Does nocturnal activity prolong gecko longevity?

In: Israel Journal of Ecology and Evolution

The majority of lizard clades are ancestrally and predominantly diurnal. The only major taxon in which most species are nocturnal is the Gekkota (geckos and pygopodids). As ectothermic thermoregulators, lizard metabolic rates are highly temperature dependent, and diurnal lizards therefore demonstrate higher metabolic rates than nocturnal ones. Furthermore, exposure to solar radiation is thought to reduce ectothermic longevity by increasing both metabolic costs and the rate of accumulating harmful mutations through UV radiation (UVC specifically). In being nocturnal, ectothermic species may reduce their intrinsic mortality rates and thus live longer. To test this hypothesis, we collected literature data on the maximum longevities of 740 lizard species, of which 185 are geckos. We examined whether geckos live longer than other lizards, and whether activity time affects gecko longevity. While geckos live relatively long for lizards of their size, their activity time was found to be unrelated to longevity, contradicting our predictions. We suggest that diurnal species may have evolved higher resistance to UV radiation via thicker, more keratinized skin. Elevated metabolic rates do not automatically equate with faster aging. Mortality through extrinsic causes (e.g., predation) may impose much stronger selective pressures than intrinsic causes.

  • Addo-Bediako A. Chown S. L. , & Gaston K. J. (2002). Metabolic cold adaptation in insects: a large-scale perspective. Funct. Ecol.16, pp. 332338.

    • Search Google Scholar
    • Export Citation
  • Adkins E. Driggers T. Ferguson G. Gehrmann W. Gyimesi Z. May E. , … & Klaphake E. (2003). Ultraviolet light and reptiles, amphibians. J. Herpetol. Med. Surg.13, pp. 2737.

    • Search Google Scholar
    • Export Citation
  • Atanasov A. T. (2005). The linear allometric relationship between total metabolic energy per life span and body mass of poikilothermic animals. Biosystems82, pp. 137142.

    • Search Google Scholar
    • Export Citation
  • Autumn K. , & De Nardo D. F. (1995). Behavioral thermoregulation increases growth rate in a nocturnal lizard. J. Herpetol.29, pp. 157162.

    • Search Google Scholar
    • Export Citation
  • Autumn K. (1999). Secondarily diurnal geckos return to cost of locomotion typical of diurnal lizards. Physiol. Biochem. Zool.72, pp. 339351.

    • Search Google Scholar
    • Export Citation
  • Autumn K. Weinstein R. B. , & Full R. J. (1994). Low cost of locomotion increases performance at low temperature in a nocturnal lizard. Physiol. Zool.67, pp. 238262.

    • Search Google Scholar
    • Export Citation
  • Autumn K. Jindrich D. DeNardo D. , & Mueller R. (1999). Locomotor performance at low temperature and the evolution of nocturnality in geckos. Evolution53, pp. 580599.

    • Search Google Scholar
    • Export Citation
  • Bauer A. (2007). The foraging biology of the Gekkota: Life in the middle. In Reilly S. McBrayer L. , & Miles D. (Eds.), Ecology Lizard (pp. 371404). Cambridge: Cambridge University Press 10.1017/CBO9780511752438.014

    • Search Google Scholar
    • Export Citation
  • Bauwens D. , & Diaz-Uriarte R. (1997). Covariation of life-history traits in lacertid lizards: a comparative study. Am. Nat.149, pp. 91111.

    • Search Google Scholar
    • Export Citation
  • Benjamin D. J. Berger J. O. Johannesson M. Nosek B. A. Wagenmakers E. J. Berk R et al. (2018). Redefine statistical significance. Nat. Hum. Behav.2, pp. 610.

    • Search Google Scholar
    • Export Citation
  • Boulenger G. A. (1885). Catalogue of the Lizards in the British Museum (Nat. Hist.) I. Geckonidae, Eublepharidae, Uroplatidae, Pygopodidae, Agamidae. London: Trustees of the British Museum.

    • Search Google Scholar
    • Export Citation
  • Breusch T. S. , & Pagan A. R. (1979). A simple test for heteroscedasticity and random coefficient variation. Econometrica47, pp. 12871294.

    • Search Google Scholar
    • Export Citation
  • Carey J. R. (2003). Longevity: the biology and demography of life span. Princeton University Press. USA.

  • Caswell H. (2007). Extrinsic mortality and the evolution of senescence. Trends Ecol. Evol.22, pp. 173174.

  • Doughty P. (1997). The effects of “fixed” clutch sizes on lizard life-histories: reproduction in the Australian velvet gecko, Oedura lesueurii . J. Herpetol.31, pp. 266272.

    • Search Google Scholar
    • Export Citation
  • Emerling C. A. Huynh H. T. Nguyen M. A. Meredith R. W. , & Springer M. S. (2015). Spectral shifts of mammalian ultraviolet-sensitive pigments (short wavelength-sensitive opsin 1) are associated with eye length and photic niche evolution. Proc. Biol. Sci.282, pp. 20151817.

    • Search Google Scholar
    • Export Citation
  • Faruki S. I. Das D. R. , & Khatun S. (2005). Effects of UV-radiation on the larvae of the lesser mealworm, Alphitobius diaperinus (Panzer)(Coleoptera: Tenebrionidae) and their progeny. Pak. J. Biol. Sci.5, pp. 444448.

    • Search Google Scholar
    • Export Citation
  • Feldman A. Sabath N. Pyron R. A. Mayrose I. , & Meiri S. (2016). Body sizes and diversification rates of lizards, snakes, amphisbaenians and the tuatara. Glob. Ecol. Biogeogr.25, pp. 187197.

    • Search Google Scholar
    • Export Citation
  • Ferguson G. W. Brinker A. M. Gehrmann W. H. Bucklin S. E. Baines F. M. , & Mackin S. J. (2010). Voluntary exposure of some western-hemisphere snake and lizard species to Ultraviolet-B radiation in the field: how much Ultraviolet-B should a lizard or snake receive in captivity? Zoo Biol.29, pp. 317334.

    • Search Google Scholar
    • Export Citation
  • Francis A. A. Lee W. H. , & Regan J. D. (1981). The relationship of DNA excision repair of ultraviolet-induced lesions to the maximum life span of mammals. Mech. Ageing Dev.16, pp. 181189.

    • Search Google Scholar
    • Export Citation
  • Freckleton R. P. Harvey P. H. , & Pagel M. (2002). Phylogenetic analysis and comparative data: a test and review of evidence. Am. Nat., 160, pp. 712726.

    • Search Google Scholar
    • Export Citation
  • Gamble T. Greenbaum E. Jackman T. R. , & Bauer A. M. (2015). Into the light: diurnality has evolved multiple times in geckos. Biol. J. Linn. Soc.115, pp. 896910.

    • Search Google Scholar
    • Export Citation
  • Garrick D. (2008). Body surface temperature and length in relation to the thermal biology of lizards. Biosci. Horizons1, pp. 136142.

    • Search Google Scholar
    • Export Citation
  • Ghanem I. , & Shamma M. (2007). Effect of non-ionizing radiation (UVC) on the development of Trogoderma granarium Everts. J. Stored Prod.43, pp. 362366.

    • Search Google Scholar
    • Export Citation
  • Häder D. P. (2001). Adaptation to UV stress in algae. In Algal adaptation to environmental stresses (pp. 173202). SpringerBerlin, Heidelberg.

    • Export Citation
  • Hamilton W. D. (1966). The moulding of senescence by natural selection. J. Theor. Biol.12, pp. 1245.

  • Hare K. M. Pledger S. Thompson M. B. Miller J. H. , & Daugherty C. H. (2010). Nocturnal lizards from a cool-temperate environment have high metabolic rates at low temperatures. J. Comp. Physiol. B180, pp. 11731181.

    • Search Google Scholar
    • Export Citation
  • Hare K. M. , & Cree A. (2016). Thermal and metabolic physiology of New Zealand lizards. In New Zealand Lizards (pp. 239267). SpringerCham.

    • Search Google Scholar
    • Export Citation
  • Hart R. W. Setlow R. B. , & Woodhead A. D. (1977). Evidence that pyrimidine dimers in DNA can give rise to tumors. Proc. Natl. Acad. Sci. U.S.A.74, pp. 55745578.

    • Search Google Scholar
    • Export Citation
  • Healy K. Guillerme T. Finlay S. Kane A. Kelly S.B.A. McClean D. et al. (2014). Ecology and mode-of-life explain lifespan variation in birds and mammals. Proc. R. Soc. Lond., B, Biol. Sci.281, pp. 20140298.

    • Search Google Scholar
    • Export Citation
  • Heidari N. Sedaratian-Jahromi A. , & Ghane-Jahromi M. (2016). Possible effects of Ultraviolet ray (UV-C) on biological traits of Callosobruchus maculatus (Col.: Chrysomelidae). J. Stored Prod.69, pp. 9198.

    • Search Google Scholar
    • Export Citation
  • Henderson R.W. & Powell R. (2009). Natural History of West Indian Reptiles and Amphibians. University Press of FloridaGainesville, Florida, U.S.A. 495 pp.

    • Search Google Scholar
    • Export Citation
  • Holmes D. J. , & Austad S. N. (1994). Fly now, die later: life-history correlates of gliding and flying in mammals. J. Mammal.75, pp. 224226.

    • Search Google Scholar
    • Export Citation
  • Hori M. Shibuya K. Sato M. , & Saito Y. (2014). Lethal effects of short-wavelength visible light on insects. Sci. Rep.4, pp. 7383.

    • Search Google Scholar
    • Export Citation
  • Huey R. B. Niewiarowski P. H. J. Kaufmann, Herron J. & C. (1989). Thermal biology of nocturnal ectotherms: is sprint performance of geckos maximal at low body temperatures? Physiol. Zool. 62, pp. 488504.

    • Search Google Scholar
    • Export Citation
  • Jablonski N. G. , & Chaplin G. (2010). Human skin pigmentation as an adaptation to UV radiation. Proc. Natl. Acad. Sci. U.S.A.107, pp. 89628968.

    • Search Google Scholar
    • Export Citation
  • Kapahi P. Chen D. Rogers A. N. Katewa S. D. Li P. W. L. Thomas E. L. , & Kockel L. (2010). With TOR, less is more: a key role for the conserved nutrient-sensing TOR pathway in aging. Cell Metab.11, pp. 453465.

    • Search Google Scholar
    • Export Citation
  • Kearney M. , & Predavec M. (2000). Do nocturnal ectotherms thermoregulate? A study of the temperate gecko Christinus marmoratus . Ecology81, pp. 29842996.

    • Search Google Scholar
    • Export Citation
  • Kirkwood T. B. (1977). Evolution of ageing. Nature270, pp. 301304.

  • Kirkwood T. B. , & Austad S. N. (2000). Why do we age? Nature408, pp. 233238.

  • Ku H. H. Brunk U. T. , & Sohal R. S. (1993). Relationship between mitochondrial superoxide and hydrogen peroxide production and longevity of mammalian species. Free Radic. Biol. Med.15, pp. 621627.

    • Search Google Scholar
    • Export Citation
  • Lah E. F. C. Musa R. N. A. R. , & Ming H. T. (2012). Effect of germicidal UV-C light (254 nm) on eggs and adult of house dustmites, Dermatophagoides pteronyssinus and Dermatophagoides farinae (Astigmata: Pyroglyhidae). Asian. Pac. J. Trop. Biomed.2, pp. 679683.

    • Search Google Scholar
    • Export Citation
  • Ley R. D. (1985). Photoreactivation of UV-induced pyrimidine dimers and erythema in the marsupial Monodelphis domestica . Proc. Natl. Acad. Sci. U.S.A.82, pp. 24092411.

    • Search Google Scholar
    • Export Citation
  • Magalhães J. P. D. Costa J. , & Church G. M. (2007). An analysis of the relationship between metabolism, developmental schedules, and longevity using phylogenetic independent contrasts. J. Gerontol. A Biol. Sci. Med. Sci.62, pp. 149160.

    • Search Google Scholar
    • Export Citation
  • Medawar P. B. (1952). An unsolved problem of biology (pp. 24). London: H. K. Lewis.

  • Meiri S. (2007). Size evolution in island lizards. Glob. Ecol. Biogeogr.16, pp. 702708.

  • Meiri S. (2010). Length–weight allometries in lizards. J. Zool.281, pp. 218226.

  • Meiri S. (2018) Traits of lizards of the world: variation around a successful evolutionary design. Glob. Ecol. Biogeogr.27, pp. 11681172.

    • Search Google Scholar
    • Export Citation
  • Meiri S. (2020). What geckos are – an ecological-biogeographic perspective. Isr. J. Ecol. Evol.

  • Møller A. P. (2008). Relative longevity and field metabolic rate in birds. J. Evol.21, pp. 13791386.

  • Norris A.L. Kunz T.H. , (2012). Effects of solar radiation on animal thermoregulation. In: Babatunde E.B. (Ed.), Solar Radiation. InTechCroatia, pp. 195220.

    • Search Google Scholar
    • Export Citation
  • O’brien, R. M. (2007). A caution regarding rules of thumb for variance inflation factors. Qual. Quant.41, pp. 673690.

  • Orme D. (2013). The caper package: comparative analysis of Phylogenetics and evolution in R. R package version5, pp. 136.

  • Pagel M. (1999). Inferring the historical patterns of biological evolution. Nature401, pp. 877.

  • Paul N. D. , & Gwynn-Jones D. (2003). Ecological roles of solar UV radiation: towards an integrated approach. Trends Ecol. Evol.18, pp. 4855.

    • Search Google Scholar
    • Export Citation
  • Pianka E. R. , & Huey R. B. (1978). Comparative ecology, resource utilization and niche segregation among gekkonid lizards in the southern Kalahari. Copeia1978, pp. 691701.

    • Search Google Scholar
    • Export Citation
  • Pinto B. J. Nielsen S. V. and Gamble T. (2019). Transcriptomic data support a nocturnal bottleneck in the ancestor to gecko lizards. Mol. Phylogenetics Evol. 141, pp. 106639.

    • Search Google Scholar
    • Export Citation
  • Promislow D. E. , & Harvey P. H. (1990). Living fast and dying young: A comparative analysis of life‐history variation among mammals. J. Zool.220, pp. 417437.

    • Search Google Scholar
    • Export Citation
  • Rastogi R. P. Kumar A. Tyagi M. B. , & Sinha R. P. (2010). Molecular mechanisms of ultraviolet radiation-induced DNA damage and repair. J. Nucleic Acids, 2010, pp. 32.

    • Search Google Scholar
    • Export Citation
  • Röll B. (2001). Multiple origin of diurnality in geckos: evidence from eye lens crystallins. Naturwissenschaften88, pp. 293296.

  • Roos J. C. , & Vincent W. F. (1998). Temperature dependence of UV radiation effects on Antarctic cyanobacteria. J. Phycol.34, pp. 118125.

    • Search Google Scholar
    • Export Citation
  • Scharf I. Feldman A. Novosolov M. Pincheira-Donoso D. Das I. Böhm M. Uetz P. Torres‐Carvajal O. Bauer A. Roll U. and Meiri S. , (2015). Late bloomers and baby boomers: ecological drivers of longevity in squamates and the tuatara. Glob. Ecol. Biogeogr.24, pp. 396405.

    • Search Google Scholar
    • Export Citation
  • Schott R. K. Bhattacharyya N. and Chang B. S. W. (2019). Evolutionary signatures of photoreceptor transmutation in geckos reveal potential adaptation and convergence with snakes. Evolution 73, pp. 19581971.

    • Search Google Scholar
    • Export Citation
  • Singaravelan N. Grishkan I. Beharav A. Wakamatsu K. Ito S. , & Nevo E. (2008). Adaptive melanin response of the soil fungus Aspergillus niger to UV radiation stress at “Evolution Canyon”, Mount Carmel, Israel. PloS one3, pp. e2993.

    • Search Google Scholar
    • Export Citation
  • Sinha R. P. & Häder D.-P . (2002). UV-induced DNA damage and repair: a review. Photochem. Photobiol. Sci. 2002, pp. 225236.

  • Snell K. R. Kokubun T. Griffiths H. Convey P. Hodgson D. A. , & Newsham K. K. (2009). Quantifying the metabolic cost to an Antarctic liverwort of responding to an abrupt increase in UVB radiation exposure. Glob. Change Biol.15, pp. 25632573.

    • Search Google Scholar
    • Export Citation
  • Sohal R. S. (1986). The rate of living theory: a contemporary interpretation. In Insect aging (pp. 2344). SpringerBerlin, Heidelberg.

    • Search Google Scholar
    • Export Citation
  • Sohal R. S. Svensson I. Sohal B. H. , & Brunk U. T. (1989). Superoxide anion radical production in different animal species. Mech. Ageing Dev.49, pp. 129135.

    • Search Google Scholar
    • Export Citation
  • Southworth L. O. Holick M. F. Chen T. C. , & Kunz T. H. (2013). Effects of sunlight on behavior and 25-hydroxyvitamin D levels in two species of Old-World fruit bats. Dermatoendocrinology5, pp. 192198.

    • Search Google Scholar
    • Export Citation
  • Speakman J. R. (2005). Body size, energy metabolism and lifespan. J. Exp. Biol.208, pp. 17171730.

  • Stapp P. (1994). Can predation explain life-history strategies in mammalian gliders?. J. Mammal.75, pp. 227228.

  • Stark G. , & Meiri S. , (2018). Cold and dark captivity: Drivers of amphibian longevity. Glob. Ecol. Biogeogr.27, pp. 13841397.

  • Stark G. Karin T. Itescu Y. Feldman A. Meiri S. , (2018). Cold and isolated ectotherms: drivers of reptilian longevity. Biol. J. Linn. Soc.125, pp. 730740.

    • Search Google Scholar
    • Export Citation
  • Tattersall I. (1987). Cathemeral activity in primates: a definition. Folia Primatol.49, pp. 200202.

  • Tidière M. Gaillard J. M. Berger V. Müller D. W. Lackey L. B. Gimenez O. , … & Lemaître J. F. (2016). Comparative analyses of longevity and senescence reveal variable survival benefits of living in zoos across mammals. Sci. Rep.6, pp. 36361.

    • Search Google Scholar
    • Export Citation
  • Tonini J. F. R. Beard K. H. Ferreira R. B. Jetz W. , & Pyron R. A. (2016). Fully-sampled phylogenies of squamates reveal evolutionary patterns in threat status. Biol. Conserv.204, pp. 2331.

    • Search Google Scholar
    • Export Citation
  • Uetz P. Freed P. & Hošek J. (eds.) (2019). The Reptile Databasehttp://www.reptile-database.org, accessed [16/07/2019].

  • Valcu M. Dale J. Griesser M. Nakagawa S. , & Kempenaers B. (2014). Global gradients of avian longevity support the classic evolutionary theory of ageing. Ecography37, pp. 930938.

    • Search Google Scholar
    • Export Citation
  • Vidan E. Roll U. Bauer A. Grismer L. Guo P. Maza E. Novosolov M. Sindaco R. Wagner P. Belmaker J. & Meiri S. , (2017). The Eurasian hot nightlife: Environmental forces associated with nocturnality in lizards. Glob. Ecol. Biogeogr.26, pp. 13161325.

    • Search Google Scholar
    • Export Citation
  • Wassmann M. Moeller R. Reitz G. , & Rettberg P. (2010). Adaptation of Bacillus subtilis cells to Archean-like UV climate: relevant hints of microbial evolution to remarkably increased radiation resistance. Astrobiology10, pp. 605615.

    • Search Google Scholar
    • Export Citation
  • Webb J. K. Pike D. A. , & Shine R. (2009). Olfactory recognition of predators by nocturnal lizards: safety outweighs thermal benefits. Behav. Ecol.21, pp. 7277.

    • Search Google Scholar
    • Export Citation
  • Werner Y. L. , & Seifan T. (2006). Eye size in geckos: asymmetry, allometry, sexual dimorphism, and behavioural correlates. J. Morphol.267, pp. 14861500.

    • Search Google Scholar
    • Export Citation
  • Williams G. C. (1957). Pleiotropy, natural selection and the evolution of senescence. Evolution11, pp. 398411.

  • Williams P. D. , & Day T. (2003). Antagonistic pleiotropy, mortality source interactions, and the evolutionary theory of senescence. Evolution57, pp. 14781488.

    • Search Google Scholar
    • Export Citation
  • Williams P. D. Day T. Fletcher Q. , & Rowe L. (2006). The shaping of senescence in the wild. Trends Ecol. Evol.21, pp. 458463.

    • Search Google Scholar
    • Export Citation
  • Wright A. F. Jacobson S. G. Cideciyan A. V. Roman A. J. Shu X. Vlachantoni D. , … & Riemersma R. A. (2004). Lifespan and mitochondrial control of neurodegeneration. Nat. Genet.36, pp. 11531158.

    • Search Google Scholar
    • Export Citation
  • Zhang C. Y. Meng J. Y. Wang X. P. Zhu F. & Lei C. L. (2011). Effects of UV-A exposures on longevity and reproduction in Helicoverpa armigera and on the development of its F1 generation. Insect Sci. 18, pp. 697702.

    • Search Google Scholar
    • Export Citation
  • Zheng Y. , & Wiens J. J. (2016). Combining phylogenomic and supermatrix approaches, and a time-calibrated phylogeny for squamate reptiles (lizards and snakes) based on 52 genes and 4162 species. Mol. Phylogenet. Evol.94, pp. 537547.

    • Search Google Scholar
    • Export Citation

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