ABSTRACT
To examine phylogenetic heterogeneity in turtle evolution, we collected thousands of high-confidence single-copy orthologs from 19 genome assemblies representative of extant turtle diversity and estimated a phylogeny with multispecies coalescent and concatenated partitioned methods. We also collected next-generation sequences from 26 turtle species and assembled millions of biallelic markers to reconstruct phylogenies based on annotated regions from the western painted turtle (Chrysemys picta bellii) genome (coding regions, introns, untranslated regions, intergenic, and others). We then measured gene tree-species tree discordance, as well as gene and site heterogeneity at each node in the inferred trees, and tested for temporal patterns in phylogenomic conflict across turtle evolution. We found strong and consistent support for all bifurcations in the inferred turtle species phylogenies. However, a number of genes, sites, and genomic features supported alternate relationships between turtle taxa. Our results suggest that gene tree-species tree discordance in these data sets is likely driven by population-level processes such as incomplete lineage sorting. We found very little effect of substitutional saturation on species tree topologies, and no clear phylogenetic patterns in codon usage bias and compositional heterogeneity. There was no correlation between gene and site concordance, node age, and DNA substitution rate across most annotated genomic regions. Our study demonstrates that heterogeneity is to be expected even in well-resolved clades such as turtles, and that future phylogenomic studies should aim to sample as much of the genome as possible in order to obtain accurate phylogenies for assessing conservation priorities in turtles. [Discordance; genomes; phylogeny; turtles.].
Subject(s)
Turtles , Animals , DNA , Genomics/methods , Phylogeny , Turtles/genetics , Untranslated RegionsABSTRACT
Transposable elements (TEs) are repetitive DNA sequences which create mutations and generate genetic diversity across the tree of life. In amniotic vertebrates, TEs have been mainly studied in mammals and birds, whose genomes generally display low TE diversity. Squamates (Order Squamata; ~11,000 extant species of lizards and snakes) show as much variation in TE abundance and activity as they do in species and phenotypes. Despite this high TE activity, squamate genomes are remarkably uniform in size. We hypothesize that novel, lineage-specific dynamics have evolved over the course of squamate evolution to constrain genome size across the order. Thus, squamates may represent a prime model for investigations into TE diversity and evolution. To understand the interplay between TEs and host genomes, we analyzed the evolutionary history of the CR1 retrotransposon, a TE family found in most tetrapod genomes. We compared 113 squamate genomes to the genomes of turtles, crocodilians, and birds, and used ancestral state reconstruction to identify shifts in the rate of CR1 copy number evolution across reptiles. We analyzed the repeat landscapes of CR1 in squamate genomes and determined that shifts in the rate of CR1 copy number evolution are associated with lineage-specific variation in CR1 activity. We then used phylogenetic reconstruction of CR1 subfamilies across amniotes to reveal both recent and ancient CR1 subclades across the squamate tree of life. The patterns of CR1 evolution in squamates contrast other amniotes, suggesting key differences in how TEs interact with different host genomes and at different points across evolutionary history.
ABSTRACT
Transposable elements (TEs) are repetitive DNA sequences which create mutations and generate genetic diversity across the tree of life. In amniote vertebrates, TEs have been mainly studied in mammals and birds, whose genomes generally display low TE diversity. Squamates (Order Squamata; including â¼11,000 extant species of lizards and snakes) show as much variation in TE abundance and activity as they do in species and phenotypes. Despite this high TE activity, squamate genomes are remarkably uniform in size. We hypothesize that novel, lineage-specific genome dynamics have evolved over the course of squamate evolution. To understand the interplay between TEs and host genomes, we analyzed the evolutionary history of the chicken repeat 1 (CR1) retrotransposon, a TE family found in most tetrapod genomes which is the dominant TE in most reptiles. We compared 113 squamate genomes to the genomes of turtles, crocodilians, and birds and used ancestral state reconstruction to identify shifts in the rate of CR1 copy number evolution across reptiles. We analyzed the repeat landscapes of CR1 in squamate genomes and determined that shifts in the rate of CR1 copy number evolution are associated with lineage-specific variation in CR1 activity. We then used phylogenetic reconstruction of CR1 subfamilies across amniotes to reveal both recent and ancient CR1 subclades across the squamate tree of life. The patterns of CR1 evolution in squamates contrast other amniotes, suggesting key differences in how TEs interact with different host genomes and at different points across evolutionary history.
Subject(s)
Evolution, Molecular , Genome , Reptiles , Retroelements , Animals , Reptiles/genetics , Reptiles/classification , Phylogeny , Lizards/genetics , Chickens/geneticsABSTRACT
Squamates include more than 11,000 extant species of lizards, snakes, and amphisbaenians, and display a dazzling diversity of phenotypes across their over 200-million-year evolutionary history on Earth. Here, we introduce and define squamates (Order Squamata) and review the history and promise of genomic investigations into the patterns and processes governing squamate evolution, given recent technological advances in DNA sequencing, genome assembly, and evolutionary analysis. We survey the most recently available whole genome assemblies for squamates, including the taxonomic distribution of available squamate genomes, and assess their quality metrics and usefulness for research. We then focus on disagreements in squamate phylogenetic inference, how methods of high-throughput phylogenomics affect these inferences, and demonstrate the promise of whole genomes to settle or sustain persistent phylogenetic arguments for squamates. We review the role transposable elements play in vertebrate evolution, methods of transposable element annotation and analysis, and further demonstrate that through the understanding of the diversity, abundance, and activity of transposable elements in squamate genomes, squamates can be an ideal model for the evolution of genome size and structure in vertebrates. We discuss how squamate genomes can contribute to other areas of biological research such as venom systems, studies of phenotypic evolution, and sex determination. Because they represent more than 30% of the living species of amniote, squamates deserve a genome consortium on par with recent efforts for other amniotes (i.e., mammals and birds) that aim to sequence most of the extant families in a clade.
Subject(s)
DNA Transposable Elements , Lizards , Animals , Phylogeny , Genomics/methods , Lizards/genetics , Snakes/genetics , Mammals/geneticsABSTRACT
There is increasing interest in the African spiny mouse (Acomys cahirinus) as a model organism because of its ability for regeneration of tissue after injury in skin, muscle, and internal organs such as the kidneys. A high-quality reference genome is needed to better understand these regenerative properties at the molecular level. Here, we present an improved reference genome for A. cahirinus generated from long Nanopore sequencing reads. We confirm the quality of our annotations using RNA sequencing data from 4 different tissues. Our genome is of higher contiguity and quality than previously reported genomes from this species and will facilitate ongoing efforts to better understand the regenerative properties of this organism.
Subject(s)
Murinae , Skin , Animals , Murinae/genetics , Muscle, Skeletal , Sequence Analysis, RNAABSTRACT
There is increasing interest in the African spiny mouse ( Acomys cahirinus ) as a model organism because of its ability for regeneration of tissue after injury in skin, muscle, and internal organs such as the kidneys. A high-quality reference genome is needed to better understand these regenerative properties at the molecular level. Here, we present an improved reference genome for A. cahirinus generated from long Nanopore sequencing reads. We confirm the quality of our annotations using RNA sequencing data from four different tissues. Our genome is of higher contiguity and quality than previously reported genomes from this species and will facilitate ongoing efforts to better understand the regenerative properties of this organism.