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Sexual size dimorphism and allometry in Liolaemus of the L. laurenti group

(Sauria: Liolaemidae): Morphologic lability in a clade of lizards with different
reproductive modes

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Zoologischer Anzeiger 252 (2013) 299–306

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Zoologischer Anzeiger
journal homepage: www.elsevier.de/jcz

Sexual size dimorphism and allometry in Liolaemus of the L. laurenti group

(Sauria: Liolaemidae): Morphologic lability in a clade of lizards with different
reproductive modes
María P. Cabrera a,∗ , Gustavo J. Scrocchi a , Félix B. Cruz b
a
Instituto de Herpetología - Fundación Miguel Lillo, Miguel Lillo 251, 4000 San Miguel de Tucumán, Tucumán, Argentina
b
Instituto de Investigaciones en Biodiversidad y Medioambiente (INIBIOMA), CONICET-UNCOMA, Centro Regional Universitario Bariloche, Universidad Nacional del Comahue, Quintral
1250, 8400 Bariloche, Río Negro, Argentina

a r t i c l e i n f o a b s t r a c t

Article history: Sexual size dimorphism is a common aspect in animals and different hypotheses to this regard
Received 27 October 2011 were generated. Additionally, Rensch’s rule is an empirical pattern that states that the degree of
Received in revised form 15 August 2012 sexual size dimorphism is more pronounced in species with larger males, and less pronounced in
Accepted 31 August 2012
those with larger females. We studied the body size differences, Rensch’s rule and sexual dimor-
Available online 16 November 2012
phism in morphological features in 22 lizard species of the Liolaemus laurenti clade. We assessed
Corresponding Editor: Julia A. Clarke.
sexual dimorphism using independent contrasts and gauged phylogenetic signal in all measured
traits. We intend to answer the following questions: (a) what is the phylogenetic signal of body
Keywords:
Sexual dimorphism
size and other morphological features?; (b) do the Liolaemus lizards of the laurenti clade follow the
Liolaemus laurenti group Rensch’s rule pattern?, and (c) do fecundity advantage or sexual selection hypotheses explain the dif-
Sexual selection ferences between sexes?. Liolaemus species show low phylogenetic signal in most of the measured
Fecundity hypothesis traits. In this group, male-larger dimorphism is more common, and several species showed no sex-
Rensch’s rule ual size dimorphism. Additionally, our results do not support Rensch’s rule. Head shape and radius
length showed sexual dimorphism suggesting sexual selection. Finally, no relationship was recov-
ered between inter-limb length and reproductive output, thus fecundity advantage hypothesis was not
supported.
© 2012 Elsevier GmbH. All rights reserved.

1. Introduction of sexual dimorphism. For example, the sexual selection hypothe-

sis that predicts that larger males will have higher reproductive
Morphological differences between the sexes are a common fea- success (Cox et al., 2003). According to this, males show larger
ture in many animals (Fairbairn, 1997; Sinsch et al., 2002), including body size or show allometric growth of structures that may be
reptiles (Fairbairn, 1997; Zamudio, 1998; Kratochvíl and Frynta, used in aggressive encounters with other males (Petrie, 1992;
2002; Cox et al., 2003; Stuart Fox, 2008; Boretto and Ibargüengoytía, Fairbairn, 1997), or may used by females to assess the quality of
2009; Frýdlová and Frynta, 2010). In lizards, males and females may their partners (Carothers, 1984; Anderson and Vitt, 1990). Now, in
differ in several traits, such as coloration, body shape, or size. How- the case of larger females, an alternative hypothesis proposed is the
ever, most comparative studies on sexual dimorphism have focused fecundity advantage hypothesis (or reproductive selection sensu
on differences in body size (Butler and Losos, 2002), because this Fairbairn, 1997) that states that female fecundity is proportional
trait has profound effects on physiology, ecology, and life-history to body size, and selection will favor larger females (Koslowski,
traits in general. 1989; Zamudio, 1998; Cox et al., 2003). Together, these hypotheses
One particular pattern related to sexual size dimorphism (SSD) may identify sexual selection on male size and fecundity (natural)
is called Rensch’s rule where SSD is proposed to be more pro- selection on female size as important influences on size dimor-
nounced when males are the larger sex (hyperallometry; Fairbairn, phism. Finally, if resources such as space or prey are limited, the
1997), conversely when females are the larger sex SSD decreases niche segregation hypothesis (Pianka and Huey, 1978) predicts
with SVL (hypoallometry). Independently of its variation with body that size dimorphism may arise through competition avoidance,
size, several hypotheses have been proposed to explain the causes promoting a more efficient use of resources by the sexes (Perez-
Mellado and de la Riva, 1993; Zamudio, 1998). These hypotheses,
however, are not mutually exclusive. For example, SSD may result
∗ Corresponding author. Tel.: +54 381 4230056; fax: +54 381 4330868. from sexual selection, but can be modulated by ecological factors
E-mail addresses: mpaucab@yahoo.com, mpaucab17@gmail.com (M.P. Cabrera). (Shine, 1989).

0044-5231/$ – see front matter © 2012 Elsevier GmbH. All rights reserved.
http://dx.doi.org/10.1016/j.jcz.2012.08.003
 Author's personal copy

300 M.P. Cabrera et al. / Zoologischer Anzeiger 252 (2013) 299–306

Previous studies on lizards showed a mix of results in regard to Among Liolaemus lizards, sex is identified from the shape of
sexual size dimorphism. Studies on some lizard groups show that the cloacae (square shaped in males, rounded in females) and the
females are the grater sex, for example phrynosomatid lizards and presence of precloacal pores, which are always present in males,
dwarf chameleons (Zamudio, 1998; Stuart Fox, 2008). Conversely although females of some species also possess precloacal pores.
eublepharid geckos and varanids show a male biased dimorphism There is also strong sexual dichromatism in most Liolaemus lizard
(Kratochvíl and Frynta, 2002; Frýdlová and Frynta, 2010). Addition- species, thus we used these characters as diagnostic for sexing spec-
ally, two broader analyses of SSD using comparative data showed imens. After using the larger third of the samples for each species,
a majority of species with larger males (Fairbairn, 1997; Cox et al., we are confident that only adult specimens were considered (see
2003). Table 1). We based adult stages on previous studies on reproduc-
Besides sexual size dimorphism, several characteristics other tive biology of Liolaemus species (Ramírez Pinilla, 1989, 1991, 1994;
than SVL show variation between sexes, especially in male biased Cruz and Ramírez Pinilla, 1996; Martori and Aun, 1997; Aun and
sexually dimorphic taxa (Kratochvíl and Frynta, 2002) but also in Martori, 1998; Vega, 1999; Martori, 2005; Cánovas et al., 2006b;
female biased species (Tubaro and Bertelli, 2003). In the case of Valdecantos and Lobo, 2007; Cruz et al., 2011) and personal obser-
male biased species, dimorphic these traits (e.g., head size) may be vations.
used during male–male combat (Kratochvíl and Frynta, 2002) or Within each species we tested for differences between
signaling (Martins et al., 2004). Thus, shape dimorphism, or the sexes in the variables mentioned above by running t-tests or
allometric growth of some features (such as head size in males Mann–Whitney tests (depending on whether the data fulfilled
or axilla–groin distance in females) may rely on the hypotheses assumptions of normality and homoscedasticity). We also modified
underlying the causal factors driving sexual size dimorphism. our alpha levels using Bonferroni corrections to take into account
We here explore these issues for the Liolaemus laurenti species the effect of multiple testing.
group (L. darwinii clade + L. wiegmannii clade; Abdala, 2007; Lobo When examining data from phylogenetically related species,
et al., 2010). The L. laurenti group belongs to the series of L. boulen- data points cannot be considered as statistically independent due to
geri of the genus Liolaemus (Abdala, 2007). The L. laurenti, group shared evolutionary history (Felsenstein, 1985; Harvey and Pagel,
is composed of approximately 30 species (Lobo et al., 2010), of 1991). On the other hand, the importance of accounting for this evo-
which we studied 22. Because this group forms a monophyletic lutionary relatedness in comparative analyses depends partially if
clade (the L. laurenti group, sensu Abdala, 2007) and shares several they show evidence of significant phylogenetic signal (Blomberg
ecological characteristics, such as habitat use (most of them are ter- et al., 2003; Garland et al., 2005). For these reasons, we run inde-
restrial generalists or sand dwellers, Tulli et al., 2009), this allows pendent contrasts analyses and tested for phylogenetic signal by
us to explore sexual dimorphism and sexually dimorphic features using a total evidence phylogenetic tree for the studied species here
within a phylogenetic context. Liolaemus lizards as use several parts (after Abdala, 2007). Because the Abdala (2007) study corresponds
of their body for signaling as do many other iguanians (Martins to a larger sample of Liolaemus species, it does not provide branch
et al., 2004). For example head bobs and push-ups are a common lengths. Therefore, we used a composite tree topology and arbi-
part of their communication system (Martins et al., 2004). Thus, trarily set the branch lengths to unity as divergence times among
head shape and forelimb characteristics are particularly interesting the different species are unclear.
traits that may drive communication ability among these lizards. We tested for phylogenetic signal of SVL and other morpho-
Additionally, within this group of species, two reproductive modes logical features using a simple randomization test executed in the
are observed: six out of the 22 species are viviparous and the rest PHYSIG program (Blomberg et al., 2003). We calculated the K statis-
oviparous. Viviparity may lead to a larger distance between axilla tic (K = 0 no phylogenetic signal, K = 1 or higher indicate actual
and groin because for a viviparous species carrying full developed phylogenetic signal) to estimate the level of phylogenetic signal
embryos needs more space than in the case of oviparous species relative to Brownian motion evolution using the tree topology and
that lay smaller undeveloped eggs, in this sense we expect that the branch lengths (Blomberg et al., 2003). For this analysis, we used
abdominal cavity (expressed in the inter-limb length, ILL) should constant branch lengths and two different branch lengths transfor-
be larger in viviparous species. mations with an Ornstein-Uhlenbeck model of evolution. Each one
Our main questions are: (a) what is the phylogenetic signal of of these transformations represent the strength of stabilizing selec-
body size and other morphological features (head shape and fore tion, where a low value of OU transformation index (d = 0.2) turns
limb sections)?; (b) do Liolaemus lizards of the laurenti clade follow the data toward a more “adaptive” scenario, meanwhile a close to
the Rensch’s rule pattern?; (c) what hypotheses explain better the 1 OU transformation (d = 0.8) tend to Brownian motion (Blomberg
differences between sexes, fecundity advantage hypothesis or sex- et al., 2003). Thus, we set the d-value equal to 0.2, thus creating a
ual selection hypothesis? more star-like topology, and equal to 0.8, resulting in a more hier-
archical topology (Blomberg et al., 2003). In the case of snout-vent
length, we introduced this variable in PHYSIG after log10 trans-
2. Materials and methods formation. All other morphological traits (i.e. head measurements
and forelimb segments lengths) were size-corrected following the
Biometric variables used in the analysis, (taken with Vernier method in Blomberg et al. (2003). We calculated the K statistic to
calipers; Mitutoyo, to 0.02 mm) were as follows: snout-vent length quantify the level of phylogenetic signal relative to what is expected
(SVL), head length (HL) from end of rostral to anterior border of ear for a character undergoing Brownian motion evolution considering
opening, head width (HW) measured at the edge of the ear open- the current topology and branch lengths (Blomberg et al., 2003). A
ing, inter-limb length (ILL) the distance between axilla and groin, K-value equal to or greater than 1 indicates that the trait shows
humerus length (HuL), radius length (RL), and manus length (ML) an expected amount of phylogenetic signal among close relatives,
(Table 1). Because we compare the effect of body size of adult speci- conversely a K-value less than 1 indicates less phylogenetic signal
mens, we calculated the arithmetic average of the largest one-third than expected and possible selection or measurement error in the
of the total sample of SVL and body measurements to obtain an indi- broad sense (including errors in estimates of phenotypes, branch
cation of asymptotic size of the studied species (see Losos et al., lengths, and topology; Blomberg et al., 2003).
2003). We used museum specimens (Appendix 1) deposited in the We ran simple regressions of IC for SVL as a measurement of
Instituto de Herpetología of the Fundación Miguel Lillo, Tucumán, sexual size dimorphism following Fairbairn (1997) taking males
Argentina. as the independent variable. We also tested for the relationship
 Author's personal copy

M.P. Cabrera et al. / Zoologischer Anzeiger 252 (2013) 299–306 301

Table 1
Mean and maximum values (±SE) of body measurements from females (♀) and males (♂) of the studied species.

Sex Snout-vent length Head length Head width Inter-limb length

Mean Max ±SE Mean Max ±SE Mean Max ±SE Mean Max ±SE

L. abaucan ♀ 51.27 54.09 0.40 11.54 12.10 0.10 10.32 10.82 0.09 24.07 25.49 0.25
♂ 52.88 56.38 0.61 12.63 13.49 0.16 11.16 11.94 0.15 23.06 24.82 0.33
L. albiceps ♀ 69.52 71.22 1.43 14.88 15.47 0.30 13.13 13.64 0.23 33.78 35.24 0.83
♂ 79.32 81.45 2.18 17.77 18.18 0.44 16.42 16.85 0.51 35.55 35.84 1.03
L. calchaqui ♀ 56.96 59.02 0.94 12.02 12.05 0.14 9.89 9.75 0.26 26.83 28.46 0.69
♂ 51.92 55.16 1.58 12.02 12.77 0.35 9.88 10.54 0.25 21.51 22.42 0.36
L. chacoensis ♀ 45.90 49.91 0.42 10.16 10.56 0.06 7.44 7.69 0.05 21.65 24.28 0.29
♂ 42.98 46.58 0.33 10.22 10.84 0.07 7.50 7.90 0.05 18.49 20.22 0.20
L. crepuscularis ♀ 58.83 61.76 1.18 12.45 12.83 0.21 11.70 11.99 0.17 27.59 29.05 0.72
♂ 54.12 56.13 0.55 12.18 12.64 0.12 11.34 11.75 0.16 22.74 24.18 0.46
L. darwinii n ♀ 53.67 56.25 0.51 11.84 12.27 0.15 10.47 10.89 0.13 25.54 26.41 0.30
♂ 54.99 58.05 0.52 12.79 13.24 0.12 11.10 11.59 0.09 24.22 25.78 0.35
L. darwinii s ♀ 54.69 57.94 0.65 11.87 12.42 0.14 10.01 10.48 0.15 25.75 27.65 0.47
♂ 52.92 56.07 0.62 12.26 12.80 0.12 10.22 10.28 0.11 22.17 23.20 0.38
L. espinozai ♀ 55.16 60.82 0.85 11.94 12.89 0.16 10.37 11.11 0.15 26.44 29.85 0.54
♂ 53.69 58.95 0.77 12.71 13.94 0.20 10.77 11.71 0.16 23.72 26.97 0.48
L. grosseorum ♀ 49.38 51.47 0.45 11.30 11.63 0.20 8.54 8.96 0.16 23.65 25.26 0.45
♂ 50.56 53.38 0.63 11.72 13.08 0.29 9.22 9.33 0.16 22.42 23.60 0.38
L. irregularis ♀ 70.49 74.87 1.59 15.20 15.53 0.33 12.74 13.20 0.26 34.73 37.66 1.05
♂ 77.59 85.74 1.51 17.52 19.44 0.38 15.49 17.29 0.34 35.41 39.32 0.74
L. koslowskyi ♀ 56.35 60.39 0.57 12.31 12.76 0.19 10.50 11.31 0.13 27.29 30.68 0.76
♂ 60.25 66.30 0.89 14.16 16.34 0.34 12.08 12.98 0.16 27.62 29.74 0.39
L. laurenti ♀ 52.11 55.13 0.43 11.65 12.13 0.12 9.47 10.33 0.15 24.80 26.13 0.34
♂ 52.59 55.20 0.45 12.12 12.52 0.10 9.98 10.41 0.09 23.15 24.67 0.27
L. lavillai ♀ 57.20 59.59 0.56 12.24 12.73 0.13 10.84 11.01 0.12 27.62 28.85 0.36
♂ 59.20 61.49 0.44 13.43 13.88 0.13 11.92 12.35 0.12 26.10 27.29 0.35
L. multimaculatus ♀ 58.54 62.81 1.53 14.30 15.72 0.53 10.86 11.40 0.21 28.06 29.24 0.92
♂ 64.48 68.41 1.83 16.72 18.14 0.60 12.24 12.87 0.29 28.57 28.43 0.85
L. olongasta ♀ 50.40 57.13 2.50 10.72 11.28 0.35 8.20 9.29 0.36 19.21 – –
♂ 55.49 59.21 1.56 12.98 13.19 0.39 9.89 10.15 0.39 24.18 25.69 0.83
L. ornatus ♀ 62.36 65.29 0.46 13.00 13.45 0.09 11.68 11.87 0.09 30.44 32.46 0.48
♂ 65.40 65.40 0.73 14.52 14.52 0.18 12.96 12.96 0.12 28.84 28.84 0.38
L. quilmes ♀ 51.45 54.74 0.33 11.50 12.03 0.07 8.92 9.29 0.06 23.99 25.51 0.22
♂ 54.66 58.72 0.41 12.89 13.69 0.10 9.92 10.50 0.08 23.27 25.03 0.25
L. riojanus ♀ 48.73 51.43 1.07 12.53 12.09 0.26 9.63 9.71 0.15 23.89 27.01 1.04
♂ 50.91 56.73 1.61 13.32 14.51 0.40 10.05 10.80 0.25 23.03 25.67 0.90
L. salinicola ♀ 58.19 62.09 0.70 13.56 14.49 0.18 10.86 11.10 0.11 27.70 30.03 0.46
♂ 69.13 73.49 0.95 16.05 16.52 0.31 13.37 14.01 0.21 29.64 31.39 0.50
L. scapularis ♀ 55.03 58.55 0.63 12.89 13.36 0.14 10.97 11.59 0.19 26.23 27.75 0.59
♂ 63.81 68.53 0.77 15.61 16.69 0.22 12.76 13.96 0.26 28.14 29.91 0.49
L. uspallatensis ♀ 58.50 62.51 0.98 13.02 13.53 0.25 11.25 11.54 0.18 28.12 30.26 0.56
♂ 57.58 60.91 1.21 13.44 13.72 0.21 11.25 11.89 0.33 25.66 28.82 1.04
L. wiegmannii ♀ 48.68 51.38 0.77 12.73 13.13 0.17 9.10 9.18 0.13 25.04 25.77 0.57
♂ 48.07 53.23 1.48 13.40 14.74 0.40 9.23 10.03 0.26 23.17 24.71 0.68

Sex Humerus length Radius length Manus length

Mean Max ±SE Mean Max ±SE Mean Max ±SE

L. abaucan ♀ 5.27 5.75 0.10 6.70 7.02 0.05 8.93 8.97 0.07
♂ 5.54 6.07 0.12 7.02 7.39 0.10 9.05 9.39 0.13
L. albiceps ♀ 5.76 6.07 0.19 7.95 8.11 0.18 10.71 10.85 0.15
♂ 6.87 6.51 0.22 9.33 9.72 0.22 12.18 12.54 0.22
L. calchaqui ♀ 5.25 5.14 0.24 6.84 7.06 0.12 8.26 8.90 0.37
♂ 4.48 5.05 0.26 6.49 6.93 0.20 8.18 8.61 0.18
L. chacoensis ♀ 4.81 5.07 0.06 5.57 5.81 0.07 7.32 7.53 0.05
♂ 4.73 4.95 0.05 5.14 5.34 0.06 7.01 7.21 0.06
L. crepuscularis ♀ 5.27 5.17 0.22 6.81 7.00 0.15 8.20 8.47 0.21
♂ 4.99 5.27 0.10 6.68 6.89 0.09 8.17 8.29 0.11
L. darwinii n ♀ 5.14 5.34 0.11 6.90 7.09 0.10 7.92 7.95 0.12
♂ 5.46 5.62 0.10 6.94 7.10 0.11 8.21 8.38 0.10
L. darwinii s ♀ 5.27 5.81 0.14 6.97 7.11 0.09 8.32 8.31 0.11
♂ 5.05 5.17 0.10 6.93 7.13 0.11 8.25 8.47 0.12
L. espinozai ♀ 5.53 5.81 0.13 6.53 6.72 0.07 8.24 8.76 0.11
♂ 5.90 6.46 0.17 6.67 7.02 0.08 8.55 8.91 0.10
L. grosseorum ♀ 4.94 5.06 0.16 6.29 6.47 0.08 7.56 7.65 0.14
♂ 4.82 5.09 0.15 6.42 6.80 0.12 7.80 8.64 0.20
L. irregularis ♀ 6.52 6.57 0.18 8.51 8.66 0.24 11.31 11.01 0.48
♂ 7.01 7.33 0.27 9.67 10.34 0.16 12.49 12.85 0.17
L. koslowskyi ♀ 5.87 5.92 0.10 7.10 7.57 0.09 8.83 9.02 0.11
♂ 6.37 7.37 0.19 7.90 8.58 0.12 9.63 10.40 0.14
L. laurenti ♀ 5.61 5.77 0.13 6.66 7.08 0.11 7.97 8.28 0.10
♂ 5.46 5.62 0.10 6.80 6.98 0.07 7.94 8.11 0.08
L. lavillai ♀ 5.08 5.24 0.10 6.75 6.69 0.08 8.56 8.41 0.15
♂ 5.33 5.51 0.08 7.24 7.38 0.07 9.10 9.25 0.12
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302 M.P. Cabrera et al. / Zoologischer Anzeiger 252 (2013) 299–306

Table 1 (Continued )

Sex Humerus length Radius length Manus length

Mean Max ±SE Mean Max ±SE Mean Max ±SE

L. multimaculatus ♀ 8.18 8.15 0.53 6.12 6.49 0.43 7.88 7.47 0.30
♂ 8.19 8.78 0.39 6.81 8.23 0.46 9.50 9.65 0.34
L. olongasta ♀ 5.82 6.44 0.63 4.79 – – 7.56 – –
♂ 6.73 7.26 0.28 7.32 8.54 0.70 9.60 10.16 0.70
L. ornatus ♀ 5.11 5.25 0.09 7.56 7.65 0.06 8.77 8.82 0.09
♂ 5.57 5.57 0.07 8.22 8.22 0.08 9.49 9.49 0.10
L. quilmes ♀ 4.73 4.79 0.05 5.15 5.40 0.05 7.57 7.83 0.05
♂ 5.13 5.17 0.06 5.78 6.01 0.05 8.20 8.51 0.07
L. riojanus ♀ 6.08 6.64 0.26 5.31 4.89 0.22 7.33 6.41 0.47
♂ 6.21 6.52 0.27 5.57 5.57 0.26 7.54 7.72 0.29
L. salinicola ♀ 5.66 6.27 0.15 7.26 7.49 0.10 9.24 9.82 0.16
♂ 6.57 6.67 0.16 8.41 8.75 0.14 10.62 10.66 0.18
L. scapularis ♀ 5.47 5.70 0.13 6.71 7.15 0.13 8.70 9.11 0.12
♂ 6.62 6.82 0.22 7.97 8.38 0.11 10.15 11.01 0.23
L. uspallatensis ♀ 5.85 6.33 0.29 8.04 8.24 0.15 10.25 10.36 0.12
♂ 5.91 6.14 0.17 8.07 8.15 0.12 10.41 10.67 0.25
L. wiegmannii ♀ 6.22 5.93 0.21 6.41 6.23 0.27 7.58 8.32 0.26
♂ 5.55 5.36 0.22 6.06 6.33 0.17 7.70 8.01 0.20

between SSD and snout-vent length (SVL) of each sex. To test the independent contrasts (IC) for the log10 of every morpholog-
different hypotheses that may explain sexual size dimorphism, we ical trait measured. For calculating independent contrasts we
ran comparative regressions for the head, fore-limb and inter-limb used the PDAP 1.15 module (Midford et al., 2003) in Mesquite
measurements from each sex against the mean SVL of the largest 2.74 (Maddison and Maddison, 2010), all regressions were forced
one-third for each species. We used this traditional method for scal- through the origin (Garland et al., 1992). Particular attention was
ing to SVL; however, we are ware of the potential problems from paid to slope in order to determine deviation from isometry.
using SVL as predicting variable especially in the case of ILL since Liolaemus species of the L. laurenti group show different repro-
it was suggested to be an artifact of inappropriate scaling to a sex- ductive modes (some species are oviparous and some viviparous).
ually dimorphic trait (snout–vent length) (Kratochvíl et al., 2003). Cei et al. (2003) proposed that inter-limb length (ILL) may vary
We used conventional statistics and we also calculated indepen- in relationship to the space necessary for eggs or larger full term
dent contrasts, since the trait values of related species are linked in embryos to be carried in Liolaemus lizards. Thus, we ran a phylo-
a hierarchical fashion (Felsenstein, 1985) (Fig. 1). We calculated genetically based ANCOVA (PDANCOVA, Garland et al., 1993) with
log10 SVL as covariate, to investigate whether viviparous Liolaemus
species show larger inter-limb length (ILL) than oviparous ones
by using reproductive mode as the categorical variable. We also
obtained brood and clutch size from 12 species of Liolaemus from
the L. laurenti group (data from Ramírez Pinilla, 1991, 1994; Cruz
and Ramírez Pinilla, 1996; Martori and Aun, 1997; Martori, 2005
and specimens from FML collection dissected by the authors). Thus,
we evaluate if female ILL is an indicator of reproductive mode and
if number of future offspring is an indicator of the volume needed
for carrying eggs or embryos. In the case of phylogenetically based
ANOVA or ANCOVA, an empirical null distribution of F-statistics
was generated using PDSIMUL taking into account the phylogeny,
then analyzed with PDANOVA (Garland et al., 1993). We ran 1000
simulations using a speciational model of evolution that sets all
branch lengths equal to one.

3. Results

None of the K values obtained for the untransformed branch

length analysis were greater than one for any of the variables stud-
ied, including SVL (Table 2). However, LH and LR of males and
SSD of males showed significant results. Because branch length
may influence the degree of phylogenetic signal, we ran Ornstein-
Ulhlenbeck (OU) transformations. In the case of OU transformations
that mimick a star phylogeny like structure (d = 0.2), male humerus
and radius length showed K scores greater than 1 in our data set,
suggesting a trend for stabilizing selection in these features in males
but not females (Table 1). None of the variables showed K-values
greater than one for an OU transformation of 0.8. However, in the
case of randomization tests, humerus and radius lengths and SSD of
males showed significant P-values, indicating the presence of sim-
Fig. 1. Cladogram of Liolaemus laurenti group used in the analysis (after Abdala, ilarity among closely related species greater than what would be
2007). Branches in gray: species with females with SVL greater than males. expected by chance (Blomberg et al., 2003).
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Table 2 Table 4
Phylogenetic signal based on k values and simulations (P value). K values higher Regression of major axis (RMA) between Independent contrasts (IC) of snout-vent
than one or P values lower than 0.05 indicate the presence of phylogenetic signal. length (SVL) of males and females (males as predictive variable). Regressions were
run for all the 22 species in the L. laurenti group studied here (g.l. 20), for species
No transformation OU transformation where male are the larger sex (10 species, d.f. 8) and species female as the larger sex
d = 0.8 d = 0.2 (6 species, d.f. 4).
k value P k value P k value P Variable r2 Slope P
SVLf 0.203 0.987 0.383 0.958 0.867 0.679 All species SVL 0.846 0.631 <0.000
SVLm 0.245 0.962 0.454 0.927 0.876 0.641 Male biased SVL 0.971 0.786 <0.000
HLf 0.549 0.070 0.874 0.088 0.951 0.306 Female biased SVL 0.910 0.696 <0.009
HLm 0.483 0.412 0.734 0.673 0.846 0.785
HWf 0.224 0.890 0.413 0.897 0.871 0.638
HWm 0.351 0.316 0.629 0.32 0.871 0.690
ILLf 0.413 0.282 0.642 0.622 0.878 0.674 Table 5
iILLm 0.283 0.643 0.601 0.314 1.034 0.108 Regressions of log10 transformed body measurements versus log10 transformed SVL
LHf 0.345 0.467 0.693 0.243 1.001 0.193 from the species studied. We used raw data and independent contrasts, in the later
LHm 0.446 0.008 0.808 0.009 1.093 0.028 case the regression was forced through the origin.
LRf 0.286 0.628 0.540 0.559 0.931 0.409
Variable Raw data Independent contrasts
LRm 0.372 0.042 0.773 0.005 1.149 0.004
LMf 0.331 0.771 0.622 0.586 0.880 0.580 r2 Slope P r2 Slope P
LMm 0.347 0.834 0.647 0.888 0.728 0.599
HLf 0.74 0.673 <0.001 0.799 0.692 <0.001
Ssd vs f 0.503 0.094 0.765 0.257 0.908 0.531
HLm 0.774 0.978 <0.001 0.899 1.002 <0.001
Ssd vs m 0.554 0.043 0.819 0.176 0.886 0.671
HWf 0.772 0.969 <0.001 0.805 0.888 <0.001
HWm 0.934 1.367 <0.001 0.939 1.336 <0.001
ILLf 0.899 1.196 <0.001 0.935 1.002 <0.001
After comparison of body size and morphological variables IILLm 0.742 0.902 <0.001 0.804 0.986 <0.001
LHf 0.139 0.357 0.087 0.077 0.236 0.209
between males and females within each species, we observed sig-
LHm 0.365 0.725 0.003 0.286 0.525 0.011
nificant differences in several cases (Table 3). Among the 22 species LRf 0.475 0.788 <0.001 0.632 0.877 <0.001
studied, ten species showed to be male biased, five were signifi- LRm 0.811 1.138 <0.001 0.823 1.310 <0.001
cantly female biased species in SVL and seven species showed no LMf 0.709 0.803 <0.001 0.792 0.799 <0.001
LMm 0.837 1.103 <0.001 0.831 1.239 <0.001
significant different, although males were the larger sex in six of
them (Table 3). Additionally, across species in this group, males
tend to show larger HL, HW, HuL, RL and ML and females tend to
show a relatively larger ILL (Table 3). The analyses of the relationship of body parts between sexes
We observed a positive and significant relationship between after conventional as well as phylogenetically based analyses (IC)
male and female snout-vent length (males as determining factor) reveal that; limb sections (except for humerus length for females
in overall (Table 4). A positive relationship was also observed for after Bonferroni correction), head measurements and ILL were sig-
the 10 male-biased and the six female-biased species (Table 4). nificantly greater with SVL. Interestingly, HW, radius and manus
Additionally, our results show that IC SSD is positively related to length of males, and ILL of females, showed a slope greater than one
IC body size (r2 = 0.432; slope = 0.297; d.f. = 20; P < 0.009). Rensch’s (Table 5), supporting the hypothesis of allometry (all t-test values
rule pattern is not supported because the slope of these regression were higher than 7.52, P < 0.001 indicating differences from isome-
were lower than 1. Thus, This Liolaemus lizards show a significant try). The rest of the variables exhibit slopes lower than one (Table 5)
sexual size dimorphism among species, but Rensch’s rule pattern and therefore negative allometry presumption was observed for
is absent. these variables.

Table 3
Body size, body measurements, and sexual size dimorphism index (SDI, sensu Gobbons and Lovich, 1990) comparisons between sexes for each species. Boldface denotes
significant differences when males are larger than females, boldface and italics significant with females as the larger sex. t = t-test; U Mann–Whitney test.

Species SVL HL HW HuL RL ML ILL SDI

t or U P t or U P t or U P t or U P t or U P t or U P t or U P

L. abaucan t3.16 0.002 t6.29 0.000 t5.42 0.000 t0.39 0.696 t1.73 0.086 t0.356 0.722 t-6.4 0.000 0.0103
L. albiceps U11.00 0.008 U11.00 0.007 U14.50 0.020 U28.00 0.236 U13.00 0.014 U18.00 0.042 U15.50 0.025 0.0314
L. calchaqui U2.00 0.028 U2.00 0.028 U12.00 0.104 U4.00 0.075 U8.00 0.347 U10.50 0.676 U4.00 0.009−0.0168
L. chacoensis t-5.52 0.000 t6.12 0.000 t4.74 0.000 U35.00 0.491 t-2.07 0.039 U3204.50 0.109 t-7.16 0.000−0.0179
L. crepuscularis U8.00 0.002 U30.00 0.048 U44.00 0.118 U34.00 0.362 U39.50 0.634 U44.00 0.905 U2.00 0.000−0.0237
L. darwinii N t1.80 0.047 t4.72 0.000 t3.66 0.000 t1.66 0.102 t-0.45 0.653 t1.43 0.158 t-5.09 0.000 0.0078
L. darwinii S t1.96 0.049 t7.35 0.000 t2.12 0.039 t-0.16 0.869 t0.99 0.323 t-0.40 0.690 t-5.71 0.000−0.0081
L. espinozai t-1.44 0.153 t8.36 0.000 t6.93 0.000 t1.28 0.204 t2.99 0.003 t2.65 0.009 t-7.07 0.000−0.0076
L. grosseorum t 0.69 0.490 U68.00 0.174 t2.47 0.020 t0.28 0.778 t-1.08 0.289 t0.488 0.629 t0.59 0.001 0.0092
L. irregularis U27.00 0.022 t2.96 0.006 U20.00 0.007 U61.00 0.750 t2.71 0.012 t2.29 0.031 U18.00 0.005 0.0314
L. koslowskyi t2.02 0.047 t8.06 0.000 t8.06 0.000 t0.42 0.674 t3.92 0.000 t4.52 0.000 U103.00 0.000 0.0227
L. laurenti t0.79 0.427 t7.13 0.000 t1.52 0.133 t-0.42 0.672 t0.09 0.928 t-0.18 0.850 U118.00 0.000 0.0002
L. lavillai t2.82 0.007 U51.00 0.000 U60.00 0.000 t0.97 0.335 t2.98 0.004 t2.84 0.007 t-6.01 0.000 0.0076
L. multimaculatus t5.94 0.038 t2.81 0.015 t1.38 0.004 t1.10 0.987 t1.06 0.313 t3.33 0.005 t0.51 0.697 0.0088
L. ornatus U206.00 0.000 U105.00 0.000 t6.35 0.000 t2.52 0.014 t4.33 0.000 t3.67 0.000 t-6.39 0.000−0.0063
L. olongasta t1.72 0.40 t4.27 0.001 t1.98 0.023 t1.48 0.183 0.0004
L. quilmes t6.04 0.000 t9.22 0.000 t6.73 0.000 t3.19 0.001 t5.83 0.000 U2503.00 0.000 t-8.42 0.000 0.0175
L. riojanus t1.06 0.303 t1.55 0.141 t1.34 0.199 t0.35 0.731 t0.73 0.475 t0.39 0.698 t0.69 0.537 0.0206
L. salinicola t9.26 0.000 U21.50 0.004 U4.00 0.000 t-0.66 0.507 t0.98 0.330 U9.00 0.000 t3.54 0.001 0.0248
L. scapularis t8.42 0.000 t2.54 0.014 t0.95 0.345 t0.22 0.826 t1.19 0.239 U287.00 0.473 t2.96 0.004 0.0408
L. uspallatensis U38.00 0.963 U67.00 0.000 U34.00 0.683 U25.00 0.221 U35.50 0.785 U34.00 0.683 U10.00 0.009 0.0386
L. wiegmannii t0.39 0.695 U40.00 0.229 t0.49 0.629 t2.34 0.045 t0.99 0.334 t0.34 0.736 t0.21 0.049 0.0089
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304 M.P. Cabrera et al. / Zoologischer Anzeiger 252 (2013) 299–306

Table 6 expectations of hyperallometry in SVL based on the differences

Phylogenetically informed analysis of variance (ANOVA), and phylogenetically
found in some species of Liolaemus lizards (Villavicencio et al., 2003;
informed analysis of covariance (ANCOVA, SVL as covariate) comparing oviparous
and viviparous species within the L. laurenti clade. Cánovas et al., 2006a; Laspiur et al., 2006; Laspiur and Acosta, 2007)
our results do not support this hypothesis. Noticeably, one seminal
Analysis Variable F(20;1) P
paper on Rensch’s rule (Fairbairn, 1997) mentions that male biased
ANOVA SVLf 24.35 0.263 iguanian lizards show a lower than one slope when testing allom-
ANOVA SVLm 24.40 0.502 etry in accordance with our results for SVL. These results indicate
ANOVA SSD 23.13 0.779
the need of further and deeper analyses on the role of body size in
ANCOVA ILLf 124.99 0.899
ANCOVA ILLm 93.50 0.979 iguanian lizards, since there is at least one entire group that shows
female biased dimorphism (Phrynosoma; Zamudio, 1998).
SVL: snout-vent length; SSD: sexual size dimorphism; ILL: inter-limb length; f:
females; m: males. Ecological and evolutionary implications may be important for
snout-vent length (e.g., metabolism, predator–prey interactions,
mate choice, male–male interactions, fecundity) and therefore
The analysis testing for the potential differences between may have an effect on sexual size dimorphism. Interestingly, and
oviparous and viviparous species of the L. laurenti species group despite of being the second most speciose genus in the world, Lio-
showed no significant differences after phylogenetically informed laemus show quite simple assembly compositions (Videla, 1983;
ANOVAS/ANCOVAS for SVL, SSD or ILL (reproductive mode as Vega and Bellagamba, 1990; Vega, 1993; Schulte et al., 2004),
response variable, Table 6). Additionally, there was no relation- probably as a consequence of low levels of habitat structuring
ship between IC of clutch or brood size and IC of log10 ILL for the and limited resource availability (which may affect some aspects
twelve species for which we have complete data (r2 = 0.22; d.f. 11; such as growth). These latter aspects may be important selective
P = 0.102). pressures for small body size in Liolaemini lizards (Espinoza et al.,
2004). If this is the case, it is possible that the limitations imposed by
4. Discussion small body size have implications on other aspects of life-history,
for example sexual size dimorphism. The evolution of SVL in Lio-
Tests for phylogenetic signal generally confirm the relevance of laemini (SVL ranges from 40 to 105 mm) appears thus less variable
taking into account phylogenetic structure and branch lengths in compared to other lizard taxa, such as the tropical genera Ano-
comparative analyses (Blomberg et al., 2003). Our results showed lis (Losos, 2009; Thomas et al., 2009) as well as Varanus lizards
that for all variables, K statistic values were lower than one and gen- (Frýdlová and Frynta, 2010; Collar et al., 2011), both showing a wide
erally non significant. Interestingly, K values lower than one seem range of body sizes and a different SSD evolution.
to be a common aspect in analyses that include Liolaemini lizards Most morphological traits correlated positively with SVL in
(Vanhooydonck et al., 2010; Tulli et al., 2011, this study), similar males and females; however, only some of them showed allomet-
to what was observed by Kohlsdorf et al. (2008) for tropidurine ric slopes (head length and width, radius length and manus length,
lizards. Apparently, morphology is generally evolutionarily labile in Table 5) and particularly these allometric variables were only
these two Neotropical clades. Nonetheless, some analyses indicate observed for the males of the Liolaemus laurenti clade. Theoretically,
that phylogenetic signal is not always absent in Liolaemini lizards two important functions have been attributed to favor allome-
(for example, Tulli et al., 2009, 2012). It is possible that the scant try of head size: ecological segregation in diet (Schoener, 1971;
SVL variation within each one of the two subclades in the L. laurenti Camilleri and Shine, 1990; Shine, 1991; Perez-Mellado and de la
group (Fig. 1; Abdala, 2007) may influence the results of the present Riva, 1993) and sexual selection involving male–male interactions
study. Interestingly, after branch length manipulation, we observed (male contest competition; Kratochvíl and Frynta, 2002; Reaney
that as OU transformations ‘d’ values decrease from untransformed and Whiting, 2002). Additional evidence leads us to suggest sexual
(d = 1) to d = 0.8 and then to d = 0.2, the phylogenetic signal becomes selection in Liolaemus head and distal limb dimensions, head-bobs
higher than one in several traits (ILL of males, LH of males and and push-ups displays (Martins et al., 2004) and male–male inter-
females and finally RL of males, but only limb sections of males actions, although these remain poorly documented (Kozykariski,
were significant). This pattern indicates that it is likely stabilizing 2010). Additionally, studies on the home range of some Liolae-
selection in these features. Nevertheless, we have to be cautious mus species indicate that males show some hierarchic structure
because the sample size is 22 species, and sample size problems according to the size of their home range (Frutos and Belver, 2007;
may still exist in this kind of analysis (Blomberg et al., 2003). Robles and Halloy, 2009), suggesting male–male interactions and
Our results for sexual dimorphism and sexual size dimorphism therefore evidence of sexual selection. Finally, our results are con-
index (SDI, sensu Gibbons and Lovich, 1990; Table 2) indicate that cordant with Vanhooydonck et al. (2010) who also suggested that
in overall, males are larger than females. From individual species head shape and bite force in males of Liolaemus species are more
16 of the 22 species showed larger males, but only ten showed sig- related to sexual selection than to natural selection. In a previ-
nificant differences. Females are the larger sex in six of the species, ous study, Cei et al. (2003) suggested that the distance between
but only five are significantly larger than males. Previous studies fore and hind legs (ILL) is related and viviparous species should
of sexual size dimorphism in lizards show both cases, female as have larger ILL. Our results show that females are highly dimorphic
well as male-biased groups of species (e.g., Phrynosoma Zamudio, in ILL suggesting support for the fecundity advantage hypothesis
1998; geckos Kratochvíl and Frynta, 2002; dwarf chameleons Stuart (Fairbairn, 1997). However, we found no differences in SVL nor in
Fox, 2008; varanids Frýdlová and Frynta, 2010). A broader analysis ILL between oviparous and viviparous species within the L. laurenti
of SSD in near of 500 species indicates that sexual size dimor- clade. Additionally, there was not positive relationship between ILL
phism is a common feature in this group of animals (Cox et al., and fecundity (number of eggs or embryos) in this group of lizards
2003). With regard to macroevolutionary pattern called Rensch’s either. It is important to notice that these variables do not fully
rule (defined as the increase of SSD with SVL in male-biales species represent fecundity. For example, few fully developed embryos
or the decrease of SSD with SVL in female biased species; Fairbairn, may need more space and maternal investment than many early
1997; Stuart Fox, 2008), the literature show mixed results in lizards. developing eggs.
For example, some species show no relationship between SSD Liolaemus are highly conservative in some attributes (morphol-
and SVL (Zamudio, 1998), while others do (Kratochvíl and Frynta, ogy, Tulli et al., 2009, 2011; metabolic rate, Cruz et al., 2011) and
2002; Stuart Fox, 2008; Frýdlová and Frynta, 2010). Despite our less conservative in some others (bite force, Vanhooydonck et al.,
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M.P. Cabrera et al. / Zoologischer Anzeiger 252 (2013) 299–306 305

2010; clinging ability, Tulli et al., 2011). In our study, Liolaemus Garland Jr., T., Harvey, P.H., Ives, A.R., 1992. Procedures for the analysis of com-
lizards showed a phylogenetically variable morphology and offered parative data using phylogenetic independent contrasts. Systematic Biology 41,
18–32.
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limb (radius and manus lengths) dimensions based on the observed of covariance by computer simulation. Systematic Biology 42, 265–292.
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parative physiology. Journal of Experimental Biology 208, 3015–3035.
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et al., 2004), this probably constrained body size evolution and slider turtle (Trachemys scripta). Herpetological Monographs 4, 1–29.
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Acknowledgments Biology 21, 647–917.
Koslowski, J., 1989. Sexual size dimorphism: a life history perspective. Oikos 54,
A. Herrel and R. Cox helped with their comments on early ver- 253–256.
Kozykariski, M., 2010. Organización social y dispersión en reptiles patagónicos: eval-
sions of the manuscript. Two anonymous reviewers and the Editor uando los efectos de la filogenia y el ambiente. Unpublished Doctoral Thesis,
contributed with their corrections. C. Abdala generously gave his Universidad Nacional de Córdoba, Argentina.
comments and allowed us to use the cladogram of Liolaemus lau- Kratochvíl, L., Frynta, D., 2002. Body size, male combat and the evolution of sex-
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01205 (to FBC) and PIP 5780 (to EOL and GJS). Kratochvíl, L., Fokt, Rehák, I., Frynta, D., 2003. Misinterpretation of character scaling:
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