Introduction
Understanding the relative contribution of deterministic and stochastic processes during community assembly represents a major unresolved issue in microbial ecology (Dini-Andreote et al. , 2015; Antwis et al. , 2017; Zhou and Ning, 2017; Tripathi et al. , 2018). Unravelling the mechanisms that drive shifts in community composition is crucial for understanding the functions and ultimately the ecosystem processes that microbial communities are able to deliver (Salleset al. , 2009; Crowther et al. , 2014; Laforest-Lapointeet al. , 2017). Succession, the study of how biological communities reorganise through time after disturbances (Johnson, 1979; Chang and Turner, 2019), provides valuable insight into community assembly (Chang and HilleRisLambers, 2016). Understanding succession in microbial communities can, therefore, help to disentangle the relative importance of deterministic and stochastic processes on community assembly (Tripathi et al. , 2018).
The composition of communities during succession can be driven by deterministic mechanisms (environmental conditions and biotic filters) and stochastic processes (dispersal, drift, speciation and priority effects) (Hubbell, 2001; Vellend, 2010; Nemergut et al. , 2013; Chang and HilleRisLambers, 2016). For microbial communities it has been hypothesised that during the early stages of succession, communities are largely governed by stochastic events, and only as succession continues does the relative strength of deterministic processes begin to cause directional changes in community composition (Dini-Andreote et al. , 2015, 2016). However, if stochastic processes such as dispersal are not limiting, they may overpower deterministic processes and the system remains ecologically neutral (Hubbell, 2001).
Studies on fungal succession have mostly focused on belowground soil and root-associated communities (Blaalid et al. , 2012; Brown and Jumpponen, 2014; Davey et al. , 2015; Dini-Andreote et al. , 2016; Dong et al. , 2016; Turner et al. , 2019). These studies have repeatedly shown that fungal community assembly during later successional stages is deterministic (Brown and Jumpponen, 2014; Dini-Andreote et al. , 2016; Gao et al. , 2019; Turneret al. , 2019). Both abiotic (e.g. carbon, nitrogen, pH and phosphorus) and biotic (e.g. plant species richness, composition, root exudates and microbial competition) factors are drivers of belowground microbial community composition patterns (Dini-Andreote et al. , 2016; Dong et al. , 2016; Turner et al. , 2019). While some evidence exists for both linked (Davey et al. , 2015) and decoupled (Turner et al. , 2019) trends of succession between plant communities and belowground fungal communities, generalisable patterns across different fungal guilds are still unclear.
Disentangling the relative influence that host-associated and environmental factors play in determining host-endophyte composition represents a major theme in endophyte ecology (Antwis et al. , 2017; Harrison and Griffin, 2020), as these fungi are an important aspect in plant performance and health (Compant et al. , 2019). Host identity appears to be one of the most important drivers of foliar fungal endophyte community composition (Terhonen et al. , 2019). Host-specific defence mechanisms, the host-specific production of various enzymes, secondary metabolites and concentration differences of nutrients and molecules within their leaves directly influence the composition of foliar fungal endophyte communities (Kembel and Mueller, 2014; Cordovez et al. , 2019; Darlison et al. , 2019; Tellezet al. , 2020). Geographic distance is another important factor influencing community composition, with community dissimilarity generally increasing with geographic distance due to dispersal limitation (Soininen et al. , 2007). Evidence for distance decay in foliar fungal endophytes is mixed. Some evidence points to the absence of such a relationship at both small (Cordier et al. , 2012; Oono et al. , 2017) and large scales (Vincent et al. , 2016; Barge et al. , 2019; U’Ren et al. , 2019), while other studies show evidence of distance decay, especially for rare foliar fungal endophyte taxa (Vaz et al. , 2014; David et al. , 2016; Koide et al. , 2017; Oono et al. , 2017). Climate, a major factor driving the community composition of plants, seems to have less influence on determining the composition of fungal endophytes, particularly at fine scales (Compant et al. , 2010; Santoyoet al. , 2017). Water availability in particular affects some fungal endophytes’ ability to germinate and persist (Arnold, 2007; Peayet al. , 2016). The effect of climate on endophyte composition may also be indirect: through its effect on host composition and physiology fungal endophyte community composition may be affected (Compant et al. , 2010; Terhonen et al. , 2019).
Plant community composition structures soil and root-associated fungal communities due to the strong biotic filter imposed by plant hosts (Carney and Matson, 2006; Hausmann and Hawkes, 2009; Hoch et al. , 2019; Hu et al. , 2019). However, how plant community composition structures fungal endophyte composition is yet to be directly assessed (Griffin and Carson, 2018; Griffin et al. , 2019). Therefore, directly linking plant community composition to foliar fungal endophyte composition may help to disentangle the factors responsible for structuring these fungal communities and ultimately help to understand how this scales-up to mediate plant microbial ecosystem functioning relationships (Laforest-Lapointe et al. , 2017; Griffin et al. , 2019; Harrison and Griffin, 2020).
In contrast to community composition, species richness considers only the number of species. A number of factors affect foliar fungal endophyte species richness (Arnold and Lutzoni, 2007; Unterseheret al. , 2007; Lau et al. , 2013; Griffin et al. , 2019; Harrison and Griffin, 2020). Host identity appears to be one of the most important drivers (Lau et al. , 2013; Peay et al. , 2016; U’Ren et al. , 2019; Yao et al. , 2019). Other factors, including host age or height, microhabitat (e.g., moisture, light intensity and temperature) and plant richness, can also shape foliar fungal endophyte richness (Bernstein and Carroll, 1977; Unterseher et al. , 2007; Zimmerman and Vitousek, 2012; Scholtysiket al. , 2013; Oono et al. , 2015; Griffin et al. , 2019). Yet, few studies have simultaneously assessed how multiple factors drive patterns of foliar fungal endophyte richness.
The aim of this study is to assess patterns and drivers of foliar fungal endophyte community assembly in a system undergoing deterministic vegetation succession. Our objectives were to a) test whether foliar fungal endophyte communities follow a deterministic successional trend as displayed by the woody tree communities in the same study system; and b) determine the relative contribution of host species identity, surrounding tree composition, geographic distance and abiotic variables to endophyte composition and richness.