Theory of Island Biogeography
The dynamic equilibrium theory of island biogeography is an influential framework for understanding species diversity patterns. Its original proponents (MacArthur & Wilson 1967) predicted two general patterns: (1) larger islands have more species at equilibrium, since extinction rates decline and colonization rates increase with increased area and (2) islands at a greater distance from the “mainland” or source population have fewer species at equilibrium, as colonization rates decrease with distance. Traditionally applied to groups of oceanic islands, the theory has recently been used to understand microbial biogeography across patchy, island-like systems. These include roots (Peay et al. 2007), leaves (Andrews et al. 1987; Kinkelet al. 1987), lakes or pools (Reche et al. 2005), and non-human animal organs (Loudon et al. 2016; Moeller et al. 2017). The theory has also been applied to other discrete habitats that are separated by sharp differences in temperature (Whitakeret al. 2003; Darcy et al. 2018), substrate textural or chemical qualities such as oxygen availability or host-secreted metabolites (Loudon et al. 2016), or other abiotic factors that have been shown to structure microbial distributions.
Results from several studies support the general relationship between microbial diversity and island size, although there is no consensus on how habitat size is measured amongst varying “island-like” systems (Itescu 2019). For example, Darcy and colleagues (2018) observed that bacterial diversity within cryoconite holes in Antarctic glaciers is positively correlated with hole area, whereas Bell et al. (2005) found bacterial genetic diversity in water-filled tree holes increased with water volume. Studies have also found fungal species richness increases with tree host population size in arctic and alpine environments (Chlebicki & Olejniczak 2007) and as a function of tree photosynthetic tissue volume in ectomycorrhizal fungi (Peay et al. 2007; Glassman et al. 2017a). Yet, some studies fail to detect a significant relationship between species diversity and island area, such as AM fungal communities on true islands, bacterial richness in oak litter patches and filamentous fungi on apple leaves (Kinkelet al. 1987; Davison et al. 2018; Spiesman et al.2018). In some cases, the lack of an observed relationship is likely because environmental heterogeneity relevant for the focal taxa does not scale with island size (Teittinen & Soininen 2015).
The mechanisms that produce island area and microbial diversity patterns are still debated. Recent studies have found these patterns hold even after explicitly accounting for environmental variables. For example, forest fragment size predicted diversity of root-associated fungi in a dominant tree even after accounting for the effects of soil carbon (Vannette et al. 2016). Dinnage et al. (2019) determined that tree size explained more variation in rhizobia diversity than other edaphic factors. Various host-associated microbial clades have differing responses to ecological drift, host size, and other environmental factors (Chlebicki & Olejniczak 2007; Dinnage et al. 2019; Liet al. 2020). Bacterial alpha diversity increased with island area, which may be explained by differences in overall immigration and extinction rates. However, fungal beta diversity increased with area, which instead suggests an effect of greater microenvironmental variation in larger patch sizes. Further research into mechanisms underlying diversity-area patterns may clarify such differences across taxa, although studying processes such as local extinction in microbial communities may not be straightforward, particularly in natural systems (but see Andrews et al. 1987).
Empirical evidence that microbial diversity and community similarity decline as a function of distance from the source population is mixed across the literature, reflecting taxon-specific patterns as well as the need for more research. A significant challenge in applying island biogeographic theory to microbial communities in island-like systems is that the microorganism source, or “mainland” population, is often difficult to define, and thus most studies instead consider only distances among islands. Interestingly, most of the studies that assess the effects of distance from the mainland have used the roots of isolated or planted pine trees as “islands” and a denser, nearby pine forest as the “mainland” (Peay et al. 2010, 2012; Bahramet al. 2013; Glassman et al. 2017a, b). For example, Bahram et al . (2013) and Glassman et al . (2017a) both found that ectomycorrhizal community similarity and diversity declined with increased distance from the natural forest’s edge. The majority of studies examining how distance among ”islands” shapes community similarity and diversity find spatial autocorrelation. For instance, communities of hot spring-dwelling archaea (Whitaker et al. 2003) and protists in lakes (Lepère et al. 2013) become more dissimilar as a function of distance, rather than variation in environmental factors. This suggests that for these organisms, the difficulties of dispersing among patches of suitable habitat is more important for community structure than environmental filtering.
Exceptions to the predictions of island biogeographic theory reveal that the relative importance of environmental filtering and dispersal limitation is taxon- and scale-specific. For example, Vannette et al . (2016) determined that the degree of forest fragment isolation was important in structuring the communities of some classes of root-associated fungi but not others. In other cases, lack of support may instead be due to the spatial scale considered. Darcy et al . (2018) observed positive spatial autocorrelation of cryoconite glacier hole bacterial communities among glaciers, but very little within glaciers, suggesting that had they sampled at a smaller scale, they may not have found evidence in line with island biogeographic theory. The importance of scale is also taxon-specific because taxa differ in their dispersing and colonizing abilities (Peay et al. 2012), likely explaining why Teittinen & Soininen (2015) did not find spatial structuring of diatom communities in springs. Overall, more manipulative experiments to assess why and how taxa differ in their dispersal capacities would help assess the relevance of an island-distance relationship for microorganisms.