Phylogenomic conflict coincides with rapid morphological innovation

Abstract

Evolutionary biologists have long recognized that rates of phenotypic change vary widely throughout time and across lineages. Researchers have been particularly fascinated with evolutionary 'radiations'--periods during which novel phenotypic characteristics and new species emerge at an unusually high rate. Despite considerable speculation and empirical testing of the geologic, environmental, and ecological contexts coinciding with the radiations of major lineages, our understanding of how population processes during these epochs contribute to emergent macroevolutionary patterns in phenotypic change remains poor. However, the increasing prevalence of phylogenomic datasets over the past decade has revealed that phylogenomic conflict, frequently caused by population-level processes, is often highest at the origin of major lineages. We reconstruct patterns in both rates of morphological change and levels of phylogenomic conflict across six clades to identify whether the large spikes in the rate of phenotypic change that accompany major radiations coincide with elevated conflict. We found that the most conflict-rich regions of the six clades also tended to experience the highest rates of morphological evolution, suggesting that the complex population processes that underlie evolutionary radiations leave signatures at deep phylogenetic scales in both genomic and phenotypic data. Thus, closer examination of the drivers and implications of phylogenomic conflict may permit us to make improved connections between micro- and macroevolution, vastly increasing our understanding of the processes that shape the origin of major lineages across the Tree of Life.

Gene duplications and phylogenomic conflict underlie major pulses of phenotypic evolution in gymnosperms

“…21). This finding is in line with a recent study 13 documenting a similar correspondence in multiple clades across the Tree of Life. Figure 3 clearly shows that the branches with the highest rates of morphological evolution also have extreme levels of gene-tree conflict.…”

“…Morphological reconstructions on the species-tree were performed using Maximum Parsimony, following the procedure of Parins-Fukuchi et al 13 , briefly outlined here. Each trait was reconstructed on the phylogeny, and then the number of state changes along each branch was tallied—this is considered the degree or level of phenotypic ‘innovation’ or ‘novelty’ along each branch.…”

“…Thus, these represent two different, albeit not mutually exclusive, processes that might shape macroevolutionary patterns of morphological evolution in plants. We reconstructed levels of phenotypic innovation or novelty (defined here simply as state changes along a branch) and rates (state changes/time) for each branch in the phylogeny 13 and plotted these against corresponding levels of gene duplication and gene-tree conflict (Figs. 2 and 3).…”

“…For example, analyses of the relationship between WGD and diversification have produced conflicting results 5,6,7,8 , and no studies to our knowledge have examined whether spikes in gene duplication tend to directly coincide with bursts of phenotypic novelty on a macroevolutionary scale, although clearly gene duplications have facilitated the origins of numerous key traits in plants 9,10,11 . It is possible that other processes — e.g., major fluctuations in population size during rapid speciation events, in concert with extrinsic factors such as climate change or ecological opportunity—may contribute more fundamentally to major phases of morphological innovation and diversification 12,13 . More realistically, however, these various phenomena may interact in complex ways to shape macroevolutionary patterns in plants and, more broadly, across the Tree of Life, and detailed case studies are needed to disentangle their relative contributions to the origins of phenotypic and taxonomic diversity.…”

“…It is possible that some of the phylogenetically deeper spikes in phenotypic innovation are exaggerated due to prevalent extinction of stem lineages with intermediate morphologies. However, the sudden appearance of major lineages with distinct morphologies is a common phenomenon across the Tree of Life 13 , and neofunctionalization of duplicate genes (and/or other results of gene or genome duplication) may serve as an important driver of instances of radical and rapid phenotypic change. A better integration of fossil and phylogenomic data might offer important insight into this question.…”