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.