[en] Background and aims – The isolation of populations inside forest refugia during past climate changes has widely been hypothesized as a major driver of tropical plant diversity. Environmental conditions can also influence patterns of diversity by driving divergent selection leading to local adaptation and, potentially, ecological speciation. Genetic and phylogenetic approaches are frequently used to study the diversification of African tree clades. However, the environmental space occupied by closely related species or intra-specific gene pools is barely quantified, though needed to properly test hypotheses on diversification processes.
Methods – Using species distribution models, we determined the bioclimatic constraints on the distribution of closely related species and intra-specific gene pools. Our study model, Erythrophleum (Fabaceae - Caesalpinioideae), is a tropical tree genus widespread across Africa, and vastly investigated for genetics. Here, we combined the available phylogenetic data with information on niche divergence to explore the role of ecology into diversification at the species and gene pool levels.
Key results – Ecological speciation through climate has probably played a key role in the evolution of the Erythrophleum species. The differential climatic niche of the species indicated adaptive divergence along rainfall gradients, that have probably been boosted by past climate fluctuations. At the gene pool level, past climate changes during the Pleistocene have shaped genetic diversity, though within Erythrophleum suaveolens, adaptive divergence also occurred.
Conclusions – We believe that ecological speciation is a key mechanism of diversification for tropical African tree species, since such climatic niche partition exist among many other genera. Modeling the environmental niche of closely related taxa, and testing for niche differentiation, combined with divergence dates offered new insights on the process of diversification.
Disciplines :
Sciences de l’environnement & écologie
Auteur, co-auteur :
Gorel, Anaïs ; Université de Liège - ULiège > Ingénierie des biosystèmes (Biose) > Gestion des ressources forestières et des milieux naturels
Duminil, Jérôme; Evolutionary Biology and Ecology, CP160/12, Faculté des Sciences, Université Libre de Bruxelles, 50 Av. F. Roosevelt, 1050 Brussels, Belgium
Doucet, Jean-Louis ; Université de Liège - ULiège > Ingénierie des biosystèmes (Biose) > Laboratoire de Foresterie des régions trop. et subtropicales
Fayolle, Adeline ; Université de Liège - ULiège > Ingénierie des biosystèmes (Biose) > Gestion des ressources forestières et des milieux naturels
Langue du document :
Anglais
Titre :
Ecological niche divergence associated with species and populations differentiation in Erythrophleum (Fabaceae, Caesalpinioideae)
Allouche O., Tsoar A., Kadmon R. (2006) Assessing the accuracy of species distribution models: prevalence, kappa and the true skill statistic (TSS). Journal of Applied Ecology 43: 1223-1232. https://doi.org/10.1111/j.1365-2664.2006.01214.x
Anderson R.P. (2003) Real vs. artefactual absences in species distributions: tests for Oryzomys albigularis (Rodentia: Muridae) in Venezuela. Journal of Biogeography 30: 591-605. https://doi. org/10.1046/j.1365-2699.2003.00867.x
Baldwin R.A. (2009) Use of Maximum Entropy Modeling in Wildlife Research. Entropy 11: 854-866. https://doi.org/https://doi. org/10.3390/e11040854
Bivand R., Rundel C. (2014) rgeos: Interface to Geometry Engine -Open Source (‘GEOS’). Available from: https://rdrr.io/cran/rgeos/[accessed 4 Feb. 2019].
Blach-Overgaard A., Svenning J.-C., Dransfield J., Greve M., Balslev H. (2010) Determinants of palm species distributions across Africa: the relative roles of climate, non-climatic environmental factors, and spatial constraints. Ecography 33: 380-391. https://doi.org/10.1111/j.1600-0587.2010.06273.x
Blair M.E., Sterling E.J., Dusch M., Raxworthy C.J., Pearson R.G. (2013) Ecological divergence and speciation between lemur (Eulemur) sister species in Madagascar. Journal of Evolutionary Biology 26: 1790-1801. https://doi.org/10.1111/jeb.12179
Bongers F., Poorter L., Van Rompaey R.S.A.R., Parren M.P.E. (1999) Distribution of twelve moist forest canopy tree species in Liberia and Côte d’Ivoire: response curves to a climatic gradient. Journal of Vegetation Science 10: 371-382. https://doi. org/10.2307/3237066
Couvreur T.L.P., Forest F., Baker W.J. (2011) Origin and global diversification patterns of tropical rain forests: inferences from a complete genus-level phylogeny of palms. BMC Biology 9: 44. https://doi.org/10.1186/1741-7007-9-44
Damasceno R., Strangas M.L., Carnaval A.C., Rodrigues M.T., Moritz C. (2014) Revisiting the vanishing refuge model of diversification. Frontiers in Genetics 5: 1-12. https://doi. org/10.3389/fgene.2014.00353
Dauby G., Duminil J., Heuertz M., Koffi G.K., Stévart T., Hardy O.J. (2014) Congruent phylogeographical patterns of eight tree species in Atlantic Central Africa provide insights into the past dynamics of forest cover. Molecular Ecology 23: 2299-2312. https://doi.org/10.1111/mec.12724
Deblauwe V., Droissart V., Bose R., Sonké B., Blach-Overgaard A., Svenning J.-C., Wieringa J.J., Ramesh B.R., Stévart T., Couvreur T.L.P. (2016) Remotely sensed temperature and precipitation data improve species distribution modelling in the tropics: Remotely sensed climate data for tropical species distribution models. Global Ecology and Biogeography 25: 443-454. https://doi.org/10.1111/geb.12426
Donkpegan A.S.L. (2017) Histoire évolutive du complexe Afzelia Smith (Leguminosae -Caesalpinioideae) dans les écosystèmes forestiers et savanicoles en Afrique tropicale. PhD Thesis, University of Liège, Liège, Belgium.
Donoghue M.J., Edwards E.J. (2014) Biome shifts and niche evolution in plants. Annual Review of Ecology, Evolution, and Systematics 45: 547-572. https://doi.org/10.1146/annurev-ecolsys-120213-091905
Dransfield J., Uhl N.W. (2008) Genera palmarum: the evolution and classification of palms. Kew, Royal Botanic Gardens.
Duminil J., Heuertz M., Doucet J.-L., Bourland N., Cruaud C., Gavory F., Doumenge C., Navascués M., Hardy O.J. (2010) Cp-DNA-based species identification and phylogeography: application to African tropical tree species. Molecular Ecology 19: 5469-5483. https://doi.org/10.1111/j.1365-294X.2010.04917.x
Duminil J., Brown R.P., Ewédjè E.-E.B., Mardulyn P., Doucet J.-L., Hardy O.J. (2013) Large-scale pattern of genetic differentiation within African rainforest trees: insights on the roles of ecological gradients and past climate changes on the evolution of Erythrophleum spp (Fabaceae). BMC Evolutionary Biology 13: 195. https://doi.org/10.1186/1471-2148-13-195
Duminil J., Mona S., Mardulyn P., Doumenge C., Walmacq F., Doucet J.-L., Hardy O.J. (2015) Late Pleistocene molecular dating of past population fragmentation and demographic changes in African rain forest tree species supports the forest refuge hypothesis. Journal of Biogeography 42: 1443-1454. https://doi. org/10.1111/jbi.12510
Engelbrecht B.M.J., Comita L.S., Condit R., Kursar T.A., Tyree M.T., Turner B.L., Hubbell S.P. (2007) Drought sensitivity shapes species distribution patterns in tropical forests. Nature 447: 80-82. https://doi.org/10.1038/nature05747
Fayolle A., Swaine M.D., Bastin J.-F., Bourland N., Comiskey J.A., Dauby G., Doucet J.-L., Gillet J.-F., Gourlet-Fleury S., Hardy O.J., Kirunda B., Kouamé F.N., Plumptre A.J. (2014) Patterns of tree species composition across tropical African forests. Journal of Biogeography 41: 2320-2331. https://doi.org/10.1111/jbi.12382
Fayolle A., Swaine M.D., Aleman J, et al. (2019) A sharp floristic discontinuity revealed by the biogeographic regionalization of African savannas. Journal of Biogeography 46: 454-465. https://doi.org/10.1111/jbi.13475
Gaviria J., Turner B.L., Engelbrecht B.M.J. (2017) Drivers of tree species distribution across a tropical rainfall gradient. Ecosphere 8: e01712. https://doi.org/10.1002/ecs2.1712
Gerz M., Guillermo Bueno C., Ozinga W.A., Zobel M., Moora M. (2018) Niche differentiation and expansion of plant species are associated with mycorrhizal symbiosis. Journal of Ecology 106: 254-264. https://doi.org/10.1111/1365-2745.12873
Gonmadje C.F., Doumenge C., Sunderland T.C.H., Balinga M.P.B., Sonké B. (2012) Analyse phytogéographique des forêts d’Afrique Centrale: le cas du massif de Ngovayang (Cameroun). Plant Ecology and Evolution 145: 152-164. https://doi. org/10.5091/plecevo.2012.573
Gorel A-P., Fayolle A., Doucet J-L. (2015) Écologie et gestion des espèces multi-usages du genre Erythrophleum (Fabaceae-Caesalpinioideae) en Afrique (synthèse bibliographique). Biotechnologie, Agronomie, Société et Environnement 19: 415-429.
Graham C.H., Ron S.R., Santos J.C., Schneider C.J., Moritz C. (2004) Integrating phylogenetics and environmental niche models to explore speciation mechanisms in dendrobatid frogs. Evolution 58: 1781-1794. https://doi.org/10.1554/03-274
Guisan A., Thuiller W. (2005) Predicting species distribution: offering more than simple habitat models. Ecology Letter 8: 993-1009. https://doi.org/10.1111/j.1461-0248.2005.00792.x
Hanley J.A., McNeil B.J. (1982) The meaning and use of the area under a receiver operating characteristic (ROC) curve. Radiology 143: 29-36. https://doi.org/10.1148/radiology. 143.1.7063747
Hardy O.J., Born C., Budde K., et al. (2013) Comparative phylogeography of African rain forest trees: A review of genetic signatures of vegetation history in the Guineo-Congolian region. Comptes Rendus Geoscience 345: 284-296. https://doi. org/10.1016/j.crte.2013.05.001
Heibl C., Calenge C. (2011) phyloclim: Integrating phylogenetics and climatic niche modelling. R Package. Available from: https://rdrr.io/cran/phyloclim/[accessed 20 Sep. 2010].
Hijmans R.J., Cameron S.E., Parra J.L., Jones P.G., Jarvis A. (2005) Very high resolution interpolated climate surfaces for global land areas. International Journal of Climatology 25: 1965-1978. https://doi.org/10.1002/joc.1276
Holstein N., Renner S.S. (2011) A dated phylogeny and collection records reveal repeated biome shifts in the African genus Coccinia (Cucurbitaceae). BMC evolutionary biology 11: 28. https://doi.org/10.1186/1471-2148-11-28
Knouft J.H., Losos J.B., Glor R.E., Kolbe J.J. (2006) Phylogenetic analysis of the evolution of the niche in lizards of the Anolis sagrei group. Ecology 87: S29-S38. https://doi.org/10.1890/0012-9658(2006)87[29:PAOTEO]2.0.CO;2
Linder H.P. (2014) The evolution of African plant diversity. Frontiers in Ecology and Evolution 2: 38. https://doi.org/10.3389/fevo.2014.00038
Lönnberg E. (1929) The development and distribution of the African fauna in connection with and depending upon climatic changes. Arkiv för zoologi 21A: 1-33.
Losos J.B., Leal M., Glor R.E., et al. (2003) Niche lability in the evolution of a Caribbean lizard community. Nature 424: 542-545. https://doi.org/10.1038/nature01814
Maharjan S.K., Poorter L., Holmgren M., Bongers F., Wieringa J.J., Hawthorne W.D. (2011) Plant functional traits and the distribution of West African rain forest trees along the rainfall gradient: functional taits affect species distribution. Biotropica 43: 552-561. https://doi.org/10.1111/j.1744-7429.2010.00747.x
Maley J. (1996) The African rain forest-main characteristics of changes in vegetation and climate from the Upper Cretaceous to the Quaternary. Proceedings of the Royal society of Edinburgh section B 104: 31-73. https://doi.org/10.1017/S0269727000006114
Markesteijn L., Poorter L. (2009) Seedling root morphology and biomass allocation of 62 tropical tree species in relation to drought-and shade-tolerance. Journal of Ecology 97: 311-325. https://doi.org/10.1111/j.1365-2745.2008.01466.x
Mayr E., O’Hara R.J. (1986) The biogeographic evidence supporting the Pleistocene forest refuge hypothesis. Evolution 40: 55-67. https://doi.org/10.2307/2408603
Muscarella R., Galante P.J., Soley-Guardia M., Boria R.A., Kass J.M., Uriarte M., Anderson R.P. (2014) ENMeval: An R package for conducting spatially independent evaluations and estimating optimal model complexity for Maxent ecological niche models. Methods in Ecology and Evolution 5: 1198-1205. https://doi.org/10.1111/2041-210X.12261
Nakazato T., Warren D.L., Moyle L.C. (2010) Ecological and geographic modes of species divergence in wild tomatoes. American Journal of Botany 97: 680-693. https://doi.org/10.3732/ajb.0900216
Nosil P. (2012) Ecological Speciation. Oxford, Oxford University Press. https://doi.org/10.1093/acprof:oso bl/9780199587100.001.0001
Peterson A.T. (2011) Ecological niche conservatism: a time-structured review of evidence. Journal of Biogeography 38: 817-827. https://doi.org/10.1111/j.1365-2699.2010.02456.x
Philippon N., Cornu G., Monteil L., Gond V., Moron V., Pergaud J., Sèze G., Bigot S., Camberlin P., Doumenge C., Fayolle A., Ngomanda A. (accepted 2018) The light-deficient climates of Western Central African evergreen forests. Environmental Research Letters. https://doi.org/10.1088/1748-9326/aaf5d8
Phillips S.J., Anderson R.P., Schapire R.E. (2006) Maximum entropy modeling of species geographic distributions. Ecological Modelling 190: 231-259. https://doi.org/10.1016/j.ecolmodel. 2005.03.026
R Core Team (2015) R: A language and environment for statistical computing. Vienna, Austria, R Foundation for Statistical Computing. Available from: https://www.R-project.org/[accessed 15 Dec. 2015].
Rolland J., Salamin N. (2016) Niche width impacts vertebrate diversification. Global Ecology and Biogeography 25: 1252-1263. https://doi.org/10.1111/geb.12482
Rundell R.J., Price T.D. (2009) Adaptive radiation, nonadaptive radiation, ecological speciation and nonecological speciation. Trends in Ecology & Evolution 24: 394-399. https://doi. org/10.1016/j.tree.2009.02.007
Schnitzler J., Graham C.H., Dormann C.F., Schiffers K., Linder H.P. (2012) Climatic niche evolution and species diversification in the Cape flora, South Africa. Journal of Biogeography 39: 2201-2211. https://doi.org/10.1111/jbi.12028
Schoener T.W. (1968) The Anolis lizards of Bimini: resource partitioning in a complex fauna. Ecology 49: 704-726. https://doi. org/10.2307/1935534
Sexton J.P., Montiel J., Shay J.E., Stephens M.R., Slatyer R.A. (2017) Evolution of Ecological Niche Breadth. Annual Review of Ecology, Evolution, and Systematics 48: 183-206. https://doi.org/10.1146/annurev-ecolsys-110316-023003
Simões M., Breitkreuz L., Alvarado M., et al. (2016) The evolving theory of evolutionary radiations. Trends in Ecology & Evolution 31: 27-34. https://doi.org/10.1016/j.tree.2015.10.007
Sosef M.S.M. (1994) Refuge begonias: taxonomy, phylogeny, and historical biogeography of Begonia Sect. Loasibegonia and Sect. Scutobegonia in Relation to Glacial Rain Forest Refuges in Africa. Wageningen Agricultural University Papers, Studies in Begoniaceae 5. Wageningen, Wageningen Agricultural University.
Sterck F., Markesteijn L., Toledo M., Schieving F., Poorter L. (2014) Sapling performance along resource gradients drives tree species distributions within and across tropical forests. Ecology 95: 2514-2525. https://doi.org/10.1890/13-2377.1
Suchel J.B. (1990) Les modalités du passage du régime climatique boréal au régime climatique austral dans le sud-ouest camerounais. Cahiers du Centre de Recherche de Climatologie 13: 63-76.
Swaine M.D. (1996) Rainfall and soil fertility as factors limiting forest species distributions in Ghana. Journal of Ecology 84: 419-428. https://doi.org/10.2307/2261203
Tosso D.F. (2018) Evolution et adaptation fonctionnelle des arbres tropicaux: le cas du genre Guibourtia Benn. PhD Thesis, University of Liège, Liège, Belgium.
Vanzolini P.E., Williams E.E. (1981) The vanishing refuge: a mechanism for ecogeographic speciation. Papéis Avulsos de Zoologia 34: 251-255.
Warren D.L., Glor R.E., Turelli M. (2008) Environmental niche equivalency versus conservatism: quantitative approaches to niche evolution. Evolution 62: 2868-2883. https://doi. org/10.1111/j.1558-5646.2008.00482.x
Warren D.L., Seifert S.N. (2011) Ecological niche modeling in Maxent: the importance of model complexity and the performance of model selection criteria. Ecological Applications 21: 335-342. https://doi.org/10.1890/10-1171.1
White F. (1978) The taxonomy, ecology and chorology of African Ebenaceae I. The Guineo-Congolian species. Bulletin du Jardin botanique national de Belgique 48: 245-358. https://doi. org/10.2307/3667933
White F. (1983) The vegetation of Africa, a descriptive memoir to accompany the UNESCO/AETFAT/UNSO vegetation map of Africa. Paris, UNESCO.
Zachos J., Pagani M., Sloan L., Thomas E., Billups K. (2001) Trends, rhythms, and aberrations in global climate 65 Ma to present. Science 292: 686-693. https://doi.org/10.1126/science. 1059412
