Mid-Pleistocene origin and phylogeographical signatures of recurrent expansion-fragmentation of a highly inbred and endangered African timber legume - 2025
African rain forest; Genetic diversity; Inbreeding; Pericopsis; Pleistocene; Range expansion
Abstract :
[en] Past climatic oscillations have influenced the genetic diversity and distribution patterns of tropical African tree species, and possibly their mating system. To explore these effects, we investigated the phylogeography of Pericopsis elata (Fabaceae), an endangered timber species with a high selfing rate and a fragmented Guineo-Congolian distribution with three gene pools: Upper Guinea (UG, west Africa), the Sangha River Interval (SRI, western Central Africa), and Congolia (C, Congo Basin). Our dated phylogeny of 51 plastomes indicates that P. elata diverged from P. angolensis, a dry woodland species, during the Mid-Pleistocene and had spread to UG by 210 000 years ago. Central African plastomes diverged 99 000 years ago but those from the SRI show more recent divergence. Nuclear microsatellites confirm the strong differentiation between the C and SRI clusters, and reveal contrasting evolutionary histories. While the C cluster exhibited moderate inbreeding and secondary selfing rate, the SRI cluster displayed a westward decay of diversity with high secondary selfing rate and strong fine-scale spatial genetic structure. Our findings suggest recurrent range expansion–fragmentation of P. elata since the Mid-Pleistocene, with a probable refugium in northern Republic of Congo, followed by a recent westward expansion into Cameroon facilitated by selfing, providing clues about the vegetation history of the SRI. The genetic peculiarities of the different gene pools must be considered in efforts to conserve and exploit this species sustainably.
Ranavat, Surabhi ; Evolutionary Biology and Ecology, Faculté des Sciences, Université Libre de Bruxelles (ULB) , Av. F.D. Roosevelt 50, 1050, Brussels ,
Sergeant, Saskia; Evolutionary Biology and Ecology, Faculté des Sciences, Université Libre de Bruxelles (ULB) , Av. F.D. Roosevelt 50, 1050, Brussels ,
Assumani, Dieu-Merci; Evolutionary Biology and Ecology, Faculté des Sciences, Université Libre de Bruxelles (ULB) , Av. F.D. Roosevelt 50, 1050, Brussels , ; Faculté de Gestion des Ressources Naturelles Renouvelables, Université de Kisangani , B.P. 2012, Av. Kitima 3, Kisangani , ; Institut National pour l’Etude et la Recherche Agronomiques (INERA – Yangambi) , Yangambi ,
Sonké, Bonaventure; University of Yaoundé I, Plant Systematic and Ecology Laboratory , Yaoundé, PO Box 047 ,
Bouka, Gaël U D; Laboratory of Biodiversity and Ecosystems and Environmental Management, Faculty of Science and Technology, Marien Ngouabi University , Brazzaville, PO Box 69 ,
Bourland, Nils; Royal Museum for Central Africa, Service of Wood Biology , 13 Leuvensesteenweg, Tervuren, 3080 ,
Andrews S. FastQC: A Quality Control Tool for High Throughput Sequence Data. 2010. http://www.bioinformatics.babraham.ac.uk/projects/fastqc
Angbonda D-MA, Monthe FK, Bourland N et al. Seed and pollen dispersal and fine-scale spatial genetic structure of a threatened tree species: Pericopsis elata (Harms) Meeuwen (Fabaceae). Tree Genetics & Genomes 2021;17:27.
Angbonda D-MA, Ilunga-Mulala CM, Bourland N et al. Inbreeding depression affects the growth of seedlings of an African timber species with a mixed mating reproductive system, Pericopsis elata (Harms) Meeuwen. Heredity 2024;133:238–48. https://doi.org/10.1038/s41437-024-00709-x
Biwolé AB, Dainou K, Fayolle A et al. Light response of seedlings of a central African timber tree species, Lophira alata (Ochnaceae), and the definition of light requirements. Biotropica 2015;47:681–8. https://doi.org/10.1111/btp.12258
Boom AF, Migliore J, Kaymak E et al. Plastid introgression and evolution of African miombo woodlands: new insights from the plastome‐based phylogeny of Brachystegia trees. Journal of Biogeography 2021;48:933–46. https://doi.org/10.1111/jbi.14051
Bostoen K, Clist B, Doumenge C et al. Middle to late Holocene paleoclimatic change and the early Bantu expansion in the rain forests of Western Central Africa. Current Anthropology 2015;56:354–84. https://doi.org/10.1086/681436
Bouckaert R, Vaughan TG, Barido-Sottani J et al. BEAST 2.5: an advanced software platform for Bayesian evolutionary analysis. PLoS Computational Biology 2019;15:e1006650. https://doi.org/10.1371/journal.pcbi.1006650
Bourland N, Kouadio YL, Fétéké F et al. Ecology and management of Pericopsis elata (Harms) Meeuwen (Fabaceae) populations: a review. Biotechnology, Agronomy, Society and Environment 2012;16:486–98.
Bourland N, Cerisier F, Daïnou K et al. How tightly linked are Pericopsis elata (Fabaceae) patches to anthropogenic disturbances in Southeastern Cameroon? Forests 2015;6:293–310. https://doi.org/10.3390/f6020293
Brncic TM, Willis KJ, Harris DJ et al. Fire and climate change impacts on lowland forest composition in Northern Congo during the last 2580 years from palaeoecological analyses of a seasonally flooded swamp. The Holocene 2009;19:79–89. https://doi.org/10.1177/0959683608098954
Bürkli A, Sieber N, Seppälä K et al. Comparing direct and indirect selfing rate estimates: when are population-structure estimates reliable? Heredity 2017;118:525–33. https://doi.org/10.1038/hdy.2017.1
Chen S, Zhou Y, Chen Y et al. fastp: an ultra-fast all-in-one FASTQ preprocessor. Bioinformatics 2018;34:i884–90. https://doi.org/10.1093/bioinformatics/bty560
Choi I-S, Cardoso D, De Queiroz LP et al. Highly resolved Papilionoid legume phylogeny based on plastid phylogenomics. Frontiers in Plant Science 2022;13:823190. https://doi.org/10.3389/fpls.2022.823190
Couvreur TLP, Dauby G, Blach‐Overgaard A et al. Tectonics, climate and the diversification of the tropical African terrestrial flora and fauna. Biological Reviews 2021;96:16–51.
Danecek P, Bonfield JK, Liddle J et al. Twelve years of SAMtools and BCFtools. GigaScience 2021;10:giab008. https://doi.org/10.1093/gigascience/giab008
Dauby G, Duminil J, Heuertz M et al. Congruent phylogeographical patterns of eight tree species in Atlantic Central Africa provide insights into the past dynamics of forest cover. Molecular Ecology 2014;23:2299–312. https://doi.org/10.1111/mec.12724
David P, Pujol B, Viard F et al. Reliable selfing rate estimates from imperfect population genetic data. Molecular Ecology 2007;16:2474–87. https://doi.org/10.1111/j.1365-294X.2007.03330.x
De La Estrella M, Cervantes S, Janssens SB et al. The impact of rainforest area reduction in the Guineo‐Congolian region on the tempo of diversification and habitat shifts in the Berlinia clade (Leguminosae). Journal of Biogeography 2020;47:2728–40. https://doi.org/10.1111/jbi.13971
Demenou BB, Migliore J, Heuertz M et al. Plastome phylogeography in two African rain forest legume trees reveals that Dahomey Gap populations originate from the Cameroon Volcanic Line. Molecular Phylogenetics and Evolution 2020;150:106854. https://doi.org/10.1016/j.ympev.2020.106854
Dick CW, Hardy OJ, Jones FA et al. Spatial scales of pollen and seed-mediated gene flow in tropical rain forest trees. Tropical Plant Biology 2008;1:20–33. https://doi.org/10.1007/s12042-007-9006-6
Doucet J-L. L’alliance délicate De la Gestion Forestière et de la Biodiversité dans les Forêts du Centre du Gabon. Ph.D. Thesis, University of Liége, 2003.
Doucet J-L, Daïnou K, Ligot G et al. Enrichment of Central African logged forests with high-value tree species: testing a new approach to regenerating degraded forests. International Journal of Biodiversity Science, Ecosystem Services & Management 2016;12:83–95. https://doi.org/10.1080/21513732.2016.1168868
Doyle JJ, Doyle JL. Isolation of plant DNA from fresh tissue. Focus 1990;12:13–5.
Dupont LM, Donner B, Schneider R et al. Mid-Pleistocene environmental change in tropical Africa began as early as 1.05 Ma. Geology 2001;29:195–8. https://doi.org/10.1130/0091-7613(2001)0290195:mpecit2.0.co;2
Elenga H, Maley J, Vincens A et al. Palaeoenvironments, Palaeoclimates and Landscape Development in Atlantic Equatorial Africa: A Review of Key Sites Covering the last 25 Kyrs. Past Climate Variability through Europe and Africa. Dordrecht: Springer, 2004, 181–98.
Gillet J-F, Doucet J-L. A commented checklist of woody plants in the Northern Republic of Congo. Plant Ecology and Evolution 2012;145:258–71. https://doi.org/10.5091/plecevo.2012.648
Giresse P, Maley J, Chepstow-Lusty A. Understanding the 2500 yr BP rainforest crisis in West and Central Africa in the framework of the Late Holocene: Pluridisciplinary analysis and multi-archive reconstruction. Global and Planetary Change 2020;192:103257.
Gorel A, Hardy OJ, Dauby G et al. Climatic niche lability but growth form conservatism in the African woody flora. Ecology Letters 2022;25:1164–76. https://doi.org/10.1111/ele.13985
Grollemund R, Branford S, Bostoen K et al. Bantu expansion shows that habitat alters the route and pace of human dispersals. Proceedings of the National Academy of Sciences of the United States of America 2015;112:13296–301. https://doi.org/10.1073/pnas.1503793112
Guidosse Q, du Jardin P, White L et al. Gabon’s green gold: a bibliographical review of thirty years of research on okoumé (Aucoumea klaineana Pierre). Biotechnology, Agronomy, Society and Environment 2022;26:30–42.
Hardy OJ. Population genetics of autopolyploids under a mixed mating model and the estimation of selfing rate. Molecular Ecology Resources 2016;16:103–17. https://doi.org/10.1111/1755-0998.12431
Hardy OJ, Vekemans X. SPAGeDi. a versatile computer program to analyse spatial genetic structure at the individual or population levels. Molecular Ecology Notes 2002;2:618–20.
Hardy OJ, Charbonnel N, Fréville H et al. Microsatellite allele sizes: a simple test to assess their significance on genetic differentiation. Genetics 2003;163:1467–82. https://doi.org/10.1093/genetics/163.4.1467
Hardy OJ, Born C, Budde K et al. Comparative phylogeography of African rain forest trees: a review of genetic signatures of vegetation history in the Guineo-Congolian region. Comptes Rendus. Géoscience 2013;345:284–96. https://doi.org/10.1016/j.crte.2013.05.001
Helmstetter AJ, Béthune K, Kamdem NG et al. Individualistic evolutionary responses of Central African rain forest plants to Pleistocene climatic fluctuations. Proceedings of the National Academy of Sciences of the United States of America 2020;117:32509–18. https://doi.org/10.1073/pnas.2001018117
Hills R. Pericopsis elata. The IUCN Red List of Threatened Species. 2020:e.T33191A67802601. https://dx.doi.org/10.2305/IUCN.UK.2020-3.RLTS.T33191A67802601.en
Hubau W, Van Den Bulcke J, Van Acker J et al. Charcoal‐inferred Holocene fire and vegetation history linked to drought periods in the Democratic Republic of Congo. Global Change Biology 2015;21:2296–308. https://doi.org/10.1111/gcb.12844
Koenen EJM, Ojeda DI, Bakker FT et al. The origin of the legumes is a complex paleopolyploid hylogenomic tangle closely associated with the Cretaceous–Paleogene (K–Pg) mass extinction event. Systematic Biology 2021;70:508–26. https://doi.org/10.1093/sysbio/syaa041
Koski MH, Layman NC, Prior CJ et al. Selfing ability and drift load evolve with range expansion. Evolution Letters 2019;3:500–12. https://doi.org/10.1002/evl3.136
Kouadio YL. Mesures Sylvicoles en vue d’améliorer la Gestion des Populations d’essences Forestières Commerciales de l’Est du Cameroun. Ph.D. Thesis, University of Liége, 2009.
Kozlov AM, Darriba D, Flouri T et al. RAxML-NG: a fast, scalable and user-friendly tool for maximum likelihood phylogenetic inference. Bioinformatics 2019;35:4453–5. https://doi.org/10.1093/bioinformatics/btz305
Leigh JW, Bryant D. Full‐feature software for haplotype network construction. Methods in Ecology and Evolution 2015;6:1110–6.
Li H. Aligning Sequence Reads, Clone Sequences and Assembly Contigs with BWA-MEM. 2013, arXiv:1303.3997v2 [q-bio.GN].
Loiselle BA, Sork VL, Nason J et al. Spatial genetic structure of a tropical understory shrub, Psychotria officinalis (Rubiaceae). American Journal of Botany 1995;82:1420–5. https://doi.org/10.1002/j.1537-2197.1995.tb12679.x
Maley J, Doumenge C, Giresse P et al. Late Holocene forest contraction and fragmentation in central Africa. Quaternary Research 2018;89:43–59. https://doi.org/10.1017/qua.2017.97
Malhi Y, Adu-Bredu S, Asare RA et al. African rainforests: past, present and future. Philosophical Transactions of the Royal Society of London, Series B: Biological Sciences 2013;368:20120312. https://doi.org/10.1098/rstb.2012.0312
Matvijev K, Dellicour S, Kaymak E et al. Spatially explicit phylogeographical reconstruction sheds light on the history of the forest cover in the Congo Basin. Journal of Biogeography 2022;49:2256–68. https://doi.org/10.1111/jbi.14507
Micheneau C, Dauby G, Bourland N et al. Development and characterization of microsatellite loci in Pericopsis elata (Fabaceae) using a cost-efficient approach. American Journal of Botany 2011;98:e268–70. https://doi.org/10.3732/ajb.1100070
Migliore J, Lézine A-M, Hardy OJ. The recent colonization history of the most widespread Podocarpus tree species in Afromontane forests. Annals of Botany 2020;126:73–83. https://doi.org/10.1093/aob/mcaa049
Miller CS, Gosling WD. Quaternary forest associations in lowland tropical West Africa. Quaternary Science Reviews 2014;84:7–25. https://doi.org/10.1016/j.quascirev.2013.10.027
Morin-Rivat J, Fayolle A, Favier C et al. Present-day central African forest is a legacy of the 19th century human history. eLife 2017;6:e20343. https://doi.org/10.7554/eLife.20343
Paradis E, Schliep K. Ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics 2019;35:526–8. https://doi.org/10.1093/bioinformatics/bty633
Pennell MW, Eastman JM, Slater GJ et al. geiger v2.0: an expanded suite of methods for fitting macroevolutionary models to phylogenetic trees. Bioinformatics 2014;30:2216–8. https://doi.org/10.1093/bioinformatics/btu181
Pieters A. Natural Regeneration in the Equatorial Forest of the Yangambi Region, Applied to Afrormosia elata Harms. Leuven, 1994.
Piñeiro R, Hardy OJ, Tovar C et al. Contrasting genetic signal of recolonization after rainforest fragmentation in African trees with different dispersal abilities. Proceedings of the National Academy of Sciences of the United States of America 2021;118:e2013979118. https://doi.org/10.1073/pnas.2013979118
Pritchard JK, Stephens M, Donnelly P. Inference of population structure using multilocus genotype data. Genetics 2000;155:945–59. https://doi.org/10.1093/genetics/155.2.945
QGIS.org, 2023, QGIS Geographic Information System. Open Source Geospatial Foundation Project. http://qgis.org
Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods in Ecology and Evolution 2012;3:217–23. https://doi.org/10.1111/j.2041-210x.2011.00169.x
Rstudio Team. RStudio: Integrated Development for R. 2020. http://www.rstudio.com/
Schmitt DN, Lupo KD, Amaye GT et al. New Holocene radiocarbon dates from the heart of the Sangha River Interval, Southwestern Central African Republic. Journal of African Archaeology 2023;21:81–91. https://doi.org/10.1163/21915784-bja10025
Seidensticker D. Pikunda-Munda and Batalimo-Maluba. African Archaeological Review 2024;41:317–44. https://doi.org/10.1007/s10437-024-09576-7
Smith SA, Donoghue MJ. Rates of molecular evolution are linked to life history in flowering plants. Science 2008;322:86–9. https://doi.org/10.1126/science.1163197
UNEP-WCMC. Report on Species/Country Combinations Selected for Review by the Plants Committee Following CoP17. Cambridge: UNEP World Conservation Monitoring Centre, 2018.
Vanden Abeele S, Janssens SB, Piñeiro R et al. Evidence of past forest fragmentation in the Congo Basin from the phylogeography of a shade-tolerant tree with limited seed dispersal: Scorodophloeus zenkeri (Fabaceae, Detarioideae). BMC Ecology and Evolution 2021;21:50. https://doi.org/10.1186/s12862-021-01781-1
Vekemans X, Hardy OJ. New insights from fine‐scale spatial genetic structure analyses in plant populations. Molecular Ecology 2004;13:921–35. https://doi.org/10.1046/j.1365-294x.2004.02076.x
Vivien J, Faure J-J. Arbres Des Forêts Denses d’Afrique Centrale. Paris: Ministére des relations extérieures, cooperation et développement, Agence de cooperation culturelle et technique, 1985, 414–5.
White F. The Guineo-Congolian region and its relationships to other Phytochoria. Bulletin du Jardin botanique national de Belgique/Bulletin van de National Plantentuin van België 1979;49:11–55.
White F. The Vegetation of Africa; a Descriptive Memoir to Accompany the UNESCO/AETFAT/UNSO Vegetation Map of Africa. Paris: UNESCO, 1983.
Winn AA, Elle E, Kalisz S et al. Analysis of inbreeding depression in mixed-mating plants provides evidence for selective interference and stable mixed mating. Evolution 2011;65:3339–59. https://doi.org/10.1111/j.1558-5646.2011.01462.x
Wright ES. DECIPHER: harnessing local sequence context to improve protein multiple sequence alignment. BMC Bioinformatics 2015;16:1–14.
Wright ES. RNAconTest: comparing tools for noncoding RNA multiple sequence alignment based on structural consistency. RNA 2020;26:531–40. https://doi.org/10.1261/rna.073015.119
Zébazé D, Gorel A, Gillet J-F et al. Natural regeneration in tropical forests along a disturbance gradient in South-East Cameroon. Forest Ecology and Management 2023;547:121402. https://doi.org/10.1016/j.foreco.2023.121402
