Multiple and Independent Phases of Transposable Element Amplification in the Genomes of Piciformes (Woodpeckers and Allies)

Abstract

The small and conserved genomes of birds are likely a result of flight-related metabolic constraints. Recombination-driven deletions and minimal transposable element (TE) expansions have led to continually shrinking genomes during evolution of many lineages of volant birds. Despite constraints of genome size in birds, we identified multiple waves of amplification of TEs in Piciformes (woodpeckers, honeyguides, toucans, and barbets). Relative to other bird species’ genomic TE abundance (< 10% of genome), we found ∼17–30% TE content in multiple clades within Piciformes. Several families of the retrotransposon superfamily chicken repeat 1 (CR1) expanded in at least three different waves of activity. The most recent CR1 expansions (∼4–7% of genome) preceded bursts of diversification in the woodpecker clade and in the American barbets + toucans clade. Additionally, we identified several thousand polymorphic CR1 insertions (hundreds per individual) in three closely related woodpecker species. Woodpecker CR1 insertion polymorphisms are maintained at lower frequencies than single nucleotide polymorphisms indicating that purifying selection is acting against additional CR1 copies and that these elements impose a fitness cost on their host. These findings provide evidence of large scale and ongoing TE activity in avian genomes despite continual constraint on genome size.

De Novo Assembly of a Chromosome-Scale Reference Genome for the Northern FlickerColaptes auratus

“…Two independent waves of CR1 proliferation were detected, with a large proportion of CR1 elements being of relatively young or medium age, as estimated by a molecular clock (Figure 2). These results echo Manthey et al (2018), who also uncovered multiple independent waves of CR1 proliferation across Piciformes. Window analysis of repetitive elements suggested that the distribution of these elements was uneven across the assembly, both within and across scaffolds ( Figure 1C).…”

“…The paradoxical conjunction of shallow genetic divergence and marked phenotypic differentiation echoes the genomic dynamics of other avian hybrid zones, namely the golden-winged Vermivora chrysoptera and blue-winged Vermivora cyanoptera complex, wherein only a few genomic regions associated with genes that determine plumage color and pattern differentiate the two species (Toews et al 2016). A chromosome-level reference genome for the complex will not only facilitate the identification of the genetic basis of phenotypes (Kratochwil and Meyer 2015), a long-standing goal in evolutionary biology research, but also provide researchers a valuable resource for the examination of emerging fields in genome biology, such as the evolutionary dynamics of transposable element proliferation (Manthey, Moyle, and Boissinot 2018), for which woodpeckers are especially well suited.…”

A highly contiguous genome for the Golden-fronted Woodpecker (Melanerpes aurifrons) via a hybrid Oxford Nanopore and short read assembly

“…Woodpeckers and allies are the exception. Manthey et al [21] demonstrated that TE occurred at higher frequency across several genera of woodpeckers (17-30%), due principally to expansion of CR1 TEs (15-17% of total TEs). Our finding of nearly 22% attributable to CR1 TEs represents a higher proportion of a woodpecker genome than any reported by Manthey et al Because Manthey et al's technical approach likely underestimates TE content, direct comparisons should be considered tentative, but our result does represent the highest CR1 proportion reported for any avian genome.…”

“…More recently, woodpeckers have gained attention for the high amount of repetitive DNA found in their genomes relative to other bird taxa [17][18][19], the result of high levels of genome-wide transposable elements (TEs), which are scarce in most bird genomes [20]. Manthey et al [21] surveyed several woodpecker genomes, and found that TEs make up 17-31% of woodpecker genomes, compared to <10% for other bird species. Increasingly, researchers have suggested that TEs may play a critical role in driving avian evolution [20,22].…”

Disentangling the determinants of transposable elements dynamics in vertebrate genomes using empirical evidences and simulations

“…Sudden bursts of transposition are common in TEs, and have been documented in a variety of species [46–50]. This idiosyncrasy limits direct comparisons between TEs and SNPs, since mutation rates are usually considered constant for the latter.…”