Abstract

Since the sequencing of the zebra finch genome it has become clear that avian genomes, while largely stable in terms of chromosome number and gene synteny, are more dynamic at an intrachromosomal level. A multitude of intrachromosomal rearrangements and significant variation in transposable element (TE) content have been noted across the avian tree. TEs are a source of genome plasticity, because their high similarity enables chromosomal rearrangements through nonallelic homologous recombination, and they have potential for exaptation as regulatory and coding sequences. Previous studies have investigated the activity of the dominant TE in birds, chicken repeat 1 (CR1) retrotransposons, either focusing on their expansion within single orders, or comparing passerines with nonpasserines. Here, we comprehensively investigate and compare the activity of CR1 expansion across orders of birds, finding levels of CR1 activity vary significantly both between and within orders. We describe high levels of TE expansion in genera which have speciated in the last 10 Myr including kiwis, geese, and Amazon parrots; low levels of TE expansion in songbirds across their diversification, and near inactivity of TEs in the cassowary and emu for millions of years. CR1s have remained active over long periods of time across most orders of neognaths, with activity at any one time dominated by one or two families of CR1s. Our findings of higher TE activity in species-rich clades and dominant families of TEs within lineages mirror past findings in mammals and indicate that genome evolution in amniotes relies on universal TE-driven processes.

Highlights

  • Following rapid radiation during the Cretaceous-Paleogene transition, birds have diversified to be the most species-rich lineage of extant amniotes (Ericson et al 2006; Jarvis et al 2014; Wiens 2015)

  • From the output of CARP, we manually identified and curated chicken repeat 1 (CR1) with the potential for recent expansion based on the presence of protein domains necessary for retrotransposition, homology to previously described CR1s, and the presence of a distinctive 30 structure

  • Early comparisons of avian genomes were restricted to the chicken and zebra finch, where high level comparisons of synteny and karyotype led to the conclusion that bird genomes were largely stable compared with mammals (Ellegren 2010), the discovery of many intrachromosomal rearrangements across birds (Skinner and Griffin 2012; Zhang et al 2014; Farre et al 2016; Hooper and Price 2017) and interchromosomal recombination in falcons, parrots, and sandpipers (O’Connor et al 2018; Coelho et al 2019; Pinheiro et al 2021) has shown that at a finer resolution for comparison, the avian genome is rather dynamic

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Summary

Introduction

Following rapid radiation during the Cretaceous-Paleogene transition, birds have diversified to be the most species-rich lineage of extant amniotes (Ericson et al 2006; Jarvis et al 2014; Wiens 2015). In comparison to both mammals and non-avian reptiles, birds have much more compact genomes (Gregory et al 2007). Smaller genome sizes correlate with higher metabolic rate and the size of flight muscles (Hughes and Hughes 1995; Wright et al 2014). The decrease in avian genome size occurred in an ancestral dinosaur lineage over 200 Ma, well before the evolution of flight (Organ et al 2007). A large factor in the smaller genome size of birds in comparison to other amniotes is a big reduction in repetitive content (Zhang et al 2014)

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