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Loss of macroevolutionary species fitness explains the rise and fall of clades

Nature Ecology & Evolution volume 9, pages 2346–2357 (2025)Cite this article

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Abstract

How and why species diversity varies over geological timescales remains disputed. Debate revolves around the existence of equilibrium dynamics, the predominance of adaptive radiations and the relative importance of speciation and extinction in driving diversity trajectories. We analyse the evolutionary history of 27 radiations of plants, arthropods and vertebrates, with phylogenetic information incorporating extinct and extant species under a new ‘fossilized birth–death diffusion’ model that provides a detailed characterization of past diversification and resulting diversity dynamics. Here, lineages undergo speciation and extinction rates that diffuse continuously in time and generate fossils with rates that can vary with stratigraphy. Clade diversity trajectories follow rise and decline dynamics, with fast accumulation following recurrent speciation while slowdowns and losses are modulated primarily by changes in extinction. Diversity dynamics do not appear to be governed by clade-level processes expected from adaptive radiations or diversity dependence. Rather, these patterns emerge from dynamics at the species level, where lineages tend to become increasingly vulnerable to extinction and less likely to speciate with time. Those species that counteract this trend create and maintain biodiversity through deep time. The rise and fall of clades results from species-level fates.

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Fig. 1: Rise, decline and fall of diversity show asymmetries for 27 taxonomic groups.
The alternative text for this image may have been generated using AI.
Fig. 2: Relative importance of speciation versus extinction in driving diversification dynamics.
The alternative text for this image may have been generated using AI.
Fig. 3: Diversity trajectories and their underlying diversification dynamics across subclades.
The alternative text for this image may have been generated using AI.
Fig. 4: The insidious loss of macroevolutionary species fitness.
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Data availability

All data used for the empirical analyses are available via Zenodo at https://doi.org/10.5281/zenodo.15535408 (ref. 76).

Code availability

All code used for the empirical analyses is available via Zenodo at https://doi.org/10.5281/zenodo.15535408 (ref. 76). Inference of the CFBD, eFBD and FBDD models can be found in the Tapestree package v0.4.1 for Julia available at https://github.com/ignacioq/Tapestree.jl.

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Acknowledgements

We thank the Morlon lab for early discussion of these ideas. D.S. received funding from ETH Zurich and the Swedish Foundation for Strategic Environmental Research MISTRA within the framework of the research programme BIOPATH (F 2022/1448). H.M. received funding from the ANR (ANR-21-CE02-0010).

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Authors and Affiliations

  1. Institut de Biologie de l’ENS (IBENS), Département de Biologie, École Normale Supérieure, CNRS, INSERM, Université PSL, Paris, France

    Ignacio Quintero, Jérémy Andréoletti & Hélène Morlon

  2. Department of Biosystems Science and Engineering, ETH Zurich, Basel, Switzerland

    Daniele Silvestro

  3. Department of Biological and Environmental Sciences, University of Gothenburg, Gothenburg, Sweden

    Daniele Silvestro

  4. Gothenburg Global Biodiversity Centre, University of Gothenburg, Gothenburg, Sweden

    Daniele Silvestro

  5. Swiss Institute of Bioinformatics, Basel, Switzerland

    Daniele Silvestro

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  1. Ignacio Quintero
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  2. Jérémy Andréoletti
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Contributions

I.Q. and H.M. designed the research and wrote most of the paper. I.Q. and J.A. developed the model and implemented the code. I.Q. synthesized the empirical data and conducted the analyses. D.S. discussed and introduced model ideas. All authors contributed to writing.

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Correspondence to Ignacio Quintero.

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Extended data

Extended Data Fig. 1 The fossilized birth-death diffusion (FBDD) model with data augmentation (DA).

A An empirical (reconstructed) fossilized birth-death (FBD) tree, with fossils depicted as blue squares. Those fossils that do not have descendants in the empirical tree are labelled ‘tip fossils’ and the rest are labelled as ‘sampled ancestors’. B One sample from the posterior of a complete (data augmented) tree, in which unsampled (unobserved because of extinction or undersampling at the present) lineages are probabilistically ‘imputed’ using Bayesian DA. These ‘augmented’ lineages are shown in gray while the original empirical tree is left in black (notice that these black lineages are perfectly compatible with the reconstructed tree in A). C The latent speciation and D the latent extinction rates that follow a Geometric Brownian motion (GBM) from the posterior DA tree as specified by the FBDD (warmer colors represent higher rates). For extinction we show a subsection of the rates in the tree where the latter are now shown as the y axis.

Extended Data Fig. 2 Impact of number of fossils per tree size on turnover rates.

Posterior mean turnover rates (that is, μ/λ) based on 1000 posterior samples from the eFBD against the number of fossils per tree size (number of tips, both extant or extinct) for the 27 taxa studied here. With even a low percentage of fossils per tree size we already recover high rates of turnover. Enumeration of taxa, in order of appearance: 1) eurypterida, 2) dipnoi, 3) therocephalia, 4) sphenodontidae, 5) testudinata, 6) pterosauria, 7) dinosauria, 8) crocodylomorpha, 9) juglandaceae, 10) tetraodontiformes, 11) mauritiinae, 12) acanthuridae, 13) siganidae, 14) spheniscidae, 15) proboscidea, 16) brontotheriioidea, 17) cetacea, 18) zoarcoidei, 19) ruminantia, 20) sthenurinae, 21) folivora, 22) centrarchidae, 23) platyrrhines, 24) pinnipedia, 25) caninae, 26) equinae, 27) hominini.

Extended Data Fig. 3 Validation of fossilized birth-death diffusion (FBDD) with constant fossilization rates.

Each row represents the results for 5 scenarios that evaluate the impact of increasing rate of fossilization, from top to bottom: ψ = 0.05, ψ = 0.1, ψ = 0.5, ψ = 1.0ψ = 2.0. For each scenario, we sampled from a range of parameter values across αλ, αμ, σλ and σμ and conducted 100 simulations with subsequent inference under the FBDD. For αλ, αμ, σλ and σμ, each of the 100 simulated (true) values are shown against the posterior median and their 95 % Credible Interval (CI) based on 1000 posterior samples. Colored diagonal solid lines show the loess fit across medians, and the dashed circumscribing ones the 95% Credible Interval (CI). Black dashed lines show the 1:1 line. For ψ, the horizontal punctuated line shows the simulated (true) value, and the medians and 95% CI are shown as points and horizontal bars, respectively. Top left percentages represent the statistical coverage. We sampled the distributions of speciation and extinction along the posterior trees and show the mean relative error for speciation λ(t) and extinction μ(t) as well as their statistical coverage.

Extended Data Fig. 4 Validation of fossilized birth-death diffusion (FBDD) with varying fossilization rates.

Details as in ED figure 3 but with three scenarios of varying rates of fossilization, ψ(t), where the ‘true’ values are shown in dashed black horizontal lines.

Extended Data Fig. 5 Diversity trajectories for the 27 evolutionary radiations studied.

For each clade, 100 diversity trajectories are shown from a posterior sample of 100 complete trees. The asymmetry measured with the parametric approach (Methods) is given next to the clade name for clades in decline or fall, and the inset panel shows the distribution of Center of Gravity (CG; Methods) across the 100 trees. Caninae, Centrarchidae, and Sthenurinae are in decline, with larger diversity before the present, but because this past peak was very close to the present, the parametric model was not able to pick up a subsequent downward trend, rather just assuming is part of the expected variance. These three clades correspond then to the three points with asymmetry of 1 in main text Fig. 1.

Extended Data Fig. 6 Samples of diversity trajectories from constant birth-death simulations.

Results from the three level hierarchical auto-regressive model testing for an effect of diversity on average speciation or extinction rates (Methods). For each clade, 100 posterior samples of diversity and average speciation and extinction rates were used to conduct the regression. Posterior probabilities for diversity dependence were estimated from 1000 posterior samples from the hierarchical model. The top row shows the global effects (β2) left for speciation in blue and right for extinction in red. Note that the 95 % Credible Interval (CI) contains 0. The bottom row shows the clade specific effects of diversity on left speciation and right extinction. Clades are shown in order of first appearance. The black vertical bars, the darker-shaded rectangles and the lighter-shaded rectangles represent, respectively, the posterior mean, the 50% CI and the 95% CI.

Extended Data Fig. 7 No effect of diversity on average speciation and extinction rates.

Examples of the 800 total simulated diversity trajectories using a constant-birth death model with turnover (μ/λ) of 1, using λ = 1 and μ = 1 over 10 time units. The first 400 simulations (left) were conditioned on at least having 100 extinct tips, with 200 trajectories of clades in decline and 200 trajectories for clades that went extinct (fall). The second set of 400 simulations (right) were conditioned on clades that had from 20 to 40 tips, with 200 trajectories for clades in decline and 200 for clades that went extinct. 5 examples from each of the 200 simulations of the 4 categories above are shown.

Extended Data Fig. 8 Sample of subclade diversity trajectories for the first 14 larger taxonomic groups.

Each row is a clade, and each column is a randomly sampled diversity trajectory from a subclade (holding 20 to 40 species). Time is standardized to 1 unit. In light blue we show the subclade diversity and in black we show the Expectation of the Negative Binomial regression (Methods) of the diversity trajectory. Note the great variation in diversity trajectories across subclades for a given taxonomic group.

Extended Data Fig. 9 Sample of subclade diversity trajectories for the second 13 larger clades.

Details as in Extended Data Fig. 8 but for the remaining 13 clades.

Extended Data Fig. 10 Posterior distributions for the governing parameters from the FBDD model across evolutionary radiations.

Posterior distributions for each sample, with their density scaled for visual purposes, stacked over the set of empirical trees for each taxonomic group for, from top to bottom, αλ, αμ, σλ and σμ. For αλ and αμ, the rightmost distribution displays the overall posterior distribution given by the hierarchical cross-taxa model used to plot Fig. 4 (Methods).

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Quintero, I., Andréoletti, J., Silvestro, D. et al. Loss of macroevolutionary species fitness explains the rise and fall of clades. Nat Ecol Evol 9, 2346–2357 (2025). https://doi.org/10.1038/s41559-025-02873-7

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