Evolutionary ecology of mycorrhizal functional diversity in agricultural systems

Abstract

The root systems of most agronomic crops are colonized by diverse assemblages of arbuscular mycorrhizal fungi (AMF), varying in the functional benefits (e.g. nutrient transfer, pathogen protection, water uptake) provided to hosts. Little is known about the evolutionary processes that shape the composition of these fungal assemblages, nor is it known whether more diverse assemblages are beneficial to crop productivity. In this review we aim to identify the evolutionary selection pressures that shape AMF diversity in agricultural systems and explore whether promotion of AMF diversity can convincingly be linked to increases in agricultural productivity and/or sustainability. We then ask whether farmers can (and should) actively modify evolutionary selection pressures to increase AMF functioning. We focus on three agriculturally imposed selection regimes: tillage, fertilization, and continuous monoculture. We find that the uniform nature of these practices strongly selects for dominance of few AMF species. These species exhibit predictable, generally non-beneficial traits, namely heavy investment in reproduction at the expense of nutrient scavenging and transfer processes that are beneficial for hosts. A number of focus-points are given based on empirical and theoretical evidence that could be utilized to slow down negative selection pressures on AMF functioning, therein increasing crop benefit.

Keywords: agriculture; cooperation; mutualism; punishment; selection pressures.

Figure 1

Example of a functional trait (pathogen protection) as it relates to AMF phylogeny. Percentage of roots colonized by soil pathogens, either fusarium oxysporum or pythium sp., (y-axis) is presented as a function of AMF species (x-axis) grown on Plantago lanceolata in a greenhouse experiment. Representatives of AMF families are divided with dashed lines (families represented by values: Gl = Glomeraceae; Sc, Gi = Gigasporaceae, Ac=Acaulosporaceae; AMF species where values are missing have not been tested). The trait of pathogen protection is relatively conserved within, but differs among families. Figure taken from Powell et al. (2009).

Figure 2

Conceptual relationship between agricultural management intensity and AMF functional diversity. Through strong r-selection imposed by intensive agricultural practices (e.g. high nutrient input, low crop diversity, and high tillage frequency) diverse AMF functional traits may be lost. As management intensity increases, AMF are predicted to shift from (A) functionally diverse communities with extensive hyphal mattes and large spores to (B) AMF communities with little investment in mycelium and fast production of numerous spores.

Figure 3

Schematic representation of selective environment imposed by ‘sustainable’ management practices (left) and their influence on the AMF community (middle). Implementation of more sustainable management regimes is predicted to increase the benefit of AMF to agricultural systems by facilitating a re-establishment of AMF with functionally diverse attributes.