Rates of niche and phenotype evolution lag behind diversification in a temperate radiation

May 20th, 2019
By Gitzendanner, Matt

Folk, R. A., R. L. Stubbs, M. E. Mort, N. Cellinese, J. M. Allen, P. S. Soltis, D. E. Soltis, and R. P. Guralnick. 2019. Rates of niche and phenotype evolution lag behind diversification in a temperate radiation. PNAS 201817999. [View on publisher’s site]

Significance

Figure 1 from Folk et al 2019

Ancestral reconstruction across Saxifragales for PC1 of our dataset of 35 environmental variables; branches are colored in a rainbow scale from low ordinated values (red and yellow; hotter and to some extent wetter habitats, as well as the hottest arid habitats) to high ordinated values (green and blue; mostly colder and drier habitats). Black dots at nodes represent major ecological niche shifts (the upper 95th percentile of node–parent node differences). Red dots at nodes represent diversification shifts in the maximum credibility set. The inset density curves show tip rates for diversification (green), niche (orange), and phenotype (blue), all scaled from the minimum to the maximum reconstructed value. Around the edge are photographs of major representative habitats. Family codes are as follows: (a) Peridiscaceae, (b) Paeoniaceae, (c) Daphniphyllaceae, (d) Cercidiphyllaceae, (e) Altingiaceae, (f) Hamamelidaceae, (g) Iteaceae, (h) Grossulariaceae, (i) Saxifragaceae, (j) Cynomoriaceae, (k) Tetracarpaeaceae, (l) Aphanopetalaceae, (m) Penthoraceae, (n) Haloragaceae, and (o) Crassulaceae.

Alternative models of evolutionary processes suggest different associations between species diversification and trait evolution, but limited empirical evidence is available to test these models across large clades at global extents. Here we investigate the relative timing of species diversification and niche and phenotypic evolution across a global plant radiation (Saxifragales) with enormous phenotypic and habitat variation. We demonstrate strong temporal lags among rates, with increased diversification occurring first, followed by niche and phenotype. Accelerated diversification rates are coincident with mid-Miocene expansion of temperate biomes. Later increases in niche and phenotypic evolutionary rates argue against density-dependent diversification alone, indicating a major role for ecological opportunity. These results have broad implications for understanding diversification processes and the origin of present-day temperate biotas.

Abstract

Environmental change can create opportunities for increased rates of lineage diversification, but continued species accumulation has been hypothesized to lead to slowdowns via competitive exclusion and niche partitioning. Such density-dependent models imply tight linkages between diversification and trait evolution, but there are plausible alternative models. Little is known about the association between diversification and key ecological and phenotypic traits at broad phylogenetic and spatial scales. Do trait evolutionary rates coincide with rates of diversification, are there lags among these rates, or is diversification niche-neutral? To address these questions, we combine a deeply sampled phylogeny for a major flowering plant clade—Saxifragales—with phenotype and niche data to examine temporal patterns of evolutionary rates. The considerable phenotypic and habitat diversity of Saxifragales is greatest in temperate biomes. Global expansion of these habitats since the mid-Miocene provided ecological opportunities that, with density-dependent adaptive radiation, should result in simultaneous rate increases for diversification, niche, and phenotype, followed by decreases with habitat saturation. Instead, we find that these rates have significantly different timings, with increases in diversification occurring at the mid-Miocene Climatic Optimum (∼15 Mya), followed by increases in niche and phenotypic evolutionary rates by ∼5 Mya; all rates increase exponentially to the present. We attribute this surprising lack of temporal coincidence to initial niche-neutral diversification followed by ecological and phenotypic divergence coincident with more extreme cold and dry habitats that proliferated into the Pleistocene. A lack of density-dependence contrasts with investigations of other cosmopolitan lineages, suggesting alternative patterns may be common in the diversification of temperate lineages.

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