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Population Dynamics of Polyploids: Testing the Mechanisms of Grassland Expansions in Madagascar

Periodic Reporting for period 1 - MADGRASS (Population Dynamics of Polyploids: Testing the Mechanisms of Grassland Expansions in Madagascar)

Okres sprawozdawczy: 2022-01-10 do 2024-01-09

Madagascar is considered a biodiversity hotspot and has been of much interest with respect to species conservation as well as understanding how new species arise. Approximately 65% of Madagascar is covered in grasslands, open ecosystems dominated by grasses with little tree cover. Such ecosystems occur in both the tropics and temperate regions and rose to prominence nearly eight million years ago under paleoclimate conditions of low precipitation increasing fire. However, there is uncertainty about the degree to which Madagascar’s grasslands are natural versus anthropogenic due to deforestation and the use of fire to prepare land for agriculture or grazing. This raises difficult policy questions about which areas should be targeted for reforestation tree planting programs, which grasslands should be protected for their own unique biodiversity, and which grasslands are could be exploited for economic development by rights holders.

The action Population Dynamics of Polyploids: Testing the Mechanisms of Grassland Expansions in Madagascar (MADGRASS) aimed to resolve uncertainty in natural versus anthropogenic grasslands by leveraging genomic data and demographic modeling from dominant grass species. Genomes retain information about the geographic origin of populations and their changes in population size through time. However, grasses present two challenges to the application of standard computational tools that have been used for understanding the demographic history of, for example, humans. The first is that plants can be polyploids, such that they carry multiple copies of their genomes and this causes some deviations from assumptions made for existing mathematical models. The second is that grasses are often parts of hybridizing complexes, such that species may exchange genes or that their evolutionary history is complicated by historical gene flow. MADGRASS made progress on the theoretical and computational challenges of analyzing genomic data from polyploids and applied those advances towards understanding the demographic history of the focal grass species, Loudetia simplex, in Madagascar.
MADGRASS utilized existing collections of Loudetia simplex housed at the Royal Botanic Gardens, Kew, and filled in geographic sampling gaps with new field work conducted in March of 2022. Collections of Loudetia simplex were used to generate genomic data for 156 individuals representing 10 populations across Madagascar and continental Africa. The demographic analyses of these individuals were facilitated by the sequencing and assembly of a high-quality reference genome for a closely related species, Loudetia flavida. Final analyses and publication of genomic data are ongoing, but current analyses have indicated Loudetia simplex dispersed to Madagascar from southern Africa approximately 200,000 years ago, and expanded to their present range between 21,000 and 120,000 years ago. These results are consistent with an initial pilot study (Tiley et al. 2024) and facilitated by simulation and theoretical advances in Tiley et al. (2023a) and Tiley and Solís-Lemus (2023), as well as the development of bioinformatic tools in Tiley et al. (2023b). The present-day distribution of Loudeita simplex could be predicted by environmental data from well-accepted natural grasslands of tropical Africa (Almary et al. 2023). All outputs should provide a framework for statistically rigorous and reproducible studies of polyploid population genetics going forward, while also providing insights into the natural history of Madagascar’s grasslands.

References:
Almary TOM, White J, Rasaminirina F, Razanatsoa J, Lehmann C, Rakotoarinivo M, Ralimanana H, Vorontsova MS, Tiley GP. 2023. The grass that built the Central Highland of Madagascar: environmental niches and morphological diversity of Loudetia simplex. bioRxiv (in revision for Plants People Planet). bioRxiv doi: https://doi.org/10.1101/2023.09.25.559324
Tiley GP, Crowl AA, Almary TOM, Luke WRQ, Solofondranohatra CL, Besnard G, Lehmann CER, Yoder AD, Vorontsova MS. 2024. Genetic variation in Loudetia simplex supports the presence of ancient grasslands in Madagascar. Plants People Planet. 6:315-329.
Tiley GP, Crowl AA, Manos PS, Sessa EB, Solís-Lemus C, Yoder AD, Burleigh JG. 2023b. Benefits and Limits of Phasing Alleles for Network Inference of Allopolyploid Complexes
(in revision for Systematic Biology). bioRxiv doi: https://doi.org/10.1101.2021.05.04.442457
Tiley GP, Flouri T, Jiao X, Poelstra JW, Xu B, Zhu T, Rannala B, Yoder AD, Yang Z. 2023a. Estimation of species divergence times in presence of cross-species gene flow. Syst Biol. 72:820-836.
Tiley GP, Solís-Lemus C. 2023. Extracting diamonds: Identifiability of 4-node cycles in level-1 phylogenetic networks under a pseudolikelihood coalescent model. (under review at Scientific Reports) bioRxiv. https://doi.org/10.1101/2023.10.25.564087
The maps and projected distributions of Loudetia simplex provide evidence that grass ecosystems in Madagascar have the capacity for further expansion, and managers of protected wooded or forest ecosystems should be aware of the capacity for Loudetia simplex to dominate ecosystems after fire. This provides some actionable ecological monitoring policies that could be implemented along with training on identifying Loudetia simplex and co-occurring species. The maps currently under development alongside the demographic analyses will likely provide recommendations that tree-planting programs should reconsider some current reforestation projects in grasslands that are at least 21,000 years old, and divert efforts to edges of protected areas in eastern humid forests.

Findings should also be integrated in the public discourse and early education regarding the origins of Madagascar’s grasslands. It is frequently taught in Madagascar that the grasslands are largely of anthropogenic origin, caused by the agricultural practices and pastoralism of early settlers. MADGRASS demonstrates that grasslands are largely of natural origin, and that present-day deforestation concerns should not be confounded with the natural history of Madagascar.

Analyses of population-level variation among Loudetia simplex identified some genomic regions and individual genes that were associated with environmental variation such a precipitation seasonality. There is increasing interest in identifying such genes in grasses as anthropogenic climate change requires cereal crops to be resilient to drought and temperature stress. The value of these identified genes as selection targets against drought stress will remain uncertain until appropriate laboratory experiments for validation can be designed.
Overview of data and results from MADGRASS action.