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Abstract

The evolution of the amniotic egg was one of the great evolutionary innovations in the history of life, freeing vertebrates from an obligatory connection to water and thus permitting the conquest of terrestrial environments. Among amniotes, genome sequences are available for mammals and birds, but not for non-avian reptiles. Here we report the genome sequence of the North American green anole lizard, Anolis carolinensis. We find that A. carolinensis microchromosomes are highly syntenic with chicken microchromosomes, yet do not exhibit the high GC and low repeat content that are characteristic of avian microchromosomes. Also, A. carolinensis mobile elements are very young and diverse-more so than in any other sequenced amniote genome. The GC content of this lizard genome is also unusual in its homogeneity, unlike the regionally variable GC content found in mammals and birds. We describe and assign sequence to the previously unknown A. carolinensis X chromosome. Comparative gene analysis shows that amniote egg proteins have evolved significantly more rapidly than other proteins. An anole phylogeny resolves basal branches to illuminate the history of their repeated adaptive radiations.

Conflict of interest statement

The authors declare no competing financial interests.

Figures

Figure 1
Figure 1. Amniote phylogeny based on protein synonymous sites showing major features of amniote evolution
Major features of lizard evolution including homogenization of GC content, high sex chromosome turnover and high levels of repeat insertion are highlighted. Sex chromosome inventions are indicated in red. The X-axis is proportional to dS.
Figure 2
Figure 2. Anolis carolinensis-chicken synteny map reveals synteny of reptile microchromosomes but dissimilar GC and repeat content
(A) Very few rearrangements have occurred in the 280 million years since Anolis carolinensis and chickens diverged. A. carolinensis microchromosomes are exclusively syntenic to chicken microchromosomes. Horizontal colored bars depict the six A. carolinensis macrochromosomes (1–6) and the six (of 12) A. carolinensis microchromosomes that have sequence anchored to them that is syntenic to the chicken genome (7, 8, 9, X, LGg, LGh). Chromosomes that could be ordered by size were assigned a number; the smaller microchromosomes that could not be distinguished by size were assigned a lower case letter. Each color corresponds to a different chicken chromosome as indicated in the legend. Any part of an A. carolinensis chromosome that is syntenic to a chicken microchromosome is indicated by a lower case m. (B) Chicken microchromosomes have both higher GC content and lower repeat content than chicken macrochromosomes, whereas A. carolinensis chromosomes do not vary in GC or repeat content by chromosome size. Large circles designate the GC % of each chromosome in the chicken and lizard genomes with greater than 100 kb of sequence anchored to it. Small circles designate the percentage of the genome made up of repetitive sequence of each chromosome in the chicken (blue circles) and lizard (red circles) genomes.
Figure 3
Figure 3. The Anolis carolinensis genome lacks isochores
The A. carolinensis genome shows only very local variation in GC content, unlike the human and chicken genomes, which also show larger trends in GC variation, sometimes called ‘isochores’. Syntenic regions of human chromosome 14, chicken chromosome 5, and A. carolinensis chromosome 1 are shown. The human and chicken regions are inverted and rearranged to align with the A. carolinensis region. Blue lines depict GC % in 20 kb windows. The purple line designates the genome average. Green lines represent examples of syntenic anchors between the three genomes.
Figure 4
Figure 4. The Anolis carolinensis genome contains a newly discovered X chromosome
The X chromosome, a microchromosome, is found in (A) one copy in male Anolis carolinensis and in (B) two copies in females. The BAC 206M13 (CHORI-318 BAC library) is hybridized to the p arm of the X chromosome using FISH in both male and female metaphase spreads. 206M13 and ten other BACs showed this sex-specific pattern in cells derived from five male and five female individuals.
Figure 5
Figure 5. A phylogeny of 93 Anolis species clarifies the biogeographic history of anoles
Anolis ecomorphs derive from convergent evolution and not from frequent inter-island migration. Using conserved primer pairs distributed across the genome of Anolis carolinensis, we obtain sequences from 46 genomically diverse loci evolving at a range of evolutionary rates and representing both protein-coding and non-coding regions. Maximum likelihood analyses of this new dataset of 20 kb aligned nucleotides infer nearly all previously established anole relationships while also partially resolving the basal relationships that have plagued previous studies. White circles indicate bootstrap values <70; gray circles: 70<bs<95; black circles bs >95.

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