Abstract

Is there a correlation between miRNA diversity and levels of organismic complexity? Exhibiting extraordinary levels of morphological and developmental complexity, insects are the most diverse animal class on earth. Their evolutionary success was in particular shaped by the innovation of holometabolan metamorphosis in endopterygotes. Previously, miRNA evolution had been linked to morphological complexity, but astonishing variation in the currently available miRNA complements of insects made this link unclear. To address this issue, we sequenced the miRNA complement of the hemimetabolan Blattella germanica and reannotated that of two other hemimetabolan species, Locusta migratoria and Acyrthosiphon pisum, and of four holometabolan species, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster. Our analyses show that the variation of insect miRNAs is an artefact mainly resulting from poor sampling and inaccurate miRNA annotation, and that insects share a conserved microRNA toolkit of 65 families exhibiting very low variation. For example, the evolutionary shift toward a complete metamorphosis was accompanied only by the acquisition of three and the loss of one miRNA families.

Highlights

  • Is there a correlation between miRNA diversity and levels of organismic complexity? Exhibiting extraordinary levels of morphological and developmental complexity, insects are the most diverse animal class on earth

  • We sequenced the miRNA complement of the hemimetabolan Blattella germanica and reannotated that of two other hemimetabolan species, Locusta migratoria and Acyrthosiphon pisum, and of four holometabolan species, Apis mellifera, Tribolium castaneum, Bombyx mori and Drosophila melanogaster

  • The information is unequal, as the number of miRNAs ranges from 7 in the locust, Locusta migratoria, to 487 in the silkworm, Bombyx mori, while a recent paper described 833 miRNA genes from the locust[13]. This underrepresentation of hemimetabolan species and the dramatic inequality regarding the completeness of the miRNA complement of each species precludes any serious analysis on whether miRNAs played any role in insect evolution

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Summary

Introduction

Exhibiting extraordinary levels of morphological and developmental complexity, insects are the most diverse animal class on earth Their evolutionary success was in particular shaped by the innovation of holometabolan metamorphosis in endopterygotes. The information is unequal, as the number of miRNAs ranges from 7 in the locust, Locusta migratoria, to 487 in the silkworm, Bombyx mori, while a recent paper described 833 miRNA genes from the locust[13] This underrepresentation of hemimetabolan species and the dramatic inequality regarding the completeness of the miRNA complement of each species precludes any serious analysis on whether miRNAs played any role in insect evolution. Concerning B. germanica, we used an initial miRNA catalogue[14], together with the information of a number of new small RNA-seq datasets (including Dicer-knockdown libraries, to validate miRNA candidates) and the newly www.nature.com/scientificreports/

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