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Tempo and Mode of Spliceosomal Intron Evolution in Actin of Foraminifera

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Abstract

Spliceosomal introns are present in almost all eukaryotic genes, yet little is known about their origin and turnover in the majority of eukaryotic phyla. There is no agreement whether most introns are ancestral and have been lost in some lineage or have been gained recently. We addressed this question by analyzing the spatial and temporal distribution of introns in actins of foraminifera, a group of testate protists whose exceptionally rich fossil record permits the calibration of molecular phylogenies to date intron origins. We identified 24 introns dispersed along the sequence of two foraminiferan actin paralogues and actin deviating proteins, an unconventional type of fast-evolving actin found in some foraminifera. Comparison of intron positions indicates that 20 of 24 introns are specific to foraminifera. Four introns shared between foraminifera and other eukaryotes were interpreted as parallel gains because they have been found only in single species belonging to phylogenetically distinctive lineages. Moreover, additional recent intron gain due to the transfer between the actin paralogues was observed in two cultured species. Based on a relaxed molecular clock timescale, we conclude that intron gains in actin took place throughout the evolution of foraminifera, with the oldest introns inserted between 550 and 500 million years ago and the youngest ones acquired less than 100 million years ago.

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Abbreviations

ACT1:

actin type 1

ACT2:

actin type 2

ADP:

actin deviating protein

ARP:

actin-related protein

BS:

bootstrap support

ML:

maximum likelihood

Mya:

million years ago

NAP:

novel actin-like protein

SSU:

small subunit rRNA

SD:

standard-deviation of Bayesian relaxed molecular clock method.

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Acknowledgments

We would like to thank Elisabeth Alve, Sam Bowser, Colomban de Vargas, Evelyne Goubert, Maria Holzmann, Valérie Le Cadre, David Longet, Xavier Pochon, Stephane Polet, Magali Schweizer, and Tom Wilding for their help in collecting the foraminifera. We are grateful to Juan Montoya and Sam Bowser for providing constructive remarks on the manuscript. This research was supported by Swiss National Science Foundation Grant 3100A0-100415.

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  1. Department of Zoology and Animal Biology, University of Geneva, Sciences III, 30 Quai Ernest-Ansermet, CH-1211, Geneva 4, Switzerland

    Jérôme Flakowski, Ignacio Bolivar, José Fahrni & Jan Pawlowski

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  1. Jérôme Flakowski
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  2. Ignacio Bolivar
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  3. José Fahrni
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Correspondence to Jan Pawlowski.

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Flakowski, J., Bolivar, I., Fahrni, J. et al. Tempo and Mode of Spliceosomal Intron Evolution in Actin of Foraminifera. J Mol Evol 63, 30–41 (2006). https://doi.org/10.1007/s00239-005-0061-z

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