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Sexual dimorphism in Carinatogecko heteropholis (Minton,
Anderson, and Anderson, 1970) (Sauria: Gekkonidae) from
Mam Province, western Iran
1 BEHZAD FATHINIA, 'NASRULLAH RASTEGAR-POUYANI, AND 2HOSSEIN MOHAMADI
'DepartmentofBiology, FacultyofScience,RaziUniversity,Kermanshah,IRAN 2HeadofNaturalHistoryMuseumsandGeneticResources, De-
partmentofEnvironmentalProtectionOrganization, Tehran,IRAN
—
Abstract. Sexual dimorphism is a widespread phenomenon in animals, but so far undocumented
in Carinatogeckoheteropholis. Inthisstudy,52specimenswerecollected in Karezan, Ham province,
western Iran. The uni- and multivariate analyses performed on the morphological data revealed
that females are larger than males. All of the sexual differences were female-biased, except for the
infralabial scales.
Keywords. Carinatogeckoheteropholis sexualdimorphism, statisticalanalysis,morphology, IlamProvince,Iran
,
Citation:Fathinia,B., Rastegar-Pouyani,N.,andMohamadi,H.2011.Sexualdimorphismin Carinatogeckoheteropholis(Minton,Anderson,andAnder-
son, 1970)(Sauria:Gekkonidae)from IlamProvince,westernIran.Amphib. ReptileConserv.5(1):47-53(e27).
Introduction
Thegenus Carinatogecko Golubev and Szczerbak, 1981 food resource partitioning and sexual differences in en-
comprises three species, the Iranian keel-scaled gecko, ergyallocationtogrowth(Bairdetal. 2003).
the Iraqi keel-scaled gecko, andAnderson’s keel-scaled To ourknowledge this is the first survey on the oc-
gecko; allofthemarefoundontheIranianPlateau (Szc- currence of sexual dimorphism in the genus Carinato-
zerbak and Golubev 1996;Anderson 1999; Torki 2011). gecko. Clarifyingthe sexuallydistinctivetraitsin C. het-
TheIraqikeel-scaledgecko, Carinatogeckoheteropholis eropholis is ofevolutionary and systematic importance;
(Minton, Anderson, andAnderson 1970) is a small spe- inthispaper, wereportresults ofsucha study.
cies; its type locality in Iran is western Zagros foothills
(Anderson 1999; Fathinia 2007; Rastegar-Pouyani et al.
2007). It is hypothesized that the genus Carinatogecko Material and methods
has a double Iranian-Mesopotamian origin (Fathinia
A
2007). total of52 (28c? and 24$) adult specimens were col-
Sexual dimorphism (SD) is a common and wide- lected during summer 2010. All ofthem were collected
spread phenomenon in the animal world (Andersson byhandwiththeaidofanelectrictorchatnightonrocky
1994). Sexual size dimorphism (SSD) explains the sta- mountain sides of the Zagros Mountains in Karezan,
tus in which the males and females differ in measured Shirvan-Chardavol, Ilam Province, western Iran (Fig.
values of certain morphological characteristics. Sexual 1). Ofthese, 22 specimens were fixed in ethanol 75%
RUZM
size dimorphism (SSD) has been extensively described anddepositedinthe (RaziUniversityZoological
in reptiles (Andersson 1994; Kuo 2009). Sexual dimor- Museum) forfuture studies, andtherest (30 specimens)
phism in animals is revealed in three different aspects: werereleasedintheirrelevanthabitat24hours aftercol-
behavior, size, and shape (Selander 1972). Numerous lecting and analyzing. The coordinates ofthe study site
m
surveys have been earned out on sexual dimorphism in are33°44'N,46°29'El325 a.s.l.Eightmetricandfour
lizards(Stamps 1983;Rocha 1996;Carothers 1984;Triv- meristic variables were chosen and measured by digital
mm
ers 1976;Molina-Borja2003;Bairdetal.2003;Verrastro caliperandstereomicroscopetothenearest0.01 (Ta-
2004; Bruneretal. 2005; Kaliontzopoulouetal. 2007). ble 1). Exceptforoverall shapedifferenceswhichcanbe
Differences in the selective forces acting on male used to distinguish males from females (Fig. 2), sex of
versus female body size are the main causes of sex dif- specimens was mainly determinedbased onpresence of
ferences in adultbody size ofanimals (Cox 2006). Sex- two swellingsatthebaseoftailjustbehindventinmales
ualdimorphisminlizardsmayresultfromdifferencesin andtheirabsenceinfemales (Fig. 3).
Correspondence. 3Email:[email protected]
Amphib. ReptileConserv. | amphibian-reptile-conservation.org 047 November2011 I Volume5 I Number 1 I e27
Fathinia et al.
Figure 1. Mapshowing the coordinates ofthe studysite in Karezan region at mountainsides oftheZagros.
To determinethe significance ofsexualdimorphism themetricandmeristiccharactersaswellasthedirection
in C. heteropholis, theANOVATable as well as Princi- ofdifferences and the significant characters (P < 0.05)
palComponentAnalysis (PCA: correlationmatrix) were are summarizedinTable2.
used. The SPSS statistical software (version 13) was
usedforcarryingoutthe statisticalanalyses.
ANOVATableAnalysis
Results Metricvariables: obviousdifferencesinthevalueofvari-
ables areobservedbetweenthe sexes. Femaleshave sig-
Twelve morphological characters (eight metric and four nificantly greater values than the males for eight metric
meristic) were included in the analysis. The values for characters. In the case ofbody length and the distance
Amphib. ReptileConserv. | amphibian-reptile-conservation.org 048 November2011 I Volume5 I Number 1 I e27
Sexual dimorphism in Carinatogecko heteropholis
Figure2. Dorsal viewof male (left) and female (right) of Carinatogeckoheteropholis.
Figure 3. Presence of swelling in the male of C. heteropholisat base ofthe tail which accommodate hemipenes (left)
and theirabsence in female (right).
Amphib. ReptileConserv. | amphibian-reptile-conservation.org 049 November2011 I Volume5 I Number 1 I e27
Fathinia et al.
0.10) thanmales (3.34 +0.04) (P< 0.05).Allthemetric
variables are femalebiased. Reasons forpresence offe-
male biased sexual size dimorphism in the species are
takenupinthediscussion section.
Meristic variables: Significant differences were not
observedinmeristic variables, but SL(8.20 + 0.12), CT
(12.16+0.24),andCD(7.45+0.17)infemalesarelarger
•• ****** than SL (8.07 + 0.10), CT (11.96 + 0.21), and CD (7.32
*
+0.14) inmales. Inotherwords, thethreecharacters are
4 •* . . * . not significantly female biased. Only one out oftwelve
variables (i.e., number ofinfralabials, IL) was male bi-
ased, which inturnwas insignificant. Thevalue ofILin
males (6.85 ± 0.09) was insignificantly greaterthanthat
infemales (6.79 +0.13) (P<0.05).
-2-06000 -1,00000 Q.DD0D0 1.00000 2.00000 300000
Factor1
Principal ComponentAnalysis
Figure4. Ordination ofthe individual males and females
of Carinatogecko heteropholis on the first two principal The PCA performed on the dataset yielded three axes,
components. Note the relative degree of isolation be- which collectively explained 73.38% ofthe total varia-
tSwVeL,enTLm,alHLe,sHaWn,d LfFeLm,alLeHsL,,wFhHiLc,h aisndmaViLnliyntahtetrPibCuItedantdo tion. The PCI explains 50.788% ofthe total variation.
SLand ILin the PC2. Inspectionoftheloadingsindicatesthatcorrelationswith
all morphological measurements have the same sign
betweenforelimb-hindlimb(i.e.,SVLandFHL,respec- (positive)butnotthesamemagnitude(Table3). Thefirst
tively) females had values of36.34 + 0.63 and 18.02 + axisisaclearindicatorofbody size.Allmetricvariables
0.41 and males had 32.53 + 0.33 and 15.41 + 0.20 (P in the first axis have greater values than meristic ones,
< 0.05). Regarding the differences in extremities (fore- hence making a greater contribution in sexual discrimi-
limb, hindlimb, andtail) betweenfemales andmales we nation. The scores of the females along this axis show
observedthatfemales hadvalues of 12.96 + 0.22, 17.46 anoverlapwiththoseformales, indicatingthatalthough
+ 0.30, and 39.11 + 0.80 and males had values of 11.86 sexual dimorphism occurs between males and females,
+ 0.10, 15.95 + 0.19, and 36.74 + 0.68 for LFL, LHL, the two sexes are not completely separated from each
andTLrespectively. Headdimensions also show signifi- otherregardingthesecharacters(Fig.4).Thesecondaxis,
cant differences between the sexes. Females had values whichcontains 12.51%ofthetotalvariationisameristic
of 8.94 + 0.13 and 6.99 + 0.10 and males had 8.51 + axisthatrecordsindividualsatoneendwithlargeSLand
0.08 and6.65 +0.07forHL(headlength) andHW(head IL and relatively small SVL compared with individuals
width), respectively. Regarding the lastmetric character withsmallSLandILandrelativelylargeSVL.Thethird
(i.e.,VLorventlength),werealizedthatthischaracteris axis contains only 10.08% ofthetotalvariation, being a
significantlydifferentbetweenfemalesandmales,sothat meristic axis that records individuals with large CT and
females have significantlygreatervalues forVL (3.58 ± CD and relatively small VL at one end, compared with
individuals at the other end with small CT and CD and
relativelyhighvaluesforVL.
Table 1. The metric and meristic characters used in this
study. Discussion
Characters Definition
Carinatogeckoheteropholispresentedmarkedsexualdi-
SVL snouttoventlength morphism in general body size and several body parts,
TL lengthoftail with females being significantly larger than males in
o HL head length
£ HW headwidth eightoutof12 studiedcharacters.
2V LFL lengthofforelimb The evolutionary result of selection acting differ-
LHL lengthofhindlimb ently onbody size andtherest ofmale andfemaletraits
FHL forelimbto hindlimblength issexualsizedimorphism(SSD)(Andersson 1994).Both
VL thegreatesthorizontal length ofvent
theproximate (growthpatterns) andultimate (evolution-
o SL numberofsupralabialscales ary payoffs) causes are responsible for sexual dimor-
w IL numberofinfralabial scales phism (Stamps 1993; Cox et al. 2003; Kuo et al. 2009).
<D CCTD nnuummbbeerrooffccrhoesvsrboanrssoonndtohrestuaiml Regarding size dimorphism, the proximate cause is an
agent which creates intersexual differences in growth
rate. Among these proximate causes, two are mention-
Amphib. ReptileConserv. | amphibian-reptile-conservation.org 050 November2011 I Volume5 I Number 1 I e27
Sexual dimorphism in Carinatogecko heteropholis
Table2.Comparisonof 12morphologicalcharactersin malesandfemalesof Carinatogeckoheteropholis. SE:standard
error, D of d: Direction of difference. All measurements in millimeter (mm). Abbreviations: SVL (snout-vent length), TL
(length of tail), HL (head length), HW (head width), LFL (length of forelimb), LHL (length of hindlimb), FHL (forelimb-
hindlimb length), VL(thegreatest horizontal length ofvent), SL(numberofsupralabial scales), IL(numberof infralabial
scales), CT(numberofcrossbars on thetail), and CD (numberofchevrons on dorsum).
SEX SVL TL HL HW LFL LHL FHL VL SL IL CT CD
Mean 32.53 36.74 8.51 6.65 11.86 15.95 15.41 3.34 8.07 6.85 11.96 7.32
N 28 21 28 28 28 28 28 28 28 28 28 28
SEM 0.33 0.68 0.08 0.07 0.10 0.19 0.20 0.04 0.10 0.09 0.21 0.14
Mean 36.34 39.11 8.94 6.99 12.96 17.46 18.02 3.58 8.20 6.79 12.16 7.45
$ N 24 24 24 24 24 24 24 24 24 24 24 24
SEM 0.63 0.80 0.13 0.10 0.22 0.30 0.41 0.10 0.12 0.13 0.24 0.17
D.ofd. F>M F>M F>M F>M F>M F>M F>M F>M F>M M>F F>M F>M
P-value 0.000 0.027 0.008 0.009 0.000 0.000 0.000 0.030 0.386 0.691 0.530 0.542
able: differences in growthhormone concentrations and probablythatis why SSDinectothermsispredominant-
trade-offs in allocating energy between growth and re- ly female-biased (Trivers 1972). The SVL (snout-vent
production (John-Adler et al. 2007; Kuo et al. 2009). length) and FHL (forelimb to hindlimb length) in fe-
Presence ofdimorphismbetweenmales andfemales are males ofC. heteropholis aregreaterthanthoseinmales.
definedbythreemainforcesincluding: sexual,fecundity, In other words, the two characters, SVL and FHL, are
andnaturalselection(Olssonetal.2002;Coxetal.2003; female-biased which can be the result of fecundity se-
Kaliontzopoulouetal. 2007). lection in the species. Alarger abdominal volume is an
Ectotherms grow continuously throughout life and ultimate cause which is selectedinfemales because this
they show a tendency to produce abundant, varying feature enhances fecundity (Monnet and Cherry 2002,
numbers ofprogeny, which results in a vigorous corre- Tague2005; Kuoetal. 2009).
lation between fecundity and body size offemales, and Head sizein avariety oflizardsis male-biased (e.g.
Verrastro 2004; Smith and Nickel 2002; Vial and Stew-
art 1989;AndersonandVitt 1990; CastillaandBauwens
Table 3. Loadings from a Principal Component Analysis 1991; Mouton and van Wyk 1993; Vitt and Colli 1994;
of metric and meristic characters of Carinatogecko het-
eropholis. Variables loading strongly on each principal Barbadillo et al. 1995; Hews 1996; Smith et al. 1997;
cleonmgtpho)n,eTnLt (alreengitnhboofldt.ailA),bbHrLevi(ahteiaodnsl:enSgtVhL),(HsnWout(-hveeandt cSahsienseoeft HalL. 1(9h9e8a;dKlreantgotchh)vfalndanHdWFr(yhnetaad2w0i0d2t)h.)IinntCh.e
width), LFL (length offorelimb), LHL (length of hindlimb), heteropholis females have significantly greater values
,
FHL (forelimb-hindlimb length), VL (the greatest horizon- thanmales.Asreportedforothervertebrates, aphenom-
tal length of vent), SL (number of supralabial scales), IL enon which can support niche divergence hypothesis is
(number of infralabial scales), CT (number of crossbars dimorphism in head size (Selander 1972; Shine 1989).
on thetail), and CD (numberofchevrons on dorsum). Reproductive role hypothesis is a hypothesis that ex-
Variable PCI PC2 PC3 plains differences in head size. Females have a greater
SVL 0.958 -0.133 -0.054 contribution inreproduction (Darwin 1871) and alarger
head should maximize energy intake. This ideamay ex-
TL 0.791 0.061 0.003
plain the presence oflarger heads in females of C. het-
HL 0.884 -0.057 -0.042
eropholis.
HW
0.848 -0.087 -0.032 Further, in C. heteropholis, the volumes of LFL
LFL 0.907 -0.055 -0.031 (lengthofforelimb) andLHL(lengthofhindlimb) infe-
LHL 0.911 -0.073 -0.028 males are significantly greater than in males. Sexually
FHL 0.833 -0.066 -0.007 size-adapteddimorphismintraitssuchashead,limb,and
VL 0.756 0.254 -0.195 tail measurements are assigned to an artifact ofthe ac-
ceptance ofSVLfor scaling tobody size (Kratochvflet.
SL 0.147 0.784 -0.064
al. 2003). Moreover, we suggestthatlongerand stronger
IL 0.102 0.851 0.077 limbs are necessary to support greater distancebetween
CT 0.286 -0.156 0.748 forelimb and hindlimb (i.e., greater FHL) either in fe-
CD 0.140 0.174 0.771 malesorinmales.
Eigenvalue 6.095 1.502 1.210 Ourresults show thatin the case ofC. heteropholis
%Variance 50.788 12.513 10.085 the VL (vent length) in females is significantly greater
than in males. During mating, females with alargerVL
Cumulative 50.788 63.301 73.386
Amphib. ReptileConserv. | amphibian-reptile-conservation.org 051 November2011 I Volume5 I Number1 I e27
)
Fathinia et al.
are chosen by males. According to Andersson (1994), size dimorphism in lizards. Evolution 57(7):1653-
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Tehran University, for his assistance in the statistical Kaliontzopoulou, A., Carretero, M. A., andLlorente, G.
analysis and Rasoul Karamiani (M.Sc. student), Depart- A. 2007. Multivariate and geometric morphometries
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Shine, R. 1989. Ecological causes for the evolution of his B.A. and M.S. from
sexual dimorphism: a review of the evidence. The Isfahan and Lorestan
QuarterlyReviewofBiology64(4):419-431. universities, respectively.
His M.S. reaserch fo-
Shine, R., Keogh, S., Doughty, P., and Giragossyan,
cused on “The Biosyste-
H. 1998. Costs ofreproduction and the evolution of
matic Studyof Lizards of
sexual dimorphism in a ‘flying lizard’ Draco mela- llam Province.” At pres-
nopogon (Agamidae). Journal ofZoology (London) ent, he is a Ph.D. stu-
246(2):203-213. dent at Razi University,
Smith, G. R., Lemos-Espinal, J. A., and Ballinger, R. Kermanshah, western
E. 1997. Sexual dimorphism intwo species ofknob- Iran under supervision
scaledlizards (genusXenosaurus fromMexico.Her- of Nasrullah Rastegar-
)
Pouyani, MozafarSharif
petologica53:200-205. i,
and Eskandar Rastegar-
Smith, G. R. and Nickle, A. M. 2002. Sexual dimor-
Pouyani. His disserta-
phism in three Cuban species of curly-tailed lizards
tion research involves
(Leiocephalus). Caribbean Journal ofScience 38(1- ecology, phylogeography, molecular systematics, and
2):140-142. population genetics ofthe Iranian viper Pseudocerastes
Stamps,J.A. 1983. Sexual selection, sexualdimorphism urarachnoides in western Iran. He is also interested in
andterritorialityinlizards, p.169-204 inHuey, R. B., other reptiles, especiallysnakes.
Pianka, E. R., and Schoener, T. W. (editors). Lizard
Ecology: studies on a modelorganism. HarvardUni- Nasrullah Rastegar-
versity, Cambridge,Massachusetts. 512p. Pouyani earned his
Stamps, J. A. 1993. Sexual size dimorphism in species B.S. in Zoology from
with asymptotic growth after maturity. Biological Razi University Ker-
JournaloftheLinneanSociety50(2):123-145. manshah, Iran in
Tague, R. G. 2005. Big-bodied males help us recognize 1986 and his M.S. in
Zoology from Tehran
that females have big pelves. American Journal of
University, Tehran,
PhysicalAnthropology 127(4):392-405.
Iran in 1991, where
Torki,F. 2011.DescriptionofanewspeciesofCarinato- he studied herpetolo-
gecko (Squamata: Gekkonidae) from Iran. Salaman- gywiththeagamidsasthecentral object. Hestarted his
dra47(2):103-111. Ph.D. in Gothenburg University, Sweden in 1994 under
Trivers, R. L. 1972. Parental investment and sexual se- the advisement of Professor Goran Nilson and gradu-
lection, p. 136-179 in Campbell, B. G. (editor). Sex- ated in 1999, working on taxonomy and biogeography
ualSelectionandtheDescentofMan, theDarwinian of Iranian Plateau agamids with Trapelus as the main
Pivot.HeinemannEducationalBooks,London. 388p. object. His research interests includetaxonomyand bio-
Trivers,R.L. 1976. Sexualselectionandresource-accru- geography of the Iranian Plateau, the Middle East and
CentralAsian herpetofauna.
ingabilitiesinAnolisgarmani.Evolution30:253-269.
Verrastro, L. 2004. Sexual dimorphism in Liolae-
mus occipitalis (Iguania, Tropiduridae). Iherin- Hussein Mohamadi is
gia. Serie Zoologia 94(l):45-48. [Online]. ^B ttohrey HMeuasdeuomfsNaantudragleneHtiisc-
Available:http://www.scielo.br/scielo.php?pid=S0073-
resources, Environmental
47212004000100007&script=sci_arttext [Accessed: J Protection Organization,
14 October2011]. Tehran, Iran. He earned
Vial,L.J. andStewart,J.R. 1989.Themanifestationand his B.A. and M.S. degrees
significanceofsexualdimorphisminanguidlizards: a from the Natural Resource
casestudyofBarisiamonticola. CanadianJournalof College of Tehran Univer-
Zoology67(l):68-72. sity. His M.S. thesis was
Vitt,L.J. andColli, G.R. 1994. Geographicalecologyof I “The Ecological study of
aNeotropicallizard:Ameivaameiva (Teiidae)inBra- I the marsh Crocodile, Croc-
odyluspalustris, in Baluch-
zil. CanadianJournalofZoology72(11):1986-2008. jstan Heisnowcontinuing
his study as a Ph.D. student in environmental science,
branch of science and research at IslamicAzad Univer-
Manuscriptreceived: 21 January2011 sity. The subject of his Ph.D. thesis is “The assessment
Accepted:05September2011 ofchangingtrendsand modeling ofhabitatpreference in
Published: 05November2011 yellow Persian deer, Dama damamesopotamica.”
Amphib. ReptileConserv. | amphibian-reptile-conservation.org 053 November2011 I Volume5 I Number 1 I e27
