Article ID: WMC00877 2046-1690

Sex In Common Pet

Corresponding Author: Mr. Marc Girondot, Ecologie, Systematique et Evolution, Ecologie des Populations et des Communautes, UMR 8079 - ESE, 91405 - France

Submitting Author: Mr. Marc Girondot, Ecologie, Systematique et Evolution, Ecologie des Populations et des Communautes, UMR 8079 - ESE, 91405 - France

Article ID: WMC00877 Article Type: Review articles Submitted on:02-Oct-2010, 08:57:00 AM GMT Published on: 02-Oct-2010, 07:45:45 PM GMT Article URL: http://www.webmedcentral.com/article_view/877 Subject Categories:VETERINARY MEDICINE Keywords:Sex Determination, Temperature-Dependent Sex Determination, Chelonian, , Incubation, Genotypic-Sex Determination How to cite the article:Girondot M . Sex In Common Pet Turtles . WebmedCentral VETERINARY MEDICINE 2010;1(10):WMC00877 Source(s) of Funding: CNRS and University Paris Sud

Competing Interests: None

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Sex In Common Pet Turtles

Author(s): Girondot M

Abstract temperature of the embryo during a critical period of embryonic development designated the thermosensitive period (TSP) [4, 5]. This period begins with the appearance of gonad during embryogenesis With the growing market for pet turtles, veterinarians and encompasses the middle third of embryo are confronted with new demands. Owners or development. It is approximately the same embryonic breeders of turtles generally know that these species stages for any TSD species [6-10]. are temperature-dependent in terms of sex To demonstrate the occurrence of TSD in a species, determination, but lack specific knowledge on how it incubation of eggs at various temperatures were works. Furthermore, they need advice on how to performed and the sex of juveniles were plotted control incubation conditions taking this phenomenon against incubation temperature [11]. For some species, into account. A guide to answer the most common the curve is flat demonstrating that incubation questions is proposed: (i) In which species sex is temperature does not affect sexual determination in determined by temperature, sex chromosomes or both? the range of tested temperatures. This species will be (ii) How to choose incubation temperature for eggs of listed has having genotypic sex determination or GSD. turtles to optimize hatchling success, performance of Such a species is supposed to have sex juveniles or sex ratio? (iii) How to decipher sexual chromosomes even if they are not distinguishable on phenotype of juveniles? caryotype. When sex chromosomes can be visualized, Introduction sex determination is sometimes called CSD for Chromosomal Sex Determination [12] but most GSD will be CSD with a relevant technical analysis [e.g. 13]. The pet market is growing in all the studied When the plot of sex ratio vs. incubation temperatures countries [1-3] and veterinarians are confronted with were plotted, a tendency was revealed. Three patterns recurring demands on information of how to take care were described in : (i) MF, (ii) FM and (iii) FMF of young turtles and turtle eggs. The most common [14]. In the MF pattern, lower incubation temperatures concern is about control or knowledge of sexual are masculinizing whereas higher one are feminizing phenotype of juveniles. Indeed, pet turtle owners and the reverse is true for FM pattern. In FMF pattern, generally know the concept of thermosensibility of sex both the lower and the highest temperatures are determination, but specific knowledge necessary to feminizing whereas the intermediate ones are answer some specific questions are lacking. The masculinizing. Both sexes are produced in variable importance of sexual phenotype of turtles for owners proportions within a range of intermediate becomes evident when they want to breed the turtles. temperatures, called the transitional range of The objectives of this review is to bring up-to-date temperature (TRT). At the theoretical “pivotal information about the thermosensibility of sex temperature“ P, 50% of each sex is yielded [5]. determination in turtles, and to share this information TSD is widely distributed among of turtles (table to owners of pet turtles and to answer some specific 1). Eleven families are currently monomorphic for the questions: pattern of sex determination and two ( and (i) In which species is sex determined by temperature, Bataguridae) include species with both TSD and GSD. sex chromosomes or both? TSD could be the ancestral state in turtles. During (ii) How to choose incubation temperature for turtle evolution, 5 groups of turtles have acquired, eggs to optimize hatchling success, performances of independently, sex chromosomes [15]. Then, it is juvenile or sex ratio? possible to tentatively infer a pattern of sex (iii) How to identify the sexual phenotype of juveniles? determination (GSD or TSD) knowing the family or Sex determination in turtles sub-family that a species belongs to, except for Many species of oviparous reptiles, including sub-family Emydinae and the familyBataguridae where crocodilians, a majority of turtles, some lizards and the the analysis should be done at the level. two closely related species of Sphenodon have However, the exact reaction norm for the sex ratio vs. displayed temperature-dependent sex determination incubation temperatures is more difficult to anticipate (TSD). In these species, the differentiation of gonads with the exception of eggs that come from an already into ovaries or testes depends on the incubation studied species and population [review in 16].

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Now let’s discuss an unresolved question: is it component to validate definitively this model for turtles. possible to have both GSD and TSD at the same time Both in Green turtle, Chelonia mydas [30], and in a single species? When first discovered in turtles European Freshwater turtle, orbicularis [24, 31] [17-19], thermosensitivity of sex determination was sex specific DNA RFLP bands have been found. thought to superimpose a putative chromosomal sex However in both cases, validation with eggs incubated determination [C. Pieau, pers. comm. see also 20]. But in known conditions were lacking. Further researches rapidly a strong dichotomy between GSD and TSD should be done in this direction. species has been drawn by some authors, and GSD As a conclusion for this section, a veterinarian should and TSD were described as two incompatible states look at table 1 to identify the family or sub-family of the [21]. However, the genetic component in sex ratio has species. The main pet species are reported in table 2 been demonstrated for eggs incubated in the range of with their pattern of sex determination. For uncommon temperatures where both sexes can be produced in species, a search in specific literature must be done the European Freshwater turtle (Emys orbicularis), the [32]. If the species is not listed anywhere, the only common snapping turtle ( serpentina), the solution is to refer to the pattern in the most related (Chrysemys picta), and the map turtle species based on a composite phylogeny of turtles ( ouachitensis) [22-25]. However, this build from the most recent sources [33-40] and to infer genetic component was thought to not been able to the pattern of sex determination based on parsimony express in natural condition [22]. principles for reconstructing evolution [41]. However, a In the 80’th, the serological minor histocompatibility doubt will still exist. antigen H-Y was supposed to be a marker of the heterogametic sex and has been extensively studied How to choose incubation in the European Freshwater turtle, Emys orbicularis. temperature for eggs of turtles? When incubated at male- or female-producing temperatures, high and low expression levels were observed in serum of juveniles, irrespective of their When purchasing turtle eggs, the owner will need sexual phenotype. On the other hand, when incubated information on the best incubation procedure. The at both sexes-producing temperatures, males three main factors that should be taken into account hatchlings had low-level of expression and females are cleanliness, humidity and temperature [42]. had high-level of expression. This polymorphism of Cleanliness is important to prevent eggs from rotting expression of H-Y antigen had been proposed to [43] and pathogen transmission to the eggs [44]. If reflect the genetic component influencing sex humidity is lower than required, eggs will dehydrate determination at intermediate temperature [26, 27]. and die and if higher than required, eggs will break out Low or high temperatures override this genetic or rot. The use of moist vermiculite is recommended to component. Then for incubation at constant maintain viable hygrometry [45]. Similarly, too high temperature, most of the embryos have their sexual and low incubation temperatures could have phenotype that is determined by incubation detrimental effects on the survival of embryos and temperature except for the narrow zone of intermediate ones must be preferred. However, by temperature where both sexes are produced. When choosing a specific temperature, the owner can H-Y antigen has been studied among adults from influence the sex of offspring as seen previously but natural population, 80% of individuals have their H-Y also their performance [for example see 46, 47, 48]. antigen status (i.e. sexual genotype) conformed to There is no general conclusion on the best-required their sexual phenotype [28]. How a species could have temperature of incubation for turtle eggs. For example, TSD when incubated in artificial condition and a sex incubation at feminizing temperatures has been determination that looks like GSD in 80% of the advocated as a conservation measure for threatened individuals in natural conditions? It was proposed that species in the case of reintroduction purposes [49] but when incubation temperatures fluctuate from male to this recommendation has been criticized from a female temperature, the genetic variability in sex ecological point of view [50]. Due to the lack of determination could influence sex of the gonad and knowledge of the consequences that disrupts the that only when temperature fluctuates around very fluctuation of temperature in natural incubation of eggs high or very low temperature, it overpasses the [51], and any adverse effects on individuals of strongly genetic component. The question was debated until a feminizing conditions [52]. similar system was deciphered in an Australian lizard Recently, several authors have published data to with both sex chromosomes and TSD [29]. However, compare the effects of fluctuating versus constant we still lack a molecular marker for this genetic incubation temperature. For all the tested parameters

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(growth rate, temperature choice, locomotor turtles weigh less than 10 g [e.g. 6 g in Emys performance, immune response), fluctuating orbicularis, 10], this method cannot be used for very temperatures have a differential impact, often young turtles. Furthermore, this method is very beneficial, when compared to constant temperatures invasive and could be lethal for small turtles (pers. [46, 53-55]. obs.). I therefore recommend incubation at diurnal fluctuating The serum testosterone radioimmunoassay procedure temperatures around the pivotal temperature. Average has been used conclusively for Lepidochelys pivotal temperatures for the various turtle families or olivacea,Chelonia mydas and agassizii sub-families are shown in table 1. In case the owner [64-66]. However, species specific sexing criteria must wants a specific sex, species specific pattern of sex be developed using both plasma testosterone determination [16] should serve as a reference to concentrations and laparoscopic examination of the choose incubation temperature. An average incubation gonads [67]. The origin of serum testosterone could be temperature of 30 °C for Testudinidae, 31 °C for extragonadal, perhaps from the brain [68], and then a and 28.5 °C for Emydidae can be secondary consequence of sexual phenotype as chosen with 2 °C diurnal amplitude. demonstrated in Alligator [69]. The serum testosterone radioimmunoassay procedure cannot be used for Identification of sexual hatchling and estradiol:testosterone ratio has been phenotype of juveniles used conclusively in Caretta caretta egg chorioallantoic/amniotic fluid [70] but should be validated for other species as well before it can be Many turtle species are highly dimorphic as adults [56] recommended. but external morphology of turtle is generally not Conclusion sexually dimorphic until subadult stage [57]. Hatchling turtles typically exhibit little or no obvious dimorphism that allows for straightforward identi?cation of sex by The phenomenon of temperature-dependent sex external observation [58]. Significant sexual determination in reptiles is generally known. However dimorphism Chrysemys picta and the limit of the current knowledge of this sex expansa hatchlings were measured using determination is often not well understood. Specifically, landmark-based geometric morphometric methods. the exact nature of the relationship between TSD and This method had high accuracy in assigning sex when GSD in a single species is still controversial. The most compared with true sex (98% and 90%, respectively), recent review points out that sex determination should and cross-validation with hatchlings not used in model be viewed along a continuum TSD-GSD rather than definition revealed a correct classi?cation rate of 85% from a dichotomy [71]. [59]. Multivariate model allows for the differentiation of When confronted with the demand for incubation males and females in 4-years juvenilesGopherus conditions, the best solution will be to mimic natural polyphemus but not in hatchling Gopherus agassizii conditions of incubation and then to incubate eggs [60]. Difference in possibility to differentiate both sexes with daily fluctuating temperatures within the range of in Gopherus genus could reveal that shape viable incubation temperatures. Only when the owner morphology dimorphism is acquired during early indicates that he specifically wants one sex; for growth. Size difference between one-year old males example for breeding purpose, then incubation at low and females scripta elegans were or high nearly constant temperatures could be observed when reared in same conditions [61]. recommended. However, size assignation cannot be used when To know the sexual phenotype of hatchlings or rearing conditions are not standardized and alternative juveniles, there is at present for most species no other techniques must be used. way than to be patient and to wait until the individual External gonadal or sexual ducts morphology is acquires sexually secondary dimorphic characters generally studied by dissection of dead [62] which can be differentiated in tail length, eye colours, which cannot be recommended in the context of this claw lengths, or plastron shape depending on the review. But external gonadal morphology has been species [58] also observed by laparoscopy on live animals in Green turtles, Chelonia mydas [63] and Desert , Abbreviation(s) Gopherus agassizii [64]. Laparoscopy has been successfully used in Desert as small as 28 g total body mass. Recalling that hatchlings of most

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Illustrations Illustration 1

Sex determination among families or subfamilies of turtles.

Family or Sex Average pivotal Subfamily determination temperature TSD 31.79 °C (SD 0.50 °C) GSD - Carrettochelyidae TSD na GSD - Staurotypidae GSD - TSD na TSD na TSD FMF TSD 29.47 °C (SD 0.06 °C) TSD 29.35 °C (SD 0.62 °C) Emydidae GSD or TSD 28.56 °C (SD 0.87 °C) Emydinae GSD or TSD 27.82 °C (SD 0.70 °C) TSD 28.87 °C (SD 0.76 °C) Bataguridae GSD or TSD na Testudinidae TSD 30.09 °C (SD 0.82 °C) ALL 29.33 °C (SD 1.07 °C)

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Illustration 2

Twenty most common turtle pet species exported from US between 2002 to 2005.

Pattern of sex Scientific Family or determinati Exported from the Rank Name Common Name Sub-Family on US (2002-2005) Trachemys scripta Red-eared Slider 1 elegans Turtle Deirochelynae TSD MF 15186735 Florida Redbelly 2 nelsoni Turtle Deirochelynae TSD MF 7019251 Pseudemys 3 concinna Turtle Deirochelynae TSD MF 2566312 Trachemys 4 scripta scripta Yellowbelly Slider Deirochelynae TSD MF 1255398 Pseudemys Alabama Redbelly 5 alabamensis Turtle Deirochelynae TSD MF 961772 Pseudemys 6 floridana Florida Cooter Deirochelynae TSD MF 939583 Graptemys pseudogeogra 7 phica kohni Deirochelynae TSD MF 680795 Chelydra Common Snapping 8 serpentina Turtle Chelydridae TSD FMF 634838 Trachemys scripta 9 troostii Deirochelynae TSD MF 366648 Trachemys scripta 10 gaigeae Big Bend Slider Deirochelynae TSD MF 338396 WebmedCentral > Review articlesFlorida soft-shell Page 9 of 10 11 ferox Turtle Trionychidae GSD 256850 Pseudemys 12 peninsularis Deirochelynae TSD MF 191606 Chrysemys Western Painted 13 picta Turtle Deirochelynae TSD MF 173315 Pseudemys American Redbelly 14 rubriventris Turtle Deirochelynae TSD MF 104711 Alligator Snapping 15 temminckii Turtle Chelydridae TSD FMF 90466 Apalone Spiny soft-shell 16 spinifera Turtle Trionychidae GSD 85072 17 odoratus Common Musk Turtle Kinosternidae TSD FMF 65734 Graptemys pseudogeogra 18 phica Deirochelynae TSD MF 40979 Apalone Smooth soft-shell 19 mutica Turtle Trionychidae GSD 20892 Sternotherus Keelbacked Musk 20 carinatus Turtle Kinosternidae TSD FMF 14901 WMC00877 Downloaded from http://www.webmedcentral.com on 31-Dec-2011, 07:59:13 AM

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