Diversification dynamics in the Neotropics through time, clades and biogeographic regions

  1. Andrea S Meseguer  Is a corresponding author
  2. Alice Michel
  3. Pierre-Henri Fabre
  4. Oscar A Pérez Escobar
  5. Guillaume Chomicki
  6. Ricarda Riina
  7. Alexandre Antonelli
  8. Pierre-Olivier Antoine
  9. Frédéric Delsuc
  10. Fabien Condamine
  1. Real Jardín Botánico (RJB), CSIC, Spain
  2. University of California, Davis, United States
  3. Université de Montpellier, UMR 5554 CNRS, France
  4. Royal Botanic Gardens, United Kingdom
  5. University of Sheffield, United Kingdom

Abstract

The origins and evolution of the outstanding Neotropical biodiversity are a matter of intense debate. A comprehensive understanding is hindered by the lack of deep-time comparative data across wide phylogenetic and ecological contexts. Here, we quantify the prevailing diversification trajectories and drivers of Neotropical diversification in a sample of 150 phylogenies (12,512 species) of seed plants and tetrapods, and assess their variation across Neotropical regions and taxa. Analyses indicate that Neotropical diversity has mostly expanded through time (70% of the clades), while scenarios of saturated and declining diversity account for 21% and 9% of Neotropical diversity, respectively. Five biogeographic areas are identified as distinctive units of long-term Neotropical evolution, including Pan-Amazonia, the Dry Diagonal, and Bahama-Antilles. Diversification dynamics do not differ across these areas, suggesting no geographic structure in long-term Neotropical diversification. In contrast, diversification dynamics differ across taxa: plant diversity mostly expanded through time (88%), while a substantial fraction (43%) of tetrapod diversity accumulated at a slower pace or declined toward the present. These opposite evolutionary patterns may reflect different capacities for plants and tetrapods to cope with past climate changes.

Data availability

The chronogram dataset and the diversification results are archived in Dryad (72). All other data used or generated in this manuscript are presented in the manuscript, or its supplementary material.

The following data sets were generated

Article and author information

Author details

  1. Andrea S Meseguer

    Real Jardín Botánico (RJB), CSIC, Madrid, Spain
    For correspondence
    asanchezmeseguer@gmail.com
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0743-404X
  2. Alice Michel

    Department of Anthropology, University of California, Davis, California, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Pierre-Henri Fabre

    Institut des Sciences de l'Evolution, Université de Montpellier, UMR 5554 CNRS, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  4. Oscar A Pérez Escobar

    Royal Botanic Gardens, Kew, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Guillaume Chomicki

    Ecology and Evolutionary Biology, University of Sheffield, Sheffield, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Ricarda Riina

    Real Jardín Botánico (RJB), CSIC, Madrid, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Alexandre Antonelli

    Royal Botanic Gardens, Kew, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  8. Pierre-Olivier Antoine

    Institut des Sciences de l'Evolution, Université de Montpellier, UMR 5554 CNRS, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
  9. Frédéric Delsuc

    Institut des Sciences de l'Evolution, Université de Montpellier, UMR 5554 CNRS, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6501-6287
  10. Fabien Condamine

    Institut des Sciences de l'Evolution, Université de Montpellier, UMR 5554 CNRS, Montpellier, France
    Competing interests
    The authors declare that no competing interests exist.

Funding

Agence Nationale de la Recherche (ANR-10-LABX-25-01)

  • Pierre-Olivier Antoine
  • Frédéric Delsuc
  • Fabien Condamine

Agence Nationale de la Recherche (ANR-17-CE31-0009)

  • Pierre-Olivier Antoine
  • Frédéric Delsuc
  • Fabien Condamine

Ministerio de Ciencia e Innovación (PID2020-120145GA-I00)

  • Andrea S Meseguer

Comunidad Autonoma de Madrid, Atraccion de Talento (2019-T1/AMB-12648)

  • Andrea S Meseguer

Ministerio de Ciencia e Innovación (PID2019-108109GB-I00)

  • Ricarda Riina

Swedish Research Council (2019-05191)

  • Alexandre Antonelli

Natural Environment Research Council (NE/S014470/1)

  • Guillaume Chomicki

Swiss Orchid Foundation

  • Oscar A Pérez Escobar

Ministerio de Ciencia e Innovación (IJCI-2017-32301)

  • Andrea S Meseguer

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. David A. Donoso, Escuela Politécnica Nacional, Ecuador

Version history

  1. Preprint posted: February 25, 2021 (view preprint)
  2. Received: October 7, 2021
  3. Accepted: October 26, 2022
  4. Accepted Manuscript published: October 27, 2022 (version 1)
  5. Accepted Manuscript updated: October 28, 2022 (version 2)
  6. Version of Record published: November 16, 2022 (version 3)

Copyright

© 2022, Meseguer et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

Metrics

  • 1,889
    views
  • 502
    downloads
  • 6
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Andrea S Meseguer
  2. Alice Michel
  3. Pierre-Henri Fabre
  4. Oscar A Pérez Escobar
  5. Guillaume Chomicki
  6. Ricarda Riina
  7. Alexandre Antonelli
  8. Pierre-Olivier Antoine
  9. Frédéric Delsuc
  10. Fabien Condamine
(2022)
Diversification dynamics in the Neotropics through time, clades and biogeographic regions
eLife 11:e74503.
https://doi.org/10.7554/eLife.74503

Share this article

https://doi.org/10.7554/eLife.74503

Further reading

    1. Evolutionary Biology
    Robert Horvath, Nikolaos Minadakis ... Anne C Roulin
    Research Article

    Understanding how plants adapt to changing environments and the potential contribution of transposable elements (TEs) to this process is a key question in evolutionary genomics. While TEs have recently been put forward as active players in the context of adaptation, few studies have thoroughly investigated their precise role in plant evolution. Here, we used the wild Mediterranean grass Brachypodium distachyon as a model species to identify and quantify the forces acting on TEs during the adaptation of this species to various conditions, across its entire geographic range. Using sequencing data from more than 320 natural B. distachyon accessions and a suite of population genomics approaches, we reveal that putatively adaptive TE polymorphisms are rare in wild B. distachyon populations. After accounting for changes in past TE activity, we show that only a small proportion of TE polymorphisms evolved neutrally (<10%), while the vast majority of them are under moderate purifying selection regardless of their distance to genes. TE polymorphisms should not be ignored when conducting evolutionary studies, as they can be linked to adaptation. However, our study clearly shows that while they have a large potential to cause phenotypic variation in B. distachyon, they are not favored during evolution and adaptation over other types of mutations (such as point mutations) in this species.

    1. Evolutionary Biology
    Zhiliang Zhang, Zhifei Zhang ... Guoxiang Li
    Research Article

    Biologically-controlled mineralization producing organic-inorganic composites (hard skeletons) by metazoan biomineralizers has been an evolutionary innovation since the earliest Cambrian. Among them, linguliform brachiopods are one of the key invertebrates that secrete calcium phosphate minerals to build their shells. One of the most distinct shell structures is the organo-phosphatic cylindrical column exclusive to phosphatic-shelled brachiopods, including both crown and stem groups. However, the complexity, diversity, and biomineralization processes of these microscopic columns are far from clear in brachiopod ancestors. Here, exquisitely well-preserved columnar shell ultrastructures are reported for the first time in the earliest eoobolids Latusobolus xiaoyangbaensis gen. et sp. nov. and Eoobolus acutulus sp. nov. from the Cambrian Series 2 Shuijingtuo Formation of South China. The hierarchical shell architectures, epithelial cell moulds, and the shape and size of cylindrical columns are scrutinised in these new species. Their calcium phosphate-based biomineralized shells are mainly composed of stacked sandwich columnar units. The secretion and construction of the stacked sandwich model of columnar architecture, which played a significant role in the evolution of linguliforms, is highly biologically controlled and organic-matrix mediated. Furthermore, a continuous transformation of anatomic features resulting from the growth of diverse columnar shells is revealed between Eoobolidae, Lingulellotretidae, and Acrotretida, shedding new light on the evolutionary growth and adaptive innovation of biomineralized columnar architecture among early phosphatic-shelled brachiopods during the Cambrian explosion.