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Traits related to efficient acquisition and use of phosphorus promote diversification in Proteaceae in phosphorus‐impoverished landscapes

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Abstract

Background and aims

Plant species richness increases with declining soil phosphorus (P) availability, especially for Proteaceae in old infertile landscapes. This difference in richness might be attributed to faster diversification in lineages adapted to P-impoverished soils, i.e. species that possess specialised P-acquisition strategies, and have lower leaf P concentration ([P]) and higher seed [P]. Alternatively, a longer time for species accumulation might contribute to high species richness in low-P environments due to the geological stability of the landscapes in which they evolved.

Methods

We assessed differences in diversification of Proteaceae in P-impoverished vs. nutrient-rich environments and whether these were linked to adaptations to P-impoverished soils. We explored mature leaf and seed [P] and investigated how these traits changed over the evolutionary history of the family, and within two species-rich genera (Banksia, Hakea).

Results

Faster diversification was correlated with lower leaf and higher seed [P] for species-rich genera across the Proteaceae. For Banksia and Hakea, diversification rates peaked at relatively low leaf [P], but not at the lowest leaf [P]. Ancestral state reconstructions indicated that low leaf [P] is a trait that was likely present in the early evolution of the Proteaceae, with recent transitions to higher leaf [P] across several species-poor rainforest genera.

Conclusions

Diversification of Proteaceae correlated strongly with P-related traits. In an evolutionary context, functional cluster roots, low leaf [P] and high seed [P] were likely key innovations allowing diversification. Selection for low leaf [P] early in the evolutionary history of Proteaceae pre-adapted ancestors of this family to diversify into oligotrophic environments. We discuss how our findings are likely relevant for understanding diversification dynamics of other plant families that occur in P-impoverished environments.

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Acknowledgements

Funding was provided by Australian Research Council Discovery Grants, DP130100005 to HL, and DP200101013 to HL and PMF. HL acknowledges support from the School of Plant Biology and the Deputy Vice Chancellor Research at the University of Western Australia (DVCR-UWA) towards a writing workshop that laid the foundation for this study. FJN was supported through an Australian Government Research Training Program (RTP) Scholarship. Further support from DVCR-WA was used towards field trips to collect some of the data included in this paper. We acknowledge the Department of Biodiversity, Conservation and Attractions (WA; permit no. SW019140 and no. FT61000353) for their permission to examine plants on land under their administration. PMF thanks the Chinese Academy of Sciences President’s International Fellowship Initiative (No.2018VBB0008) for funding. PMF and PF thank Zhou Bo for assistance, and the Biogeochemistry Laboratory, Xishuangbanna Tropical Botanical Garden for analysing the leaf P concentration of Helicia spp. in southern China. SDH acknowledges funding from an Australian Research Council Discovery Outstanding Researcher Award associated with a Discovery Grant DP140103357, as well as grants from the Great Southern Development Commission and the Jack Family Trust. We would like to thank the following people for their help in sample collection Roberta Dayrell, Qi Shen, Christiana Staudinger, and Jun Wasaki. We also thank Renske Onstein for discussions and help on theory relevant to the simulations of QuaSSE analyses.

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Correspondence to Hans Lambers.

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Responsible Editor: Jeffrey Walck.

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Patrick E. Hayes and Francis J. Nge contributed equally to this work.

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Hayes, P.E., Nge, F.J., Cramer, M.D. et al. Traits related to efficient acquisition and use of phosphorus promote diversification in Proteaceae in phosphorus‐impoverished landscapes. Plant Soil 462, 67–88 (2021). https://doi.org/10.1007/s11104-021-04886-0

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  • DOI: https://doi.org/10.1007/s11104-021-04886-0

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