Specialists, generalists and the shape of the ecological niche in fungi

The terms ‘generalist’ and ‘specialist’ are commonly used to describe a species’ ecology but their precise meaning is rarely considered. In particular, are specialists specialised in all aspects of their lives, or in only some or only one? In technical terms, is niche breadth correlated among niche dimensions? Recent research on three ecological guilds of fungi – arbuscular mycorrhizas, plant pathogens and saprotrophs – allows us to investigate the degree of co-specialisation among niche dimensions. These studies suggest that fungi can specialise independently on climatic, edaphic and biotic conditions and resources, although evidence from saprotrophs suggests that specialisation on different climatic conditions is correlated. Quantifying niche shape has important implications for understanding how species will respond to global change. The idea of the niche has been among the most important, yet controversial, in ecology for over a century (Chase & Leibold, 2003). The theory of evolution by natural selection considers a species’ fitness in a particular environment, but it was Grinnell’s (1917) paper on ‘The niche-relationships of the California thrasher’ that explicitly defined the ecological niche as a set of environmental conditions occupied by a species. These conditions included dietary requirements, climatic tolerances and interactions with other species, such as predators. Some years later, Elton (1927) defined the niche from the perspective of a species’ role in foodwebs and its impact on consumable resources such as prey populations. However, it was Hutchinson (1957) who introduced the revolutionary concept of the n-dimensional hypervolume to define the niche and to allow, at least in theory, the niche to be empirically quantified. In Hutchinson’s conceptual model, any number of limiting factors to species population growth, be they conditions such as temperature or resources such as prey, form dimensions of the hyperspace within which the species’ fundamental niche sits (Blonder et al., 2014). The fundamental niche is defined as the niche in the absence of biotic interactions such as competition or facilitation (Carscadden et al., 2020). Ecological theories such as the Volterra–Gause competitive exclusion principle are conceptualised in Hutchinson’s model, by stating that where the fundamental niche volumes of two species overlap, only the more competitive species will survive. The realised niche of a species is then any element of the fundamental niche that does not overlap with another, plus any parts of the intersection inwhich that species is the superior competitor (Hutchinson, 1957). Realised niches should therefore always be smaller than fundamental niches (Sober on&Arroyo-Pe~ na, 2017), except when positive interactions such as mutualism are considered (Carscadden et al., 2020). The concept of ecological specialisation, and comparison between specialists and generalists, can be visualised as variation in the extent of the niche along different axes or the volume of the n-dimensional niche (Fig. 1). The magnitude of the niche on a particular axis is often termed the niche width or breadth (Sexton et al., 2017). A fundamental question in evolutionary ecology is: what determines niche breadth and how does it evolve (Sexton et al., 2017; Carscadden et al., 2020)? In the absence of competition, we might expect a species to evolve the capacity to survive under all conditions and exploit all resources. However, there must be competitive advantages to specialising, notwithstanding any biological constraints such as the implausibility of the capacity to consume prey of any size.Many models of niche evolution expect a trade-off between performance and breadth, summed up by the phrase ‘Jack of all trades, master of none’. However, such trade-offs remain only weakly supported by empirical evidence, and trade-off mechanisms such as antagonistic pleiotropy operate mainly under specific conditions (Bono et al., 2017). Other niche evolution models indicate that specialisation can evolve without the need for trade-offs, for example when specialists spend more time in particular environments and so beneficial alleles are fixed more rapidly than in generalist subpopulations (Whitlock, 1996). Whereas niche breadth evolution over one niche axis has been investigated by numerous models and empirical studies (reviewed in Sexton et al., 2017), the relationship between niche breadths on different axes remains largely unexplored (Carscadden et al., 2020). Is specialisation on niche axes correlated, or uncorrelated? Is a specialist a specialist in all niche dimensions? Grinnell (1917) describes the California thrasher as preferring warm, moist environments (i.e. narrow abiotic niche axes) but having a very diverse omnivorous diet (i.e. wide resource niche axis). No correlations among niche axes were detected within the genus Lasthenia, an annual plant of ephemeral pools inCalifornia (Emery et al., 2012), whereas in global analyses of amphibians and reptiles, temperature and precipitation niche breadths were positively correlated (Bonetti &Wiens, 2014; Lin &Wiens, 2017; Liu et al., 2020).Whether niche breadths are correlated or not has important implications for issues such as climate change impacts on populations. For species with narrow thermal tolerances,migration to track optimal climates will be facilitated if other niche axes are broad (Carscadden et al., 2020). Recent research on different guilds of fungi (Table 1) allows the question of niche breadth correlations to be addressed (Maynard et al., 2019;Chaloner et al., 2020;Davison et al., 2021).Writing in the New Phytologist, Davidson et al used 327 soil samples from around the world to estimate mean and standard deviation (SD) of some soil chemical properties and two climatic parameters, mean annual temperature andmean annual precipitation, for each of 230 arbuscular mycorrhizal fungal (AMF) taxa (Davison et al., 2021).