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Afro-alpine flagships revisited II: elucidating the evolutionary relationships and species boundaries in the giant senecios (Dendrosenecio, Asteraceae)

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Abstract

Alpine plant radiations are common across all major mountain systems of the world, and have been regarded as the main explanation for the species diversity found within these areas. To study the mechanisms behind the origin of this diversity, it is necessary to determine phylogenetic relationships and species boundaries in radiating alpine groups. The genus Dendrosenecio (Asteraceae) is an iconic example of a tropical-alpine plant radiation in the East African high mountains. To this date, limited sampling of molecular markers has resulted in insufficient phylogenetic resolution and infrageneric classification, hindering a comprehensive understanding of the drivers of diversification. Here, we used Hyb-Seq and the Compositae1061 probe set to generate targeted nuclear and off-target plastid DNA data for 42 samples representing all currently accepted 11 species. We combined coalescent methods and paralogy analysis to infer phylogenetic relationships, estimate divergence times and evaluate species boundaries. Lineage differentiation in Dendrosenecio seems to have occurred between the Late Miocene and the Pleistocene, starting when the first high elevation habitats became available in East Africa. We retrieved four major clades corresponding to four geographically distant mountain groups, testifying the importance of allopatric speciation in the early diversification of the group. Cytonuclear discordance suggested the occurrence of historical hybridization following occasional long-distance dispersal between mountain groups. The species delimitation analysis favored 10 species, but only five were fully supported, suggesting that population-level studies addressing processes such as ecological speciation and hybridization after secondary contact are needed to determine the current diversity found in the genus.

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Availability of data and material

Raw reads that were generated for the current study are available under NCBI SRA BioProject PRJNA729901 (see Supplementary Information Table S1 for accession numbers).

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Acknowledgements

Collection of plant material was carried out in several field expeditions to Kenya, Uganda and Tanzania, sponsored by the Norwegian Programme for Development, Research and Higher Education (NUFU): 2007/1058: AFROALP-II—Afroalpine sky islands: genetic versus taxonomic biodiversity, climate change, and conservation to Sileshi Nemomissa and Christian Brochmann, and by the Research Council of Norway 274607: SpeciationClock—How fast does the 'speciation clock' tick in selfing versus outcrossing lineages? to C. Brochmann. Sileshi Nemomissa, Geoffrey Mwachala, Pantaleo Munishi and Felly Tusiime are acknowledged for their involvement in these projects. We thank the Uganda National Council for Science and Technology, Uganda Wildlife Authority, Tanzanian Commission for Science and Technology, Tanzania National Parks Authority, and National Museums of Kenya for permission to conduct fieldwork, and the staff at the ETH, O, EA, MHU, SUA and NHT herbaria for curation of our specimens. We also thank Leopoldo Medina and the staff at the MA herbarium for providing outgroup samples. Sequencing and data analysis was supported by the Czech Science Foundation GAČR project No. 20-10878S: Tropical-alpine plant radiations: an intercontinental comparison of timing and the role of allopatry, hybridization and niche differentiation to Roswitha Schmickl and Filip Kolář. The study was also supported by long-term research development project No. RVO 67985939 of the Czech Academy of Sciences. Computational resources were supplied by the project "e-Infrastruktura CZ" (e-INFRA LM2018140) provided within the program Projects of Large Research, Development and Innovations Infrastructures. The authors thank Lenka Flašková, Petra Caklová and Jiřina Josefiová for laboratory assistance; Roman Ufimov, Tomaš Fer, Soňa Píšová for help with data analysis; and LabAllience members, Jeff Doyle and the two anonymous reviewers for their useful comments.

Funding

This study was supported by the Czech Science Foundation GAČR project No. 20-10878S; the long-term research development project No. RVO 67985939 of the Czech Academy of Sciences; the Norwegian Programme for Development, Research and Higher Education (NUFU) project No. 2007/1058; and by the Research Council of Norway project No. 274607.

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RS, JMG, AG, FK and CB conceived and designed the research. AG, DC, LG, AZ, GE, CB and FK performed the fieldwork and curated the plant material. LS performed DNA extractions and library preparation. JMG processed the data, performed phylogenetic and species delimitation analyses and led the manuscript preparation together with AG. MK performed the divergence times analysis. RS supervised the analyses and the manuscript preparation. CB, FK and RS facilitated the project by logistic and infrastructure support. All authors contributed to the text.

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Correspondence to Abel Gizaw or Juan Manuel Gorospe.

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Gizaw, A., Gorospe, J.M., Kandziora, M. et al. Afro-alpine flagships revisited II: elucidating the evolutionary relationships and species boundaries in the giant senecios (Dendrosenecio, Asteraceae). Alp Botany 132, 89–105 (2022). https://doi.org/10.1007/s00035-021-00268-5

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