Karyotypic Evolution of Sauropsid Vertebrates Illuminated by Optical and Physical Mapping of the Painted Turtle and Slider Turtle Genomes

Abstract

Recent sequencing and software enhancements have advanced our understanding of the evolution of genomic structure and function, especially addressing novel evolutionary biology questions. Yet fragmentary turtle genome assemblies remain a challenge to fully decipher the genetic architecture of adaptive evolution. Here, we use optical mapping to improve the contiguity of the painted turtle (Chrysemys picta) genome assembly and use de novo fluorescent in situ hybridization (FISH) of bacterial artificial chromosome (BAC) clones, BAC-FISH, to physically map the genomes of the painted and slider turtles (Trachemys scripta elegans). Optical mapping increased C. picta’s N50 by ~242% compared to the previous assembly. Physical mapping permitted anchoring ~45% of the genome assembly, spanning 5544 genes (including 20 genes related to the sex determination network of turtles and vertebrates). BAC-FISH data revealed assembly errors in C. picta and T. s. elegans assemblies, highlighting the importance of molecular cytogenetic data to complement bioinformatic approaches. We also compared C. picta’s anchored scaffolds to the genomes of other chelonians, chicken, lizards, and snake. Results revealed a mostly one-to-one correspondence between chromosomes of painted and slider turtles, and high homology among large syntenic blocks shared with other turtles and sauropsids. Yet, numerous chromosomal rearrangements were also evident across chelonians, between turtles and squamates, and between avian and non-avian reptiles.

Divergence and hybridization in sea turtles: Inferences from genome data show evidence of ancient gene flow between species

“…Fossil and molecular calibrations based on mitochondrial DNA (mtDNA) or few nuclear loci indicate that this event occurred around 100 million years ago (Duchene et al, 2012 ; Naro‐Maciel et al, 2008 ). Despite their long divergence time, all extant sea turtles have the same chromosomal number (2n = 56) and synteny between chromosomes is found not only within the Chelonioidea superfamily but it extends to the entire Testudines, including freshwater and terrestrial turtles (Lee et al, 2020 ). This is likely a consequence of the low mutation and evolutionary rates in turtles (Avise et al, 1992 ; Lee et al, 2020 ).…”

“…Despite their long divergence time, all extant sea turtles have the same chromosomal number (2n = 56) and synteny between chromosomes is found not only within the Chelonioidea superfamily but it extends to the entire Testudines, including freshwater and terrestrial turtles (Lee et al, 2020 ). This is likely a consequence of the low mutation and evolutionary rates in turtles (Avise et al, 1992 ; Lee et al, 2020 ). In turn, the slow‐paced evolution may delay the onset of genomic incompatibilities after divergence, and this hypothesis is supported by the fact that turtle species with overlapping geographic distributions often hybridize (Buskirk et al, 2005 ; Fritz et al, 2008 ; Karl et al, 1995 ; Vilaça et al, 2012 ).…”

Thermosensitive sex chromosome dosage compensation in ZZ/ZW softshell turtles,Apalone spinifera

“…A control dataset of 390 autosomal genes was extracted at random from the set of putative autosomal genes localized in putative autosomal scaffolds. Homologues of these two sets of Apalone Z-linked and autosomal genes were also extracted from the Chrysemys genome [60][61][62] where they are all autosomal since this species lacks sex chromosomes [42].…”

Characterization of the First Turtle Organoids: A Model for Investigating Unique Adaptations with Biomedical Potential

“…Because of their biology and phylogenic position, turtles hold clues to unlock numerous biological mysteries, including current biomedical questions. Indeed, turtles are an emerging model for ecology, evolution, and human health (Valenzuela, 2009), currently studied to understand physiology, life histories, chromosome evolution, as ecotoxicology sentinels, and to decipher biological pathways for sexual development and reproduction (Bista & Valenzuela, 2020; Chaousis et al, 2021; Congdon et al, 2022; Lee et al, 2020; Mizoguchi et al, 2022; Montiel et al, 2016; Sabath et al, 2016; Thépot, 2021). But while reptile genomics is thriving, reptilian transgenics remains challenging despite pioneering in vivo gene editing in anole lizards (Rasys et al, 2019) and recent work in mourning geckos (Lozito et al, 2021).…”