The rise of angiosperms pushed conifers to decline during global cooling

Abstract

Competition among species and entire clades can impact species diversification and extinction, which can shape macroevolutionary patterns. The fossil record shows successive biotic turnovers such that a dominant group is replaced by another. One striking example involves the decline of gymnosperms and the rapid diversification and ecological dominance of angiosperms in the Cretaceous. It is generally believed that angiosperms outcompeted gymnosperms, but the macroevolutionary processes and alternative drivers explaining this pattern remain elusive. Using extant time trees and vetted fossil occurrences for conifers, we tested the hypotheses that clade competition or climate change led to the decline of conifers at the expense of angiosperms. Here, we find that both fossil and molecular data show high congruence in revealing 1) low diversification rates, punctuated by speciation pulses, during warming events throughout the Phanerozoic and 2) that conifer extinction increased significantly in the Mid-Cretaceous (100 to 110 Ma) and remained high ever since. Their extinction rates are best explained by the rise of angiosperms, rejecting alternative models based on either climate change or time alone. Our results support the hypothesis of an active clade replacement, implying that direct competition with angiosperms increased the extinction of conifers by pushing their remaining species diversity and dominance out of the warm tropics. This study illustrates how entire branches on the Tree of Life may actively compete for ecological dominance under changing climates.

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

“…Future biogeographic analyses integrating fossil evidence might shed light on the geographic context of these coordinated climatic-diversification shifts. In general, our results challenge suggestions that recent climatic cooling precipitated macroevolutionary declines in conifers 54 (Supplementary Information). The Northern and Southern Hemispheres, however, clearly do show distinct patterns with respect to the extinction and turnover of conifer diversity during the Cenozoic 21 , and numerous extant gymnosperm species (especially cycads) are at risk of extinction due to pressures including habitat destruction 55,56,57 .…”

Angiosperms versus gymnosperms in the Cretaceous

“…A major challenge in all evolutionary biology is to understand what factors regulate the long-term origination and extinction of taxa and thus the rise and fall of entire clades. This challenge is increased further by accumulating evidence that each clade may follow different diversity trajectories through time (3). These different trajectories may result from the fact that contrasting causes of speciation and extinction may lead to some clades rising, declining, or replacing each other (3).…”

“…As a botany student in the mid-1960s, I was taught this not as a hypothesis but as an "established fact." In PNAS, Condamine et al (3) use all of the available fossil and molecular data for conifers to test the competing hypotheses that competition from angiosperms, climate change, or time alone led to the decline of conifers to the benefit of angiosperms. Results from detailed numerical analyses suggest that the increased extinction rates of conifers in the Mid-and Late Cretaceous are most parsimoniously interpreted as a response to the rise of angiosperms, and the alternative hypotheses of climate change or time alone as drivers of the conifer demise are falsified (3).…”

“…Their maximum-likelihood and Bayesian methods integrate the possible role of abiotic (climate change) and biotic (relative diversity of angiosperms) factors as possible drivers of conifer patterns. The most probable model is that angiosperms outcompeted conifers during the rapid rise of angiosperms in the Mid-Cretaceous under conditions of long-term global cooling (3). Is this general type of conclusion the likely scenario in the long-term evolutionary history of other plant groups?…”

Mountain radiations are not only rapid and recent: Ancient diversification of South American frog and lizard families related to Paleogene Andean orogeny and Cenozoic climate variations

“…Although in phylogenetic studies, diversity dependence is typically tested within a single clade (Etienne et al 2012), our phylogeny-based diversification model can be extended to allow for competition among species that are not closely related, but share similar ecological niches (Condamine et al 2020).…”