\documentclass[10pt]{article}

\usepackage{fullpage}
\usepackage{setspace}
\usepackage{parskip}
\usepackage{titlesec}
\usepackage[section]{placeins}
\usepackage{xcolor}
\usepackage{breakcites}
\usepackage{lineno}
\usepackage{hyphenat}





\PassOptionsToPackage{hyphens}{url}
\usepackage[colorlinks = true,
            linkcolor = blue,
            urlcolor  = blue,
            citecolor = blue,
            anchorcolor = blue]{hyperref}
\usepackage{etoolbox}
\makeatletter
\patchcmd\@combinedblfloats{\box\@outputbox}{\unvbox\@outputbox}{}{%
  \errmessage{\noexpand\@combinedblfloats could not be patched}%
}%
\makeatother


\usepackage{natbib}




\renewenvironment{abstract}
  {{\bfseries\noindent{\abstractname}\par\nobreak}\footnotesize}
  {\bigskip}

\titlespacing{\section}{0pt}{*3}{*1}
\titlespacing{\subsection}{0pt}{*2}{*0.5}
\titlespacing{\subsubsection}{0pt}{*1.5}{0pt}


\usepackage{authblk}


\usepackage{graphicx}
\usepackage[space]{grffile}
\usepackage{latexsym}
\usepackage{textcomp}
\usepackage{longtable}
\usepackage{tabulary}
\usepackage{booktabs,array,multirow}
\usepackage{amsfonts,amsmath,amssymb}
\providecommand\citet{\cite}
\providecommand\citep{\cite}
\providecommand\citealt{\cite}
% You can conditionalize code for latexml or normal latex using this.
\newif\iflatexml\latexmlfalse
\providecommand{\tightlist}{\setlength{\itemsep}{0pt}\setlength{\parskip}{0pt}}%

\AtBeginDocument{\DeclareGraphicsExtensions{.pdf,.PDF,.eps,.EPS,.png,.PNG,.tif,.TIF,.jpg,.JPG,.jpeg,.JPEG}}

\usepackage[utf8]{inputenc}
\usepackage[T2A]{fontenc}
\usepackage[ngerman,polish,english]{babel}



\usepackage{float}








\begin{document}

\title{Sexual dimorphism in morphology and bite force in the mountain dragon,
Diploderma batangense (Squamata: Anguidae), from the Hengduan Mountains
in western China}



\author[1]{Ling Li}%
\author[2]{Gang Wang}%
\author[3]{Yuhao Wen}%
\author[3]{Yihua Xiang}%
\author[3]{Peng Guo}%
\author[1]{Bingjun Dong}%
\author[4]{Yayong Wu}%
\affil[1]{Shenyang Normal University}%
\affil[2]{Chengdu Normal University}%
\affil[3]{Yibin University}%
\affil[4]{Chengdu Institute of Biology}%


\vspace{-1em}



  
  \date{June 14, 2024}


\begingroup
\let\center\flushleft
\let\endcenter\endflushleft
\maketitle
\endgroup





\selectlanguage{english}
\begin{abstract}
Lizards exhibit sexual dimorphism in various phenotypic traits and
capability performance (e.g. bite force), while the patterns of sexual
dimorphism vary among genera and species. The relationship between
morphology and function is dynamic, and selective pressures can
differentially affect bite performance in different sexes. Here, we
analyzed sexual dimorphism in morphological traits and bite force and
explored the determinants of bite force in the mountain dragon
(Diploderma batangense) from western China. A total of 135 individuals
were collected, and nine morphological characteristics and bite force
were measured. We found a significant male bias in morphology and bite
force performance, with males found to be larger than females in regard
to head size, body size, limb length, tail length and bite force, which
could be explained by sexual selection. Results also showed that bite
force was positively correlated with head size, with the determinant
affecting bite force differing between males( mouth length) and females(
head width), which may be related to their different roles in
reproduction. This study provides a reference for understanding the
ecological adaptability of mountain dragons in the field and lays a
foundation for revealing the mechanism of bite force variation between
the sexes.%
\end{abstract}%



\sloppy


\textbf{Sexual dimorphism in morphology and bite forceinthe mountain
dragon,}Diploderma\emph{batangense} \textbf{(Squamata: Anguidae), from}
\textbf{the Hengduan Mountains in western China}

Ling Li\textsuperscript{1,2}, Gang Wang\textsuperscript{3}, Yuhao
Wen\textsuperscript{2}, Yihua Xiang\textsuperscript{2}, Peng
Guo\textsuperscript{2}, Bingjun Dong\textsuperscript{1}, Yayong
Wu\textsuperscript{2}

\begin{enumerate}
\tightlist
\item
  College of Life Sciences, Shenyang Normal University, Shenyang,
  Liaoning 110034, China
\item
  Faculty of Agriculture, Forest and Food Engineering, Yibin University,
  Yibin, Sichuan 644000, China
\item
  College of Chemistry and Life Sciences, Chengdu Normal University,
  Chengdu, Sichuan 611130, China
\end{enumerate}

Correspondence

Bingjun Dong, College of Life Sciences, Shenyang Normal University,
Shenyang, Liaoning 110034, China. Yayong Wu, Faculty of Agriculture,
Forest and Food Engineering, Yibin University, Yibin, Sichuan 644000,
China.

Email:\emph{dongbingjun@synu.edu.cn}(DBJ);
\emph{cdwyy201101@163.com}(WYY)

\textbf{Abstract:} Lizards exhibit sexual dimorphism in various
phenotypic traits and capability performance (e.g. bite force), while
the patterns of sexual dimorphism vary among genera and species. The
relationship between morphology and function is dynamic, and selective
pressures can differentially affect bite performance in different sexes.
Here, we analyzed sexual dimorphism in morphological traits and bite
force and explored the determinants of bite force in the mountain dragon
(\emph{Diploderma batangense} ) from western China. A total of 135
individuals were collected, and nine morphological characteristics and
bite force were measured. We found a significant male bias in morphology
and bite force performance, with males found to be larger than females
in regard to head size, body size, limb length, tail length and bite
force, which could be explained by sexual selection. Results also showed
that bite force was positively correlated with head size, with the
determinant affecting bite force differing between males (mouth length)
and females (head width), which may be related to their different roles
in reproduction. This study provides a reference for understanding the
ecological adaptability of mountain dragons in the field and lays a
foundation for revealing the mechanism of bite force variation between
the sexes.

\textbf{Keywords:} Bite force; Lizards; Sexual dimorphism; Morphology;
Sexual selection

\textbf{Introduction}

Sexual dimorphism, including differences in size, color, and capability
performance between the two sexes of a species, is widespread in
amphibians (Sch\selectlanguage{ngerman}äuble, 2004), reptiles (Zhong et al., 2017), mammals
(Mitani et al., 1996), birds (Fairbairn \& Shine, 1993), and
invertebrates (Jozet-Alves et al., 2008). Three main hypotheses have
been proposed to explain the evolution of sexual dimorphism in animals
(Cruz-Elizalde et al., 2021). The first proposes that male-biased sexual
dimorphism can be explained by sexual selection, in which larger males
gain greater advantages in resource allocation, territorial defense, and
mate choice (Endler \& Houde, 1995; Cruz-Elizalde et al., 2021). In
contrast, the female-biased fecundity advantage hypothesis suggests that
larger females are selectively favored by natural selection and tend to
produce larger litter clutches/size or egg production/offspring size
(Cox et al., 2003; Pincheira\selectlanguage{english}-Donoso \& Hunt, 2017; Cruz\selectlanguage{english}-Elizalde et al.,
2021). The third hypothesis of intraspecific niche divergence proposed
by Rand (1967) and Schoener (1967) suggests that differential use of one
or several resources (e.g., food, microhabitats, and territory) can
reduce male-female competition when resources were limited (Bolnick \&
Doebeli, 2003; Pincheira\selectlanguage{english}-Donoso et al., 2018). Sexual dimorphism in
morphological traits and performance is prominent in many lizard
species, which can be explained by the above hypotheses (Cruz-Elizalde
et al., 2020, 2021). Indeed, sexual selection, fecundity advantage, and
niche divergence are not mutually exclusive and may have combined
effects on body size and other sexually dimorphic characteristics (Ji et
al., 2006; Dashevsky et al., 2013; Zhu et al., 2022). In general, males
are larger in body size (e.g., body length and mass) but smaller in
reproductive-related characteristics (e.g., body cavity) than females
(Olsson et al., 2002). Consequently, it can be difficult to determine
the causes of sexual dimorphism associated with each hypothesis (Cox et
al., 2003; Kuo, 2009).

In reptiles, bite force is a comprehensive measure of performance across
multiple ecological and behavioral activities, including resource
allocation, territorial defense, aggressive interactions, and mate
acquisition (Huyghe et al., 2005; Kaliontzopoulou et al., 2012; Naretto
et al., 2022). In general, adults with a greater bite force are more
likely to win intrasexual contests (Wegener et al., 2019; Taverne et
al., 2020). Furthermore, during copulation, male lizards often bite the
abdomen or neck of the female to restrict movement or escape, thereby
increasing their mating success rate (Noble \& Bradley, 1933; Herrel et
al., 1996; Herrel et al., 2010). In most reptile species, males tend to
exhibit larger biting capacity than females (Herrel et al., 2007;
Sagonas et al., 2014; Naretto et al., 2022). For example, male Achala
copper lizards (\emph{Pristidactylus achalensis} ) demonstrate stronger
bite force than females, including lateral and frontal bites (Naretto et
al., 2022). Furthermore, in species showing no differences in body size
between males and females, head size may still exhibit dimorphism due to
the intrinsic differences in energy requirements between males and
females, leading to dimorphism in bite force (McBrayer \& Anderson,
2007). In this context, females may evolve specific physical structures
(e.g., feeding structure) to enhance energy acquisition under selective
pressure (Bulte et al., 2008). For example, female northern map turtles
(\emph{Graptemys geographica} ) can consume larger snails and access
more food resources than males due to their stronger biting capacity
(Bulte et al., 2008).

Investigating the association between sexual dimorphism in morphology
and bite force has been a topic of research in reptiles for many years.
Notably, several studies have reported that head morphology directly
affects bite force (Herrel et al., 2007; Sagonas et al., 2014; Naretto
et al., 2022) and differences in head size generate different functional
consequences (McBrayer \& Anderson, 2007). In general, taller and wider
heads are associated with larger bite force, resulting in species, age,
and sex differences (Taverne et al., 2020). As such, differences in bite
performance between males and females are expected due to sexual
dimorphism in head size, which is common in lizards (Herrel et al.,
2007). However, the best predictors of bite force tend to differ between
the sexes due to differences in bite use (e.g., intrasexual competition,
intersexual interactions, and diet) (Herrel et al., 2007; Naretto et
al., 2022). For example, the traits that best predict bite force differ
between male and female tuatara (\emph{Sphenodon punctatus} ), which is
likely due to sexual selection (Herrel et al., 2010). Variation in bite
force between the sexes is often caused by differences in overall size,
especially variation in bite force driven by specific head traits (e.g.,
head width and depth) (Lappin et al., 2006; McBrayer \& Anderson, 2007).
Despite the assumption that observed differences in head size lead to
parallel differences in bite force, which are dependent on the bones and
muscles of the head, the relationship between head size and bite force
remains unclear (Herrel et al., 2007; Huyghe et al., 2009). Differences
in jaw muscle architecture and physiology, including skeletal lever
system, pennation angle, muscle arrangement, and relative size, may
result in differences in bite force (Herrel et al., 2007; Fabre et al.,
2014). Consequently, exploring the link between bite force and
morphology in sexual dimorphism may help to disentangle the potential
mechanisms related to the evolution of sexual dimorphism
(Kaliontzopoulou et al., 2012). A significant association between
morphology and bite force in sexually dimorphic species may provide
empirical evidence for the co-evolution of both traits and may point to
the joint effect of selection on form and function.

In the current study, we explored sexual dimorphism in morphological
traits and bite force in\emph{Diplodermabatangense} , an oviparous
lizard species endemic to small areas of brush habitat along the upper
Jinsha River near Batang County, Sichuan Province, China (Wang et al.,
2021). The species has been listed as a ``National Protected Key Wild
Animal'' in China since 2021, primarily due to anthropogenic disturbance
and habitat loss caused by hydropower and road construction, resulting
in fewer thermoregulatory sites. At present, little is known about the
biology and ecology of \emph{D. batangense} , thereby limiting
species-specific management strategies. Here, we investigated a \emph{D.
batangense} population in the type locality and addressed two main
questions: (1) Do males and females differ in morphological traits and
bite force? (2) Is there a relationship between head morphology and bite
force in this species?

\textbf{Materials and Methods}

\textbf{Study site}

The study was carried out in the upper Jinsha Valley in Batang County
(29.46degN, 99.06degE, 2\selectlanguage{english} 497 m a.s.l.) on the Sichuan-Tibet border in
western China (Fig. 1). The area is characterized by a typical dry-hot
valley-plateau climate, with a dry spring, cool summer, rainy autumn,
and warm winter. Annual average temperature is 13.8 degC, with minimum and
maximum monthly means of 3.9 degC and 19.9 degC in December and June,
respectively. Annual mean precipitation is 500 mm, with more than 80\%
falling between June and September. The region shows sparse vegetation
habitat, low vegetation cover (less than 50\%), and sandy and rocky soil
substrate. The vegetation is dominated by shrubs (e.g.,\emph{Indigofera
lenticellata} , \emph{Sophora moorcroftiana} , and\emph{Rumex hastatus}
) and herbs (e.g., \emph{Incarvillea arguta} and\emph{Artemisia
stechmanniana} ).

\textbf{Fig. 1} Distribution (a), habitat (b), and a male specimen (c)
of \emph{Diploderma batangense} . Red dot represents specific study
site.

\textbf{Animal sampling}

A total of 135 \emph{D. batangense} lizards (77 males and 58 females)
were captured by lasso during daylight hours (10:00am--17:00pm) in
August 2020. The capture location was marked using a uniquely coded
plastic card. Each lizard was sexed by hemipenis eversion and dorsal
color pattern. Bite force and body temperature (BT) were measured
immediately after capture. All lizards were numbered and taken to a
makeshift laboratory in cloth bags. All lizards were released to their
original capture site after collection of data. All animal procedures
were carried out in accordance with and approved by the Animal Care and
Use Committee at Yibin University (YBU2020005).

\textbf{Morphometrics}

For all lizards, the following data were collected using a digital
caliper (DL91200, Deli, Ningbo, China) to the nearest 0.01 mm:
snout-vent length (SVL); tail length (TL, distance from vent to tail
tip); abdomen length (AL, distance from posterior base of forelimb to
anterior base of hindlimb); head length (HL, distance from anterior tip
of rostral scale to posterior aspect of parietal); head width (HW,
maximum width of head taken at posterior end of mandible); head height
(HH, distance from gular region to highest part of head); mouth length
(ML, distance from tip of snout to end of opening); forelimb length
(FLL, distance from forelimb to wrist joint); and hindlimb length (HLL,
distance from hindlimb to ankle joint). Body mass (BM) was determined
using a digital scale (I-2000, Mengfu, Dongguan, China) to the nearest
0.01 g.

\textbf{Bite force}

To explore the relationship between bite force and BT, anal temperature
was collected before each bite using an ultra-thin catheter electronic
thermocouple (UT323, +0.01deg C; Victor, Shenzhen, China) in the cloaca.
\emph{In vivo} bite force was measured using a piezoelectric force
transducer instrument (VXT500, 0--50 N; Viste, Shenzhen, China),
consisting of a pair of bite plates (2 mm thick, accurate to 0.1 N),
hand-charged amplifier, and digital display. To reduce damage to teeth,
the end of each steel plate was covered with non-toxic rubber. The
instrument was calibrated before each bite. The bite plate was placed at
the unilateral molar, a posterior bite position where maximum bite force
can be recorded. During measurement, bite force data were collected by
gently pinching the head and tail. Bite force was measured three times
per individual, and the maximum value was the maximal bite force for
each lizard (McBrayer \& Anderson, 2007). Bite force trials were
separately conducted three times in the field and indoors to minimize
variation. Based on the six tests, only the maximum bite force value and
the corresponding anal temperature were retained for further analysis.

\textbf{Statistical analysis}

To investigate differences in morphological traits and bite force
between males and females, we first performed analysis of variance
(ANOVA) for morphological measurements (SVL, BM, HL, HW, FLL, and HLL)
and bite force values. As some samples (TL, AB, HH, ML, and bite force)
showed non-normality, we also used the nonparametric Mann-Whitney (U)
test. To determine the effect of individual SVL on morphology and bite
performance, we further examined the relative differences in
morphological traits and bite force between the sexes using similar
methods while controlling for the effect of SVL (covariate).

To test whether morphological traits could explain the observed sexual
dimorphism in bite performance, we first examined the relationship
between bite force and head morphology for both sexes using univariate
linear regression. Next, we performed stepwise multiple regression
analysis to confirm which morphological traits were the best predictors
of variation in bite force for males and females.

Significance level was set to \emph{P} \textless{} 0.05. All data
analyses were performed using SPSS v26.0 (SPSS Inc., Chicago, IL, USA)
and graphs were generated using OriginLab Professional v2021b.

\textbf{Results}

\textbf{Sexual dimorphism inmorphology}

Marked morphological dimorphism was observed between the male and female
lizards. Males were significantly larger than females in all
morphological traits measured (SVL: \emph{F} \textsubscript{1,
133}=13.047, \emph{p} = 0.001; BM: \emph{F} \textsubscript{1, 133} =
18.797,\emph{p} \textless{} 0.001; HL: \emph{F} \textsubscript{1, 133} =
64.170,\emph{p} \textless{} 0.001; HW: \emph{F} \textsubscript{1, 133} =
53.253,\emph{p} \textless{} 0.001; TL: \emph{Z} \textsubscript{1, 133} =
-7.656,\emph{p} \textless{} 0.001; HH: \emph{Z} \textsubscript{1, 133} =
-5.810,\emph{p} \textless{} 0.001; ML: \emph{Z} \textsubscript{1, 133} =
-6.585,\emph{p} \textless{} 0.001; FLL: \emph{F} \textsubscript{1, 133}
= 63.407, \emph{p} \textless{} 0.001; HLL, \emph{F} \textsubscript{1,
133}= 73.092, \emph{p} \textless{} 0.001, Table 1, Figure 2), except for
AL (\emph{Z} \textsubscript{1, 133} = -0.691, \emph{p =} 0.498, Table 1,
Figure 2d). In addition, for a given SVL, males had greater head size
(HW: \emph{F} \textsubscript{1, 133} = 44.112, \emph{p} = 0.005;
HL:\emph{F} \textsubscript{1, 133} = 71.294, \emph{p} \textless{} 0.001;
logHH: \emph{F} \textsubscript{1, 133}= 30.462, \emph{p
\textless{}}0.001; logML: \emph{F} \textsubscript{1, 133} = 43.027,
\emph{p \textless{}} 0.001), weight (\emph{F} \textsubscript{1, 133} =
5.513,\emph{p =} 0.020), TL (\emph{F} \textsubscript{1, 133} = 79.160,
\emph{p \textless{}} 0.001), and limb length (FLL: \emph{F}
\textsubscript{1, 133} = 49.567, \emph{p \textless{}} 0.001;
HLL:\emph{F} \textsubscript{1, 133} = 54.447, \emph{p \textless{}}
0.001, Table 1) compared to females.

\textbf{Figure 2} Comparison of morphological characteristics and bite
force between male and female \emph{Diploderma batangense} . a) SVL,
snout-vent length; b) BM, body mass; c) TL, tail length; d) AL, abdomen
length; e) HL, head length; f) HW, head width; g) HH, head height; h)
ML, mouth length; i) FLL, forelimb length; j) HLL, hindlimb length; k)
Bite force; l) Ventral surface of male and female. Gray filled is male
and no fill is female; * Significant differences (\emph{p} \textless{}
0.001).

\textbf{Sexual dimorphism in bite force and itsdeterminants}

No significant relationship was detected between bite force and BT
in\emph{D. batangense} (\emph{F} \textsubscript{1, 133} = 0.22, \emph{p}
= 0.133). However, significant differences in bite force were found
between males and females. In comparison to females, males had
significantly larger absolute bite force (\emph{F} \textsubscript{1,
133} = -4.494, \emph{p \textless{}} 0.001, Table 1, Figure 2k) and
relative bite force (\emph{F} \textsubscript{1, 133} = 10.610, \emph{p
=} 0.001).

Univariate linear regression analysis showed that bite force was
positively correlated with HL, HW, HH, and ML (Table 2, Figure 3).
Multiple stepwise regression analysis showed that the determinants of
bite force were ML in males (\emph{R\textsuperscript{2}} = 0.467,
\emph{p} = 0.002; Table 2) and HW in females
(\emph{R\textsuperscript{2}} = 0.378, \emph{p} \textless{} 0.001; Table
2).

\textbf{Figure 3} Relationship between bite force and head morphology
in\emph{Diploderma batangense} . Relationships between bite force and
head length (HL) (a), head width (HW) (b), head height (HH) (c), and
bite force and mouth length (MF) (d). Red points represent females and
black points represent males.

\textbf{Discussion}

Lizards exhibit sexual dimorphism in various phenotypic traits and
behaviors, such as size, shape, weight, coloration, bite force, and
locomotor performance (Cox et al., 2003). Three patterns of sexual
dimorphism have been identified in lizards (Cruz\selectlanguage{english}-Elizalde et al., 2021),
including male-biased (Herrel et al., 2010), female-biased (Cox et al.,
2009), and unbiased (Schwarzkopf, 2005), which vary among different
genera and families (Cox et al., 2007; Cruz\selectlanguage{english}-Elizalde et al., 2021).
The\emph{D. batangense} population from the Hengduan Mountains
demonstrated obvious male-biased morphology and bite force
performance\emph{.} Notably, the\emph{D. batangense} males were markedly
larger (i.e., equivalent body size) than females in terms of head size
(HL, HW, HH, and ML), body size (SVL and BM), limb length (FLL and HLL),
and tail length (TL), with stronger bite force, although no differences
in AL were observed. This male-biased pattern has been widely reported
in the lizard family, including in \emph{Tropidurus}(Tropiduridae),
\emph{Anolis}(Dactyloidae), \emph{Varanus} (Varanidae),
\emph{Sceloporus}(Phrynosomatidae), and \emph{Diploderma} (Anguidae)
(Cox et al., 2007; Kuo et al., 2009; Jimenez-Arcos et al., 2017).
Interestingly, Kuo et al., (2009) reported that closely related species
\emph{D. swinhonis}(previously \emph{Japalura swinhonis} ) shows marked
male-biased sexual dimorphism in all morphological variables, but when
controlling for body size, males had proportionately longer and wider
heads, but shorter body length and limbs. Xiong et al., (2022) also
found that \emph{D. micangshanensis}shows significant male-biased sexual
dimorphism in all morphological variables, except for trunk length, but
when controlling for SVL, only head shape (HL, HW, HH, and ML) and trunk
length differ significantly between the sexes. Differences in sexual
dimorphism between closely related species may be related to differences
in habitats (Da et al., 2014), as reported in\emph{Podarcis}
\emph{hispanica} and\emph{P. bocagei} (Kaliontzopoulou et al., 2012).

Male-biased sexual dimorphism is usually explained by sexual selection,
which predicts that males will evolve morphological features and
capacities that enhance mating success, whether through improved
fighting ability against other males or a better chance of attracting
females (Endler \& Houde, 1995; Cruz-Elizalde et al., 2021). Previous
studies have shown that larger males (e.g., larger body size and head
shape) are more likely to outcompete and gain access to better resources
such as food, territory, and mates during antagonistic encounters
(Herrel et al., 2010; Hierlihy et al., 2013). Food availability is a
determining factor of intraspecific competition in many lizard species
(Pafilis et al., 2009; Donihue et al., 2016).\emph{Diploderma
batangense}inhabits dry-hot valleys characterized by relatively scarce
food sources. In the studied \emph{D. batangense} population, aggressive
male-male interactions were relatively common during and outside the
mating season, with larger individuals more likely to win in aggressive
interactions for food (unpublished data). Forced copulation is an
important reproductive strategy in various territorial lizards (Rodda,
1992; Herrel et al., 2010), in which females struggle physically and
violently in an apparent attempt to escape mounting males (Burghardt \&
Rand 1982). \emph{Diploderma batangense} also showed aggressive and
forceful behavior during copulation, in which a male approached a female
and grasped her neck with his jaws. Therefore, the larger body size and
bite force in \emph{D. batangense} may be related to actual mating
success and fitness (Lappin \& Husak, 2005; Herrel et al., 2010).

Bite force is a comprehensive measure of trait performance in multiple
activities, including courtship, conflict, and hunting, especially in
males (Herrel et al., 2007; Kaliontzopoulou et al., 2012; Sagonas et
al., 2014; Herrel et al., 2018). Individual bite force capacity is
directly related to head size (McBrayer \& Anderson, 2007; Herrel et
al., 2010; Kaliontzopoulou et al., 2012), generally increasing with head
size (Deeming et al., 2022; Naretto et al., 2022). This phenomenon was
found in present study, where bite force was positively correlated with
head size (HL, HW, HH and ML). Understandably, a larger head results in
a larger cross-sectional area of jaw muscles and more developed
jaw-cranial musculature, thus generating greater bite force (Herrel et
al., 2001). Therefore, increasing head height and cross-sectional area
of the jaw muscles may be a mechanism for increasing occlusal force
(McBrayer \& Anderson, 2007). Head length, head width, and mouth length
can also affect bite force (Herrel et al., 2001; Sagonas et al., 2014),
not unexpectedly as bite performance can be influenced by the size of
the jaw musculature, ratio of the upper and lower jaws, insertion point
and direction of jaw musculature, and microstructure of the muscle
fibers (Herrel et al., 1998; Kaliontzopoulou et al., 2012). Thus,
external head morphology is a readily accessible proxy for the joint
action of structural components. Interestingly, Lappin and Husak (2005)
found only a weak correlation between external head size and bite force
in male collared lizards (\emph{Crotaphytus collaris} ) and suggested
that internal skull structure may be a key determinant of bite force.
Consequently, there is growing recognition that the underlying
musculature may drive changes in bite force, as demonstrated in various
\emph{Anolis} lizard species, in which the adductor externus and
pseudotemporalis muscles are considered good determinants of bite force
(Wittorski et al., 2016). Herrel et al., (2007) also proposed that
testosterone levels can affect the size of the adductor muscles of the
outer jaw and may play an important role in regulating bite force.
However, further study is necessary to fully elucidate the determinants
of bite force.

Bite performance is expected to vary between males and females due to
differences in head shape and size (Herrel et al., 2007). Therefore, the
best predictors of maximal bite force capacity tend to differ by sex.
For example, lower jaw length is the best predictor of bite force in
\emph{Anolis carolinensis} males, whereas head width and jaw-closing
in-lever are the best predictors in females (Herrel et al., 2007). In
our study, the best predictors of bite force also differed between the
males (ML) and females (HW). This difference may be explained from a
structure-function relationship: i.e., with the relative increase in
head width, the adductor cavity in males is significantly larger than
that in females, which may accommodate larger mandibular adductor
muscles and enhance interactions between muscles and skull, thus
improving bite force strength (Lappin et al., 2006; Sagonas et al.,
2014). The jaw musculature and skeletal system are closely related to
bite force, and it is clear from the principle of leverage that the
larger the male force arm (lower jaw length), the greater the bite force
generated (Herrel et al., 2007; Herrel et al., 2010; Wittorski et al.,
2016). Sexual dimorphism in lizard bite force is generally thought to be
related to fighting or territorial defense in males, with an added
advantage in intrasexual competition (Naretto et al., 2022) and forced
mating success (Sagonas et al., 2014). Even among males of similar body
length, success in combat and forced mating appears to favor those with
greater body robustness, head size, and bite force (Lappin et al.,
2006). Differences in head size and performance may also be related to
differences in reproductive allocation between the sexes, with females
investing more in reproduction than males and requiring higher energy
intake (Bulte et al., 2008). Thus, head width, the best predictor of
bite force in females, may be related to energy requirements for
follicular development and offspring rearing (Naretto et al., 2022).
Although there was no advantage in head width between the \emph{D.
batangense} females and males, females with wider heads had a larger
bite force compared to other females, and thus may be able to feed on
larger food items and provide more energy for their offspring.

\textbf{Summary}

Relatively few studies have been conducted on sexual dimorphism in
\emph{Diploderma} species, although previous studies suggested that
male-biased sexual dimorphism was the dominant pattern in the genus (Kuo
et al., 2009; Xiong et al., 2022). In the present study, \emph{D.
batangense} showed male-biased sexual dimorphism in morphology and bite
force, consistent with the sexual selection hypothesis. Furthermore, the
best predictors of bite force differed between the sexes (ML in males
and HW in females). However, it remains unclear how the intrinsic skull
and muscle structures affect bite force in this species. As such,
further anatomical analysis of the head structure is required, together
with intraspecific (sex) comparisons of body color, behavior, and
resource use (diet and microhabitat). In addition, given the high
diversity of species and habitats in the genus, further study on
interspecific differences in bite force among species in different
habitats is necessary.

\textbf{Acknowledgments}

This project was supported by the National Key R\&D Program of China
(2022YFC2602500), Second Tibetan Plateau Scientific Expedition and
Research (STEP) Program (2019QZKK0501), National Natural Science
Foundation of China (31801980 and 32001114), Sichuan Science and
Technology Plan Project (2019JDKP0016), and Natural Science Foundation
of Liaoning Province of China (2021-MS-241). We thank Zhang He and Tang
Kui for their help in data collection. We also thank Songwen Tan for
suggestions in analysis. We are grateful to the reviewers and editors
for their comments and corrections of the manuscript.

\textbf{ORCID}

\emph{Ling Li}https://orcid.org/0000-0002-7650-2280

\emph{Gang Wang} https://orcid.org/0000-0002-0764-1615

\emph{Yuhao Wen} https://orcid.org/0000-0002-3115-7444

\emph{Yihua Xiang} https://orcid.org/0000-0003-0185-0106

\emph{Peng Guo} https://orcid.org/0000--0001--5585--292X

\emph{Bingjun Dong} https://orcid.org/0000-0001-8727-401X

\emph{Yayong Wuhttps://orcid.org/0000-0003-2752-4085}

\textbf{Competing Interests}

The authors declare no competing interests.

\textbf{Author Contributions}

\textbf{Ling Li} : Data curation (Lead), Formal analysis (Lead),
Investigation (Lead), Resources (Lead), Visualization (Lead), Writing --
original draft (Lead), Writing -- review \& editing (Equal);\textbf{Gang
Wang} : Formal analysis (Supporting), Writing -- review \& editing
(Equal); \textbf{Yuhao Wen} : Data curation (Supporting), Investigation
(Equal); \textbf{Yihua Xiang} : Data curation (Supporting),
Investigation (Equal); \textbf{Peng Guo} : Conceptualization (Equal),
Writing -- review \& editing (Equal); \textbf{Bingjun Dong} :
Conceptualization (Equal), Writing -- review \& editing
(Equal);\textbf{Yayong Wu} : Funding acquisition (Lead), Investigation
(Equal), Supervision (Lead), Writing -- review \& editing (Lead).

\textbf{Data Accessibility Statement}

All morphological data for all individuals are deposited in Dryad

\emph{https://doi.org/10.5061/dryad.9kd51c5nc.}

\textbf{References}

Bolnick, D. I., \& Doebeli, M. (2003). Sexual dimorphism and adaptive
speciation: two sides of the same ecological coin.~\emph{Evolution}
.~57(11): 2433-2449. doi: 10.1111/j.0014-3820.2003.tb01489.x.

Bulte, G., Irschick, D. J., \& Blouin-Demers, G. (2008). The
Reproductive Role Hypothesis Explains Trophic Morphology Dimorphism in
the Northern Map Turtle. \emph{Functional Ecology} . 22(5): 824--830.
doi:10.HH/j.1365-2435.2008.01422.x.

Burghardt, G. M., \& Rand, A. S. (Eds.). (1982). Iguanas of the world:
their behavior, ecology, and conservation. New Jersey: Noyes
Publications.

Cox, R. M., Skelly, S. L., \& John\selectlanguage{english}-Alder, H. B. (2003). A comparative
test of adaptive hypotheses for sexual size dimorphism in
lizards.\emph{Evolution} . 57(7): 1653-1669.
doi:10.1111/j.0014-3820.2003.tb00371.x.

Cox, R. M., Butler, M. A., \& John-Alder, H. B. (2007). The evolution of
sexual size dimorphism in reptiles. In D.J. Fairbairn, W.U. Blanckenhorn
and T. Szekely (Eds.), Sex, size \& gender roles: Evolutionary studies
of sexual size dimorphism (pp. 38-49). Oxford, UK: Oxford University
Press.

Cox, R. M., Stenquist, D. S., \& Calsbeek, R. (2009). Testosterone,
growth and the evolution of sexual size dimorphism. \emph{Journal of
Evolutionary Biology} . 22(8): 1586-1598.
doi:10.1111/j.1420-9101.2009.01772.x.

Cruz-Elizalde, R., Ramirez-Bautista, A., Pacheco, L. F. R., Lozano, A.,
\& Rodriguez-Romero, F. D. J. (2020). Sexual dimorphism in size and
shape among populations of the lizard \emph{Sceloporus
variabilis}(\emph{Squamata: Phrynosomatidae} ). \emph{Zoology} . 140:
125781. doi:10.1016/j.zool.2020.125781.

Cruz\selectlanguage{english}-Elizalde, R., Villamar\selectlanguage{english}-Duque, T. E., \& Ramirez\selectlanguage{english}-Bautista, A.
(2021). Sexual dimorphism in size and shape in the viviparous
lizard\emph{Abronia taeniata} (Squamata: Anguidae) in central
Mexico.\emph{Acta Zoologica} . 102(2): 220-226. doi:10.1111/azo.12329.

Dashevsky, D., Meik, J. M., Mocino\selectlanguage{english}-Deloya, E., Setser, K., \& Schaack,
S. (2013). Patterns of sexual dimorphism in Mexican alligator
lizards,\emph{Barisia imbricata} . \emph{Ecology and Evolution} .3(2):
255-261. doi:10.1002/ece3.455\emph{.}

Da Silva, J. M., Herrel, A., Measey, G. J., \& Tolley, K. A. (2014).
Sexual dimorphism in bite performance drives morphological variation in
chameleons. \emph{PLoS One} . 9(1): e86846.
doi:10.1371/journal.pone.0086846.

Deeming, D. C. (2022). Inter\selectlanguage{english}-relationships among body mass, body
dimensions, jaw musculature and bite force in reptiles. \emph{Journal of
Zoology} . 318(1): 23-33. doi:10.1111/jzo.12981.

Donihue, C. M., Brock, K. M., Foufopoulos, J., \& Herrel, A. (2016).
Feed or fight: testing the impact of food availability and intraspecific
aggression on the functional ecology of an island
lizard.\emph{Functional Ecology} . 30(4): 566-575.
doi:10.1111/1365-2435.12550.

Endler, J. A., \& Houde, A. E. (1995). Geographic variation in female
preferences for male traits in \emph{Poecilia reticulata}
.\emph{Evolution} . 49(3): 456-468.
doi:10.1111/j.1558-5646.1995.tb02278.x\emph{.}

Fabre, A. C., Andrade, D. V., Huyghe, K., Cornette, R., \& Herrel, A.
(2014). Interrelationships between bones, muscles, and performance:
biting in the lizard \emph{Tupinambis merianae} . \emph{Evolutionary
Biology} . 41(4): 518-527. doi:10.1007/s11692-014-9286-3.

Fairbairn, J., \& Shine, R. (1993). Patterns of sexual size dimorphism
in seabirds of the Southern Hemisphere. \emph{Oikos} . 68(1): 139-145.
doi:10.2307/3545319.

Herrel, A., Van Damme, R., \& De Vree, F. (1996). Sexual dimorphism of
head size in \emph{Podarcis hispanica} \emph{atrata} : testing the
dietary divergence hypothesis by bite force analysis. \emph{Netherlands
Journal of Zoology} . 46 (3.4): 253-262.

Herrel, A., Aerts, P., \& De Vree, D. (1998). Static biting in lizards:
functional morphology of the temporal ligaments. \emph{Journal of
Zoology} . 244(1): 135-143. Doi:10.1111/j.1469-7998.1998.tb00015.x.

Herrel, A., De Grauw, E. D., \& Lemos\selectlanguage{english}-Espinal, J. A. (2001). Head shape
and bite performance in xenosaurid lizards. \emph{Journal of
Experimental Zoology} . 290(2): 101-107. doi:10.1002/jez.1039.

Herrel, A., McBrayer, L. D., \& Larson, P. M. (2007). Functional basis
for sexual differences in bite force in the lizard \emph{Anolis
carolinensis} . \emph{Biological Journal of the Linnean Society} .
91(1): 111-119. doi:10.1111/j.1095-8312.2007.00772.x\emph{.}

Herrel, A., Moore, J. A., Bredeweg, E. M., \& Nelson, N. J. (2010).
Sexual dimorphism, body size, bite force and male mating success in
tuatara. \emph{Biological Journal of the Linnean Society} . 100(2):
287-292. doi:10.1111/j.1095-8312.2010.01433.x.

Herrel, A., Petrochic, S., \& Draud, M. (2018). Sexual dimorphism, bite
force and diet in the diamondback terrapin. \emph{Journal of Zoology} .
304(3): 217-224. doi:10.1111/jzo.12520.

Hierlihy, C. A., Garcia-Collazo, R., Chavez Tapia, C. B., \& Mallory, F.
F. (2013). Sexual dimorphism in the lizard \emph{Sceloporus siniferus} :
support for the intraspecific niche divergence and sexual selection
hypotheses. \emph{Salamandra} . 49: 1-6.

Huyghe, K., Vanhooydonck, B., Scheers, H., Molina-Borja, M., \& Van
Damme, R. (2005). Morphology, performance and fighting capacity in male
lizards, \emph{Gallotia galloti} . \emph{Functional Ecology} . 19(5):
800-807. doi:10.1111/j.1365-2435.2005.01038.x.

Huyghe, K., Herrel, A., Adriaens, D., Tadi\selectlanguage{polish}ć, \selectlanguage{english}Z., \& Van Damme, R.
(2009). It is all in the head: morphological basis for differences in
bite force among colour morphs of the Dalmatian wall
lizard.\emph{Biological Journal of the Linnean Society} . 96(1): 13-22.
doi:10.1111/j.1095-8312.2008.01103.x.

Ji, X., Lin, L. H., Lin, C. X., Qiu, Q. B., \& Du, Y. (2006). Sexual
dimorphism and female reproduction in the many-lined sun skink
(\emph{Mabuya multifasciata} ) from China. \emph{Journal of Herpetology}
. 40(3): 351-357.

Jozet-Alves, C., Mod\selectlanguage{ngerman}éran, J., \& Dickel, L. (2008). Sex differences in
spatial cognition in an invertebrate: the cuttlefish. \emph{Proceedings
of the Royal Society B: Biological Sciences} . 275(1646): 2049-2054.
doi:10.1098/rspb.2008.0501.

Jiménez-Arcos, V. H., Sanabria-Urbán, S., \& Cueva del Castillo, R.
(2017). The interplay between natural and sexual selection in the
evolution of sexual size dimorphism in \emph{Sceloporus} lizards
(\emph{Squamata:Phrynosomatidae} ). \emph{Ecology and Evolution} . 7(3):
905-917. doi:10.1002/ece3.2572.

Kaliontzopoulou, A., Adams, D. C., van der Meijden, A., Perera, A., \&
Carretero, M. A. (2012). Relationships between head morphology, bite
performance and ecology in two species of Podarcis wall
lizards.\emph{Evolutionary Ecology} . 26(4): 825-845.
doi:10.1007/s10682-011-9538-y.

Kuo, C. Y. (2009). Sexual size and shape dimorphism in an agamid lizard,
\emph{Japalura swinhonis} (Squamata: Lacertilia: Agamidae).
\emph{Zoological Studies.} 48(3): 351-361.

Lappin, A. K., \& Husak, J. F. (2005). Weapon performance, not size,
determines mating success and potential reproductive output in the
collared lizard (\emph{Crotaphytus collaris} ). \emph{The American
Naturalist} . 166(3): 426-436.

Lappin, A. K., Hamilton, P. S., \& Sullivan, B. K. (2006). Bite-force
performance and head shape in a sexually dimorphic crevice-dwelling
lizard, the common chuckwalla {[}\emph{Sauromalus ater} (=
obesus){]}.\emph{Biological Journal of the Linnean Society} . 88(2):
215-222. doi:10.1111/j.1095-8312.2006.00615.x.

McBrayer, L. D., \& Anderson, R. A. (2007). Sexual size dimorphisms and
bite force in the northern alligator lizard, \emph{Elgaria coerulea}
.\emph{Journal of Herpetology} . 41(4): 554-559. doi:10.1670/07-045.1.

Mitani, J. C., Gros-Louis, J., \& Richards, A. F. (1996). Sexual
dimorphism, the operational sex ratio, and the intensity of male
competition in polygynous primates. \emph{The American Naturalist} .
147(6): 966-980. doi:10.2307/2463187.

Naretto, S., Cabezas-Cartes, F., López Juri, G., \& Chiaraviglio, M.
(2022). Intraspecific variability of bite force in Achala copper lizards
in a sexual selection context: who bites harder and when and
why?.\emph{Biological Journal of the Linnean Society} . 136(2): 282-292.
doi:10.1093/biolinnean/blac034.

Noble, G. K., \& Bradley, H. T. (1933). The mating behavior of lizards;
its bearing on the theory of sexual selection. \emph{Annals of the New
York Academy of Sciences} . 35(1): 25-100.
doi:10.1111/j.1749-6632.1933.tb55365.x.

Olsson, M., Shine, R., Wapstra, E., Ujvari, B., \& Madsen, T. (2002).
Sexual dimorphism in lizard body shape: the roles of sexual selection
and fecundity selection. \emph{Evolution} . 56(7):1538-1542. doi:
10.1111/j.0014-3820.2002.tb01464.x.

Pafilis, P., Meiri, S., Foufopoulos, J., \& Valakos, E. (2009).
Intraspecific competition and high food availability are associated with
insular gigantism in a lizard.\emph{Naturwissenschaften} . 96(9):
1107-1113. doi:10.1007/s00114-009-0564-3.

Pincheira\selectlanguage{english}-Donoso, D., \& Hunt, J. (2017). Fecundity selection theory:
concepts and evidence. \emph{Biological Reviews} . 92(1): 341-356.
doi:10.1111/brv.12232.

Pincheira\selectlanguage{english}-Donoso, D., Tregenza, T., Butlin, R. K., \& Hodgson, D. J.
(2018). Sexes and species as rival units of niche saturation during
community assembly. \emph{Global Ecology and Biogeography} . 27(5):
593-603. doi:10.1111/geb.12722\emph{.}

Rand, A. S. (1967). Ecology and social organization in Anolis
lineatopus. \emph{Proceedings of the United States National Museum} .
122, 1-79.

Rodda G. H. (1992). The mating behavior of \emph{Iguana iguana}
.\emph{Smithsonian Contributions to Zoology} . 534: 1-40.

Sagonas, K., Pafilis, P., Lymberakis, P., Donihue, C. M., Herrel, A., \&
Valakos, E. D. (2014). Insularity affects head morphology, bite force
and diet in a Mediterranean lizard. \emph{Biological Journal of the
Linnean Society} . 112(3): 469-484. doi:10.1111/bij.12290.

Schoener, T. W. (1967). The ecological significance of sexual size
di-morphism in the lizard \emph{Anolis conspersus} . \emph{Science} .
155(3761): 474-477. doi:10.1126/scien ce.155.3761.474.

Schauble, C. S. (2004). Variation in body size and sexual dimorphism
across geographical and environmental space in the
frogs\emph{Limnodynastes tasmaniensis and L. peronii} . \emph{Biological
Journal of the Linnean Society} . 82(1): 39-56.
doi:10.1111/j.1095-8312.2004.00315.x\emph{.}

Schwarzkopf, L. (2005). Sexual dimorphism in body shape without sexual
dimorphism in body size in water skinks (\emph{Eulamprus quoyii}
).\emph{Herpetologica} . 61(2): 116-123. doi:10.1655/04-66\emph{.}

Taverne, M., King-Gillies, N., Krajnovi\selectlanguage{polish}ć, \selectlanguage{english}M., Lisi\selectlanguage{polish}č\selectlanguage{english}i\selectlanguage{polish}ć, \selectlanguage{english}D., Mira, \selectlanguage{ngerman}Ó.,
Petricioli, D., Saboli\selectlanguage{polish}ć, \selectlanguage{english}I., \selectlanguage{polish}Š\selectlanguage{english}tambuk, A., Tadi\selectlanguage{polish}ć, \selectlanguage{english}Z., \& Vigliotti, C.
(2020). Proximate and ultimate drivers of variation in bite force in the
insular lizards \emph{Podarcis melisellensis} and \emph{Podarcis sicula}
. \emph{Biological Journal of the Linnean Society} . 131(1): 88-108.
doi:10.1093/biolinnean/blaa091.

Wang, K., Ren, J. L., Wu, J. W., Jiang, K., Jin, J. Q., Hou, S.
B.,Zheng, P, Y., Xie, F., Siler, C. D., \& Che, J. (2021). Systematic
revision of Mountain Dragons (Reptilia: Agamidae: Diploderma) in China,
with descriptions of six new species and discussion on their
conservation. \emph{Journal of Zoological Systematics and Evolutionary
Research} . 59(1): 222-263. doi:10.1111/jzs.12414.

Wegener, J. E., Mulder, K. P., Pringle, R. M., Losos, J. B., \& Kolbe,
J. J. (2019). Head size of male and female lizards increases with
population density across island populations in the
Bahamas.\emph{Breviora} . 566(1): 1-9. doi:10.3099/0006-9698-566.1.1.

Wittorski, A., Losos, J. B., \& Herrel, A. (2016). Proximate
determinants of bite force in \emph{Anolis} lizards. \emph{Journal of
Anatomy} . 228(1): 85-95. doi:10.1111/joa.12394\emph{.}

Xiong, J., Bai, Y., Li, G., \& You, Z. (2022). Sexual dimorphism in the
mountain dragon, \emph{Diploderma micangshanensis} (Squamata:
Lacertilia: Agamidae) from central China.\emph{Animal Biology} . 1(aop):
1-10. doi:10.1163/15707563-bja10085.

Zhong, G. H., Liu, Q., Li, C., Peng, P., \& Guo, P. (2017). Sexual
dimorphism and geographic variation in the asian lance-headed pitviper
\emph{Protobothrops mucrosquamatus}in the mainland china. \emph{Asian
Herpetological Research} . 8(2): 118-122.
doi:10.16373/j.cnki.ahr.160011.

Zhu, F., Chen, L., Guo, P., Xu, Y., \& Liu, Q. (2022). Sexual Dimorphism
and Geographic Variation of the White-lipped Pit Viper
(\emph{Trimeresurus albolabris} ) in China.\emph{Current herpetology} .
41(1): 24-34. doi:10.5358/hsj.41.24.\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Fig/Fig}

\end{center}
\end{figure}

\textbf{Hosted file}

\verb`Fig. 2.eps`  available at \url{https://authorea.com/users/574987/articles/618463-sexual-dimorphism-in-morphology-and-bite-force-in-the-mountain-dragon-diploderma-batangense-squamata-anguidae-from-the-hengduan-mountains-in-western-china}\selectlanguage{english}
\begin{figure}[H]
\begin{center}
\includegraphics[width=0.70\columnwidth]{figures/Fii/Fii}

\end{center}
\end{figure}

\textbf{Hosted file}

\verb`Table1.docx`  available at \url{https://authorea.com/users/574987/articles/618463-sexual-dimorphism-in-morphology-and-bite-force-in-the-mountain-dragon-diploderma-batangense-squamata-anguidae-from-the-hengduan-mountains-in-western-china}

\textbf{Hosted file}

\verb`Table2.docx`  available at \url{https://authorea.com/users/574987/articles/618463-sexual-dimorphism-in-morphology-and-bite-force-in-the-mountain-dragon-diploderma-batangense-squamata-anguidae-from-the-hengduan-mountains-in-western-china}

\selectlanguage{english}
\FloatBarrier
\end{document}

