Volume 38 Issue 2
Mar.  2017
Turn off MathJax
Article Contents
Yang Wang, Zhi-Gao Zeng, Liang Ma, Shu-Ran Li, Wei-Guo Du. Food restriction affects maternal investment but not neonate phenotypes in a viviparous lizard. Zoological Research, 2017, 38(2): 81-87. doi: 10.24272/j.issn.2095-8137.2017.011
Citation: Yang Wang, Zhi-Gao Zeng, Liang Ma, Shu-Ran Li, Wei-Guo Du. Food restriction affects maternal investment but not neonate phenotypes in a viviparous lizard. Zoological Research, 2017, 38(2): 81-87. doi: 10.24272/j.issn.2095-8137.2017.011

Food restriction affects maternal investment but not neonate phenotypes in a viviparous lizard

doi: 10.24272/j.issn.2095-8137.2017.011
Funds:  Foundation items:This study was supported by the grant from the National Natural Science Fund for Distinguished Young Scholars (31525006)
More Information
  • Corresponding author: Wei-Guo Du
  • Received Date: 2017-01-24
  • Rev Recd Date: 2017-03-03
  • Publish Date: 2017-03-18
  • Food availability significantly affects an animal's energy metabolism, and thus its phenotype, survival, and reproduction. Maternal and offspring responses to food conditions are critical for understanding population dynamics and life-history evolution of a species. In this study, we conducted food manipulation experiments in field enclosures to identify the effect of food restriction on female reproductive traits and postpartum body condition, as well as on hatchling phenotypes, in a lacertid viviparous lizard from the Inner Mongolian desert steppe of China. Females under low-food availability treatment (LFT) had poorer immune function and body condition compared with those under high-food availability treatment (HFT). The food availability treatments significantly affected the litter size and litter mass of the females, but not their gestation period in captivity or brood success, or the body size, sprint speed, and sex ratio of the neonates. Females from the LFT group had smaller litter sizes and, therefore, lower litter mass than those from the HFT group. These results suggest that female racerunners facing food restriction lay fewer offspring with unchanged body size and locomotor performance, and incur a cost in the form of poor postpartum body condition and immune function. The flexibility of maternal responses to variable food availability represents an important life strategy that could enhance the resistance of lizards to unpredictable environmental change.
  • loading
  • [1]
    Abell AJ. 1999. Variation in clutch size and offspring size relative to environmental conditions in the lizard Sceloporus virgatus. Journal of Herpetology, 33(2):173-180.
    Acheampong E, Campbell RW, Diekmann ABS, St John MA. 2011. Food availability effects on reproductive strategy:The case of Acartia tonsa (Copepoda:Calanoida). Marine Ecology Progress Series, 428:151-159.
    Ballinger RE. 1977. Reproductive strategies:food availability as a source of proximal variation in a lizard. Ecology, 58(3):628-635.
    Ballinger RE, Congdon JD. 1980. Food resource limitation of body growth rates in Sceloporus scalaris (Sauria, Iguanidae). Copeia, 1980(4):921-923.
    Bartlett J. 1988. Male Mating success and paternal care in Nicrophorus vespilloides (Coleoptera, Silphidae). Behavioral Ecology and Sociobiology, 23(5):297-303.
    Bleu J, Le Galliard JF, Fitze PS, Meylan S, Clobert J, Massot M. 2013. Reproductive allocation strategies:A long-term study on proximate factors and temporal adjustments in a viviparous lizard. Oecologia, 171(1):141-151.
    Bonnet X, Bradshaw D, Shine R. 1998. Capital versus income breeding:An ectothermic perspective. Oikos, 83(2):333-342.
    Bonnet X, Naulleau G, Shine R, Lourdais O. 2001. Short-term versus long-term effects of food intake on reproductive output in a viviparous snake, Vipera aspis. Oikos, 92(2):297-308.
    Brown GP, Shilton CM, Shine R. 2011. Measuring amphibian immunocompetence:Validation of the phytohemagglutinin skin-swelling assay in the cane toad, Rhinella marina. Methods in Ecology and Evolution, 2(4):341-348.
    Caley MJ, Schwarzkopf L, Shine R. 2001. Does total reproductive effort evolve independently of offspring size? Evolution, 55(6):1245-1248.
    Clout MN, Elliott GP, Robertson BC. 2002. Effects of supplementary feeding on the offspring sex ratio of kakapo:A dilemma for the conservation of a polygynous parrot. Biological Conservation, 107(1):13-18.
    Donelson JM, McCormick MI, Munday PL. 2008. Parental condition affects early life-history of a coral reef fish. Journal of Experimental Marine Biology and Ecology, 360(2):109-116.
    Douhard M, Plard F, Gaillard JM, Capron G, Delorme D, Klein F, Duncan P, Loe LE, Bonenfant C. 2014. Fitness consequences of environmental conditions at different life stages in a long-lived vertebrate. Proceedings of the Royal Society B:Biological Sciences, 281(1785):20140276.
    Du WG, Ji X, Shine R. 2005. Does body-volume constrain reproductive output in lizards? Biology Letters, 1(1):98-100.
    Du WG. 2006. Phenotypic plasticity in reproductive traits induced by food availability in a lacertid lizard, Takydromus septentrionalis. Oikos, 112(2):363-369.
    Dunham AE. 1978. Food availability as a proximate factor influencing individual growth rates in the iguanid lizard Sceloporus Merriami. Ecology, 59(4):770-778.
    Einum S, Fleming IA. 1999. Maternal effects of egg size in brown trout (Salmo trutta):norms of reaction to environmental quality. Proceedings of the Royal Society B:Biological Sciences, 266(1433):2095-2100.
    Flemming A F, Blackburn D G. 2003. Evolution of placental specializations in viviparous African and South American lizards. Journal of Experimental Zoology Part A, 299A(1):33-47.
    Fox CW, Mousseau TA. 1998. Maternal effects as adaptations for transgenerational phenotypic plasticity in insects. Maternal Effects as Adaptations. New York:Oxford University Press, 159-177.
    Hafer N, Ebil S, Uller T, Pike N. 2011. Transgenerational effects of food availability on age at maturity and reproductive output in an asexual collembolan species. Biology Letters, 7(5):755-758.
    Hamilton WD. 1967. Extraordinary sex ratios. Science, 156(3774):477-488.
    Hegemann A, Matson KD, Flinks H, Tieleman BI. 2013. Offspring pay sooner, parents pay later:Experimental manipulation of body mass reveals trade-offs between immune function, reproduction and survival. Frontiers in Zoology, 10:77.
    Hillesheim E, Stearns SC. 1991. The responses of Drosophila melanogaster to artificial selection on body weight and its phenotypic plasticity in two larval food environments. Evolution, 45(8):1909-1923.
    Hogstedt G. 1981. Effect of additional food on reproductive success in the Magpie (Pica pica). Journal of Animal Ecology, 50(1):219-229.
    Hoy SR, Millon A, Petty SJ, Whitfield DP, Lambin X. 2016. Food availability and predation risk, rather than intrinsic attributes, are the main factors shaping the reproductive decisions of a long-lived predator. Journal of Animal Ecology, 85(4):892-902.
    Hsu BY, Dijkstra C, Darras VM, de Vries B, Groothuis TGG. 2016. Maternal adjustment or constraint:Differential effects of food availability on maternal deposition of macro-nutrients, steroids and thyroid hormones in rock pigeon eggs. Ecology and Evolution, 6(2):397-411.
    Iglesias-Carrasco M, Head ML, Cabido C. 2016. Habitat dependent effects of experimental immune challenge on lizard anti-predator responses. Behavioral Ecology and Sociobiology, 70(11):1931-1939.
    Irschick DJ, Losos JB. 1998. A comparative analysis of the ecological significance of maximal locomotor performance in Caribbean anolis lizards. Evolution, 52(1):219-226.
    Itonaga K, Jones SM, Wapstra E. 2012a. Do gravid females become selfish? Female allocation of energy during gestation. Physiological and Biochemical Zoology, 85(3):231-242.
    Itonaga K, Jones SM, Wapstra E. 2012b. Effects of maternal basking and food quantity during gestation provide evidence for the selective advantage of matrotrophy in a viviparous lizard. PLoS One, 7(7):e41835.
    Jakob EM, Marshall SD, Uetz GW. 1996. Estimating fitness:A comparison of body condition indices. Oikos, 77(1):61-67.
    Johnson JC, Miles LS, Trubl PJ, Hagenmaier A. 2014. Maternal effects on egg investment and offspring performance in black widow spiders. Animal Behaviour, 91:67-73.
    Jones SKC, Munn AJ, Penman TD, Byrne PG. 2015. Long-term changes in food availability mediate the effects of temperature on growth, development and survival in striped marsh frog larvae:Implications for captive breeding programmes. Conservation Physiology, 3(1):cov029.
    Kitaysky AS, Wingfield JC, Piatt JF. 1999. Dynamics of food availability, body condition and physiological stress response in breeding black-legged kittiwakes. Functional Ecology, 13(5):577-584.
    Komdeur J, Daan S, Tinbergen J, Mateman C. 1997. Extreme adaptive modification in sex ratio of the Seychelles warbler's eggs. Nature, 385(6616):522-525.
    Krist M, Munclinger P. 2015. Context dependence of maternal effects:Testing assumptions of optimal egg size, differential, and sex allocation models. Ecology, 96(10):2726-2736.
    Le Galliard JF, Le Bris M, Clobert J. 2003. Timing of locomotor impairment and shift in thermal preferences during gravidity in a viviparous lizard. Functional Ecology, 17(6):877-885.
    Lehman S, Smith AA. 1988. Regional differentiation in the stomach of the green anole. The Anatomical Record, 220(4):364-368.
    Li H, Ji X, Qu YF, Gao JF, Zhang L. 2006. Sexual dimorphism and female reproduction in the multi-ocellated racerunner (Eremias multiocellata) (Lacertidae). Acta Zoologica Sinica, 52(2):250-255.
    Ma L, Sun BJ, Li SR, Sha W, Du WG. 2014. Maternal thermal environment induces plastic responses in the reproductive life history of oviparous lizards. Physiological and Biochemical Zoology, 87(5):677-683.
    Meserve PL, Vásquez H, Kelt DA, Gutiérrez JR, Milstead WB. 2016. Patterns in arthropod abundance and biomass in the semiarid thorn scrub of Bosque Fray Jorge national park, north-central Chile:A preliminary assessment. Journal of Arid Environments, 126:68-75.
    Neuman-Lee LA, Fokidis HB, Spence AR, Van der Walt M, Smith GD, Durham S, French SS. 2015. Food restriction and chronic stress alter energy use and affect immunity in an infrequent feeder. Functional Ecology, 29(11):1453-1462.
    Olsson M, Wapstra E, Olofsson C. 2002. Offspring size-number strategies:Experimental manipulation of offspring size in a viviparous lizard (Lacerta vivipara). Functional Ecology, 16(1):135-140.
    Ramírez-Bautista A, Balderas-Valdivia C, Vitt LJ. 2000. Reproductive ecology of the whiptail lizard Cnemidophorus lineatissimus (Squamata:Teiidae) in a tropical dry forest. Copeia, 2000(3):712-722.
    Ramírez-Pinilla MP. 2006. Placental transfer of nutrients during gestation in an Andean population of the highly matrotrophic lizard genus mabuya (squamata:scincidae). Herpetological Monographs, 20(1):194-204.
    Raveh S, Vogt D, Kölliker M. 2016. Maternal programming of offspring in relation to food availability in an insect (Forficula auricularia). Proceedings of the Royal Society B:Biological Sciences, 283(1828):20152936.
    Rollinson N, Hutchings JA. 2013. Environmental quality predicts optimal egg size in the wild. The American Naturalist, 182(1):76-90.
    Rollinson N, Rowe L. 2016. The positive correlation between maternal size and offspring size:Fitting pieces of a life-history puzzle. Biological Reviews, 91(4):1134-1148.
    Rosenfeld CS, Roberts RM. 2004. Maternal diet and other factors affecting offspring sex ratio:A review. Biology of Reproduction, 71(4):1063-1070.
    Sheldon BC, Verhulst S. 1996. Ecological immunology:Costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology & Evolution, 11(8):317-321.
    Shine R. 2003. Effects of pregnancy on locomotor performance:An experimental study on lizards. Oecologia, 136(3):450-456.
    Sinervo B, Licht P. 1991. Proximate constraints on the evolution of egg size, number, and total clutch mass in lizards. Science, 252(5010):1300-1302.
    Smith CC, Fretwell SD. 1974. The optimal balance between size and number of offspring. The American Naturalist, 108(962):499-506.
    Styrsky JD, Dobbs RC, Thompson CF. 2000. Food-supplementation does not override the effect of egg mass on fitness-related traits of nestling house wrens. Journal of Animal Ecology, 69(4):690-702.
    Sun LX, Shine R, Zhao DB, Tang ZR. 2002. Low costs, high output:Reproduction in an insular pit-viper (Gloydius shedaoensis, Viperidae) from north-eastern China. Journal of Zoology, 256(4):511-521.
    Tang XL, Yue F, Yan XF, Zhang DJ, Xin Y, Wang C, Chen Q. 2012. Effects of gestation temperature on offspring sex and maternal reproduction in a viviparous lizard (Eremias multiocellata) living at high altitude. Journal of Thermal Biology, 37(6):438-444.
    Tieleman BI, Dijkstra TH, Klasing KC, Visser GH, Williams JB. 2008. Effects of experimentally increased costs of activity during reproduction on parental investment and self-maintenance in tropical house wrens. Behavioral Ecology, 19(5):949-959.
    Trivers RL, Willard DE. 1973. Natural selection of parental ability to vary the sex ratio of offspring. Science, 179(4068):90-92.
    Uller T, Isaksson C, Olsson M. 2006. Immune challenge reduces reproductive output and growth in a lizard. Functional Ecology, 20(5):873-879.
    Vaissi S, Sharifi M. 2016. Changes in food availability mediate the effects of temperature on growth, metamorphosis and survival in endangered yellow spotted mountain newt:Implications for captive breeding programs. Biologia, 71(4):444-451.
    Vinkler M, Bainová H, Albrecht T. 2010. Functional analysis of the skin-swelling response to phytohaemagglutinin. Functional Ecology, 24(5):1081-1086.
    Wang Y, Zeng ZG, Li SR, Bi JH, Du WG. 2016. Low precipitation aggravates the impact of extreme high temperatures on lizard reproduction. Oecologia, 182(4):961-971.
    Wapstra E, Warner DA. 2010. Sex allocation and sex determination in squamate reptiles. Sexual Development, 4(1-2):110-118.
    Warner DA, Lovern MB, Shine R. 2007. Maternal nutrition affects reproductive output and sex allocation in a lizard with environmental sex determination. Proceedings of the Royal Society B:Biological Sciences, 274(1611):883-890.
    Warner DA, Lovern MB. 2014. The maternal environment affects offspring viability via an indirect effect of yolk investment on offspring size. Physiological and Biochemical Zoology, 87(2):276-287.
    Warner DA, Buckelew AM, Pearson PR, Dhawan A. 2015. The effect of prey availability on offspring survival depends on maternal food resources. Biological Journal of the Linnean Society, 115(2):437-447.
    Williams LH. 1966. Observations on the life history of the poplar hawk moth, Laothoe Populi L. Part I. Mating, egg laying and larval development and behaviour. Physiological Entomology, 41(7-9):93-102.
    Winne CT, Willson JD, Gibbons JW. 2006. Income breeding allows an aquatic snake Seminatrix pygaea to reproduce normally following prolonged drought-induced aestivation. Journal of Animal Ecology, 75(6):1352-1360.
    Zamora-Camacho FJ, Reguera S, Moreno-Rueda G. 2016. Elevational variation in body-temperature response to immune challenge in a lizard. PeerJ, 4:e1972.
    Zeng ZG, Bi JH, Li SR, Wang Y, Robbins TR, Chen SY, Du WG. 2016. Habitat alteration Influences a desert steppe lizard community:Implications of species-specific preferences and performance. Herpetological Monographs, 30(1):34-48.
    Zhu H, Wang DL, Wang L, Fang J, Sun W, Ren BZ. 2014. Effects of altered precipitation on insect community composition and structure in a meadow steppe. Ecological Entomology, 39(4):453-461.
  • Relative Articles

    [1] Kai Wang, Jia-Wei Wu, Ke Jiang, Jin-Min Chen, Ben-Fu Miao, Cameron D. Siler, Jing Che. A new species of Mountain Dragon (Reptilia: Agamidae: Diploderma) from the D. dymondi complex in southern Sichuan Province, China. Zoological Research, 2019, 40(5): 456-465.  doi: 10.24272/j.issn.2095-8137.2019.034
    [2] Lorenzo Alibardi. Immunodetection of ephrin receptors in the regenerating tail of the lizard Podarcis muralis suggests stimulation of differentiation and muscle segmentation. Zoological Research, 2019, 40(5): 416-426.  doi: 10.24272/j.issn.2095-8137.2019.046
    [3] Lorenzo Alibardi. Tail regeneration reduction in lizards after repetitive amputation or cauterization reflects an increase of immune cells in blastemas. Zoological Research, 2018, 39(6): 413-423.  doi: 10.24272/j.issn.2095-8137.2018.050
    [4] JIANG Jie, WU Zheng-jun, YU Hai, HUANG Cheng-ming, WANG Zhen-xing. Prey Discrimination Mechanisms of Chinese Crocodile Lizard (Shinisaurus crocodilurus). Zoological Research, 2009, 30(5): 553-558.  doi: 10.3724/SP.J.1141.2009.05554
    [5] ZHANG Hua, YANG Xiao-dong, DU Jie, WU Yi-xue. Influence of Soil Temperature and Moisture on the Cocoon Production and Hatching of the Exotic Earthworm Pontoscolex corethrurus . Zoological Research, 2008, 29(3): 305-312.  doi: 10.3724/SP.J.1141.2008.03305
    [6] ZHANG Yong-pu, YING Xue-ping, JI Xiang. Ultrastructure of the Spermatozoon of the Northern Grass Lizard (Takydromus septentrionalis) with Comments on the Variability of Sperm Morphology Among Lizard Taxa. Zoological Research, 2005, 26(5): 518-526.
    [7] XU Xue-feng, WU Yi-lian, ZHANG Jian-long. Influence of Thermal and Hydric Environments on Egg Incubation,Hatching Success,and Hatchling Traits in a Lacertid Lizard,Eremias brenchleyi. Zoological Research, 2005, 26(1): 55-60.
    [8] DU Wei-guo, LIN Chi-xian, SHOU Lu, JI Xiang. Morphological Correlates of Locomotor Performance in Four Species of Lizards Using Different Habitats. Zoological Research, 2005, 26(1): 41-46.
    [9] LIN Chi-xian, QIU Qing-bo, LIN Long-hui, JI Xiang. Sexual Dimorphism and Reproductive Output in Reevese's Butterfly Lizards,Leiolepis reevesi. Zoological Research, 2004, 25(6): 477-483.
    [10] FU Cui-zhang, RAO Ren, WU Ji-hua, CHEN Jia-kuan, LEI Guang-chun. Effects of Density and Food Availability on Growth and Cannibalism in Basin-raising Larval Salamanders (Hynobius amjiensis). Zoological Research, 2003, 24(3): 186-190.
    [11] XU Xue-feng, WU Yi-lian. Changes of Material and Energy in Eggs of Lacertid Lizards,Eremias brenchleyi During Incubation at Mount Qianshan,Anhui. Zoological Research, 2003, 24(2): 106-110.
    [12] LI Gui-Fen, MENG Shao-Quan, JIANG Shi-Ting. Connections of Rostrolateral Area of the Anterior Dorsal Ventricular Ridge in Lizard Gekko gecko. Zoological Research, 2001, 22(1): 74-77.
    [13] XU Xue-Feng, CHEN Xue-Jun, JI Xiang. Selected Body Temperature,Thermal Tolerance and Influence of Temperature on Food Assimilation and Locomotor Performance in Lacertid Lizards,Eremias brenchleyi. Zoological Research, 2001, 22(6): 443-448.
    [14] QIU Qing-Bo, MA Xiao-Mei, JI Xiang. Ontogenetic Shifts of Morphology and Food Habits in the Oriental Garden Lizard,Calotes versicolor (Agamidae). Zoological Research, 2001, 22(5): 367-374.
    [15] ZHANG Yong-Pu, JI Xiang. Ontogenetic Changes of Sexual Dimorphism in Head Size and Food Habit in Grass Lizard,Takydromus septentrionalis. Zoological Research, 2000, 21(3): 181-186.
    [16] LI Ren-de, SHENG Jian-ming. Circadian and Seasonal Variation of Blood Sugar Content of Lizard Phrynocephalus przewalskii. Zoological Research, 1999, 20(6): 477-478.
    [17] JI Xiang, XU Xue-feng, LIN Zhi-hua. Influence of Incubation Temperature on Characteristics of Dinodon rufozonatum (Reptilia:Colubridae) Hatchlings,With Comments on The Function of Residual Yolk. Zoological Research, 1999, 20(5): 342-346.
    [18] LI Ren-de, CHEN Qiang, LIU Nai-fa. Effects of Body Temperature on Electrocardiograms of Lizard Eremias multiocellata. Zoological Research, 1998, 19(4): 269-276.
    [19] LIN Zhi-hua, JI Xiang. The Effects of Thermal and Hydric Environments on Incubating Eggs and Hatchlings of The Grass Lizard,Takydromus septentrionalis. Zoological Research, 1998, 19(6): 439-445.
    [20] LI Ren-de, LIU Nai-fa. The Influence of Environmental Temperatures on Body Temperatures of Phrynocephalus przewalskii and Eremias multiocellata and Their Selectionsof Environmental Temperatures. Zoological Research, 1992, 13(1): 47-52.
  • 加载中


    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (612) PDF downloads(3210) Cited by()
    Proportional views


    DownLoad:  Full-Size Img  PowerPoint