The western painted turtle genome, a model for the evolution of extreme physiological adaptations in a slowly evolving lineage

Abstract

BackgroundWe describe the genome of the western painted turtle, Chrysemys picta bellii, one of the most widespread, abundant, and well-studied turtles. We place the genome into a comparative evolutionary context, and focus on genomic features associated with tooth loss, immune function, longevity, sex differentiation and determination, and the species' physiological capacities to withstand extreme anoxia and tissue freezing.ResultsOur phylogenetic analyses confirm that turtles are the sister group to living archosaurs, and demonstrate an extraordinarily slow rate of sequence evolution in the painted turtle. The ability of the painted turtle to withstand complete anoxia and partial freezing appears to be associated with common vertebrate gene networks, and we identify candidate genes for future functional analyses. Tooth loss shares a common pattern of pseudogenization and degradation of tooth-specific genes with birds, although the rate of accumulation of mutations is much slower in the painted turtle. Genes associated with sex differentiation generally reflect phylogeny rather than convergence in sex determination functionality. Among gene families that demonstrate exceptional expansions or show signatures of strong natural selection, immune function and musculoskeletal patterning genes are consistently over-represented.ConclusionsOur comparative genomic analyses indicate that common vertebrate regulatory networks, some of which have analogs in human diseases, are often involved in the western painted turtle's extraordinary physiological capacities. As these regulatory pathways are analyzed at the functional level, the painted turtle may offer important insights into the management of a number of human health disorders.

Toward consilience in reptile phylogeny: miRNAs support an archosaur, not lepidosaur, affinity for turtles

“…2), robustly support an archosaur, rather than a lepidosaur, affinity for turtles. Indeed, the latter analysis strongly supports a sister group relationship between crown turtles and crown archosaurs, as do most recent studies addressing amniote interrelationships using gene sequence data (Zardoya and Meyer 1998, Hedges and Poling 1999, Kumazawa and Nishida 1999, Iwabe et al 2005, Shen et al 2011, Tzika et al 2011, Chiari et al 2012, Crawford et al 2012, Fong et al 2012, Shaffer et al 2013, Wang et al 2013, Lu et al 2013). …”

“…If the morphological hypothesis that turtles represent the extant sister group of living reptiles accurately reflects turtle origins, it would indicate that virtually the entire genome (Matsuda et al 2005, Shedlock et al 2007), including mitochondrial genes (Zardoya and Meyer 1998, Kumazawa and Nishida 1999), ribosomal RNA genes (Hedges and Poling 1999), protein coding genes (Hedges and Poling 1999, Iwabe et al 2005, Shen et al 2011, Tzika et al 2011, Chiari et al 2012, Fong et al 2012, Shaffer et al 2013, Wang et al 2013, Lu et al 2013), ultraconserved elements (Crawford et al 2012), and miRNAs (Figs. 1 and 2), exhibit astonishing levels of homoplasy in a surprisingly congruent pattern.…”

“…Because published genomes are now available for C. picta (Shaffer et al 2013) and A. mississippensis (St John et al 2012), the near-complete complements of miRNAs from these two taxa were assembled (ESM 1–2, respectively). In addition, the reads from C. livia were used to query the recently released pigeon genome (Shapiro et al 2013), and its near-complete miRNA repertoire was assembled (ESM 3).…”

“…Rieppel and deBraga 1996, deBraga and Rieppel 1997, Rieppel and Reisz 1999, Li et al 2008, Lyson et al 2012); and iii), turtles are the sister taxon to, or are nested within, Archosauria (birds and crocodylians; supported mainly by gene-sequence datasets e.g. Zardoya and Meyer 1998, Hedges and Poling 1999, Kumazawa and Nishida 1999, Iwabe et al 2005, Shen et al 2011, Tzika et al 2011, Chiari et al 2012, Crawford et al 2012, Fong et al 2012, Shaffer et al 2013, Wang et al 2013, Lu et al 2013). In the absence of a well-resolved phylogenetic hypothesis for Amniota, outstanding macroevolutionary questions, including those regarding the acquisition of the unique turtle body plan, cannot be adequately addressed.…”

It's more than stamp collecting: how genome sequencing can unify biological research

“…It also identified the ling fish and not the coelacanth as the closest living relative to the tetrapods [102]. N The genome of the Western painted turtle, Chrysemys picta bellii , shows an extraordinary slow rate of sequence evolution and allowed identification of genes involved in tolerance to freezing and oxygen deprivation [103]. O Male peregrine falcon, representing just one of 48 bird species sequenced by Zhang et Al.…”