Article ID: WMC00877 2046-1690 Sex In Common Pet Turtles 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, Reptile, 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 WebmedCentral > Review articles Page 1 of 10 WMC00877 Downloaded from http://www.webmedcentral.com on 31-Dec-2011, 07:59:13 AM 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 Turtle 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 Reptiles: (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 family 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 (Emydidae 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 genus 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]. WebmedCentral > Review articles Page 2 of 10 WMC00877 Downloaded from http://www.webmedcentral.com on 31-Dec-2011, 07:59:13 AM 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, Emys 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 (Chelydra serpentina), the solution is to refer to the pattern in the most related painted turtle (Chrysemys picta), and the map turtle species based on a composite phylogeny of turtles (Graptemys 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