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Macroevolutionary shift in the size of amphibian genomes and the role of life history and climate

Abstract

The evolution and great diversity of genome size has been of long-standing interest to biologists, but has seldom been investigated on a broad phylogenetic scale. Here we present a comparative quantitative analysis of factors shaping genome size evolution in amphibians, the extant class of vertebrates with the largest variation in genome size. We find that amphibian genomes have undergone saltations in size, although these are rare and the evolutionary history of genome size in amphibians has otherwise been one of gradual, time-dependent variation (that is, Brownian motion). This macroevolutionary homogeneity is remarkable given the evolutionary and ecological diversity of most other aspects of the natural history of amphibians. Contrary to previous claims, we find no evidence for associations between life cycle complexity and genome size despite the high diversity of reproductive modes and the multiple events of independent evolution of divergent life cycles in the group. Climate (temperature and humidity) affects genome size indirectly, at least in frogs, as a consequence of its effect on premetamorphic developmental period, although directionality of the relationship between developmental period and genome size is not unequivocal.

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All genome size measurements generated for this study are available in the supplementary information.

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Acknowledgements

We would like to thank C. Spencer at the Museum of Vertebrate Zoology (Berkeley), M.-O. Rödel and F. Tillack at the Museum für Naturkunde (Berlin), S. Loader and J. Streicher at the Natural History Museum (London), B. Alvarez and I. Martinez-Solano at the Museo Nacional de Ciencias Naturales (Madrid), V. Gvoždík at the Academy of Sciences (Brno) for tissue loans and L. Asencio Vazquez for assistance with laboratory work. M.W. and D.J.G. thank the many persons and organizations that have facilitated the collection of caecilian materials used in this work, especially S. Maddock and the Direction de l’Environment, de l’Aménagement et du Logement and the Conseil Scientifique Régional du Patrimonie Naturel (Guyane). Funding was provided by Spanish National Research Plan (CGL2017-83407-P) awarded to I.G.-M., Swiss National Science Fund (P2BSP3_158846) awarded to H.C.L. and the Darwin Initiative (19-002) awarded to D.J.G.

Author information

H.C.L., I.G.-M., D.J.G. and M.W. were all involved in planning and executing the project. D.J.G. and M.W. contributed key samples and H.C.L. obtained de novo genome size estimates and performed data analyses with input from I.G.-M. H.C.L. wrote the first version of the manuscript, to which all other authors thereafter contributed.

Competing interests

The authors declare no competing financial interests.

Correspondence to Ivan Gomez-Mestre.

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https://doi.org/10.1038/s41559-018-0674-4

Further reading

Fig. 1: Amphibian phylogeny with clades painted to reflect shifts in Ornstein–Uhlenbeck parameters according to the best performing 1lou model for genome size evolution.
Fig. 2: Phenogram showing ancestral state reconstructions for genome size evolution in amphibians under the two best performing mvMORPH models (two-trait mean Brownian motion in colour, three-trait mean Brownian motion underlain in grey).
Fig. 3: Rate estimates for genome size evolution for the three amphibian orders showing posterior distributions as estimated by BAMM showing mean rates per clade and through time.
Fig. 4: Best-scoring phylogenetic path analysis models.