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.

Keywords: competition; gymnosperms; macroevolution; paleoenvironment.

Fig. 1.

An overview of hypothetical determinants of conifer diversification over time. Conifer evolution was punctuated by (A) four known mass extinction events (red arrows). Biotic events (B), such as the evolution of leaf shape and the appearance of competitor clades (e.g., angiosperms), are likely to be important drivers of diversification. Environmental (abiotic) changes may also impact diversity dynamics, including the paleoclimate (C), with global temperature (red curve highlighting the cooling and warming events), atmospheric carbon (black curve), or sea-level fluctuations (blue curve), as well as the paleogeology (D), such as plate tectonic movements (global paleogeographic changes) or volcanism. CAMP, Central Atlantic magmatic province. C, Carboniferous; D, Devonian; J, Jurassic; K, Cretaceous; Ng, Neogene; P, Permian; Pg, Paleogene; Tr, Triassic.

Fig. 2.

Global diversification of conifers inferred from a molecular phylogeny and the fossil record. (A) Time-calibrated phylogeny of conifers and significant shifts in diversification rates (shown by red circles) inferred with an episodic birth–death model (SI Appendix, Table S1). Six shifts of diversification rates were identified: two shifts occurred at the end of the Permian (a single red circle for the two), one occurred during the Cretaceous terrestrial revolution (rise of angiosperms), one occurred at the end of the Oligocene, and two shifts were found in the Pliocene and Pleistocene (a single red circle for the two). (B) Rates of origination (blue), extinction (red), and net diversification rates (black; the difference between origination and extinction) inferred from a fossil-based analysis at the genus level, including Cordaitales, under the Bayesian approach implemented in PyRate (SI Appendix, Fig. S3 shows analyses without Cordaitales). Solid lines indicate mean posterior rates, and the shaded areas show 95% credibility intervals. Taken together, the phylogeny-based (A) and fossil-based (B) diversifications show 1) that diversification of conifers was low and punctuated by periods of extinction, 2) that the increase in extinction initiated in the Middle Cretaceous, and 3) the Cenozoic decline of conifers. The vertical dashed lines indicate the boundaries between geological boundaries and major mass extinction events. C, Carboniferous; Ceph., Cephalotaxaceae; D, Devonian; J, Jurassic; K, Cretaceous; Ng, Neogene; P, Permian; Pg, Paleogene; Sciad., Sciadopityaceae; Tax., Taxaceae; Tr, Triassic.

Fig. 3.

Drivers of conifer diversification dynamics according to two putative causes of rate variation: global temperature changes (A) and angiosperm diversity (B). Based on oxygen isotopes (69), the mean global temperature curve is a proxy for the main climatic events in the last 350 My. The changes of angiosperm diversity through time show the rise of angiosperms during the Cretaceous as inferred by fossil-based analyses of vascular plants (27). Solid lines indicate mean parameter estimates (C) and mean posterior estimates (D) of the rates, and the shaded areas show CIs and 95% credibility intervals, respectively. Taken together, the phylogeny-based (C) and fossil-based (D) correlations show that 1) changes in angiosperm diversity correlate positively with extinction rates of conifers and 2) the variation of temperatures correlates negatively with extinction rate of conifers. C, Carboniferous; D, Devonian; J, Jurassic; K, Cretaceous; Ng, Neogene; P, Permian; Pg, Paleogene; Tr, Triassic.