Megaevolutionary dynamics and the timing of evolutionary innovation in reptiles

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Abstract

The origin of phenotypic diversity among higher clades is one of the most fundamental topics in evolutionary biology. However, due to methodological challenges, few studies have assessed rates of evolution and phenotypic disparity across broad scales of time to understand the evolutionary dynamics behind the origin and early evolution of new clades. Here, we provide a total-evidence dating approach to this problem in diapsid reptiles. We find major chronological gaps between periods of high evolutionary rates (phenotypic and molecular) and expansion in phenotypic disparity in reptile evolution. Importantly, many instances of accelerated phenotypic evolution are detected at the origin of major clades and body plans, but not concurrent with previously proposed periods of adaptive radiation. Furthermore, strongly heterogenic rates of evolution mark the acquisition of similarly adapted functional types, and the origin of snakes is marked by the highest rates of phenotypic evolution in diapsid history.

Abstract

The dynamics of how major clades and body plans arise and evolve in deep time remain poorly understood. Here, Simões et al. report major time lags between phases of rapid phenotypic change at the origin of major reptile lineages and periods of fast molecular change and adaptive radiation.

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The Cambrian conundrum: early divergence and later ecological success in the early history of animals.

Douglas Erwin, Marc Laflamme, Sarah Tweedt … (2011)

Diverse bilaterian clades emerged apparently within a few million years during the early Cambrian, and various environmental, developmental, and ecological causes have been proposed to explain this abrupt appearance. A compilation of the patterns of fossil and molecular diversification, comparative developmental data, and information on ecological feeding strategies indicate that the major animal clades diverged many tens of millions of years before their first appearance in the fossil record, demonstrating a macroevolutionary lag between the establishment of their developmental toolkits during the Cryogenian [(850 to 635 million years ago (Ma)], and the later ecological success of metazoans during the Ediacaran (635 to 541 Ma) and Cambrian (541 to 488 Ma) periods. We argue that this diversification involved new forms of developmental regulation, as well as innovations in networks of ecological interaction within the context of permissive environmental circumstances.

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The genomic substrate for adaptive radiation in African cichlid fish

David Brawand, Catherine E. Wagner, Yang I. Li … (2014)

Cichlid fishes are famous for large, diverse and replicated adaptive radiations in the Great Lakes of East Africa. To understand the molecular mechanisms underlying cichlid phenotypic diversity, we sequenced the genomes and transcriptomes of five lineages of African cichlids: the Nile tilapia (Oreochromis niloticus), an ancestral lineage with low diversity; and four members of the East African lineage: Neolamprologus brichardi/pulcher (older radiation, Lake Tanganyika), Metriaclima zebra (recent radiation, Lake Malawi), Pundamilia nyererei (very recent radiation, Lake Victoria), and Astatotilapia burtoni (riverine species around Lake Tanganyika). We found an excess of gene duplications in the East African lineage compared to tilapia and other teleosts, an abundance of non-coding element divergence, accelerated coding sequence evolution, expression divergence associated with transposable element insertions, and regulation by novel microRNAs. In addition, we analysed sequence data from sixty individuals representing six closely related species from Lake Victoria, and show genome-wide diversifying selection on coding and regulatory variants, some of which were recruited from ancient polymorphisms. We conclude that a number of molecular mechanisms shaped East African cichlid genomes, and that amassing of standing variation during periods of relaxed purifying selection may have been important in facilitating subsequent evolutionary diversification.

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A Total-Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera

Fredrik Ronquist, Seraina Klopfstein, Lars Vilhelmsen … (2012)

Phylogenies are usually dated by calibrating interior nodes against the fossil record. This relies on indirect methods that, in the worst case, misrepresent the fossil information. Here, we contrast such node dating with an approach that includes fossils along with the extant taxa in a Bayesian total-evidence analysis. As a test case, we focus on the early radiation of the Hymenoptera, mostly documented by poorly preserved impression fossils that are difficult to place phylogenetically. Specifically, we compare node dating using nine calibration points derived from the fossil record with total-evidence dating based on 343 morphological characters scored for 45 fossil (4--20 complete) and 68 extant taxa. In both cases we use molecular data from seven markers (∼5 kb) for the extant taxa. Because it is difficult to model speciation, extinction, sampling, and fossil preservation realistically, we develop a simple uniform prior for clock trees with fossils, and we use relaxed clock models to accommodate rate variation across the tree. Despite considerable uncertainty in the placement of most fossils, we find that they contribute significantly to the estimation of divergence times in the total-evidence analysis. In particular, the posterior distributions on divergence times are less sensitive to prior assumptions and tend to be more precise than in node dating. The total-evidence analysis also shows that four of the seven Hymenoptera calibration points used in node dating are likely to be based on erroneous or doubtful assumptions about the fossil placement. With respect to the early radiation of Hymenoptera, our results suggest that the crown group dates back to the Carboniferous, ∼309 Ma (95% interval: 291--347 Ma), and diversified into major extant lineages much earlier than previously thought, well before the Triassic. [Bayesian inference; fossil dating; morphological evolution; relaxed clock; statistical phylogenetics.]

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Author and article information

Contributors

Tiago R. Simões:

ORCID: http://orcid.org/0000-0003-4716-649X

tsimoes@fas.harvard.edu

Journal

Journal ID (nlm-ta): Nat Commun

Journal ID (iso-abbrev): Nat Commun

Title: Nature Communications

Publisher: Nature Publishing Group UK (London )

ISSN (Electronic): 2041-1723

Publication date (Electronic): 3 July 2020

Publication date PMC-release: 3 July 2020

Publication date Collection: 2020

Volume: 11

Electronic Location Identifier: 3322

Affiliations

[1 ]ISNI 000000041936754X, GRID grid.38142.3c, Department of Organismic and Evolutionary Biology & Museum of Comparative Zoology, , Harvard University, ; Cambridge, MA 02138 USA

[2 ]GRID grid.17089.37, Department of Biological Sciences, , University of Alberta, ; Edmonton, AB T6G 2E9 Canada

[3 ]GRID grid.17089.37, Department of Earth and Atmospheric Sciences, , University of Alberta, ; Edmonton, AB T6G 2E9 Canada

Author information

Tiago R. Simões http://orcid.org/0000-0003-4716-649X

Michael W. Caldwell http://orcid.org/0000-0002-2377-3925

Stephanie E. Pierce http://orcid.org/0000-0003-0717-1841

Article

Publisher ID: 17190

DOI: 10.1038/s41467-020-17190-9

PMC ID: 7335191

PubMed ID: 32620878

SO-VID: ffb69a30-4b2c-447c-893e-3ef60333e8fc

License:

Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

History

Date received : 12 October 2019

Date accepted : 17 June 2020

Funding

Funded by: FundRef https://doi.org/10.13039/100007229, Harvard University;

Award ID: Alexander Agassiz Postdoctoral Fellowship

Award Recipient : Tiago R. Simões

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ScienceOpen disciplines: Uncategorized

Keywords: evolution,palaeontology,phylogenetics

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ScienceOpen disciplines: Uncategorized

Keywords: evolution, palaeontology, phylogenetics

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Megaevolutionary dynamics and the timing of evolutionary innovation in reptiles

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Crocodylian evolution

Most cited references 67

The Cambrian conundrum: early divergence and later ecological success in the early history of animals.

The genomic substrate for adaptive radiation in African cichlid fish

A Total-Evidence Approach to Dating with Fossils, Applied to the Early Radiation of the Hymenoptera

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