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Draft Genome of the Common Snapping Turtle, Chelydra Serpentina, a Model For

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Draft Genome of the Common Snapping Turtle, Chelydra Serpentina, a Model For G3: Genes|Genomes|Genetics Early Online, published on September 30, 2020 as doi:10.1534/g3.120.401440 1 Draft Genome of the Common Snapping Turtle, Chelydra serpentina, a Model for 2 Phenotypic Plasticity in Reptiles 3 4 Debojyoti Das*1, Sunil Kumar Singh*1, Jacob Bierstedt*, Alyssa Erickson*, Gina L.J. Galli†, 5 Dane A. Crossley II‡, and Turk Rhen* 6 7 * Department of Biology, University of North Dakota, Grand Forks, North Dakota 58202, USA 8 9 † Division of Cardiovascular Sciences, School of Medical Sciences, University of Manchester, 10 Manchester M13 9NT, UK 11 12 ‡ Department of Biological Sciences, University of North Texas, Denton, Texas 76203, USA 13 14 1 These authors contributed equally to this work 15 16 17 18 19 20 21 22 23 1 © The Author(s) 2020. Published by the Genetics Society of America. 24 Running title: Snapping turtle genome assembly 25 26 Key words: Snapping turtle, Chelydra serpentina, genome assembly, genome annotation, 27 phenotypic plasticity 28 29 Corresponding author: 30 Turk Rhen 31 Department of Biology 32 10 Cornell Street 33 University of North Dakota 34 Grand Forks, North Dakota 58202, USA 35 36 Phone: 1-701-777-4667 37 Fax: 1-701-777-2623 38 e-mail: [email protected] 39 40 41 42 43 44 45 46 2 47 Abstract 48 Turtles are iconic reptiles that inhabit a range of ecosystems from oceans to deserts and climates 49 from the tropics to northern temperate regions. Yet, we have little understanding of the genetic 50 adaptations that allow turtles to survive and reproduce in such diverse environments. Common 51 snapping turtles, Chelydra serpentina, are an ideal model species for studying adaptation to 52 climate because they are widely distributed from tropical to northern temperate zones in North 53 America. They are also easy to maintain and breed in captivity and produce large clutch sizes, 54 which makes them amenable to quantitative genetic and molecular genetic studies of traits like 55 temperature-dependent sex determination. We therefore established a captive breeding colony 56 and sequenced DNA from one female using both short and long reads. After trimming and 57 filtering, we had 209.51Gb of Illumina reads, 25.72Gb of PacBio reads, and 21.72 Gb of 58 Nanopore reads. The assembled genome was 2.258 Gb in size and had 13,224 scaffolds with an 59 N50 of 5.59Mb. The longest scaffold was 27.24Mb. BUSCO analysis revealed 97.4% of core 60 vertebrate genes in the genome. We identified 3.27 million SNPs in the reference turtle, which 61 indicates a relatively high level of individual heterozygosity. We assembled the transcriptome 62 using RNA-Seq data and used gene prediction software to produce 22,812 models of protein 63 coding genes. The quality and contiguity of the snapping turtle genome is similar to or better 64 than most published reptile genomes. The genome and genetic variants identified here provide a 65 foundation for future studies of adaptation to climate. 66 67 68 69 3 70 INTRODUCTION 71 Turtles are a monophyletic group of reptiles recognized by their shell, a unique adaptation 72 that makes them an iconic animal (Lyson et al. 2013). There are 356 turtle species divided 73 between two suborders. The Cryptodira or hidden-necked turtles include 263 species, while the 74 Pleurodira or side-necked turtles include 93 species (Rhodin et al. 2017). Phylogenomic analysis 75 of 26 species across 14 known families has produced a well-resolved tree showing relationships 76 among 11 cryptodiran and 3 pleurodiran families (Shaffer et al. 2017). Since their origin 220 77 million years ago, turtles have evolved the ability to inhabit a wide array of aquatic and 78 terrestrial ecosystems, ranging from oceans to deserts. Yet, turtles are one of the most threatened 79 vertebrate groups. Roughly 60% of turtle species on the IUCN Red List (2017) are considered 80 vulnerable, endangered, or critically endangered (Stanford et al. 2018). Habitat destruction, 81 overharvest, and international trade are the main causes of population decline (Bohm et al. 2013, 82 Stanford et al. 2018). 83 Climate change is another major concern, especially for turtles with temperature-dependent 84 sex determination (TSD) (Mitchell and Janzen 2010, Santidrian Tomillo et al. 2015, Hays et al. 85 2017). Although incubation studies have only been carried out on a subset of species, most 86 turtles examined (81%) exhibit TSD (Ewert et al. 2004). Phylogenetic analyses indicate that 87 TSD is the ancestral mode of sex determination and that genotypic sex determination evolved 88 independently several times (Janzen and Krenz 2004, Valenzuela and Adams 2011, Pokorna and 89 Kratochvil 2016). In addition to its effect on the gonads, incubation temperature has a significant 90 impact on growth, physiology, and behavior in turtles and other reptiles (Rhen and Lang 2004, 91 Noble et al. 2018, While et al. 2018, Singh et al. 2020). 4 92 Temperature effects are a specific example of a broader phenomenon called phenotypic 93 plasticity in which environmental factors alter phenotype (Via and Lande 1985, Scheiner 1993, 94 Agrawal 2001, Angilletta 2009, Warner et al. 2018). Organisms can also maintain phenotypic 95 stability in the face of variable environments. Physiologists call this homeostasis while 96 developmental biologists call it canalization. Although plasticity and stability appear to be 97 distinct strategies for dealing with environmental variation, they actually represent ends of a 98 continuum of potential responses. Plasticity/stability often has a genetic basis with different 99 individuals being more or less responsive to environmental influences. We must decipher 100 genome-environment interactions to understand the role plasticity/stability plays in allowing 101 turtles to survive and reproduce in diverse climates from the tropics to temperate regions. 102 Genomic resources will facilitate research on the evolution of phenotypic plasticity, 103 homeostasis, and developmental canalization in turtles. To date, genomes from six turtle species 104 in five families have been sequenced (Shaffer et al. 2013, Wang et al. 2013, Tollis et al. 2017, 105 Cao et al. 2019, https://www.ncbi.nlm.nih.gov/bioproject/PRJNA415469/], but each of these 106 species lives and reproduces in a much narrower range of climates than the common snapping 107 turtle (Chelydra serpentina). Here we assemble and annotate the first draft genome for the 108 snapping turtle, which is the most widespread and abundant species in the family Chelydridae. 109 The contiguity and completeness of the snapping turtle genome is similar to or better than 110 other reptiles and is adequate for reuse in functional and comparative genomic studies. Several 111 characteristics make the snapping turtle a good model for turtle biology. This species is one of 112 the most extensively studied turtles (Steyermark et al. 2008, While et al. 2018), providing a 113 wealth of baseline information for genetic, genomic, epigenomic, and transcriptomic analyses of 114 cell and developmental biology, physiology, behavior, ecology and evolution. This species 5 115 produces large clutches (30-95 eggs/clutch) and is easy to breed and rear in captivity, making 116 genetic studies feasible. We therefore established a captive breeding colony to study phenotypic 117 variation in TSD (Janzen 1992, Rhen and Lang 1998, Ewert et al. 2005, Rhen et al. 2015, 118 Schroeder et al. 2016). Controlled breeding reveals that variation in TSD within populations is 119 highly heritable and that population differences in sex ratio at warm incubation temperatures are 120 also heritable (Hilliard and Rhen, unpublished results). Yet, population differences in sex ratio at 121 cool incubation temperatures are due to genetic dominance and/or non-genetic maternal effects, 122 illustrating genome-environment interactions (Hilliard and Rhen, unpublished results). These 123 findings provide a solid foundation for genome-wide association studies to identify specific loci 124 that influence thermosensitivity (Schroeder et al. 2016). 125 The genome will also be useful for studying other ecologically important traits and 126 characterizing population genomic variation. Such studies will provide insight into genetic 127 adaptation to climate because snapping turtles range from tropical to northern temperate zones. 128 For example, snapping turtles display counter-gradient variation in developmental rate with 129 latitude: northern alleles speed embryonic developmental rate to counteract the impact of cooler 130 soil temperatures at higher latitudes (Hilliard and Rhen, unpublished results). Another 131 remarkable trait is their ability to tolerate hypoxic conditions. Eggs buried underground 132 periodically experience low oxygen conditions (e.g., when soil is saturated with water after 133 heavy rains). Hypoxia during embryogenesis programs subsequent performance in low oxygen 134 environments: cardiomyocytes from juvenile snapping turtles exposed to hypoxia as embryos 135 have enhanced myofilament Ca2+-sensitivity and ability to curb production of reactive oxygen 136 species when compared to juveniles exposed to normoxic conditions as embryos (Ruhr et al. 137 2019). Such findings have broader implications for understanding cardiac hypoxia 6 138 tolerance/susceptibility across vertebrates: i.e. most human diseases of the heart are due to 139 insufficient oxygen supply. A contiguous, well-annotated genome is critical for epigenomic 140 studies of developmentally plastic responses to temperature and oxygen levels as well as other 141 abiotic factors and ecological interactions. For instance, future studies will correlate genome- 142 wide patterns of DNA methylation with transcriptome-wide patterns of gene expression in hearts 143 of juvenile turtles exposed to hypoxic conditions as embryos. 144 The genome will also be valuable for comparative studies with other Chelydridae, which are 145 listed as vulnerable on the ICUN Red List (2017): Macrochelys temminckii in North America, 146 Chelydra rossignoni in Central America, and Chelydra acutirostris in South America. Finally, 147 we expect this draft will serve as a template for refinement and improvement of the snapping 148 turtle genome assembly.
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