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How do the physiological traits of a lizard change during its invasion of an oceanic island?

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Abstract

Physiology is crucial for the survival of invasive species in new environments. Yet, new climatic conditions and the limited genetic variation found within many invasive populations may influence physiological responses to new environmental conditions. Here, we studied the case of the delicate skinks (Lampropholis delicata) invading Lord Howe Island (LHI), Australia. On LHI, the climate is different from the mainland source of the skinks, and independent introduction events generated invasive populations with distinct genetic backgrounds. To understand how climate and genetic background may shape physiological responses along biological invasions, we compared the physiological traits of a source and two invasive (single-haplotype and multi-haplotype) populations of the delicate skink. For each population, we quantified physiological traits related to metabolism, sprint speed, and thermal physiology. We found that, for most physiological traits analysed, population history did not influence the ecophysiology of delicate skinks. However, invasive populations showed higher maximum speed than the source population, which indicates that locomotor performance might be a trait under selection during biological invasions. As well, the invasive population with a single haplotype was less cold-tolerant than the multi-haplotype and source populations. Our results suggest that limited genetic variability and climate may influence physiological responses of invasive organisms in novel environments. Incorporating the interplay between genetic and physiological responses into models predicting species invasions can result in more accurate understanding of the potential habitats those species can occupy.

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Fig. 1

available at Bureau of Meteorology (2021); see also Supplementary material. Populations of Lampropholis delicata have been established in LHI in the 1980s. Dashed lines represent the mean monthly maximum and minimum temperatures across the years. For more details of the historical climate for Coffs Harbour and LHI see Tables S1, S2 and S3

Fig. 2
Fig. 3
Fig. 4

source population (Coffs Harbour), invasive-multi-haplotype (central region of LHI) and invasive-single-haplotype (North Bay) invasive populations of Lampropholis delicata. The grey dots represent individual observations for each population

Fig. 5

source population (Coffs Harbour), invasive-multi-haplotype (central region of LHI) and invasive-single-haplotype (North Bay) invasive populations of Lampropholis delicata. The dots represent the average speed at each temperature, and the whiskers represent the standard deviation

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References

  • Amundsen PA, Knudsen R, Klemetsen A (2007) Intraspecific competition and density dependence of food consumption and growth in Arctic charr. J Anim Ecol 76:149–158

    Article  PubMed  Google Scholar 

  • Angilletta MJ Jr (2001) Thermal and physiological constraints on energy assimilation in a widespread lizard (Sceloporus undulatus). Ecology 82(11):3044–3056

    Article  Google Scholar 

  • Angilletta MJ Jr (2006) Estimating and comparing thermal performance curves. J Therm Biol 31(7):541–545

    Article  Google Scholar 

  • Araújo MB, Ferri-Yáñez F, Bozinovic F, Marquet PA, Valladares F, Chown SL (2013) Heat freezes niche evolution. Ecol Lett 16(9):1206–1219

    Article  PubMed  Google Scholar 

  • Autumn K, Weinstein RB, Full RJ (1994) Low cost of locomotion increases performance at low temperature in a nocturnal lizard. Physiol Zool 67(1):238–262

    Article  Google Scholar 

  • Barrett RD, Schluter D (2008) Adaptation from standing genetic variation. Trends Ecol Evol 23(1):38–44

    Article  PubMed  Google Scholar 

  • Batabyal A, Balakrishna S, Thaker M (2017) A multivariate approach to understanding shifts in escape strategies of urban lizards. Behav Ecol Sociobiol 71(5):83

    Article  Google Scholar 

  • Bates D, Mächler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. arXiv:1406.5823

  • Blouin-Demers G, Nadeau P (2005) The cost–benefit model of thermoregulation does not predict lizard thermoregulatory behavior. Ecology 86(3):560–566

    Article  Google Scholar 

  • Bureau of Metereology (2021) Climate statistics for Australian locations. Australian Government. http://www.bom.gov.au/climate/data/index.shtml

  • Cabezas-Cartes F, Kubisch EL, Ibargüengoytía NR (2014) Consequences of volcanic ash deposition on the locomotor performance of the Phymaturus spectabilis lizard from Patagonia, Argentina. J ExperZool A 321(3):164–172

    Google Scholar 

  • Chaplin K (2013) Intra-specific hybridisation of the delicate skink (Lampropholis delicata) on Lord Howe Island. Unpublished Honours Thesis, School of Biological Sciences, Monash University, Australia

  • Chapple DG, Hoskin CJ, Chapple SN, Thompson MB (2011) Phylogeographic divergence in the widespread delicate skink (Lampropholis delicata) corresponds to dry habitat barriers in eastern Australia. BMC Evol Biol 11(1):191

    Article  PubMed  PubMed Central  Google Scholar 

  • Chapple DG, Miller KA, Kraus F, Thompson MB (2013) Divergent introduction histories among invasive populations of the delicate skink (Lampropholis delicata): has the importance of genetic admixture in the success of biological invasions been overemphasized? Divers Distrib 19(2):134–146

    Article  Google Scholar 

  • Chapple DG, Miller KA, Chaplin K, Barnett L, Thompson MB, Bray RD (2014) Biology of the invasive delicate skink (Lampropholis delicata) on Lord Howe Island. Aust J Zool 62(6):498–506

    Article  Google Scholar 

  • Chejanovski ZA, Avilés-Rodríguez KJ, Lapiedra O, Preisser EL, Kolbe JJ (2017) An experimental evaluation of foraging decisions in urban and natural forest populations of Anolis lizards. Urban Ecosyst 20(5):1011–1018

    Article  Google Scholar 

  • Chevin LM, Lande R, Mace GM (2010) Adaptation, plasticity, and extinction in a changing environment: towards a predictive theory. PLoS Biol 8(4):e1000357

    Article  PubMed  PubMed Central  Google Scholar 

  • Christiansen JS, Sparboe M, Sæther BS, Siikavuopio SI (2015) Thermal behaviour and the prospect spread of an invasive benthic top predator onto the Euro-Arctic shelves. Divers Distrib 21(9):1004–1013

    Article  Google Scholar 

  • Clusella-Trullas S, Chown SL (2014) Lizard thermal trait variation at multiple scales: a review. J Comp Physiol B 184(1):5–21

    Article  PubMed  Google Scholar 

  • Cromie GL, Chapple DG (2012) Impact of tail loss on the behaviour and locomotor performance of two sympatric Lampropholis skink species. PLoS ONE 7(4):e34732

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • De Meester G, Lambreghts Y, Briesen B, Smeuninx T, Tadić Z, Van Damme R (2018) Hunt or hide: how insularity and urbanization affect foraging decisions in lizards. Ethology 124(4):227–235

    Article  Google Scholar 

  • Dlugosch KM, Parker IM (2008) Founding events in species invasions: genetic variation, adaptive evolution, and the role of multiple introductions. Mol Ecol 17(1):431–449

    Article  CAS  PubMed  Google Scholar 

  • Dowd WW, King FA, Denny MW (2015) Thermal variation, thermal extremes and the physiological performance of individuals. J Exp Biol 218(12):1956–1967

    Article  PubMed  Google Scholar 

  • Feltz CJ, Miller GE (1996) An asymptotic test for the equality of coefficients of variation from k populations. Stat Med 15(6):647–658

    Article  Google Scholar 

  • Frankham R (2005) Resolving the genetic paradox in invasive species. Heredity 94(4):385–385

    Article  CAS  PubMed  Google Scholar 

  • Fraser S, Grigg GC (1984) Control of thermal conductance is insignificant to thermoregulation in small reptiles. Physiol Zool 57(4):392–400

    Article  Google Scholar 

  • Garland T Jr, Hankins E, Huey RB (1990) Locomotor capacity and social dominance in male lizards. Funct Ecol 4:243–250

    Article  Google Scholar 

  • Goulet CT, Thompson MB, Chapple DG (2017) Repeatability and correlation of physiological traits: do ectotherms have a “thermal type”? Ecol Evol 7(2):710–719

    Article  PubMed  Google Scholar 

  • Gvoždík L (2012) Plasticity of preferred body temperatures as means of coping with climate change? Biol Let 8(2):262–265

    Article  Google Scholar 

  • Gunderson AR, Stillman JH (2015) Plasticity in thermal tolerance has limited potential to buffer ectotherms from global warming. Proc R Soc B 282(1808):20150401

    Article  PubMed  PubMed Central  Google Scholar 

  • Hanski I, Gyllenberg M (1993) Two general metapopulation models and the core-satellite species hypothesis. Am Nat 142(1):17–41

    Article  Google Scholar 

  • Hermisson J, Pennings PS (2005) Soft sweeps: molecular population genetics of adaptation from standing genetic variation. Genetics 169(4):2335–2352

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hochachka PW, Somero GN (2002) Biochemical adaptation. Oxford University Press, Oxford

    Google Scholar 

  • Hoffmann AA, Chown SL, Clusella-Trullas S (2013) Upper thermal limits in terrestrial ectotherms: how constrained are they? Funct Ecol 27(4):934–949

    Article  Google Scholar 

  • Hothorn T, Bretz F, Westfall P, Heiberger RM, Schuetzenmeister A, Scheibe S, Hothorn MT (2016) Package ‘multcomp’. Simultaneous inference in general parametric models. Project for Statistical Computing, Vienna, Austria

  • Huey RB, Stevenson RD (1979) Integrating thermal physiology and ecology of ectotherms: a discussion of approaches. Am Zool 19(1):357–366

    Article  Google Scholar 

  • Hulme PE (2009) Trade, transport and trouble: managing invasive species pathways in an era of globalization. J Appl Ecol 46(1):10–18

    Article  Google Scholar 

  • Hutchinson MN, Thompson MB, Stewart JR (2005) Lampropholis delicata (Delicate skink, rainbow skink) Introduction. Herpetological Review 36:450–451

    Google Scholar 

  • Itescu Y, Schwarz R, Meiri S, Pafilis P (2017) Intraspecific competition, not predation, drives lizard tail loss on islands. J Anim Ecol 86(1):66–74

    Article  PubMed  Google Scholar 

  • Johnson RN, Starks PT (2004) A surprising level of genetic diversity in an invasive wasp: Polistes dominulus in the northeastern United States. Ann Entomol Soc Am 97(4):732–737

    Article  Google Scholar 

  • Kearney M, Shine R, Porter WP (2009) The potential for behavioral thermoregulation to buffer “cold-blooded” animals against climate warming. Proc Natl Acad Sci 106(10):3835–3840

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kellermann V, Overgaard J, Hoffmann AA, Fløjgaard C, Svenning JC, Loeschcke V (2012) Upper thermal limits of Drosophila are linked to species distributions and strongly constrained phylogenetically. Proc Natl Acad Sci 109(40):16228–16233

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kelley AL (2014) The role thermal physiology plays in species invasion. Conserv Physiol 2(1):cou045

    Article  PubMed  PubMed Central  Google Scholar 

  • Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2004) Genetic variation increases during biological invasion by a Cuban lizard. Nature 431(7005):177–181

    Article  CAS  PubMed  Google Scholar 

  • Kolbe JJ, Glor RE, Schettino LR, Lara AC, Larson A, Losos JB (2007) Multiple sources, admixture, and genetic variation in introduced Anolis lizard populations. Conserv Biol 21(6):1612–1625

    Article  PubMed  Google Scholar 

  • Lavergne S, Molofsky J (2007) Increased genetic variation and evolutionary potential drive the success of an invasive grass. Proc Natl Acad Sci 104(10):3883–3888

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Leal M, Gunderson AR (2012) Rapid change in the thermal tolerance of a tropical lizard. Am Nat 180(6):815–822

    Article  PubMed  Google Scholar 

  • Lee CE (2002) Evolutionary genetics of invasive species. Trends Ecol Evol 17(8):386–391

    Article  Google Scholar 

  • Lennox R, Choi K, Harrison PM, Paterson JE, Peat TB, Ward TD, Cooke SJ (2015) Improving science-based invasive species management with physiological knowledge, concepts, and tools. Biol Invasions 17(8):2213–2227

    Article  Google Scholar 

  • Lighton JRB (2008) Measuring metabolic rates: a manual for scientists. Oxford University Press, New York

    Book  Google Scholar 

  • Litmer AR, Murray CM (2019) Critical thermal tolerance of invasion: comparative niche breadth of two invasive lizards. J Thermal Biol 86:102432

    Article  Google Scholar 

  • Llewelyn J, Phillips BL, Alford RA, Schwarzkopf L, Shine R (2010) Locomotor performance in an invasive species: cane toads from the invasion front have greater endurance, but not speed, compared to conspecifics from a long-colonised area. Oecologia 162(2):343–348

    Article  PubMed  Google Scholar 

  • Lockwood BL, Somero GN (2011) Invasive and native blue mussels (genus Mytilus) on the California coast: the role of physiology in a biological invasion. J Exp Mar Biol Ecol 400(1–2):167–174

    Article  Google Scholar 

  • Lockwood JL, Hoopes MF, Marchetti MP (2013) Invasion ecology. Blackwell Publishing, Oxford

    Google Scholar 

  • Logan ML, Duryea MC, Molnar OR, Kessler BJ, Calsbeek R (2016) Spatial variation in climate mediates gene flow across an island archipelago. Evolution 70(10):2395–2403

    Article  PubMed  Google Scholar 

  • Logan ML, Neel LK, Nicholson DJ, Stokes AJ, Miller CL, Chung AK, Cox CL (2021) Sex-specific microhabitat use is associated with sex-biased thermal physiology in Anolis lizards. J Exp Biol 224(2):jeb235697

    PubMed  Google Scholar 

  • Marwick B, Krishnamoorthy K (2018) cvequality: tests for the equality of coefficients of variation from multiple groups. R software package version 0.1, p 3

  • McCann S, Greenlees MJ, Newell D, Shine R (2014) Rapid acclimation to cold allows the cane toad to invade montane areas within its Australian range. Funct Ecol 28(5):1166–1174

    Article  Google Scholar 

  • Merritt L, Matthews PG, White CR (2013) Performance correlates of resting metabolic rate in garden skinks Lampropholis delicata. J Comp Physiol B 183(5):663–673

    Article  PubMed  Google Scholar 

  • Michelangeli M, Goulet CT, Kang HS, Wong BB, Chapple DG (2018) Integrating thermal physiology within a syndrome: locomotion, personality and habitat selection in an ectotherm. Funct Ecol 32(4):970–981

    Article  Google Scholar 

  • Miller KA, Duran A, Melville J, Thompson MB, Chapple DG (2017) Sex-specific shifts in morphology and colour pattern polymorphism during range expansion of an invasive lizard. J Biogeogr 44(12):2778–2788

    Article  Google Scholar 

  • Mittan CS, Zamudio KR (2019) Rapid adaptation to cold in the invasive cane toad Rhinella marina. Conserv Physiol 7(1):75

    Article  Google Scholar 

  • Moule H, Chaplin K, Bray RD, Miller KA, Thompson MB, Chapple DG (2015) A matter of time: temporal variation in the introduction history and population genetic structuring of an invasive lizard. Curr Zool 61(3):456–464

    Article  Google Scholar 

  • Muñoz MM, Bodensteiner BL (2019) Janzen’s hypothesis meets the Bogert effect: connecting climate variation, thermoregulatory behavior, and rates of physiological evolution. Integr Org Biol 1(1):oby002

    Article  PubMed  PubMed Central  Google Scholar 

  • Muñoz MM, Losos JB (2018) Thermoregulatory behavior simultaneously promotes and forestalls evolution in a tropical lizard. Am Nat 191(1):E15–E26

    Article  PubMed  Google Scholar 

  • Nei M (2005) Selectionism and neutralism in molecular evolution. Mol Biol Evol 22(12):2318–2342

    Article  CAS  PubMed  Google Scholar 

  • Orr HA, Unckless RL (2008) Population extinction and the genetics of adaptation. Am Nat 172(2):160–169

    Article  PubMed  Google Scholar 

  • Overgaard J, Andersen JL, Findsen A, Pedersen PB, Hansen K, Ozolina K, Wang T (2012) Aerobic scope and cardiovascular oxygen transport is not compromised at high temperatures in the toad Rhinella marina. J Exp Biol 215(20):3519–3526

    CAS  PubMed  Google Scholar 

  • Padfield D, O’Sullivan H (2020) rTPC: an R package for helping fit thermal performance curves. R package version 0.1.0.

  • Phillips BL, Llewelyn J, Hatcher A, Macdonald S, Moritz C (2014) Do evolutionary constraints on thermal performance manifest at different organizational scales? J Evol Biol 27(12):2687–2694

    Article  CAS  PubMed  Google Scholar 

  • Prentis PJ, Pavasovic A (2013) Understanding the genetic basis of invasiveness. Mol Ecol 22(9):2366–2368

    Article  CAS  PubMed  Google Scholar 

  • Prosser C, Hudson S, Thompson MB (2006) Effects of urbanization on behavior, performance, and morphology of the garden skink, Lampropholis guichenoti. J Herpetol 40(2):151–159

    Article  Google Scholar 

  • Sagonas K, Valakos ED, Pafilis P (2013) The impact of insularity on the thermoregulation of a Mediterranean lizard. J Therm Biol 38(8):480–486

    Article  Google Scholar 

  • Seebacher F, Franklin CE (2011) Physiology of invasion: cane toads are constrained by thermal effects on physiological mechanisms that support locomotor performance. J Exp Biol 214(9):1437–1444

    Article  PubMed  Google Scholar 

  • Seebacher F, White CR, Franklin CE (2015) Physiological plasticity increases resilience of ectothermic animals to climate change. Nat Clim Chang 5(1):61–66

    Article  Google Scholar 

  • Sinervo B (1990) Evolution of thermal physiology and growth rate between populations of the western fence lizard (Sceloporus occidentalis). Oecologia 83(2):228–237

    Article  CAS  PubMed  Google Scholar 

  • Somero GN (2010) The physiology of climate change: how potentials for acclimatization and genetic adaptation will determine ‘winners’ and ‘losers.’ J Exp Biol 213(6):912–920

    Article  CAS  Google Scholar 

  • Somero GN (2012) The physiology of global change: linking patterns to mechanisms. Ann Rev Mar Sci 4:39–61

    Article  PubMed  Google Scholar 

  • Stroud JT, Colom M, Ferrer P, Palermo N, Vargas V, Cavallini M, Jones I (2019) Behavioral shifts with urbanization may facilitate biological invasion of a widespread lizard. Urban Ecosyst 22(3):425–434

    Article  Google Scholar 

  • Tingley R, Thompson MB, Hartley S, Chapple DG (2016) Patterns of niche filling and expansion across the invaded ranges of an Australian lizard. Ecography 39(3):270–280

    Article  Google Scholar 

  • van Heerwaarden B, Malmberg M, Sgrò CM (2016) Increases in the evolutionary potential of upper thermal limits under warmer temperatures in two rainforest Drosophila species. Evolution 70(2):456–464

    Article  PubMed  Google Scholar 

  • Walsh S, Goulet CT, Wong BB, Chapple DG (2018) Inherent behavioural traits enable a widespread lizard to cope with urban life. J Zool 306(3):189–196

    Article  Google Scholar 

  • Wilson S, Swan G (2021) A complete guide to reptiles of Australia. New Holland, Australia

    Google Scholar 

  • Winchell KM, Maayan I, Fredette JR, Revell LJ (2018) Linking locomotor performance to morphological shifts in urban lizards. Proc R Soc B 285(1880):20180229

    Article  PubMed  PubMed Central  Google Scholar 

  • Withers PC (2001) Design, calibration and calculation for flow-through respirometry systems. Aust J Zool 49(4):445–461

    Article  Google Scholar 

  • Žagar A, Carretero MA, Marguč D, Simčič T, Vrezec A (2018) A metabolic syndrome in terrestrial ectotherms with different elevational and distribution patterns. Ecography 41(10):1728–1739

    Article  Google Scholar 

  • Zedrosser A, Dahle B, Swenson JE (2006) Population density and food conditions determine adult female body size in brown bears. J Mammal 87(3):510–518

    Article  Google Scholar 

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Acknowledgements

We thank three anonymous reviewers, and the handling editor, for their insightful comments.

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Contributions

DGC, CTG and AY conceived and designed the experiments; AN conducted the fieldwork; AY performed the experiments; AY, CTG and ROA performed the analyses; ROA and AY wrote the first version of the manuscript. All authors contributed to and approved the final version. ROA and AY contributed equally to the manuscript.

Corresponding author

Correspondence to Rodolfo O. Anderson.

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Human/Animal rights

All animal experiments were approved by the Animal Ethics Committee—School of Biological Sciences, Monash University, reference number 16736. All patients included in this study gave consent to participate in this research and to publish the data contained within this article. All the data used in this study are provided in the manuscript; the data can also be found in Bridges data repository (https://doi.org/10.26180/16864024).

Additional information

Communicated by Donald Miles.

Our study examines how climate and intraspecific genetic variation may influence the physiological traits of an invasive species.

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Young, A., Anderson, R.O., Naimo, A. et al. How do the physiological traits of a lizard change during its invasion of an oceanic island?. Oecologia 198, 567–578 (2022). https://doi.org/10.1007/s00442-021-05054-y

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