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Eremias Multiocellata) Living at High Altitude

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Eremias Multiocellata) Living at High Altitude See discussions, stats, and author profiles for this publication at: http://www.researchgate.net/publication/257160343 Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude ARTICLE in JOURNAL OF THERMAL BIOLOGY · OCTOBER 2012 Impact Factor: 1.51 · DOI: 10.1016/j.jtherbio.2012.03.002 CITATIONS READS 7 100 7 AUTHORS, INCLUDING: Xiaolong Tang Feng Yue Lanzhou University Central China Normal University 17 PUBLICATIONS 60 CITATIONS 31 PUBLICATIONS 209 CITATIONS SEE PROFILE SEE PROFILE Cui Wang University of Helsinki 6 PUBLICATIONS 16 CITATIONS SEE PROFILE Available from: Xiaolong Tang Retrieved on: 21 October 2015 Journal of Thermal Biology 37 (2012) 438–444 Contents lists available at SciVerse ScienceDirect Journal of Thermal Biology journal homepage: www.elsevier.com/locate/jtherbio Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude Xiao-Long Tang 1, Feng Yue 1, Xue-Feng Yan, De-Jiu Zhang, Ying Xin, Cui Wang, Qiang Chen n Institute of Biochemistry and Molecular Biology, School of Life Science, Lanzhou University, Lanzhou 730000, China article info abstract Article history: Temperature-dependent sex determination (TSD) is well studied in many species of reptiles, but little is Received 26 April 2011 known on how geographic distribution and altitude affect the sex ratio. In the present study, we Accepted 9 March 2012 focused on a population of a viviparous lizard with TSD (Eremias multiocellata) that lives at high Available online 17 March 2012 altitudes (E2900 m) in Tianzhu, Gansu province, China. Gestation temperature had a notable effect on Keywords: the offspring sex ratio, gestation period, and the mother’s body mass. The mothers produced female Viviparous lizard biased offspring at 25 1C but male biased offspring at 35 1C. All female lizards lost weight during Eremias multiocellata pregnancy, and the least loss of the body mass was observed at 31 1C. The gestation period increased in Gestation temperature a non-linear fashion as ambient temperature was reduced. Average litter size was elevated with an TSD increase of gestation temperatures, reached a maximum at 31 1C, and then declined at 35 1C. Compared Maternal reproduction with a previous study on a Minqin population which lives at a lower altitude (E1400 m) and warmer climate, the present study obtained a less skewed sex ratio of offspring in the Tianzhu population. Geographic variations also affected offspring morphology between the two populations; females collected from Tianzhu produced larger litters but with a smaller body weight of offspring. These differences may be caused by the adaptive response to the cool climatic and high-altitude environ- mental conditions. & 2012 Elsevier Ltd. All rights reserved. 1. Introduction male offspring increasing in colder years (Wapstra et al., 2009). If cohort sex ratio bias at birth leads to adult sex ratio bias, long- Reptiles exhibit both genotypic (GSD) and environmental- term directional changes in thermal conditions may have impor- dependent sex determination (ESD) (Bull, 1983; Valenzuela tant effects on population dynamics. However, previous studies et al., 2003). The most common form of ESD is Temperature- also found viviparous lizards living at different extreme climatic dependent sex determination (TSD), a typical case of phenotypic conditions could regulate maternal behavior (Wapstra et al., plasticity, where sex is determined after fertilization is affected by 2004), or even alter their sex-determining mechanisms to avoid the environment temperature (Bull, 1983). The TSD phenomenon dramatic changes at population level (Pen et al., 2010). and its mechanisms have been studied in many reptiles. Since A great deal of work illustrated that geographic variations may Robert and Thompson (2001) first reported that TSD does indeed influence population dynamics through multiple pathways, includ- occur in a viviparous lizard, four live-bearing lizards were shown ing sexual selection (Blanckenhorn et al., 2006; Møller, 2004), to exhibit TSD (Ji et al., 2006; Wapstra et al., 2004; Zhang et al., reproduction (Angilletta et al., 2006; ChamaillE´ -Jammes et al., 2010). These studies were innovative and provide new arguments 2006; Dunn, 2004), and offspring phenotype (Du and Shine, for explaining the mechanism of TSD. It is also important to 2008; Du and Feng, 2008; Ji et al., 2006; Shine and Harlow, understand thermal adaptation of these TSD species under 1996). These variations may not only depend on the direct effects different environmental conditions. A recent study on a natural of environmental conditions (Angilletta et al., 2002), but also have population of viviparous lizard with TSD (Niveoscincus ocellatus) more complex causes such as adaptive phenotypic plasticity and found sex ratios varied significantly from year to year and closely the timing of life history events in response to local environmental tracked thermal conditions in the field, with the proportion of conditions (Pulido and Berthold, 2004; Wapstra et al., 2009). For instance, following Bergmann’s rule, a species of larger size were found in colder environments, and species of smaller size were n Corresponding author at: Institute of Biochemistry and Molecular Biology, found in warmer regions. But there exist many fields where inverse School of Life Science, Lanzhou University, 222 Tian Shui South Road, Lanzhou phenomenon appear, that the body size of ectotherm species may 730000, China. Tel./fax: þ86 931 8915316. E-mail addresses: [email protected], [email protected] (Q. Chen). change smaller as the ascending altitude and cooler temperatures 1 Both authors contributed equally to this work. (Ashton, 2001; Ashton and Feldman, 2003). In addition, under 0306-4565/$ - see front matter & 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.jtherbio.2012.03.002 X.-L. Tang et al. / Journal of Thermal Biology 37 (2012) 438–444 439 different environmental conditions, the pregnant females may 2.2. Constant gestation temperature experiment change output strategies. For example, some pregnant females produce ‘‘small clutches with big eggs’’ but the reverse situations The lizards were captured in late May and brought to our are found in some other species (Sinervo, 1990). However, most of laboratory in Lanzhou University. For each lizard, sex was identi- these studies were focused at the species level and investigated the fied by hemipene eversion and the morphological traits (body relationship between offspring sex ratio and varied incubation mass and SVL) were measured. In some reptile species, females temperature. How thermal environments affect female reproduc- could adjust their offspring sex ratios in response to imbalances in tive characters and offspring sex ratio in different populations the population adult sex ratio, which is known as operational sex remain an eristic question (Escobedo-Galva´netal.,2011; ratio (OSR) (Thompson et al., 2003; Warner and Shine, 2007). In Kallimanis, 2010; Witt et al., 2010). order to exclude the influence of the OSR, we collected the same Global warming is being shown to significantly affects the numbers of adult male and female lizards in the present study. 48 ecosystem (Arago´ n et al., 2010; Parmesan and Yohe, 2003) and female and 48 male lizards were divided equally into four groups climatic conditions and this could drive offspring sex ratios in using random sampling methods. Each group was comprised of species with TSD, which could potentially lead to local extinction six cages, two females and two males were maintained in one (Janzen, 1994). However, if ectotherms live in considerably cooler cage (60 Â 30 Â 40 cm3). A cut a toe method was used environments than their optimum, they may take advantage of for individual identification. Four constant temperatures were warming temperature by basking and would benefit more from a provided (25, 29, 31 and 35 1C) from 0900 to 1700, and during the warmer climate (Huey and Tewksbury, 2009). In order to learn rest of the time, the temperature inside the cage was consistent more about the possible variations on offspring sex ratio and with the room temperature. The room lights were programmed to female reproductive characters in cool environmental conditions, a 12 h lighting: 12 h dark cycle (0700–1900 h) in order to we chose a high altitude-inhabiting viviparous lizard Eremias simulate natural light. The bottom of cage was covered with multiocellata in Tianzhu, Gansu province, China. This population 5 mm silver sand and cage temperature (set temperature70.3 1C) lives vibrantly in mountain area, although the mean temperatures was kept constantly by electronic temperature control device at reproductive season were lower than its optimal temperature (WMZK-10, Shanghai Medical Instrument). The room tempera- (Yan et al., 2011). Our previous study on Minqin population ture was controlled at 1870.5 1C, and the temperature inside the showed that E. multiocellata is a TSD species (Zhang et al., cage fell to room temperature at night. Sufficient mealworms and 2010). The present study aims to investigate (1) whether effects water were provided every two days during entire experiment. of gestation temperature on offspring sex ratios are different in high- and low-altitude populations and (2) possible adaptive 2.3. Field experiment as control group characteristics of Tianzhu population in offspring phenotypic plasticity and female fecundity. The control groups consisting of 12 female and 12 male lizards raised in semi-natural enclosures. The field enclosure (4 Â 3.5 m2) was constructed of 100 cm high zinc-gilt iron sheet with 50 cm buried underground to prevent lizards escaping. A fine wire net 2. Materials and methods was placed over the enclosure to keep lizards from being eaten by predators. Bumpy ground with sparse grass was artificially built 2.1. Study species and several bricks were placed in each enclosure to give lizards opportunity to choose their optimal temperature or basking E. multiocellata have been studied extensively over the past places.
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