Abstract
Understanding how historical and current environmental suitability and human impacts affect the genetic diversity on a large scale is essential to species management planning. However, most studies in conservation genetics are carried out at a local or regional scale and rarely on broad spatial scales such as an entire biome. We evaluated the relative contribution of historical and current environmental suitability, current landscape features and human impacts to explain genetic diversity, allelic richness and inbreeding variation among populations, using Euterpe edulis and the Atlantic forest as the model system. We fitted linear mixed models within a multiple competing hypotheses approach with model selection based on Akaike’s Information Criteria. We showed that overall genetic diversity was lower in sites with absence of large seed dispersers and higher in sites with historically stable climate. Both seedling and adults showed to be negatively influenced by human impact factors; with adults mainly affected by the reduction of forest cover while seedlings by the loss of large seed dispersers. Thus, the current pattern of genetic diversity in E. edulis is the result of historical instability during the mid-Holocene and recent anthropogenic impacts, mainly those that affect important ecological process such as seed dispersal. Thus, an efficient plan for species conservation must account for human impacts and environmental suitability and also assess the genetic diversity of seedlings and adults in fragmented landscapes.
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References
Aguilar R, Quesada M, Ashworth L et al (2008) Genetic consequences of habitat fragmentation in plant populations: susceptible signals in plant traits and methodological approaches. Mol Ecol 17:5177–5188. doi:10.1111/j.1365-294X.2008.03971.x
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. doi:10.1111/j.1365-2664.2006.01214.x
Andersen LW, Fog K, Damgaard C (2004) Habitat fragmentation causes bottlenecks and inbreeding in the European tree frog (Hyla arborea). Proc Biol Sci 271:1293–1302. doi:10.1098/rspb.2004.2720
Araújo MB, New M (2007) Ensemble forecasting of species distributions. Trends Ecol Evol 22:42–47. doi:10.1016/j.tree.2006.09.010
Arnaud-Haond S, Teixeira S, Massa SI et al (2006) Genetic structure at range edge: low diversity and high inbreeding in Southeast Asian mangrove (Avicennia marina) populations. Mol Ecol 15:3515–3525. doi:10.1111/j.1365-294X.2006.02997.x
Barbet-Massin M, Jiguet F, Albert CH, Thuiller W (2012) Selecting pseudo-absences for species distribution models: how, where and how many? Methods Ecol Evol 3:327–338. doi:10.1111/j.2041-210X.2011.00172.x
Barton, K (2016) MuMIn: multi-model inference, R package version 1.15.6.
Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. J Stat Softw 67:1–48. doi:10.18637/jss.v067.i01
Boscolo D, Metzger JP (2011) Isolation determines patterns of species presence in highly fragmented landscapes. Ecography 34:1018–1029. doi:10.1111/j.1600-0587.2011.06763.x
Breed MF, Gardner MG, Ottewell KM et al (2012) Shifts in reproductive assurance strategies and inbreeding costs associated with habitat fragmentation in Central American mahogany. Ecol Lett 15:444–452. doi:10.1111/j.1461-0248.2012.01752.x
Burnham KKP, Anderson DRD (2002) Model selection and multimodel inference: a practical information-theoretic approach. Springer, New York
Carnaval ACOQ, Hickerson MJ, Haddad CFB et al (2009) Stability predicts genetic diversity in the Brazilian Atlantic forest hotspot. Science 323:785–789. doi:10.1126/science.1166955
Carvalho CS, Ribeiro MC, Côrtes MC et al (2015) Contemporary and historic factors influence differently genetic differentiation and diversity in a tropical palm. Heredity 115:216–224. doi:10.1038/hdy.2015.30
Collevatti RG, Grattapaglia D, Hay JD (2001) Population genetic structure of the endangered tropical tree species Caryocar brasiliense, based on variability at microsatellite loci. Mol Ecol 10:349–356. doi:10.1046/j.1365-294X.2001.01226.x
Collevatti RG, Lima-Ribeiro MS, Terribile LC et al (2014) Recovering species demographic history from multi-model inference: the case of a Neotropical savanna tree species. BMC Evol Biol 14:1–13. doi:10.1186/s12862-014-0213-0
Conte R, dos Reis SM, Mantovani A, Vencovsky R (2008) Genetic structure and mating system of Euterpe edulis Mart. Populations: a comparative analysis using microsatellite and allozyme markers. J Hered 99:476–482. doi:10.1093/jhered/esn055
Côrtes MC, Uriarte M, Lemes MR et al (2013) Low plant density enhances gene dispersal in the Amazonian understory herb Heliconia acuminata. Mol Ecol 22:5716–5729. doi:10.1111/mec.12495
Dawson TP, Jackson ST, House JI et al (2011) Beyond predictions: biodiversity conservation in a changing climate. Science 332:53–58. doi:10.1126/science.1200303
DiBattista JD (2007) Patterns of genetic variation in anthropogenically impacted populations. Conserv Genet 9:141–156. doi:10.1007/s10592-007-9317-z
Diniz-Filho JAF, Nabout JC, Bini LM et al (2009) Niche modelling and landscape genetics of Caryocar brasiliense (Pequi tree: Caryocaraceae) in Brazilian Cerrado: an integrative approach for evaluating central-peripheral population patterns. Tree Genet Genomes 5:617–627. doi:10.1007/s11295-009-0214-0
Dirzo R, Miranda A (1991) Altered patterns of herbivory and diversity in the forest understory: a case study of the possible consequences of contemporary defaunation. In: Price PW et al (eds) Plant–animal interactions: evolutionary ecology in tropical and temperate regions. Wiley, New York, pp 273–287
Eycott AE, Stewart GB, Buyung-Ali LM et al (2012) A meta-analysis on the impact of different matrix structures on species movement rates. Landsc Ecol 27:1263–1278. doi:10.1007/s10980-012-9781-9
Fahrig L (2003) Effects of habitat fragmentation on biodiversity. Annu Rev Ecol Evol Syst 34:487–515. doi:10.1146/annurev.ecolsys.34.011802.132419
Ferrier S, Watson G, Pearce J, Drielsma M (2002) Extended statistical approaches to modelling spatial pattern in biodiversity in northeast New South Wales. I. Species-level modelling. Biodivers Conserv 11:2275–2307. doi:10.1023/A:1021302930424
Fielding AH, Bell JF (1997) A review of methods for the assessment of prediction errors in conservation presence/absence models. Environ Conserv 24:38–49. doi:10.1017/S0376892997000088
Foley JA, DeFries R, Asner GP et al (2005) Global consequences of land use. Science 309:570–574. doi:10.1126/science.1111772
Frankham R, Lees K, Montgomery ME et al (1999) Do population size bottlenecks reduce evolutionary potential? Anim Conserv 2:255–260. doi:10.1111/j.1469-1795.1999.tb00071.x
Gaiotto FA, Grattapaglia D, Vencovsky R (2003) Genetic structure, mating system, and long-distance gene flow in heart of palm (Euterpe edulis Mart.). J Hered 94:399–406. doi:10.1093/jhered/esg087
Galetti M, Fernandez JC (1998) Palm heart harvesting in the Brazilian Atlantic forest: changes in industry structure and the illegal trade. J Appl Ecol 35:294–301. doi:10.1046/j.1365-2664.1998.00295.x
Galetti M, Guevara R, Côrtes MC et al (2013) Functional extinction of birds drives rapid evolutionary changes in seed size. Science 340:1086–1090. doi:10.1126/science.1233774
García C, Jordano P, Godoy JA (2007) Contemporary pollen and seed dispersal in a Prunus mahaleb population: patterns in distance and direction. Mol Ecol 16:1947–1955. doi:10.1111/j.1365-294X.2006.03126.x
Gaston KJ (2000) Global patterns in biodiversity. Nature 405:220–227. doi:10.1038/35012228
Ghazoul J (2005) Pollen and seed dispersal among dispersed plants. Biol Rev Camb Philos Soc 80:413–443. doi:10.1017/S1464793105006731
González-Varo JP, Arroyo J, Aparicio A (2009) Effects of fragmentation on pollinator assemblage, pollen limitation and seed production of Mediterranean myrtle (Myrtus communis). Biol Conserv 142:1058–1065. doi:10.1016/j.biocon.2009.01.017
Gugger PF, Ikegami M, Sork VL (2013) Influence of late Quaternary climate change on present patterns of genetic variation in valley oak, Quercus lobata. Mol Ecol 22:3598–3612. doi:10.1111/mec.12317
Henderson A, Galeano-Garces G, Bernal R (1997) Field guide to the palms of the Americas. Princeton University Press, Princeton
Hewitt G (2000) The genetic legacy of the Quaternary ice ages. Nature 405:907–913. doi:10.1038/35016000
Hijmans RJ, Cameron SE, Parra JL et al (2005) Very high resolution interpolated climate surfaces for global land areas. Int J Climatol 25:1965–1978. doi:10.1002/joc.1276
Hoffmann AA, Willi Y (2008) Detecting genetic responses to environmental change. Nat Rev Genet 9:421–432. doi:10.1038/nrg2339
Holbrook KM (2011) Home range and movement patterns of toucans: implications for seed dispersal. Biotropica 43:357–364. doi:10.1111/j.1744-7429.2010.00710.x
Huber PR, Greco SE, Thorne JH (2010) Spatial scale effects on conservation network design: trade-offs and omissions in regional versus local scale planning. Landsc Ecol 25:683–695. doi:10.1007/s10980-010-9447-4
Hughes AR, Inouye BD, Johnson MTJ et al (2008) Ecological consequences of genetic diversity. Ecol Lett 11:609–623. doi:10.1111/j.1461-0248.2008.01179.x
IPCC (2007) Climate change 2007: synthesis report. In: Core Writing Team, Pachauri RK, Reisinger A (eds) Contribution of working groups I, II and III to the Fourth Assessment Report of the Intergovernmental Panel on Climate Change. IPCC, Geneva
Jordano P, García C, Godoy JA, García-Castaño JL (2007) Differential contribution of frugivores to complex seed dispersal patterns. Proc Natl Acad Sci 104:3278–3282. doi:10.1073/pnas.0606793104
Jump AS, Marchant R, Peñuelas J (2009) Environmental change and the option value of genetic diversity. Trends Plant Sci 14:51–58. doi:10.1016/j.tplants.2008.10.002
Keller LF, Waller DM (2002) Inbreeding effects in wild populations. Trends Ecol Evol 17:230–241. doi:10.1016/S0169-5347(02)02489-8
Kramer AT, Ison JL, Ashley MV, Howe HF (2008) The Paradox of forest fragmentation genetics. Conserv Biol 22:878–885. doi:10.1111/j.1523-1739.2008.00944.x
Landguth EL, Cushman S a, Schwartz MK et al (2010) Quantifying the lag time to detect barriers in landscape genetics. Mol Ecol 19:4179–4191. doi:10.1111/j.1365-294X.2010.04808.x
Leite YLR, Costa LP, Loss AC et al (2016) Neotropical forest expansion during the last glacial period challenges refuge hypothesis. Proc Natl Acad Sci 113:201513062. doi:10.1073/pnas.1513062113
Lowe AJ, Boshier D, Ward M et al (2005) Genetic resource impacts of habitat loss and degradation; reconciling empirical evidence and predicted theory for neotropical trees. Heredity 95:255–273. doi:10.1038/sj.hdy.6800725
Markl JS, Schleuning M, Forget PM et al (2012) Meta-analysis of the effects of human disturbance on seed dispersal by animals. Conserv Biol 26:1072–1081. doi:10.1111/j.1523-1739.2012.01927.x
Miraldo A, Li S, Borregaard MK et al (2016) An Anthropocene map of genetic diversity. Science 353:1532–1535. doi:10.1126/science.aaf4381
Morante-Filho JC, Faria D, Mariano-Neto E, Rhodes J (2015) Birds in anthropogenic landscapes: the responses of ecological groups to forest loss in the Brazilian Atlantic forest. PLoS ONE 10:1–18. doi:10.1371/journal.pone.0128923
Ortego J, Riordan EC, Gugger PF, Sork VL (2012) Influence of environmental heterogeneity on genetic diversity and structure in an endemic southern Californian oak. Mol Ecol 21:3210–3223. doi:10.1111/j.1365-294X.2012.05591.x
Ortego J, Gugger PF, Sork VL (2015) Climatically stable landscapes predict patterns of genetic structure and admixture in the Californian canyon live oak. J Biogeogr 42:328–338. doi:10.1111/jbi.12419
Pacheco LF, Simonetti JA (2000) Genetic structure of a mimosid tree deprived of it seed disperser, the spider monkey. Conserv Biol 14:1766–1775. doi:10.1046/j.1523-1739.2000.99182.x
Pauls SU, Nowak C, Bálint M, Pfenninger M (2013) The impact of global climate change on genetic diversity within populations and species. Mol Ecol 22:925–946. doi:10.1111/mec.12152
Phillips SJ, Dudík M (2008) Modeling of species distributions with Maxent: new extensions and a comprehensive evaluation. Ecography 31:161–175. doi:10.1111/j.0906-7590.2008.5203.x
Pujol AB, Zhoua S, Vilasa JS, Pannella JR (2009) Reduced inbreeding depression after species range expansion. Proc Natl Acad Sci 106: 15379–15383. doi:10.1073/pnas.0902257106
Rands MRW, Adams WM, Bennun L et al (2010) Biodiversity conservation: challenges beyond 2010. Science 329:1298–1303. doi:10.1126/science.1189138
Reis MS, Fantini AC, Nodari RO, Reis A, Guerra MP, Mantovani A (2000) Management and conservation of natural populations in Atlantic rainforest: the case study of palm heart (Euterpe edulis Martius). Biotropica 32:894–902. doi:10.1111/j.1744-7429.2000.tb00627.x
Ribeiro MC, Metzger JP, Martensen AC et al (2009) The Brazilian Atlantic forest: how much is left, and how is the remaining forest distributed? Implications for conservation. Biol Conserv 142:1141–1153. doi:10.1016/j.biocon.2009.02.021
Ribeiro MC, Martensen AC, Metzger JP et al (2011) The Brazilian Atlantic forest: a shrinking biodiversity hotspot. In: Zachos FE, Habel JC (eds) Biodiversity hotspots. Springer, New York, pp 405–434
Tabarelli M, Aguiar AV, Ribeiro MC et al (2010) Prospects for biodiversity conservation in the Atlantic Forest: Lessons from aging human-modified landscapes. Biol Conserv 143:2328–2340. doi:10.1016/j.biocon.2010.02.005
Thuiller W, Lafourcade B, Engler R, Araújo MB (2009) BIOMOD—a platform for ensemble forecasting of species distributions. Ecography 32:369–373. doi:10.1111/j.1600-0587.2008.05742.x
Uriarte M, Anciães M, da Silva MTB et al (2011) Disentangling the drivers of reduced long-distance seed dispersal by birds in an experimentally fragmented landscape. Ecology 92:924–937. doi:10.1890/10-0709.1
Van Geert A, Van Rossum F, Triest L (2008) Genetic diversity in adult and seedling populations of Primula vulgaris in a fragmented agricultural landscape. Conserv Genet 9:845–853. doi:10.1007/s10592-007-9409-9
Walter RP, Cena CJ, Morgan GE, Heath DD (2012) Historical and anthropogenic factors affecting the population genetic structure of ontario’s inland lake populations of walleye (Sander vitreus). J Hered 103:831–841. doi:10.1093/jhered/ess066
Wright SJ (2003) The myriad consequences of hunting for vertebrates and plants in tropical forests. Perspect Plant Ecol Evol Syst 6:73–86. doi:10.1078/1433-8319-00043
Young A, Boyle T, Brown T (1996) The population genetic consequences of habitat fragmentation for plants. Trends Ecol Evol 11:413–418. doi:10.1016/0169-5347(96)10045-8
Zurbuchen A, Landert L, Klaiber J et al (2010) Maximum foraging ranges in solitary bees: only few individuals have the capability to cover long foraging distances. Biol Conserv 143:669–676. doi:10.1016/j.biocon.2009.12.003
Acknowledgements
This work was supported by the competitive grants from CNPq (Project No. 445353/2014-7) and CAPES (PROCAD Project No. 88881.068425/2014-01) which we gratefully acknowledge. CSC received a CNPq grant (Project No. 401258/2012-2) and a scholarship from Fundação de Amparo à Pesquisa do Estado de São Paulo (FAPESP, No. 2014/01029-5). LBM receives a fellowship from CAPES Ciências sem Fronteira (Project CSF-PAJT/CAPES No. 88881.030318/2013-01). RGC and MCR have been continuously supported by grants and scholarships from CNPq and CAPES. MCR is funded by FAPESP (Project No. 2013/50421-2).
Author Contributions
C.S.Carvalho conceptualized and performed the study, analyzed the data and wrote the paper. M.C.Ribeiro, R.G.Collevatti and L. Ballesteros-Mejia participated in the study design, analyzed the data and contributed to writing the paper. M.C.Côrtes assisted in the data analyses and contributed to writing the paper. A.S.Santos contributed to the study conception and to writing the paper.
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Carvalho, C.d., Ballesteros-Mejia, L., Ribeiro, M.C. et al. Climatic stability and contemporary human impacts affect the genetic diversity and conservation status of a tropical palm in the Atlantic Forest of Brazil. Conserv Genet 18, 467–478 (2017). https://doi.org/10.1007/s10592-016-0921-7
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DOI: https://doi.org/10.1007/s10592-016-0921-7