Qiaohan HU,Yusong LIN,Xia QIU,et al.High-elevation Adaptation of Motion Visual Display Modifications in the Toad-Headed Agamid Lizards (Phrynocephalus)[J].Asian Herpetological Research(AHR),2022,13(1):53-63.[doi:10.16373/j.cnki.ahr.210049]
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High-elevation Adaptation of Motion Visual Display Modifications in the Toad-Headed Agamid Lizards (Phrynocephalus)
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Asian Herpetological Research[ISSN:2095-0357/CN:51-1735/Q]

Issue:
2022 VoI.13 No.1
Page:
53-63
Research Field:
Publishing date:
2022-03-25

Info

Title:
High-elevation Adaptation of Motion Visual Display Modifications in the Toad-Headed Agamid Lizards (Phrynocephalus)
Author(s):
Qiaohan HU12 Yusong LIN1 Xia QIU12 Jinzhong FU13 and Yin QI1*
1 Chengdu Institute of Biology, Chinese Academy of Sciences, Chengdu 610041, China
2 University of Chinese Academy of Sciences, Beijing 101400, China
3 Departments of Integrative Biology, University of Guelph, Guelph, Ontario N1G 2W1, Canada
Keywords:
high-elevation adaptation lizard motion visual display Phrynocephalus signal complexity
PACS:
-
DOI:
10.16373/j.cnki.ahr.210049
Abstract:
Understanding the process of adaptation is a key mission in modern evolutionary biology. Animals living at high elevations face challenges in energy metabolism due to several environmental constraints (e.g., oxygen supply, food availability, and movement time). Animal behavioral processes are intimately related to energy metabolism, and therefore, behavioral modifications are expected to be an important mechanism for high-elevation adaptation. We tested this behavioral adaptation hypothesis using variations of motion visual displays in toad-headed agamid lizards of the genus Phrynocephalus. We predicted that complexity of visual motion displays would decrease with the increase of elevation, because motion visual displays are energetically costly. Displays of 12 Phrynocephalus species were collected with elevations ranging from sea level to 4600 m. We quantified display complexity using the number of display components, display duration, pathways of display components, as well as display speed for each species. Association between display complexity and elevation was analyzed using the phylogenetic generalized least squares (PGLS) model. We found that both the number of display components and the average value of tail coil speed were negatively correlated with elevation, suggesting that toad-headed lizards living at high-elevation areas reduced their display complexity to cope with the environmental constraints. Our research provides direct evidence for high-elevation adaptation from a behavioral aspect and illustrates the potential impacts of environment heterogeneity on motion visual display diversification.

References:

Akinrodoye M. A., Lui F. 2021. Neuroanatomy, Somatic Nervous System. Treasure Island, USA: StatPearls Publishing
Beall C. M. 2007. Two routes to functional adaptation: Tibetan and Andean high-altitude natives. Proc Natl Acad Sci USA, 104: 8655–8660
Bennett A. F. 1978. Activity metabolism of the lower vertebrates. Annu Rev Physiol, 40: 447–469
Bennett A. F., Gleeson T. T., Gorman G. C. 1981. Anaerobic metabolism in a lizard (Anolis bonairensis) under natural conditions. Physiol Zool, 54: 237–241
Bian X., Chandler T., Pinilla A., Peters R. A. 2019. Now You See Me, Now You Don’t: Environmental conditions, signaler behavior, and receiver response thresholds interact to determine the efficacy of a movement-based animal signal. Front Ecol Evol, 7: 130
Bian X., Elgar M. A., Peters R. A. 2016. The swaying behavior of Extatosoma tiaratum: Motion camouflage in a stick insect? Behav Ecol, 27: 83–92
Biro P. A., Stamps J. A. 2010. Do consistent individual differences in metabolic rate promote consistent individual differences in behavior? Trends Ecol Evol, 25: 653–659
Cheviron Z. A., Brumfield R. T. 2012. Genomic insights into adaptation to high-altitude environments. Heredity, 108: 354–361
Clark C. J. 2012. The role of power versus energy in courtship: What is the ‘energetic cost’ of a courtship display? Anim Behav, 84: 269–277
Decourcy K. R., Jenssen T. A. 1994. Structure and use of male territorial headbob signals by the lizard Anolis carolinensis. Anim Behav, 47: 251–262
Endler J. A. 1992. Signals, signal conditions, and the direction of evolution. Am Nat, 139: S125–S153
Erecińska M., Silver I. A. 2001. Tissue oxygen tension and brain sensitivity to hypoxia. Respir Physiol, 128: 263–276
Fischer J., Wadewitz P., Hammerschmidt K. 2017. Structural variability and communicative complexity in acoustic communication. Anim Behav, 134: 229–237
Fleishman L. J., Pallus A. C. 2010. Motion perception and visual signal design in Anolis lizards. Proc Biol Sci, 277: 3547–3554
Freckleton R. P., Harvey P. H., Pagel M. 2002. Phylogenetic analysis and comparative data: A test and review of evidence. Am Nat, 160: 712–726
Freeberg T. 2006. Social complexity can drive vocal complexity: Group size and information in chickadee calls in Carolina chickadees. Psychol Sci, 17: 557–561
Freeberg T. M., Dunbar R. I. M., Ord T. J. 2012. Social complexity as a proximate and ultimate factor in communicative complexity. Philos Trans R Soc Lond B Biol Sci, 367: 1785–1801
Greenberg N., MacLean P. D. 1978. Behavior and Neurology of Lizards: An Interdisciplinary Colloquium. Maryland, USA: DHEW publication
Hao Y., Xiong Y., Cheng Y., Song G., Jia C., Qu Y., Lei F. 2019. Comparative transcriptomics of 3 high-altitude passerine birds and their low-altitude relatives. Proc Natl Acad Sci USA, 116: 11851–11856
Hedrick T. L. 2008. Software techniques for two- and three-dimensional kinematic measurements of biological and biomimetic systems. Bioinspir Biomim, 3: 1–6
Jenssen T. A. 1977. Display diversity in anoline lizards and problems of interpretation. Behavior and neurology of lizards. Am Zool, 17: 203–215
Kingsbury L., Huang S., Wang J., Gu K., Golshani P., Wu Y. E., Hong W. 2019. Correlated neural activity and encoding of behavior across brains of socially interacting animals. Cell, 178: 429–446
Kotiaho J. S., Alatalo R. V., Mappes J., Nielsen M. G., Parri S., Rivero A. 1998. Energetic costs of size and sexual signaling in a wolf spider. Proc Biol Sci, 265: 2203–2209
Laidre M. E., Johnstone R. A. 2013. Animal signals. Curr Biol, 23: 829–833
Li J. T., Gao Y. D., Xie L., Deng C., Shi P., Guan M. L., Huang S., Ren J. L., Wu D. D., Ding L., Huang Z. Y., Nie H., Humphreys D. P., Hillis D. M., Wang W. Z., Zhang Y. P. 2018. Comparative genomic investigation of high-elevation adaptation in ectothermic snakes. Proc Natl Acad Sci USA, 115: 8406–8411
Lynch M. 1991. Methods for the analysis of comparative data in evolutionary biology. Evolution, 45: 1065–1080
Mai C. L., Liao J., Zhao L., Liu S. M., Liao W. B. 2017. Brain size evolution in the frog Fejervarya limnocharis supports neither the cognitive buffer nor the expensive brain hypothesis. J Zool, 302: 63–72
Martins E. P., Labra A., Halloy M., Tolman Thompson J. 2004. Large-scale patterns of signal evolution: An interspecific study of Liolaemus lizard headbob displays. Anim Behav, 68: 453–463
McComb K., Semple S. 2005. Coevolution of vocal communication and sociality in primates. Biol Lett, 1: 381–385
Miller C. T., Osmanski M. 2008. Evolution of Communicative Flexibility–complexity, Creativity, and Adaptability in Human and Animal Communication. Cambridge, USA: The MIT Press, 368
Mowles S. L. 2014. The physiological cost of courtship: Field cricket song results in anaerobic metabolism. Anim Behav, 89: 39–43
Mu?oz M., Losos J. 2017. Thermoregulatory behavior simultaneously promotes and forestalls evolution in a tropical Lizard. Am Nat, 191: 15–26
Myers N., Mittermeier R. A., Mittermeier C. G., da Fonseca G. A. B., Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature, 403: 853–858
Nadhurou B., Gamba M., Andriaholinirina N. V., Ouledi A., Giacoma C. 2016. The vocal communication of the mongoose lemur (Eulemur mongoz): Phonation mechanisms, acoustic features and quantitative analysis. Ethol Ecol Evol, 28: 241–260
Nelson X. J., Jackson R. R. 2007. Complex display behaviour during the intraspecific interactions of myrmecomorphic jumping spiders (Araneae, Salticidae). J Nat Hist, 41: 1659–1678
Olesen S. P. 1986. Rapid increase in blood-brain barrier permeability during severe hypoxia and metabolic inhibition. Brain Res, 368: 24–29
Ord T. J., Blumstein D. T., Evans C. S. 2001. Intrasexual selection predicts the evolution of signal complexity in lizards. Proc Biol Sci, 268: 737–744
Ord T. J., Martins E. P. 2006. Tracing the origins of signal diversity in anole lizards: Phylogenetic approaches to inferring the evolution of complex behavior. Anim Behav, 71: 1411–1429
Orme D., Freckleton R., Thomas G., Petzoldt T., Fritz S., Isaac N., Pearse W. 2013. Caper: Comparative analyses of phylogenetics and evolution in R. Methods Ecol Evol, 3: 145–151
Pagel M. 1999. The maximum likelihood approach to reconstructing ancestral character states of discrete characters on phylogenies. Syst Biol, 48: 612–622
Patricelli G. L. 2016. New dimensions in animal communication: The case for complexity. Curr Opin Behav Sci, 12: 80–89
Peckre L., Kappeler P. M., Fichtel C. 2019. Clarifying and expanding the social complexity hypothesis for communicative complexity. Behav Ecol Sociobiol, 73: 11
Peters R. A., Ramos J. A., Hernandez J., Wu Y., Qi Y. 2016. Social context affects tail displays by Phrynocephalus vlangalii lizards from China. Sci Rep, 6: 31573
Petrie M., Tim H., Carolyn S. 1991. Peahens prefer peacocks with elaborate trains. Anim Behav, 41: 323–331
Qi Y., Li S. S., Suo L., Li H., Wang Y. Z. 2011. An ethogram of the toad-headed lizard Phrynocephalus vlangalii during the breeding season. Asian Herpetol Res, 2: 110–116
Qiu X., Fu J. Z., Qi Y. 2018. Tail waving speed affects territorial response in the toad-headed Agama Phrynocephalus vlangalii. Asian Herpetol Res, 9: 181–187
Qu Y. H., Chen C. H., Chen X. M., Hao Y., She H. S., Wang M. X., Ericson P. G. P., Lin H. Y., Cai T. L, Song G., Jia C. X,, Chen C. Y., Zhang H. L., Li J., Liang L. P., Wu T. Y., Zhao J. Y., Gao Q., Zhang G. J., Zhai W. W., Zhang C., Zhang Y. E., Lei F. M. 2021. The evolution of ancestral and species-specific adaptations in snow finches at the Qinghai–Tibet Plateau. Proc Natl Acad Sci USA, 118: e2012398118
Ramirez J. M., Folkow L. P., Blix A. S. 2007. Hypoxia tolerance in mammals and birds: From the wilderness to the clinic. Annu Rev Physiol, 69: 113–143
Ramos J. A., Peters R. A. 2017. Motion-based signaling in sympatric species of Australian agamid lizards. J Comp Physiol A, 203: 661–671
Refsnider J. M., Qian S. S., Streby H. M., Carter S. E., Clifton I. T., Siefker A. D., Vazquez T. K. 2018. Reciprocally transplanted lizards along an elevational gradient match light environment use of local lizards via phenotypic plasticity. Funct Ecol, 32: 1227–1236
Revell L. J. 2012. Phytools: An R package for phylogenetic comparative biology (and other things). Methods Ecol Evol, 3: 217–223
Ros A. F. H., Becker K., Oliveira R. F. 2006. Aggressive behaviour and energy metabolism in a cichlid fish, Oreochromis mossambicus. Physiol Behav, 89: 164–170
Rosenthal G. G. 2007. Spatiotemporal dimensions of visual signals in animal communication. Annu Rev Ecol Evol Syst, 38: 155–178
Shannon C. E. 1948. A mathematical theory of communication. Bell Syst. tech, 27: 379–423
Solovyeva E. N., Lebedev V. S., Dunayev E. A., Nazarov R. A., Bannikova A. A., Che J., Murphy R. W., Poyarkov N. A. 2018. Cenozoic aridization in Central Eurasia shaped diversification of toad-headed agamas (Phrynocephalus?; Agamidae, Reptilia). PeerJ, 6: e4543
Storz J. F. 2021. High-Altitude Adaptation: Mechanistic insights from integrated genomics and physiology. Mol Biol Evol, 38: 2677–2691
Storz J. F., Scott G. R., Cheviron Z. A. 2010. Phenotypic plasticity and genetic adaptation to high-altitude hypoxia in vertebrates. J Exp Biol, 213: 4125–4136
Su X. P., Liu J. J., Wang F., Wang Q. H., Zhang D., Zhu B. S., Liu D. P. 2020. Effect of temperature on agonistic behavior and energy metabolism of the swimming crab (Portunus trituberculatus). Aquac, 516: 734573
Sun B. J., Wang T. T., Pike D. A., Liang L., Du W. G. 2014. Embryonic oxygen enhances learning ability in hatchling lizards. Front Zool, 11: 21
Sun Y. B., Fu T. T., Jin J. Q., Murphy R. W., Hillis D. M., Zhang Y. P., Che J. 2018. Species groups distributed across elevational gradients reveal convergent and continuous genetic adaptation to high elevations. Proc Natl Acad Sci USA, 115: 10634–10641
Tan S., Li P., Yao Z. Y., Liu G. H., Yue B. S., Fu J. Z., Chen J. F. 2021. Metabolic cold adaptation in the Asiatic toad: Intraspecific comparison along an altitudinal gradient. J Comp Physiol B, 191: 765–776
Tang X. L., Xin Y., Wang H. H., Li W. X., Zhang Y., Liang S. W., He J. Z., Wang N. B., Ma M., Chen Q. 2013. Metabolic characteristics and response to high altitude in Phrynocephalus erythrurus (Lacertilia: Agamidae), a lizard dwell at altitudes higher than any other living lizards in the world. PLoS One, 8: e71976
Vehrencamp S. 2000. Handicap, index, and conventional signal elements of bird song. Animal Signals. In Espmark Y., Amundsen T., Rosenqvist G. (Eds.), Signaling and Signal Design in Animal Communication. Trondheim. Norway: Tapir Academic Press, 277–300
Wu Q., Dang W., Hu Y. C., Lu H. L. 2018a. Altitude influences thermal ecology and thermal sensitivity of locomotor performance in a toad-headed lizard. J Therm Biol, 71: 136–141
Wu Y. Y., Ramos J. A., Qiu X., Peters R. A., Qi Y. 2018b. Female–female aggression functions in mate defence in an Asian agamid lizard. Anim Behav, 135: 215–222
Yang W. Z., Qi Y., Bi K., Fu J. Z. 2012. Toward understanding the genetic basis of adaptation to high-elevation life in poikilothermic species: A comparative transcriptomic analysis of two ranid frogs, Rana chensinensis and R. kukunoris. BMC Genet, 13: 588
Yang W. Z., Qi Y., Fu J. Z. 2014. Exploring the genetic basis of adaptation to high elevations in reptiles: A comparative transcriptome analysis of two toad-headed agamas (genus Phrynocephalus). PLoS One, 9: e112218
Yang W. Z., Qi Y., Fu J. Z. 2016. Genetic signals of high-altitude adaptation in amphibians: A comparative transcriptome analysis. BMC Genet, 17: 1–10
Yang W. Z., Qi Y., Lu B., Qiao L., Wu Y. Y., Fu J. Z. 2017. Gene expression variations in high-altitude adaptation: A case study of the Asiatic toad (Bufo gargarizans). BMC Genet, 18: 62
Yao Z. Y., Qi Y., Yue B. S., Fu J. Z. 2020. Brain size variation along altitudinal gradients in the Asiatic Toad (Bufo gargarizans). Ecol Evol, 11: 3015–3027
Zhao Y. Y., Qi Y., WangX. N., Zhao W. 2020. Resolving the energy restriction at high altitude: Variation in the digestive system of Phrynocephalus vlangalii. Anim Biol, 70: 321–331
Zhu X. X., Qiu X., Tang X. L., Qi Y. 2021. Tail display is regulated by anaerobic metabolism in an Asian agamid lizard. Integr Zool, 16: 729–740
Zhu X., Yao Z. Y., Qi Y. 2020. Tail display intensity is restricted by food availability in an Asian Agamid lizard (Phrynocephalus vlangalii). Asian Herpetol Res, 11: 240–248

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Last Update: 2022-03-25