Dataset Information

Molecular Adaptations for Sensing and Securing Prey and Insight into Amniote Genome Diversity from the Garter Snake Genome.

ABSTRACT: Colubridae represents the most phenotypically diverse and speciose family of snakes, yet no well-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and securing prey, and identify features of snake genome structure that provide insight into the evolution of amniote genomes. Analyses of the garter snake and other squamate reptile genomes highlight shifts in repeat element abundance and expansion within snakes, uncover evidence of genes under positive selection, and provide revised neutral substitution rate estimates for squamates. Our identification of Z and W sex chromosome-specific scaffolds provides evidence for multiple origins of sex chromosome systems in snakes and demonstrates the value of this genome for studying sex chromosome evolution. Analysis of gene duplication and loss in visual and olfactory gene families supports a dim-light ancestral condition in snakes and indicates that olfactory receptor repertoires underwent an expansion early in snake evolution. Additionally, we provide some of the first links between secreted venom proteins, the genes that encode them, and their evolutionary origins in a rear-fanged colubrid snake, together with new genomic insight into the coevolutionary arms race between garter snakes and highly toxic newt prey that led to toxin resistance in garter snakes.

SUBMITTER: Perry BW

PROVIDER: S-EPMC6110522 | biostudies-literature | 2018 Aug

REPOSITORIES: biostudies-literature

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Publications

Molecular Adaptations for Sensing and Securing Prey and Insight into Amniote Genome Diversity from the Garter Snake Genome.

Perry Blair W BW Card Daren C DC McGlothlin Joel W JW Pasquesi Giulia I M GIM Adams Richard H RH Schield Drew R DR Hales Nicole R NR Corbin Andrew B AB Demuth Jeffery P JP Hoffmann Federico G FG Vandewege Michael W MW Schott Ryan K RK Bhattacharyya Nihar N Chang Belinda S W BSW Casewell Nicholas R NR Whiteley Gareth G Reyes-Velasco Jacobo J Mackessy Stephen P SP Gamble Tony T Storey Kenneth B KB Biggar Kyle K KK Passow Courtney N CN Kuo Chih-Horng CH McGaugh Suzanne E SE Bronikowski Anne M AM de Koning A P Jason APJ Edwards Scott V SV Pfrender Michael E ME Minx Patrick P Brodie Edmund D ED Brodie Edmund D ED Warren Wesley C WC Castoe Todd A TA

Genome biology and evolution 20180801 8

Colubridae represents the most phenotypically diverse and speciose family of snakes, yet no well-assembled and annotated genome exists for this lineage. Here, we report and analyze the genome of the garter snake, Thamnophis sirtalis, a colubrid snake that is an important model species for research in evolutionary biology, physiology, genomics, behavior, and the evolution of toxin resistance. Using the garter snake genome, we show how snakes have evolved numerous adaptations for sensing and secur ...[more]

PMID: 30060036

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Project description:BACKGROUND: The reptiles, characterized by both diversity and unique evolutionary adaptations, provide a comprehensive system for comparative studies of metabolism, physiology, and development. However, molecular resources for ectothermic reptiles are severely limited, hampering our ability to study the genetic basis for many evolutionarily important traits such as metabolic plasticity, extreme longevity, limblessness, venom, and freeze tolerance. Here we use massively parallel sequencing (454 GS-FLX Titanium) to generate a transcriptome of the western terrestrial garter snake (Thamnophis elegans) with two goals in mind. First, we develop a molecular resource for an ectothermic reptile; and second, we use these sex-specific transcriptomes to identify differences in the presence of expressed transcripts and potential genes of evolutionary interest. RESULTS: Using sex-specific pools of RNA (one pool for females, one pool for males) representing 7 tissue types and 35 diverse individuals, we produced 1.24 million sequence reads, which averaged 366 bp in length after cleaning. Assembly of the cleaned reads from both sexes with NEWBLER and MIRA resulted in 96,379 contigs containing 87% of the cleaned reads. Over 34% of these contigs and 13% of the singletons were annotated based on homology to previously identified proteins. From these homology assignments, additional clustering, and ORF predictions, we estimate that this transcriptome contains ~13,000 unique genes that were previously identified in other species and over 66,000 transcripts from unidentified protein-coding genes. Furthermore, we use a graph-clustering method to identify contigs linked by NEWBLER-split reads that represent divergent alleles, gene duplications, and alternatively spliced transcripts. Beyond gene identification, we identified 95,295 SNPs and 31,651 INDELs. From these sex-specific transcriptomes, we identified 190 genes that were only present in the mRNA sequenced from one of the sexes (84 female-specific, 106 male-specific), and many highly variable genes of evolutionary interest. CONCLUSIONS: This is the first large-scale, multi-organ transcriptome for an ectothermic reptile. This resource provides the most comprehensive set of EST sequences available for an individual ectothermic reptile species, increasing the number of snake ESTs 50-fold. We have identified genes that appear to be under evolutionary selection and those that are sex-specific. This resource will assist studies on gene expression and comparative genomics, and will facilitate the study of evolutionarily important traits at the molecular level.

Project description:Land use and climate change are affecting the abundance and distribution of species. The Trans-Mexican Volcanic Belt (TMVB) is a very diverse region due to geological history, geographic position, and climate. It is also one of the most disturbed regions in Mexico. Reptiles are particularly sensitive to environmental changes due to their low dispersal capacity and thermal ecology. In this study, we define the important environmental variables (considering climate, topography, and land use) and potential distribution (present and future) of the five Thamnophis species present in TMVB. To do so, we used the maximum entropy modeling software (MAXENT). First, we modeled to select the most important variables to explain the distribution of each species, then we modeled again using only the most important variables and projected these models to the future considering a middle-moderate climate change scenario (rcp45), and land use and vegetation variables for the year 2050 (generated according to land use changes that occurred between years 2002 and 2011). Arid vegetation had an important negative effect on habitat suitability for all species, and minimum temperature of the coldest month was important for four of the five species. Thamnophis cyrtopsis was the species with the lowest tolerance to minimum temperatures. The maximum temperature of the warmest month was important for T. scalaris and T. cyrtopsis. Low percentages of agriculture were positive for T. eques and T. melanogaster but, at higher values, agriculture had a negative effect on habitat suitability for both species. Elevation was the most important variable to explain T. eques and T. melanogaster potential distribution while distance to Abies forests was the most important variable for T. scalaris and T. scaliger. All species had a high proportion of their potential distribution in the TMVB. However, according to our models, all Thamnophis species will experience reductions in their potential distribution in this region. T. scalaris will suffer the biggest reduction because this species is limited by high temperatures and will not be able to shift its distribution upward, as it is already present in the highest elevations of the TMVB.

Dataset Information

Molecular Adaptations for Sensing and Securing Prey and Insight into Amniote Genome Diversity from the Garter Snake Genome.

Publications

Molecular Adaptations for Sensing and Securing Prey and Insight into Amniote Genome Diversity from the Garter Snake Genome.

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