193:779–786. https://doi.org/10.1111/j.1469-8137.2011.03957.x
Willi Y, van Buskirk J, Hoffmann AA (2006) Limits to the adaptive potential of small populations. Annu Rev Ecol Evol Syst 37:433–458. https://doi.org/10.1146/annurev.ecolsys.37.091305.110145
Wimp GM, Young WP, Woolbright SA et al (2004) Conserving plant genetic diversity for dependent animal communities. Ecol Lett 7:776–780. https://doi.org/10.1111/j.1461-0248.2004.00635.x
Wright S (1940) Breeding structure of populations in relation to speciation. Am Nat 74:232–248. https://doi.org/10.1086/280891
Acknowledgments
This project was supported by “Universal” projects from CNPq (proc. 402178/2016-5) and FAPEG (Proc 201410267001736). Our research program in population genetics of Cerrado plants has been continuously supported by the project “Núcleo de Excelência em Genética e Conservação de Espécies do Cerrado” and the GENPAC research network (“Geographical Genetics and Regional Planning for natural resources in Brazilian Cerrado”), funded by CNPq, CAPES and FAPEG. This work was also developed in the context of the INCT in “Ecology, Evolution and Biodiversity Conservation” (EECBio), supported by CNPq and FAPEG (procs 465610/2014-5 and 201810267000023). Work CMRSF, RSBF, and ARG were supported by EECBio DTI fellowships, whereas AOR, ILBDB and RBP were supported by MsC, Doctoral and PNPD CAPES fellowships, respectively. JAFDF and MPCT were supported by CNPq Research Productivity Fellowships.
Author information
Authors and Affiliations
Contributions
CMRSF and ADR collected and prepared the data used in the ecological niche modeling, RBP helped in the selection of species and occurrence records for the analyses, as well as in the understanding of the phylogenetic relationships of the group. The ILBDB contributed to the construction of the ENMs. CMRSF, ADR and RSBF analyzed and interpreted the ENMs. RSBF, ARG and MPCT carried out the works that gave rise to the genetic diversity data used in the analyses and contributed to the knowledge about the population dynamics of Stryphnodendron adstringens. CMRSF, RSBF and JAFDF performed the SGDCs analyses. JAFDF and MPCT contributed with intellectual content, critically analyzing and guiding the accomplishment of each stage of the work. CMRSF wrote the original draft, and all authors contributed to the review and construction of the final version of the manuscript. ARG formatted the draft manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that there is no conflict of interest in the publication of this article.
Additional information
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
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.
About this article
Cite this article
da Silva-Filha, C.M.R., dos Santos Braga-Ferreira, R., Barbosa, I.L.B.D. et al. Genetic diversity in Stryphnodendron adstringens (Mart.) Coville (Leguminosae, Caesalpinioideae, Clade Mimosoid) and its correlation with species richness of Stryphnodendron Mart. and related genera. Braz. J. Bot 46, 1113–1127 (2023). https://doi.org/10.1007/s40415-023-00943-3
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s40415-023-00943-3