Phylogenetic tests for evolutionary innovation: the problematic link between key innovations and exceptional diversification

Abstract

Evolutionary innovation contributes to the spectacular diversity of species and phenotypes across the tree of life. 'Key innovations' are widely operationalized within evolutionary biology as traits that facilitate increased diversification rates, such that lineages bearing the traits ultimately contain more species than closely related lineages lacking the focal trait. In this article, I briefly review the inference, analysis and interpretation of evolutionary innovation on phylogenetic trees. I argue that differential rates of lineage diversification should not be used as the basis for key innovation tests, despite the statistical tractability of such approaches. Under traditional interpretations of the macroevolutionary 'adaptive zone', we should not necessarily expect key innovations to confer faster diversification rates upon lineages that possess them relative to their extant sister clades. I suggest that a key innovation is a trait that allows a lineage to interact with the environment in a fundamentally different way and which, as a result, increases the total diversification-but not necessarily the diversification rate-of the parent clade. Considered alone, branching patterns in phylogenetic trees are poorly suited to the inference of evolutionary innovation due to their inherently low information content with respect to the processes that produce them. However, phylogenies may be important for identifying transformational shifts in ecological and morphological space that are characteristic of innovation at the macroevolutionary scale.This article is part of the themed issue 'Process and pattern in innovations from cells to societies'.

Keywords: adaptive radiation; diversity-dependence; extinction; phenotypic novelty; speciation.

Figure 1.

Key innovations can facilitate an increase in clade diversity even if they fail to elevate species richness or diversification rate of the clade in which the innovation occurs relative to that of its sister taxon. (a) Idealized species richness trajectories for a clade undergoing diversity-dependent diversification within an adaptive zone with carrying capacity K₁ (orange). At time t₁, a key innovation arises that facilitates diversification within a new adaptive zone with carrying capacity K₂ (blue). (b) Corresponding net diversification rates through time for lineages from adaptive zones with carrying capacity K₁ and K₂. (c) Hypothetical phylogenetic patterns that might be observed at timepoints t₁, t₂ and t₃. At timepoint t₂, the innovation clade (blue) has reached its carrying capacity of four lineages, but the parent adaptive zone has been rendered a paraphyletic grade. By time t₃, turnover of lineages within these two adaptive zones has led to monophyly of both the ancestral and key innovation adaptive zones and the parent clade (all orange and blue lineages) contains more species (K₁ + K₂) than it would have had the key innovation not evolved.

Figure 2.

Putative adaptive zone shift in Australian honeyeaters, from an arboreal/nectarivorous foraging strategy to a terrestrial/insectivorous strategy. (a) Phylogeny of Australian honeyeaters, showing five ground-foraging taxa (thick red branches: chats and gibberbird, Epthianura and Ashbyia). Size of tip symbols denotes fraction of time spent foraging on the ground. (b) Phylogenetic principal components analysis of foraging characteristics across honeyeaters, illustrating major gap between chats and all other taxa. High scores on the ecological PC2 axis generally reflects the use of open habits and frequent ground-foraging behaviour. (c) White-fronted chat, a ground-foraging and largely insectivorous honeyeater (Epthianura albifrons by JJ Harrison, CC BY-SA 3.0). (d) Noisy friarbird, a highly nectarivorous and arboreal honeyeater (Philemon corniculatus by Fir0002/Flagstaffotos, CC BY-NC). Phylogeny ignores New Guinea species; if included, the chat clade (red) would be sister to a clade of approximately eight mostly montane rainforest species. Data in (a) and (b) from Miller et al. [43].