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

Background

We 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.

Results

Our 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.

Conclusions

Our 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.     

Development of cardiac form and function in ectothermic sauropsids

Evolutionary morphologists and physiologists have long recognized the phylogenetic significance of the ectothermic sauropsids. Sauropids have been classically considered to bridge between early tetrapods, ectotherms, and the evolution of endotherms. This transition has been associated with many modifications in cardiovascular form and function, which have changed dramatically during the course of vertebrate evolution. Most cardiovascular studies have focused upon adults, leaving the development of this critical system largely unexplored. In this essay, we attempt a synthesis of sauropsid cardiovascular development based on the limited literature and indicate fertile regions for future studies. Early morphological cardiovascular development, i.e., the basic formation of the tube heart and the major pulmonary and systemic vessels, is similar across tetrapods. Subsequent cardiac chamber development, however, varies considerably between developing chelonians, squamates, crocodilians, and birds, reflected in the diversity of adult ventricular structure across these taxa. The details of how these differences in morphology develop, including the molecular regulation of cardiac and vascular growth and differentiation, are still poorly understood. In terms of the functional maturation of the cardiovascular system, reflected in physiological mechanisms for regulating heart rate and cardiac output, recent work has illustrated that changes during ontogeny in parameters such as heart rate and arterial blood pressure are somewhat species‐dependent. However, there are commonalities, such as a β‐adrenergic receptor tone on the embryonic heart appearing prior to 60% of development. Differential gross morphological responses to environmental stressors (oxygen, hydration, temperature) have been investigated interspecifically, revealing that cardiac development is relatively plastic, especially, with respect to change in heart growth. Collectively, the data assembled here reflects the current limited morphological and physiological understanding of cardiovascular development in sauropsids and identifies key areas for future studies of this diverse vertebrate lineage. J. Morphol., 2009. © 2009 Wiley‐Liss, Inc.     

中国龟鳖物种多样性及濒危现状

本文对1949年以来我国龟鳖动物的新种和新记录、物种多样性和名录变化状况作了述评,分析了中国龟鳖物种多样性的特点及濒危现状。我国现存龟鳖动物1目6科21属41种。     

Microscopic and immunohistochemical study on the cornification of the developing beak in the turtle Emydura macquarii

The development and cornification of the ramphoteca (beak) in turtles are not known. The microscopic aspects of beak formation have been analyzed in the pleurodirian turtle Emydura macquarii using histological, immunocytochemical and ultrastructural methods. At embryonic Stage 15 the maxillar beak is originated from discontinuous placodes (one frontal and two oral) formed in the epidermis above and below the mouth that later merge into the epidermis of the beak. The mandibular beak is formed by two lateral placodes. In the placodes, basal keratinocytes in contact with local mesenchymal condensations become columnar, and generate suprabasal cells forming 5–6 layers of embryonic epidermis at Stages 17–20 and a compact shedding alpha‐layer at the base of the embryonic epidermis. These keratinocytes contain irregular or aggregated reticular bodies made of 30–40 nm thick strands of coarse filaments, mixed with tonofilaments and sparse lipid droplets. Beneath the shedding layer are present 3–4 layers of keratinocytes accumulating coarse filaments mixed with beta‐corneous packets, and underneath spindle‐shaped beta‐cells differentiate where beta‐corneous packets completely replace the reticulate bodies. Differently from scales where corneocytes partially merge, beak corneocytes remain separated but they are joined by numerous interlocking spines. The production of beta‐cells in the thick corneous layer of the developing beak, like in claws, occurs before the differentiation of beta‐cells in the body scutes. This indicates that a massive mesenchymal condensation triggers beta‐differentiation before this process is later activated in most of body scutes of the carapace and plastron. J. Morphol. 277:1309–1319, 2016. © 2016 Wiley Periodicals, Inc.     

Projected changes in climatic suitability for Kinosternon turtles by 2050 and 2070

Chelonians are expected to be negatively impacted by climate change due to limited vagility and temperature‐dependent sex determination. However, few studies have examined how freshwater turtle distributions may shift under different climate change scenarios. We used a maximum entropy approach to model the distribution of five widespread North American Kinosternon species (K. baurii, K. flavescens, K. hirtipes, K. sonoriense, and K. subrubrum) under four climate change scenarios. We found that areas with suitable climatic conditions for K. baurii and K. hirtipes are expected to decline substantially during the 21st century. In contrast, the area with suitable climate for K. sonoriense will remain essentially unchanged, while areas suitable for K. flavescens and K. subrubrum are expected to substantially increase. The centroid for the distribution of four of the five species shifted northward, while the centroid for K. sonoriense shifted slightly southward. Overall, centroids shifted at a median rate of 37.5 km per decade across all scenarios. Given the limited dispersal ability of turtles, it appears unlikely that range shifts will occur rapidly enough to keep pace with climate change during the 21st century. The ability of chelonians to modify behavioral and physiological responses in response to unfavorable conditions may allow turtles to persist for a time in areas that have become increasingly unsuitable, but this plasticity will likely only delay local extinctions.     

Microsatellite DNA markers for Podocnemis unifilis,the endangered yellow‐spotted Amazon River turtle

We developed specific primers for microsatellite DNA regions of Podocnemis unifilis and tested their utility in population genetic and paternity studies on the species and other closely related Amazonian chelonians. Seventeen microsatellite loci were polymorphic in P. unifilis and all, plus two monomorphic microsatellites in P. unifilis, were polymorphic in at least one additional chelonian species, including Peltocephalus dumeriliana.     

Survival and movements of head-started Mojave desert tortoises

Head-starting is a conservation strategy in which young animals are protected in captivity temporarily before their release into the wild at a larger size, when their survival is presumably increased. The Mojave desert tortoise (Gopherus agassizii) is in decline, and head-starting has been identified as one of several conservation measures to assist in recovery. To evaluate the efficacy of indoor head-starting, we released and radio-tracked 68 juvenile tortoises from a 2015 cohort in the Mojave National Preserve, California, USA. We released 20 tortoises at hatching (control) in September 2015, and reared 28 indoors and 20 outdoors in predator-proof enclosures for 7 months before releasing them in April 2016. We monitored tortoises at least weekly after release until 27 October 2016, and documented survivorship, movement, and surface activity. We estimated survivorship by treatment and evaluated effects of treatment, proximity to a raven (Corvus corax) nest (predator) coincidentally established after release, distance moved between monitoring events, surface activity, and release size on individual fate in a generalized linear model. Although indoor head-start tortoises reached the size of 5–6-year-old wild tortoises by release at 7 months of age, survival did not differ significantly among the 3 treatment groups. Combined annual survival was 0.44 (95% CI = 0.34–0.58). Tortoises that were closer to an active raven nest were significantly more likely to die, as were those seen more often outside their burrows and active aboveground. Predicted estimates for short-term probability of survival approached 1.0 as distance from a raven nest exceeded approximately 1.6 km. Rearing treatment, movement distance, and body size were not significant predictors of fate over the 1-year monitoring period. Head-started tortoises released ≥1.6 km from areas of raven activity will likely have higher short-term survival. Population recovery through head-starting alone is unlikely to be successful if systemic ecosystem-level issues, such as habitat degradation and conditions that promote human-subsidized predators, are not ameliorated. © 2019 The Wildlife Society.     

Mating‐induced ovulation in loggerhead sea turtles,Caretta caretta

Mating‐induced ovulation is common in mammals, but has been rarely described in other taxa. Observations of several mature female loggerhead sea turtles, Caretta caretta, held in captivity seemed to indicate that ovulation did not occur in the absence of a male. This study was designed to determine whether this was an effect of captivity or an effect of the absence of a male. Two mature female loggerheads were followed over six annual reproductive cycles. Ultrasound exams were performed approximately every 2 weeks to follow the development of follicles in the ovaries. During the first two seasons, no male was present, in the next two seasons, a mature male was present without mating, and in the final two seasons a mature male was present, mating with one or both females. When no male was present or when present without mating, ovarian follicles developed to full size, but ovulation did not occur and the follicles gradually began to decrease in diameter and undergo changes evident on ultrasound. In the fifth season, only one of the females mated, dropping two eggs after 7 days, and continued to oviposit throughout the following months (total 275 eggs). The unmated female did not ovulate, showing the same pattern as earlier seasons. In the final season, both females mated and ovulated, dropping eggs for the next four months (total 539 eggs). The following year, no males were present and neither female ovulated. This study provides clear evidence that ovulation in loggerhead sea turtles is induced by mating. Zoo Biol 27:213–225, 2008. © 2008 Wiley‐Liss, Inc.     

Trace nouvelle de locomotion de Chélonienet figures d'émersion associées dans les calcaires lithographiques de Cerin (Kimméridgien supérieur,Ain, France)

The first tetrapod Vertebrate track discovered in the late Kimmeridgian lithographic limestones of Cerin (Ain-France), is descrbed as a new ichnospecies, named Chelonichnium cerinense. The characteristics of the track, which is about 7 m long, suggest that it was made by a large Chelonian, but none of the fossil turtles known so far from Cerin is likely to be the author of these footprints. The ground on which the animal walked was apparently very wet, superficially soft, and sloping. Moreover, this track is associated to soft sediment slides, confirming emersion and slope. The depositional environment is interpreted as a platform located behind a «ribbon of islands. This irregular surface was at times emerged and terrestrial tetrapods could then leave tracks on the superficial layer.     

An updated description of the osteology of the pancake tortoise Malacochersus tornieri (Testudines: Testudinidae) with special focus on intraspecific variation

Exceptional variability in the shell of the pancake tortoise Malacochersus tornieri , both in the keratinous surficial scutes and the underlying bones, in addition to its remarkably fenestrated bony shell are unique among tortoises. Based on 14 individuals of different sizes and ages, the observed variation in M. tornieri was described in detail, with additional notes on the typically testudinid skull, inner ear and brain endocast using microCT‐scan data, as well as the limbs. Similar degrees of variation have not yet been described in any other extant turtle species and therefore seem notable in M. tornieri , and might be related to the species' unique lifestyle. Within the carapace, the peripherals and suprapygals are most variable in number. Furthermore, different combinations of peripherals are participating in the central plastral fontanelle and in some individuals additional bones take part in the formation of the plastron. J. Morphol. 278:321–333, 2017. © 2017 Wiley Periodicals, Inc.