Symbiosis catalyses niche expansion and diversification

Abstract

Interactions between species are important catalysts of the evolutionary processes that generate the remarkable diversity of life. Symbioses, conspicuous and inherently interesting forms of species interaction, are pervasive throughout the tree of life. However, nearly all studies of the impact of species interactions on diversification have concentrated on competition and predation leaving unclear the importance of symbiotic interaction. Here, I show that, as predicted by evolutionary theories of symbiosis and diversification, multiple origins of a key innovation, symbiosis between gall-inducing insects and fungi, catalysed both expansion in resource use (niche expansion) and diversification. Symbiotic lineages have undergone a more than sevenfold expansion in the range of host-plant taxa they use relative to lineages without such fungal symbionts, as defined by the genetic distance between host plants. Furthermore, symbiotic gall-inducing insects are more than 17 times as diverse as their non-symbiotic relatives. These results demonstrate that the evolution of symbiotic interaction leads to niche expansion, which in turn catalyses diversification.

Figure 1.

Predicted effects of symbiotic association between plant-feeding insects and fungi on niche expansion and diversification. In this example, a genus of gall midges (orange) that has evolved a symbiotic association with fungi is 50 per cent more diverse and uses four times as much of the host-plant phylogeny as its strictly plant-feeding sister lineage (green). Branch lengths are proportional to time, the maximum phylogenetic distance used by symbiotic gall midges is traced in orange, maximum phylogenetic distance used by strictly plant-feeding gall midges is traced in green, blank branches are not included in maximum path calculation. (Online version in colour.)

Figure 2.

Plot of zero-inflated (hurdle) generalized linear model comparing phylogenetic range used by symbiotic (orange dashed lines) and non-symbiotic (green solid lines) gall midge genera, in which the response variable is phylogenetic breadth of the host-plant phylogeny used (host-plant phylogenetic distance ∼ log(gall midge species richness)+symbiotic status | symbiotic status). For symbiotic and non-symbiotic gall midge genera of similar species richness the symbiotic genera consistently use a greater proportion of the host-plant phylogeny. (a) Fitted values for binomial portion of hurdle model. (b) Fitted values for Poisson portion of hurdle model. In both (a) and (b) CIs are plus or minus twice the s.e. from model fit. (Online version in colour.)

Figure 3.

Maximum patristic distance of host-plant taxa used by (a) polyphagous gall midge species and (b) gall midge genera with and without fungal symbionts. Gall midge taxa with fungal associations use a greater breadth of host plant taxa relative to species lacking fungal symbionts as defined by genetic distance between hosts. (c) Comparison of the species richness of plant-feeding gall midge genera with symbiotic fungal associations to relatives within their taxonomic tribes that do not have fungal associations. Means with s.e. bars are indicated on each plot. (Online version in colour.)

Figure 4.

Violin plots [56] showing comparison of the diversification (D) of non-fungally symbiotic gall midge genera with fungal-symbiotic gall midge genera suggesting fungal-symbiotic gall midge genera are diversifying at a significantly faster rate relative to their non-symbiotic relatives. Whereby, D = SR × NB/T. (Online version in colour.)