Investigating the ecological and evolutionary drivers of geoxylism in Parinari Aubl. (Chrysobalanaceae)

Understanding how traits and suites of traits evolved and interacted with the historical assembly of species comprising biomes through time can lead to a greater understanding of biome history (Couvreur et al 2015). Plant functional traits offer insights into the evolution of biomes and enable inferences to be made regarding the geographical and ecological drivers of diversity (Ringelberg et al 2020; Charles-Dominique et al 2016). While all traits are functional (Sobral 2021), some, such as the leaf economic spectrum are frequently relied upon as a lens through which to understand biome association and function. However traits such as habit, which are amalgamations of multiple physiological attributes such as herbaceousness, rooting type and woodiness, are often fundamentally linked with biome, ie the prevalence of lianas in tropical forests (Schnitzer and Bongers 2002; Schnitzer 2005; Rickenback, Pennington and Lehmann 2022) or succulents in seasonally dry tropical biomes (Schrire, Lavin and Lewis 2005; Dexter et al 2018; Gagnon et al 2019; Ringelberg et al 2020). Habit, and its associations with biomes, has been used to make inferences around biome evolution such as the development of aerial stems in Velloziaceae in the campos rupestre (Alcantara, Ree and Mello-Silva 2018), or the association of geoxyles – an underground life strategy which features only limited aerial parts and massive woody underground parts (Gomes et al 2021) - with the savanna biome (Maurin et al 2014). The geoxylic life form has also been linked to fire, and as with spinescence (Charles-Dominique et al 2016) has been used to infer the origins of fire-dominated open ecosystems in Africa (Maurin et al 2014).
Geoxyles have evolved independently from tree congeners multiple times in response to evolutionary pressures in the savanna biome (Maurin et al 2014). Although geoxyles have been documented throughout the tropics (Pausas et al 2017), what few studies there are have mainly focused on Africa (Davies et al 2016; Finckh et al 2016; Lamont, He and Pausas 2017; Meerts 2017; Gomes et al 2019; Gomes et al 2021; Meller et al 2022) and to a lesser extent South America (Simon et al 2009; Simon and Pennington 2012; Alves et al 2013). The drivers of geoxylic diversification can be frost, fire, edaphic factors, herbivory or a combination thereof (Meller et al 2022) although research has not explored whether these drivers differ by continent. Given that savannas on different continents experience distinct environmental regimes (Lehmann et al 2011; Lehmann et al 2014) it is possible that the influence of individual disturbance factors may vary in strength continentally. By utilising a genus with geoxylic species in Australia, South America, and Africa, we can significantly expand our understanding of the ecological and evolutionary drivers of this unique life form.
Parinari (Chrysobalanaceae) is a monophyletic genus of mostly tropical trees (Bardon et al 2013; Bardon et al 2016) with around 39 species distributed globally (Prance and Sothers 2003; POWO 2023) which has previously been used as part of a broader study to investigate the origin of fire adapted lineages in southern Africa (Maurin et al 2014). Unusually for a small genus, in Parinari a geoxylic form is native to each major continent (Prance 2021), with P. capensis distributed across sub-Saharan Africa, P. obtusifolia across Bolivia, Brazil and Paraguay, and P. nonda found in Australia and New Guinea. Previous work on Chyrsobalanaceae (Bardon et al 2013; Bardon et al 2016) only sequenced one geoxylic species of Parinari, and nine Parinari species in total, so questions remain regarding the evolutionary and ecological drivers of the geoxylic growth form in the genus, and whether these drivers were synchronous across all continents.
Parinari is an economically significant genus, with P. curatellifolia identified as a priority species for the regional tree domestication programme in Zimbabwe by the International Centre for Research in Agroforestry (Akinnifesi et al 2006), and P. curatellifolia and P. excelsa used in the treatment of malaria (Uys et al 2002) and as food crops (Prance 2021). Parinari species provide habitat and food for a variety of animal species, including chimpanzees (Furuichi, Hashimoto and Tashiro 2001), cavity nesting birds (Nyirenda et al 2016) and ants (Prance 1992), and can store significant carbon stocks in below ground biomass (Gomes et al 2021). Understanding the evolution and ecology of geoxylic Parinari species is crucial as they have an important role in the ecology of the tropical regions where they occur.

In this study, I aim to investigate the evolutionary history, phylogenetic relationships, and ecological adaptations of geoxylic Parinari species. I will use fire and climatic data as well as phylogenetics to explore the factors that have influenced the evolution of this unique group of plants and discuss the implications of their ecology and genetics for conservation efforts. This study will provide insights into the adaptive strategies that enable geoxylic species to thrive in disturbance prone environments and contribute to our understanding of the evolution and ecology of tropical biomes. Although Parinari nonda has been identified as a geoxyle (Prance 2021), it also appears to have a tree form (Northern Territory Government 2013). By including genetic sequences generated from both tree and geoxyle forms, I can identify whether P. nonda demonstrates mutability between two distinct growth forms and what might drive this, or whether the geoxylic form is a separate (new) species.

Research questions:
• Do the geoxylic species in Parinari share environmental niches?
-To investigate this I will use geolocation data and niche identity tests in ENMTools.
Given the different climatic ranges of savannas on different continents we expect these niches to differ but to experience the same abiotic drivers (ie seasonality, frost, fire).

• Did the geoxylic species in Parinari evolve independently and at the same time?
-To investigate this I will create a dated phylogeny for the whole genus using Sanger sequencing and building on work from Bardon et al 2013 and Bardon et al 2016.
Given the geographical dislocation between geoxylic species I expect the habit to have evolved independently. Given the similar and recent evolution of geoxyles found by Maurin et al 2014 (and Rickenback, Pennington and Lehmann 2022) I expect evolutions of the geoxylic form to be broadly synchronous, reflecting global drivers.


References
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Underground trees are little known and understudied. Using three underground tree species found in one genus, Parinari, I can explore whether the environmental factors that drive a shift to an underground form differ by continents. Using genetic data I can assess whether this shifts occur independently and asynchronously or not.