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History and Function of Scale Microornamentation in Lacertid Lizards

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History and Function of Scale Microornamentation in Lacertid Lizards JOURNALOFMORPHOLOGY252:145–169(2002) HistoryandFunctionofScaleMicroornamentation inLacertidLizards E.N.Arnold* NaturalHistoryMuseum,CromwellRoad,LondonSW75BD,UK ABSTRACTDifferencesinsurfacestructure(ober- mostfrequentlyinformsfromdryhabitatsorformsthat hautchen)ofbodyscalesoflacertidlizardsinvolvecell climbinvegetationawayfromtheground,situations size,shapeandsurfaceprofile,presenceorabsenceoffine wheredirtadhesionislessofaproblem.Microornamen- pitting,formofcellmargins,andtheoccurrenceoflongi- tationdifferencesinvolvingotherpartsofthebodyand tudinalridgesandpustularprojections.Phylogeneticin- othersquamategroupstendtocorroboratethisfunctional formationindicatesthattheprimitivepatterninvolved interpretation.Microornamentationfeaturescandevelop narrowstrap-shapedcells,withlowposteriorlyoverlap- onlineagesindifferentordersandappeartoactadditively pingedgesandrelativelysmoothsurfaces.Deviations inreducingshine.Insomecasesdifferentcombinations fromthisconditionproduceamoresculpturedsurfaceand maybeoptimalsolutionsinparticularenvironments,but havedevelopedmanytimes,althoughsubsequentovert lineageeffects,suchaslimitedreversibilityanddifferent reversalsareuncommon.Likevariationsinscaleshape, developmentalproclivities,mayalsobeimportantintheir differentpatternsofdorsalbodymicroornamentationap- peartoconferdifferentandconflictingperformancead- genesis.Thefinepitsoftenfoundoncellsurfacesare vantages.Theprimitivepatternmayreducefrictiondur- unconnectedwithshinereduction,astheyaresmaller inglocomotionandalsoenhancesdirtshedding,especially thanthewavelengthsofmostvisiblelight.J.Morphol. inground-dwellingformsfrommoisthabitats.However, 252:145–169,2002. ©2002Wiley-Liss,Inc. thissmoothmicroornamentationgeneratesshinethat maycompromisecrypticcoloration,especiallywhenscales KEYWORDS:Squamata;Lacertidae;scalemicroorna- arelarge.Manyderivedfeaturesshowcorrelationwith mentation,homoplasy;lineageeffects;friction;crypsis; suchlargescalesandappeartosuppressshine.Theyoccur shine;dirt-shedding Phylogeneticinformationmaypermitthehistory turesadditionaltothecell-likeenclosures.Also,the ofmorphologicalfeaturesthatvarycomplexly oberhautchenandunderlyinglayersmayallbe throughacladetobeatleastpartlyreconstructed. ruckedtoproduceridgesonthescalesurface(Har- Thehistorycanthenbeusedtoexploretheevolu- vey,1993).Theoverallstructureoffeaturesofthe tionaryoriginsofthevariation,inparticularbyen- oberhautchensurfaceandepidermalfoldingisre- ablingcorrelationsbetweentheappearanceofpar- ferredtohereasmicroornamentation(Ruibal,1968) ticulartraitsandchangesinselectiveregimetobe buthasalsobeentermedultradermatoglyphics recognized.Thisapproachisappliedheretothefine (Larsenetal.,1973),dermatoglyphics(Bursteinet surfacestructureofthescalesoflacertidlizards. al.,1974),microdermatoglyphics(Dowlingetal., Thescalesofsquamates(lizardsandsnakes)have 1972),microstructure(PerretandWuest,1983),and arigidouterepidermallayerof␤-keratin,the microarchitecture(Peterson,1984a). ␤-layer,whichisunderlainbythemesosandthen Squamatemicroornamentationiseasilystudied the␣-layers.Alltheseareformedfromcellspro- byscanningelectronmicroscopy(SEM)andthereis ducedbythelivingbasallayeroftheepidermis,the nowasubstantialliteratureonthesubject.Forin- stratumgerminativum.The␤-layeriscoveredby stance,publicationsdealingwithdorsalbodyscales theoberhautchen(theanglicizedformoftheoriginal include:Bryantetal.(1967),MonroeandMonroe GermanOberha¨utchen,recommendedbyIrishet (1967),Ruibal(1968),StewartandDaniel(1972, al.,1988).Bythetimethe␤-layerandoberhautchen 1973,1975),Bursteinetal.(1974),Coleandvan mature,coherentcellboundariesarenotapparent withinthem(Madersonetal.,1998).Thereareoften cell-likeenclosuresvisibleonthesurfaceoftheober- *Correspondenceto:Dr.E.N.Arnold,NaturalHistoryMuseum, hautchen,althoughitisnotcertainthattheseare CromwellRoad,LondonSW75BD,UnitedKingdom. alwaysderivedfromindividualcells.Thesurfaceof E-mail:[email protected] theoberhautchenfrequentlyexhibitsacomplex,mi- Publishedonline00Month0000in croscopical,three-dimensionalstructurefirstnoted WileyInterScience(www.interscience.wiley.com) byLeydig(1872,1873),whichusuallyincludesfea- DOI:10.1002/jmor.1096 ©2002WILEY-LISS,INC. 146 E.N. ARNOLD Devender (1976), Sammartano (1976), Gans and Natural History Museum, London. At least three Baic (1977), Gasc and Renous (1980), Groombridge specimens of each species were examined. (1980), Perret and Wuest (1982, 1983), Price (1982, The ␤-layer of the epidermis of individual scales 1983, 1989), Peterson (1984a,b), Peterson and Bezy was removed with forceps, washed in 80% alcohol, (1985), Renous et al. (1985), Bea (1986), Bowker et and, in a few cases where it was necessary, cleaned al. (1987), McCarthy (1987), Stille (1987), Bezy and further by brief ultravibration in chloroform. The Peterson (1988), Irish et al. (1988), Vaccaro et al. samples were then dried and mounted with Araldite (1988), Chiasson and Lowe (1989), Lang (1989), on scanning electron microscope stubs. After coating Price and Kelly (1989), Renous and Gasc (1989), with gold, the scales were examined using a Hitachi Harvey (1993), and Harvey and Gutberlet (1995). 2500 scanning electron microscope at 15 kV and at In spite of these extensive studies, no broad assess- magnifications from ϫ35 to ϫ10,000. Dorsal scales ment of the evolutionary factors that may cause the of 95 species were examined (Table 2) as well as development of different patterns of microornamenta- basal caudal scales of 20 species and belly scales of tion has been made. Although convincing functional 15. Estimates of cell size were made by measure- interpretations have been put forward in restricted ment of individual cells on micrographs of scale sur- instances (see Factors That May Cause Evolutionary faces enlarged ϫ5,000. Micrographs of the examined Change, below), microornamentation does not in gen- scales, together with the accession numbers of the eral correlate closely with known environmental pa- individual lizards from which they came, are depos- rameters (Price, 1982; Peterson, 1984a,b). Nor does it ited in the library of the Reptile and Amphibian seem to be a particularly good general indicator of section of the Natural History Museum. relationship, although it may include some phyloge- netic signal (see, for instance, Harvey and Gutberlet, Experimental Assessment of Dirt-Shedding 1995, on cordylid and gerrhosaurid lizards). Ability and Reflectivity Although microornamentation has sometimes been surveyed across whole taxonomic groups (e.g., The relative ability of different microornamenta- Peterson and Bezy, 1985; Lang, 1989; Harvey and tion patterns to shed dirt was tested by painting dry Gutberlet, 1995), sampling is often limited or the detached scales of large-scaled species of lacertids assemblage concerned is small, relatively uniform in with fine wet silt, produced by differential flotation ecology, or both. Lacertid lizards exhibit substantial of garden soil in water. This was allowed to dry and variation in microornamentation and, with some 23 the scale then subjected to controlled gentle wiping genera and 250 species spread over a wide range of with a truncated primary feather of a house sparrow environments, they provide an opportunity to ex- (Passer domesticus), the number of strokes neces- plore this variation more fully in a historical and sary to clean the scale giving some idea of its ten- functional context. As only a few published descrip- dency to retain dirt. Light scattering by microorna- tions of lacertid microornamentation are available mentation was assessed by directing a narrow (for instance, Lacerta vivipara [Bryant et al., 1967]; parallel beam of light at various angles at the exter- Lacerta viridis [Sammartano, 1976; Peterson, nal surfaces of detached scales of large-scaled lac- 1984a]; Podarcis hispanica [Bowker et al. 1987]), a ertids, which had been glued flat onto a plane sur- systematic survey was undertaken as the first stage face with Araldite, and noting the degree of of the investigation. dispersal of the reflected beam and whether coher- ent shine was produced. MATERIALS AND METHODS Areas of Body Examined Approach to Data Analysis Differences in squamate scale microornamenta- The very wide range of microornamentation en- tion occur not only between taxa but also on differ- countered in lacertids has a complex taxonomic dis- ent parts of the body of individual animals and even tribution. It is analyzed as follows. 1) Beginning on individual scales (Cole and Van Devender, 1976; with the microornamentation of the dorsal scales, Peterson, 1984b). In consequence, the survey con- variable features are identified and separated into ducted here has been restricted to specified areas of characters with two or more states; the distribution the skin. Most observations were made on the para- of the states of each character is then plotted on the vertebral mid-dorsal surface of the posterior body, phylogeny of the family. 2) The history of the indi- as this is often typical of a large area of the trunk vidual characters is assessed, including the direc- dorsum, but a smaller number involve the dorsal tail tion and stages of their evolution and the frequent base and the belly. multiple origin of derived states. 3) Possible corre- lations with features of the microornamentation of Specimens and Their Examination dorsal scales are looked for. These correlations may include other aspects of microornamentation, other Material was obtained from alcohol-preserved intrinsic aspects of the species concerned, or envi- specimens in the permanent reptile collection
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