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Macroevolutionary Diversification Rates Show Time Dependency Macroevolutionary diversification rates show time dependency L. Francisco Henao Diaza,b, Luke J. Harmonc, Mauro T. C. Sugawaraa,b, Eliot T. Millerd, and Matthew W. Pennella,b,1 aDepartment of Zoology, University of British Columbia, Vancouver, BC, Canada V6T 1Z4; bBiodiversity Research Centre, University of British Columbia, Vancouver, BC, Canada V6T 1Z4; cDepartment of Biological Sciences, University of Idaho, Moscow, ID 83844; and dCornell Lab of Ornithology, Cornell University, Ithaca, NY 14850 Edited by David M. Hillis, The University of Texas at Austin, Austin, TX, and approved February 28, 2019 (received for review October 22, 2018) For centuries, biologists have been captivated by the vast disparity time dependence, with the fastest rates estimated over the shortest in species richness between different groups of organisms. time scales. This time scale dependence is apparent in rates of Variation in diversity is widely attributed to differences between molecular (12) and trait evolution (13, 14) and has even been groups in how fast they speciate or go extinct. Such macroevolu- observed when estimating long-term rates of sedimentation (15). tionary rates have been estimated for thousands of groups and The prevalence of time scaling of rate estimates in other types of have been correlated with an incredible variety of organismal data, along with previous hints of a possible similar pattern in traits. Here we analyze a large collection of phylogenetic trees and speciation rates (16–20), suggest that a broader comparison is fossil time series and describe a hidden generality among these needed. Here we explore the time scaling of diversification rates seemingly idiosyncratic results: speciation and extinction rates using both phylogenetic data from the tree of life and paleobio- follow a scaling law in which both depend on the age of the group logical data from the fossil record and find evidence that there are in which they are measured, with the fastest rates in the youngest indeed general scaling laws that govern macroevolutionary dy- clades. Using a series of simulations and sensitivity analyses, we namics of speciation and extinction. demonstrate that the time dependency is unlikely to be a result of simple statistical artifacts. As such, this time scaling is likely a Results and Discussion genuine feature of the tree of life, hinting that the dynamics of Using a Bayesian approach that allows for heterogeneity across EVOLUTION biodiversity over deep time may be driven in part by surprisingly the phylogeny (21), we estimated speciation and extinction rates simple and general principles. across 104 previously published time-calibrated molecular phy- logenies of multicellular organisms that collectively contain phylogenetics | paleobiology | macroevolution | speciation | extinction 25,864 terminal branches (SI Appendix, Table S1). As many other studies have reported, we found substantial variation in both lthough once controversial, it is now widely accepted that speciation (Fig. 1A) and extinction rates (SI Appendix, Fig. S5) Aboth the traits of organisms and the environments in which across groups, ranging from 0.02 to 1.54 speciation events per – they live can influence the pace of evolution of life on Earth (1 lineage per million years—a two-orders of magnitude difference 3). In particular, there is tremendous variation between groups (16, 22–25). Remarkably, a substantial amount of this variation of organisms in the rate at which species form and go extinct. in rates can be explained simply by time alone. We found a This variation is reflected both in the wildly uneven diversity of strong negative relationship between the mean rates of both clades in the fossil record and in the imbalanced shape of the speciation and extinction and the age of the most recent common – tree of life (2 5). Our estimates of speciation and extinction rates ancestor of a group (regression on speciation rates: β = −0.542; vary by orders of magnitude when comparing different clades, P < 0.001; R2 = 0.339; on extinction rates: β = −0.548; P < 0.001; locations, or time intervals. In turn, researchers have suggested a tremendous array of Significance mechanisms that may have accelerated or slowed the accumu- lation of biodiversity. These mechanisms include aspects of or- ganisms, such as color polymorphism (6), body size (7), and Some branches of the tree of life are incredibly diverse, while many others, and of the environment, including geographic re- others are represented by only a few living species. Ultimately, this difference reflects the balance of the formation and the gion (8, 9), temperature (10), and the interactions between the extinction of species. Countless explanations have been pro- two (11). Taken as a whole, this growing body of work implicates posed for why the rates of these two processes vary between a wide variety of factors that influence speciation and/or ex- lineages, including aspects of the organisms themselves and tinction rates and suggests that the growth of the tree of life has the environments they live in. Here we reveal that a substantial been largely idiosyncratic. amount of variation in these rates is associated with a simple Despite the rapid expansion of research on variation in spe- factor: time. Younger groups appear to accumulate diversity at ciation and extinction rates, few synthetic studies have been much faster rates than older groups. This time scaling of mac- attempted. Consequently, we know little about whether or not roevolutionary rates suggests that there may be hidden gen- there are common factors that predict speciation and extinction eralities governing the diversification of life on Earth. rates across diverse taxa (2). One hurdle to such synthesis is that studies, especially those using the tree of life, often focus more Author contributions: L.F.H.D., L.J.H., and M.W.P. designed research; L.F.H.D. and M.T.C.S. on relative than absolute diversification rates. That is, studies are performed research; E.T.M. contributed new reagents/analytic tools; L.F.H.D. and M.T.C.S. focused more on whether speciation or extinction rates are analyzed data; and L.F.H.D., L.J.H., M.T.C.S., E.T.M., and M.W.P. wrote the paper. higher in one part of a phylogenetic tree than in another part, The authors declare no conflict of interest. rather than attempting to estimate those rates in absolute terms. This article is a PNAS Direct Submission. This makes comparisons across studies difficult or impossible. Published under the PNAS license. Another compelling reason to gather and compare estimates of 1To whom correspondence should be addressed. Email: [email protected]. speciation and extinction rates across clades is the potential for This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. scale-dependence. In all other instances when macroevolutionary 1073/pnas.1818058116/-/DCSupplemental. rates have been compared, these rates have shown a pattern of Published online March 25, 2019. www.pnas.org/cgi/doi/10.1073/pnas.1818058116 PNAS | April 9, 2019 | vol. 116 | no. 15 | 7403–7408 Downloaded by guest on September 29, 2021 AB 30 20 15 20 10 10 5 0 0 0.0 0.5 1.0 1.5 0.0 0.1 0.2 0.3 0.4 0.5 − − Mean λ (species Myr 1) Mean origination (genera Myr 1) Fig. 1. Histogram of mean speciation (λ) and origination rates. (A) The lowest speciation rate is for the fern family Matoniaceae (0.02), and the highest is for the subfamily Lobelioidae (1.54). (B) The lowest origination rate is for the order Pinales (0.02), and the highest is for the order Cingulata (0.34). Note that the axes have different magnitudes. R2 = 0.155) (Fig. 2 A and B). In general, regardless of the tax- environment that organisms have recently colonized will likely be onomic identity, ecological characteristics, or biogeographic associated with an increase in diversification. It is beyond the distribution of the group, younger clades appeared to be both scope of the present article to discuss what precisely constitutes speciating and going extinct faster than older groups. evidence of causality in macroevolutionary studies, but we sug- We also recovered this same scaling pattern using an in- gest that it is certainly not a coincidence that many of the regions dependent dataset of fossil time series, demonstrating that the of the world commonly recognized as hotspots of diversification time dependency of diversification rates is a general evolutionary (at least over the past several million years) are also precisely phenomenon and not simply a consequence of using extant-only those regions that harbor young groups of organisms, such as the data. We estimated origination and extinction rates from a cu- Páramo of the Andes (31), oceanic islands (32), and polar rated set of fossil time series comprising 17 orders of mammals, seas (23). 22 orders of plants, and 51 orders of marine animals (mostly Potential causes of this ubiquitous pattern fall into two main invertebrates), containing representatives from 6,144 genera (SI categories. First, our results may be statistically biased; the un- Appendix, Table S2), using the widely used per capita method derlying process of diversification may be consistent with that (25). For fossil data, we measured time as the duration over assumed by diversification models with constant rates, but our which a clade of fossil organisms existed and analyzed the for- statistical methods are biased toward recovering time dependence. mation and extinction of genera rather than species. We found Second, our results may reflect biological generality; the true dy- that both origination (β = −0.227; P < 0.001; R2 = 0.152; Fig. 2C) namics of diversification over macroevolutionary time scales show and extinction (β = −0.245; P < 0.01; R2 = 0.126; Fig.
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