Dynamics of genome size evolution in birds and mammals

Abstract

Genome size in mammals and birds shows remarkably little interspecific variation compared with other taxa. However, genome sequencing has revealed that many mammal and bird lineages have experienced differential rates of transposable element (TE) accumulation, which would be predicted to cause substantial variation in genome size between species. Thus, we hypothesize that there has been covariation between the amount of DNA gained by transposition and lost by deletion during mammal and avian evolution, resulting in genome size equilibrium. To test this model, we develop computational methods to quantify the amount of DNA gained by TE expansion and lost by deletion over the last 100 My in the lineages of 10 species of eutherian mammals and 24 species of birds. The results reveal extensive variation in the amount of DNA gained via lineage-specific transposition, but that DNA loss counteracted this expansion to various extents across lineages. Our analysis of the rate and size spectrum of deletion events implies that DNA removal in both mammals and birds has proceeded mostly through large segmental deletions (>10 kb). These findings support a unified "accordion" model of genome size evolution in eukaryotes whereby DNA loss counteracting TE expansion is a major determinant of genome size. Furthermore, we propose that extensive DNA loss, and not necessarily a dearth of TE activity, has been the primary force maintaining the greater genomic compaction of flying birds and bats relative to their flightless relatives.genome size evolution | DNA loss | transposable elements | amniotes | flight T he nature and relative importance of the molecular mechanisms and evolutionary forces underlying genome size variation has been the subject of intense research and debate (1-7). Variation in genome sizes may not always occur at a level where natural selection is strong enough to prevent genetic drift to determine their fate (neutral or effectively neutral variation) (3). Additionally, the fixation probability of slightly deleterious deletions or insertions would be higher in species with smaller effective population sizes, where natural selection acts less efficiently (3,8). On the other hand, a number of correlative associations between genome size and phenotypic traits, such as cell size (9, 10) and metabolic rate associated with powered flight (11, 12), suggest that natural selection and adaptive processes also shape genome size evolution. Teasing apart the relative importance of these two forces (drift and selection) requires a better understanding of the mode and processes by which DNA is gained and lost over long evolutionary periods in different taxa. Thus, establishing an integrated view of the contribution of gain and loss of DNA to genome size variation (or lack thereof) remains an important goal in genome biology (e.g., refs. 1, 2, 13, and 14).Most studies of genome size evolution have focused on taxa with extensive variation in genome sizes, such as flowering plants (15)(16)(17)(18)(19)(20), conifers (21), insects (22-...

A comparison of genomic islands of differentiation across three young avian species pairs

“…Following filtering, our genotype‐by‐sequencing analysis of 117 individuals from the three species complexes produced a data set of 480,714 variable and 10,868,483 invariant nucleotide sites, together accounting for roughly 0.87% of the genome (assuming a genome size of 1.3 billion base pairs; Kapusta, Suh, & Feschotte, ). When grouped into windows of 10,000 sequenced base pairs, there were 1118 windows across the whole genome (1071 windows on autosomes; 47 on the Z chromosome), with an average window length of 1.2 million base pairs.…”

Meta‐analysis of chromosome‐scale crossover rate variation in eukaryotes and its significance to evolutionary genomics

“…Our investigation thus highlights a peculiarity of plant genomes: genes tend to be located in chromosome regions crossing over relatively frequently (see also Gaut, Wright, Rizzon, Dvorak, & Anderson, ; Mezard, ; Schnable, Hsia, & Nikolau, ). As recombination is a potent mechanism of DNA loss counteracting the proliferation of transposable elements, it is possible that in many plant species, chromosome centres with a low CO rate have developed into gene‐poor regions through the accumulation of repetitive DNA (Bennetzen, ; Puchta, ; Hawkins, Grover, & Wendel, ; Schubert & Vu, ; see also Nam & Ellegren, ; Kapusta, Suh, & Feschotte, ). Nevertheless, the heterogeneity in CO rate across plant genomes on average still exceeds the heterogeneity in gene density, although not as strongly as in animals (dotted lines in Figure a).…”

Bat Biology, Genomes, and the Bat1K Project: To Generate Chromosome-Level Genomes for All Living Bat Species

“…genomesize.com). Birds, the other class of flying vertebrates, show similarly reduced genome sizes, an observation that has been used to suggest that the acquisition of flight requires a loss of genomic redundancy and a streamlining of genomic structure within vertebrates (90)(91)(92). Bats represent the lower limit of mammalian genome content and therefore can show the essential genomic information required for being mammalian.…”

“…In addition, vespertilionid bats are unique among studied mammals in harboring multiple lineages of active transposable elements that are not found in other members of the clade (93). Despite this unique accumulation, they continue to maintain small genomes, suggesting an ability to balance genomic gain from transposable repeats via the loss of genomic mass (90). Chromosome-level, high-coverage bat genomes across the order will drive a unique understanding of the limits of mammalian genome structure in general and the genomic consequences of flight adaptation in particular.…”

“…reason to expect any bat genomes to prove problematic, as the bat genomes sequenced to date are mostly ∼2 Gb (90; http://www.genomesize.com), and although some bats contain unique transposable element content by type, they are no more repetitive on average than those of other mammals (90). Scaffolding of the contigs will then be performed using the 10X Genomics read clouds and Hi-C data.…”