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. 2024 Mar 26;121(13):e2317795121.
doi: 10.1073/pnas.2317795121. Epub 2024 Mar 11.

The Angiosperm Terrestrial Revolution buffered ants against extinction

Corentin Jouault  1   2   3 , Fabien L Condamine #  2 , Frédéric Legendre #  1 , Vincent Perrichot #  3
Affiliations

The Angiosperm Terrestrial Revolution buffered ants against extinction

Corentin Jouault et al. Proc Natl Acad Sci U S A. .

Abstract

With ~14,000 extant species, ants are ubiquitous and of tremendous ecological importance. They have undergone remarkable diversification throughout their evolutionary history. However, the drivers of their diversity dynamics are not well quantified or understood. Previous phylogenetic analyses have suggested patterns of diversity dynamics associated with the Angiosperm Terrestrial Revolution (ATR), but these studies have overlooked valuable information from the fossil record. To address this gap, we conducted a comprehensive analysis using a large dataset that includes both the ant fossil record (~24,000 individual occurrences) and neontological data (~14,000 occurrences), and tested four hypotheses proposed for ant diversification: co-diversification, competitive extinction, hyper-specialization, and buffered extinction. Taking into account biases in the fossil record, we found three distinct diversification periods (the latest Cretaceous, Eocene, and Oligo-Miocene) and one extinction period (Late Cretaceous). The competitive extinction hypothesis between stem and crown ants is not supported. Instead, we found support for the co-diversification, buffered extinction, and hyper-specialization hypotheses. The environmental changes of the ATR, mediated by the angiosperm radiation, likely played a critical role in buffering ants against extinction and favoring their diversification by providing new ecological niches, such as forest litter and arboreal nesting sites, and additional resources. We also hypothesize that the decline and extinction of stem ants during the Late Cretaceous was due to their hyper-specialized morphology, which limited their ability to expand their dietary niche in changing environments. This study highlights the importance of a holistic approach when studying the interplay between past environments and the evolutionary trajectories of organisms.

Keywords: birth–death models; macroevolution; paleoenvironment; ​flowering plants; ​​Formicoidea.

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Conflict of interest statement

Competing interests statement:The authors declare no competing interest.

Figures

Fig. 1.
Fig. 1.
Main hypotheses to explain the past diversity dynamics of ants. (A) Hyper-specialization hypothesis, with the diversity of stem ants decreasing during the ATR while their extinction increased due to their inability to adapt to environmental changes. As a result, a significant positive correlation is expected between the extinction of stem ants and the rise of angiosperms. (B) Competitive extinction hypothesis with a double-wedge pattern. The expected results for this hypothesis are a significant positive correlation between the extinction of stem ants and the increase of diversity in crown ants (the same for crown ants) and a significant negative correlation between the origination of stem ants and the increase of diversity in crown ants (the same for crown ants). (C) Co-diversification hypothesis, with the diversity and origination of ants increasing synchronously to angiosperms diversification. The expected result for this hypothesis is a significant positive correlation between ant origination and the rise of angiosperms. (D) Buffer hypothesis, with the diversity of ants increasing synchronously with angiosperm diversification and extinction decreasing oppositely. The expected result for this hypothesis is a significant negative correlation between ants extinction and angiosperm diversification (i.e., angiosperms tend to decrease ants extinction). The green block represents the ATR. Silhouettes from http://phylopic.org/. Licenses at https://creativecommons.org/publicdomain/zero/1.0/ or by Corentin Jouault.
Fig. 2.
Fig. 2.
Diversification and diversity dynamics of ants. Bayesian estimates of origination (blue), extinction (red), net diversification (black, origination minus extinction) rates, and diversity of all ants inferred from paleontological data (A–C), from the combination of paleontological and neontological data (D–F) and from the combination but without singletons (G–I). Net diversification decreased during the Late Cretaceous. Ants diversified during the latest Cretaceous, the Eocene, and the Oligo-Miocene. The diversity of ant genera greatly increases just after the K/Pg, with a rebound after the Eocene (partially due to the Baltic amber). Reconstructions of diversity trajectories replicated to incorporate uncertainties around the age of the fossils. Solid lines indicate mean posterior diversity, and the shaded areas show 95% credibility intervals. The red vertical line indicates the Cretaceous–Paleogene boundary (K/Pg). The green period represents the ATR. Time is in millions of years. The color of each geological period in the chronostratigraphic scale follows that of the International Chronostratigraphic Chart (v2022/02). Silhouettes and other items by Corentin Jouault. EC, Early Cretaceous; LC, Late Cretaceous; P, Paleocene; E, Eocene; O, Oligocene; M, Miocene.
Fig. 3.
Fig. 3.
Paleoenvironmental correlates and potential drivers of the diversification dynamics of ants. Bayesian inference of correlation parameters on origination (blue: A, C, E, and G) and extinction (red: B, D, F, and H) with abiotic factors like global temperature, continental fragmentation, sea level fluctuations, global variation of atmospheric CO2 and O2; and with biotic factors like relative diversity through time of Polypodiales ferns, non-Polypodiales ferns, gymnosperms, spore-plants, and angiosperms; and diversity-dependence factors with diversity through time of ant lineages. (C and D) 19.11% of genera removed (singletons); (G and H) 11.22% of genera removed (singletons). Stars indicate a significant correlation parameter for a given variable [shrinkage weights (ω) > 0.5]. Silhouettes from http://phylopic.org/. Licenses at https://creativecommons.org/publicdomain/zero/1.0/ or by Corentin Jouault.
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