Positive and relaxed selection associated with flight evolution and loss in insect transcriptomes.

T Fatima Mitterboeck,Karen Meusemann,Jinzhong Fu,Xin Zhou,Rui Zhang,Wenhui Song,Shanlin Liu,Sarah J Adamowicz

doi:10.1093/gigascience/gix073

Abstract

The evolution of powered flight is a major innovation that has facilitated the success of insects. Previously, studies of birds, bats, and insects have detected molecular signatures of differing selection regimes in energy-related genes associated with flight evolution and/or loss. Here, using DNA sequences from more than 1000 nuclear and mitochondrial protein-coding genes obtained from insect transcriptomes, we conduct a broader exploration of which gene categories display positive and relaxed selection at the origin of flight as well as with multiple independent losses of flight. We detected a number of categories of nuclear genes more often under positive selection in the lineage leading to the winged insects (Pterygota), related to catabolic processes such as proteases, as well as splicing-related genes. Flight loss was associated with relaxed selection signatures in splicing genes, mirroring the results for flight evolution. Similar to previous studies of flight loss in various animal taxa, we observed consistently higher nonsynonymous-to-synonymous substitution ratios in mitochondrial genes of flightless lineages, indicative of relaxed selection in energy-related genes. While oxidative phosphorylation genes were not detected as being under selection with the origin of flight specifically, they were most often detected as being under positive selection in holometabolous (complete metamorphosis) insects as compared with other insect lineages. This study supports some convergence in gene-specific selection pressures associated with flight ability, and the exploratory analysis provided some new insights into gene categories potentially associated with the gain and loss of flight in insects.

Highlights

The evolution of active flight in insects has most likely had a positive impact on the species diversity of this group [1]
We observed the origin of Pterygota to be associated with significant signatures of positive selection in categories of genes tied to catabolic processes and spliceosome, the latter overlapping with gene categories represented by relaxed selection tests in lineages having undergone flight loss
This study presents an exploratory examination of the genes under positive and relaxed selection associated with the evolution and loss of flight in insects

Summary

Introduction

The evolution of active flight in insects has most likely had a positive impact on the species diversity of this group [1]. Flight, having arisen multiple times in animals, arose earliest in insects approximately 400 million years ago and characterizes the clade Pterygota [2]. In addition to the evolution of flight, pterygote insects evolved incomplete metamorphosis, which involves egg, nymph, and adult stages. These transitions paved the way for later innovations within Pterygota, such as wing folding and complete metamorphosis as occurring in holometabolous insects (i.e., egg, larval, pupal, and adult stages), which are implicated in the evolutionary success of insects [1]. Despite the advantages associated with active flight, it has been estimated that flight has been lost thousands of times within pterygotes [7], such as in lineages representing fleas, snowflies, and stick insects [8]

Methods

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Discussion

Conclusion