The danger of powerful mitochondria: life-history traits shape the evolution of bird mtDNA

Gusarov Y.S1*, Burskaya V.O2, Bushuev A.V3, Mikhailova A.G1, Efimenko B.E1, Gunbin K.V1, Popadin K.Y1,4

1 Immanuel Kant Baltic Federal University, Kaliningrad, Russian Federation

2 University of Antwerp, Antwerp, Belgium

3 Lomonosov Moscow State University

4 Ecole Polytechnique Federale de Lausanne, Lausanne, Switzerland

yurgusguss [at] mail.ru

Abstract

A>G mutation in the mitochondria heavy chain is one of the most discussed types of mutational signatures: previous studies prove its association with mtDNA chemical damage, caused by elevated energy production level. Here we study A>G mutation patterns in birds – creatures with highest energy consumption in the world. We demonstrate a highly expected excess of A>G mutation frequency in birds compared to mammals. In order to understand biochemical mechanisms, which govern A>G mutations in birds, we describe a list of associations between A>G mutation frequencies and life history traits of birds.First, we show that unlike mammals, birds demonstrate no connection between frequency of A>G mutations and most obvious chemical damage correlates: body mass, lifespan or basal metabolic rate (BMR). It is a surprising result, which we interpret as a sign of a highly optimized electron-transport chain, which produces a very stable level of chemical damage agents in a wide range of “regular” conditions. However, according to our results, there is a list of “irregular” conditions, which cause significant change of A>G mutation frequencies. Decrease of A>G mutation is caused by loss of flight: this change is in line with drastic decrease of energy consumption. We have found an increase of A>G mutation rate in diving birds (diving hypoxia is known to produce chemical damage) and in long range migrators (which are known for outstanding peak metabolism levels). The results are significant after phylogenetic generalized least squares correction and show strong phylogenetic inertia.

Keywords: mitochondria, mtDNA, birds, evolution, mutagenesis

Acknowledgements: The study is supported by RSF grant (No. 21-75-20143).