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Keywords:

  • Norops;
  • Anolis;
  • ecomorphs;
  • skeleton;
  • pectoral girdle;
  • shape analysis;
  • locomotion

ABSTRACT

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGEMENTS
  8. LITERATURE CITED

The breast-shoulder apparatus (BSA) is a structurally and kinematically complex region of lizards. Compared with the pelvic region it has received little attention, even though its morphological variation is known to be extensive. This variability has seldom been the focus of functional explanation, possibly because the BSA has been difficult to explore as a composite entity. In this study we apply geometric morphometric techniques to the analysis of the BSA in an attempt to more fully understand its configuration in relation to differential use in locomotion. Our approach centers upon the Jamaican radiation of anoline lizards (genus Norops) as a tractable, small monophyletic assemblage consisting of species representing several ecomorphs. We hypothesized that the different species and ecomorphs would exhibit variation in the configuration of the BSA. Our findings indicate that this is so, and is expressed in the component parts of the BSA, although it is subtle except for Norops valencienni (twig ecomorph), which differs greatly in morphology (and behavior) from its island congeners. We further found similarities in the BSA of N. grahami, N. opalinus (both trunk-crown ecomorphs), and N. garmani (crown giant). These outcomes are promising for associating morphology with ecomorphological specialization and for furthering our understanding of the adaptive response of the BSA to demands on the locomotor system. Anat Rec, 297:410–432, 2014. © 2014 Wiley Periodicals, Inc.


INTRODUCTION

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGEMENTS
  8. LITERATURE CITED

Locomotor forces of terrestrial tetrapods are transmitted from the limbs to the axial skeleton via the limb girdles. Evolutionary transformations that took place in the transition from the aquatic to the terrestrial environment (Clack, 2002) resulted in a segregation of the pectoral girdle from a firm association with the axial skeleton via dermal bones, to one which is less direct and mediated by the ribs, the newly-emergent sternum, and a system of ligaments (Russell and Bauer, 2008). The reverse happened in the pelvic region, whereby the once skeletally isolated pelvic girdle attained direct connection with the vertebral column via the sacroiliac articulation. Kinematically, therefore, the shoulder-region of tetrapods is more complex than the hip region.

Most studies of the limb kinematics of tetrapods have focused on the hindlimb (salamanders—Ashley-Ross, 1992; Ijspeert et al., 2005; crocodylians—Gatesy, 1991; Reilly and Elias, 1998; Hutchinson and Gatesy, 2000; Kubo and Ozaki, 2009; lizards—Reilly, 1995, 1998; Reilly and Delancey, 1997a, 1997b; Irschick and Jayne, 1999; Kubo and Ozaki, 2009; chelonians—Butcher and Blob, 2008; Wyneken et al., 2008; birds—Santi, 1990; Gatesy and Middleton, 1997; Hutchinson, 2004; mammals—Channon et al., 2010). Kinematic investigations of the forelimb, especially those incorporating a consideration of the shoulder region, are less numerous, except for the cases of birds (Goslow et al., 1989; Poore et al., 1997) and brachiating primates (Eaton, 1944; Schmidt et al., 2002; Wright-Fitzgerald et al., 2010), in which the pectoral limbs generate all, or the majority of, the propulsive forces. Analyses of pectoral kinematics have been conducted for some lizards (Renous and Gasc, 1977; Jenkins and Goslow, 1983; Peterson, 1984) and mammals (Jenkins, 1971; Klima et al., 1980; Hermanson and Altenbach, 1983; Högfors et al., 1987), but remain almost unexplored for salamanders and crocodylians (Jenkins, 1993).

As long ago as 1888 Max Fürbringer recognized the fundamental differences that exist in the anatomical arrangement of the pectoral and pelvic region (Fig. 1), and set forth the concept of the breast-shoulder apparatus (BSA) to accommodate the mobile relationships and indirect linkages between the composite (dermal and replacement bone origins) skeleton of the shoulder girdle and the axial skeleton. In its entirety, the BSA also includes the muscles and ligaments that respectively induce and control the displacement of the skeletal components that include the ribs, sternum and vertebral column. Fürbringer's (1888, 1900) considerations were almost purely descriptive.

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Figure 1. Left and anterior views of the generalized morphology of the breast-shoulder apparatus of lizards, and a similar conceptualization of the pelvic region. The number and type of joints that are found between the skeletal elements allow for different degrees of mobility between the axial skeleton and the stylopodium, depending on limb position. In the hindlimb, the acetabulum is solely associated with the mobility possible between the axial skeleton and the stylopodium (femur). In the forelimb the frame carrying the stylopodium (humerus) is able to move on the body wall anteroposteriorly and dorsoventrally, and also potentially mediolaterally in cases in which the orientation and shape of the coracosternal articulation permits this, with the coracoid translating along an obliquely-oriented articulation. (After Fürbringer, 1900; Vickaryous and Hall, 2006)

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Subsequently other authors explored the BSA in terms of its functional attributes (Skinner, 1959; Renous and Gasc, 1977; Russell and Bauer 2008), but its kinematics, other than in birds and mammals (Goslow et al., 1989; Poore et al., 1997; Jenkins, 1971; Klima et al., 1980; Hermanson and Altenbach, 1983; Högfors et al., 1987), have remained largely uninvestigated. Relative displacements in this region are more difficult to study than are those in the pelvic region, and morphological variation between taxa can be quite considerable, although the functional implications of that variation remain largely unknown (see Russell and Bauer, 2008, for a review).

The variation in the configuration of the BSA of lizards (Fürbringer, 1900; Russell and Bauer, 2008) invites further functional investigation, but qualitative descriptions of the region provide limited means of interpreting the differences that are evident. Assessment of the integrative locomotor morphology and kinematics of the BSA will benefit from a more synthetic understanding of the variability of form and configuration within and between its contributory elements.

Here we describe the variability in the morphology of the BSA in situ, employing computed tomography (CT) and geometric morphometric techniques to examine its structural components. We confine this exploratory study to a small radiation of lizards (Fig. 2, Jamaican members of the genus Norops, part of the anoline radiation, Alföldi et al., 2011; Nicholson et al., 2012) whose ecology is well understood.

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Figure 2. Phylogenetic relationships and ecomorph designations of the five Jamaican anole species. Phylogenetic hypothesis after Nicholson et al. (2012) and Alföldi et al. (2011).

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The species examined are the trunk-ground Norops lineatopus; the twig-giant N. valencienni; the trunk-crown N. grahami; the crown giant N. garmani; and the trunk-crown dwarf N. opalinus. Although the Jamaican anoles examined in this study are very closely related (Alföldi et al., 2011; Nicholson et al., 2012), they differ in their geographic distribution (Barbour, 1922; Underwood and Williams, 1959; Schoener and Schoener, 1971; Crombie et al., 1984), microhabitat preference and use (Lazell, 1966; Rand, 1967; Schoener and Schoener, 1971; Williams, 1983; Bundy et al., 1987; Landwer et al., 1995; Langerhans et al., 2006; Butler, 2007; Singhal et al., 2007), frequency and speed of locomotor movements (Hicks and Trivers, 1983; Losos, 1990a,b,c), jumping performance (Losos, 1990a; Toro et al., 2004), competition with congeners (Jenssen, 1973; Schoener, 1975), sexual interactions (Lynn and Grant, 1940; Jenssen, 1977; Lailvaux and Irschick, 2007), expression of sexual dimorphism (Jenssen and Nunez, 1994; Butler et al., 2000; Butler and Losos, 2002; Losos et al., 2003; Butler, 2007), feeding habits (Floyd and Jenssen, 1983), and external morphology (Lazell, 1966; Irschick et al., 1997; Langerhans et al., 2006; Kolbe et al., 2011). Much of the morphological variation that is correlated with sexual dimorphism and/or ecomorph designation is related to relative lengths of the pectoral limbs and elements thereof (Losos, 1990c; Powell and Russell, 1991; Irschick et al., 1997; Toro et al., 2004; Langerhans et al., 2006; Kolbe et al., 2011).

Studies exploring the morphological differences of skeletal elements of anoline ecomorphs are not abundant (Butler and Losos, 2002; Herrel et al., 2007b; Sanger et al., 2011), meaning that relationships, if any, between ecomorph designation and skeletal anatomy remain relatively unknown. Here we raise the question whether species identity or ecomorph designation are associable with skeletal features, and choose the BSA complex as a vehicle to explore that question. We do so because of the great variability shown by the BSA in lizards (Lécuru, 1968a,b; Russell and Bauer, 2008), and because the BSA is likely to be influenced by locomotor and social signalling adaptations that characterize anole species within circumscribed radiations (Beuttell and Losos, 1999; Butler and Losos, 2002; Herrel et al., 2007a).

Powell and Russell (1991) examined several external attributes of a subset of the Jamaican anole radiation, and found that the features measured (limb length, scansor area, and intergirdle distance, among others) differed among the ecomorphs investigated, and that these differences were evident throughout ontogeny. This indicated that dimensional differences among anoline ecomorphs are not simply a function of body size alone, but are characteristic of the species throughout their life spans (Losos, 1990c; Irschick et al., 1997; Losos, 2009; Kolbe et al., 2011).

Here we examine skeletal features of five anole species representing four distinctive ecomorphs (trunk-ground, trunk-crown, crown giant, twig giant, Fig. 2) that exploit different parts of the locomotor resource space and that may be expected to exhibit distinctive, but subtle, differences in locomotor mechanics. We investigate whether these are reflected in the three-dimensional configuration of the BSA. Here we pose the following questions:

  1. How much qualitatively and quantitatively observable variation exists in the morphology of the BSA of these Jamaican anoline species, and can that be expressed as observable differences between ecomorphs?
  2. Can species-specific differences of this structural complex be correlated with habitat preferences?

MATERIALS AND METHODS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGEMENTS
  8. LITERATURE CITED

We firstly provide qualitative descriptions of the BSA, and place these into a comparative framework by employing the detailed descriptions of the BSA of Iguana iguana (Iguanidae) provided by Russell and Bauer (2008). We compare this to the morphology of the BSA of Cophosaurus texanus (Phrynosomatidae). The form of the BSA in the latter is similar to that of I. iguana, whereas its absolute size is comparable to that of Norops (Fig. 3). It was, therefore, employed as a test for the resolution attainable via CT scanning for the skeletal features that have been established for the BSA of I. iguana.

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Figure 3. Boxplot showing the size range and number of specimens by sex, and ecomorph designation of each species examined in this study. Sexes could not be determined for all specimens of Cophosaurus texanus.

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We then provide a comparative summary of the form of the elements of C. texanus and Norops lineatopus, the latter representing a relatively basal branch in the phylogeny of Jamaican anoles (Fig. 2), using scanned renditions of each. Employing N. lineatopus as a baseline, we then summarize qualitative variation in the morphology of the elements of the BSA of all Jamaican Norops examined. Finally, we present an integrative summary of the variation observed in the skeletal components of the BSA among Jamaican anoles. That summary then serves as the basis for comparison with the findings of our geometric morphometric analysis of the BSA of the same taxa (and the same specimens). The phylogeny of the Jamaican anoles is still disputed (Nicholson et al., 2012; Poe, 2013; Castañeda and de Queiroz, 2013), and we, therefore, assess our data in the light of two recent phylogenetic hypotheses (Fig. 2; Alföldi et al., 2011; Nicholson et al., 2012).

Our qualitative and geometric morphometric comparison is based on the following taxa: Cophosaurus texanus (11 specimens), Norops lineatopus (31), N. valencienni (6), N. grahami (14), N. garmani (4), and N. opalinus (12). C. texanus was not included in the geometric morphometric analyses, and serves only as a qualitative baseline for the CT renditions. The description of I. iguana (Russell and Bauer, 2008) is used here in lieu of a generalized lizard to provide a qualitatively comparative framework. C. texanus is similar in size to Norops (Fig. 3), and the respective specimens can be subjected to the same radiographic scanning procedures as the latter. However, its BSA is structurally very similar to that of I. iguana, and we therefore use C. texanus to relate the thorough description of I. iguana to our analysis of Jamaican Norops.

To obtain three-dimensional renditions of the BSA of each species of Norops examined, and of Cophosaurus texanus, each specimen was scanned using a Skyscan microCT. All skeletal elements of the BSA were volumized using vsg Avizo® 6.3.1 (VSG, Visualization Sciences Group, Burlington, MA). The resulting renditions (Bruker, Billerica, MA) were used for the qualitative descriptions of all skeletal elements of the BSA, and the configured renditions were exported as obj-files. Since every scan was performed on an intact specimen, the renditions represent the in situ configuration of the skeletal components of the BSA.

All bone models were imported into Autodesk Maya® (Autodesk GmbH, Munich, Germany), within which each element can be moved independently of all others. To obtain a uniform position of elements of the BSA we employed the standardized pectoral limb configuration set out by Russell and Bauer (2008). In order to obtain that position the scapulocoracoid was shifted in the scapulocoracoid groove of the presternum in thirty-three of the 67 Norops specimens. Forty-three three-dimensional landmarks were then placed on the rendition of the BSA of each specimen, as listed in Table 1. However, a realignment as outlined above cannot guarantee unambiguous standardization of all skeletal elements, especially those related to the highly deformable rib cage. The landmark data were, thus, split into four subsets for further analysis: the vertebrae; presternum-interclavicle moiety; clavicle; and scapulocoracoid (Table 2).

Table 1. Location and type of landmarks used in this study
Landmark #LocationType
  1. All landmarks of bilaterally symmetrical elements were placed on the left side.

1Posterodorsal edge of neural canal of the first thoracic vertebraII
2Posterodorsal edge of neural canal of the third thoracic vertebraII
3Posterodorsal edge of neural canal of the fifth thoracic vertebraII
4Posterodorsal edge of neural canal of the sixth cervical vertebraII
5Posterodorsal edge of neural canal of the fourth cervical vertebraII
6Articulatory point between the vertebral column and the dorsal extremity of the first sternal ribII
7Juncture between the dorsal and ventral portion of the first sternal ribII
8Articulatory point between the first sternal rib and the sternumII
9Articulatory point between the vertebral column and the dorsal extremity of the second sternal ribII
10Juncture between the dorsal and ventral portion of the second sternal ribII
11Articulatory point between the second sternal rib and the sternumII
12Articulatory point between the vertebral column and the dorsal extremity of the third sternal ribII
13Juncture between the dorsal and ventral portion of the third sternal ribII
14Articulatory point between the third sternal rib and the sternumII
15Posteromedial extremity of the presternumII
16Anteromedial extremity of the presternumII
17Lateral extremity of the presternum at the posterior edge of the dorsal lip of the coracosternal grooveII
18Posterior-most contact point between the sternum and the interclavicleI
19Posterior-most extremity of the epicoracoidII
20Medial extremity of the epicoracoid at the medial contact with the dorsal lip of the coracosternal grooveII
21Anteromedial extremity of the epicoracoidII
22Dorsal anterior extremity of the first coracoid ray at its point of contact with the epicoracoidI
23Dorsal anterior extremity of the second coracoid ray at its point of contact with the epicoracoidI
24Medial extremity of the coracoid at its point of contact with the epicoracoidII
25Posterior extremity of the coracoid at its point of contact with the epicoracoidII
26Posterior extremity of the coracoid foramenII
27Ventral extremity of the inferior glenoid buttressII
28Anterior extremity of the glenoid fossa at the point of contact between the coracoid and scapulaII
29Dorsal extremity of the superior glenoid buttressII
30Ventroanterior extremity of the scapular ray at its point of contact with the epicoracoidII
31Anterior-most point of contact between the suprascapula and the scapulaI
32Posterior-most point of contact between the suprascapula and the scapulaI
33Dorsoposterior-most contact between the clavicle and the scapulocoracoid of the acromion regionII
34Anterior-most extremity of the suprascapulaII
35Dorsomedial extremity of the suprascapulaII
36Most posterior extremity of the suprascapulaII
37Lateral extremity of the lateral process of the interclavicleII
38Anteroventral-most extremity of the interclavicleII
39Posterior-most extremity of the articulation between the interclavicle and clavicleI
40Position of the lateral apex of the primary curvature of the clavicleIII
41Posterior extremity of the primary coracoid fenestraIII
42Ventroposterior extremity of the scapulocoracoid fenestraIII
43Dorsal extremity of the dorsolateral process of the presternumII
Table 2. Contribution of the various landmarks examined in this study to specific data subsets analyzed
LandmarksData setTotal no. landmarks
1–6, 9, 12Vetebrae8
8, 11, 14–18, 37, 38, 43Presternum-interclavicle moiety10
33, 39, 40Clavicle3
19–36, 41, 42Scapulocoracoid19

Landmarks were assembled in a Microsoft® Excel® worksheet, exported as txt-files, and analyzed using MorphoJ 1.02e (Klingenberg, 2011). All landmark sets were standardized using Procrustes superimposition (aligned by principal axis) and the covariance matrix was calculated directly from the Procrustes coordinates. Our principal component analyses (PCA) employ the covariance matrix.

Using PAST 2.17b, a broken-stick model was applied to the PCs of each data set to determine the number of PCs to be analyzed. The relevant PC scores for all data subsets were pooled, together with centroid size, logarithmic centroid size and snout-vent length (SVL). In order to test how well log-transformed centroid size (logCS) approximates body size, we employed “SPSS” 9.0.1 (IBM Corporation, Armonk, NY) to calculate Pearson's correlation coefficient with two-sided significance between logCS and logSVL. In order to test whether the data covary with size, we then computed a regression of the Procrustes raw coordinates against log-transformed centroid size using MorphoJ.

Using MorphoJ we performed a discriminant function analysis (DF) of the Procrustes coordinates to visualize the shape changes (in all four data sets) between (i) male and female individuals of N. lineatopus, and (ii) between N. lineatopus and every other species of Norops examined. Leave-one-out cross validation was performed via MorphoJ to test for discrimination between male and female representatives of N. lineatopus.

A canonical variate analysis (CVA) of the principal components was performed using “SPSS” 9.0.1, and was used to assess the distinctiveness of groups as they are defined by (i) species and (ii) ecomorph. The sample sizes per species and ecomorph correspond to the numbers provided in Fig. 3. PAST 2.17b was used to visualize the shape changes from N. lineatopus to the target Norops species as thin plate spline transformation grids (Hammer et al., 2001).

Employing the phylogenetic hypotheses of Alföldi et al. (2011) and Nicholson et al. (2012), we performed a permutation test against the null hypothesis of no phylogenetic signal in the principal component data via MorphoJ. This calculates an average shape for every species, and using 10,000 permutations reassigns each species to a different terminal node of the phylogeny, thus testing the hypothesis that the distribution of these average shapes in morphospace arose in correlation with the phylogenetic relationship between these species (Klingenberg and Gidaszewski, 2010).

RESULTS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGEMENTS
  8. LITERATURE CITED

Qualitative Comparison

Vertebral column and ribcage
Iguana iguana and Cophosaurus texanus

Both species exhibit the same gross vertebral structure. Posterior to the atlas and axis are five additional cervical vertebrae. Vertebrae 6 and 7 carry cervical ribs that wrap around the body cavity, but terminate freely some distance from the presternal plate. The eighth vertebra in the complete series is the first of the thoracics (Fig. 5a), and there are five thoracic vertebrae in total. The articulatory facet for the first sternal rib is borne laterally on the anterior third of the vertebral centrum. The first three thoracic ribs connect with the presternum, whereas the next two ribs in the anteroposterior series connect with the mesosternum.

Cophosaurus texanus and Norops lineatopus

The vertebral column of N. lineatopus is qualitatively indistinguishable from that of C. texanus (Fig. 5a).

Variation among Jamaican Norops

The vertebral column of N. lineatopus is qualitatively indistinguishable from that of all other species of Norops examined (Fig. 5a).

Presternum
Iguana iguana and Cophosaurus texanus

The presternum is a depressed, rhomboidal structure. The posterior half of the presternal plate bears articulatory facets for three sternal ribs. The demarcation between the presternum and mesosternum is clear cut. The coracoid articulates with the coracosternal groove that spans the anterolateral face of the presternum (Figs. 4 and 6). In C. texanus the dorsal lip of this sulcus does not extend to the anterior extremity of the presternal plate, although it does in I. iguana. The presternum of C. texanus bears a short but prominent lateral process that extends from the posterior extremity of the dorsal lip of the sulcus. I. iguana lacks such a process.

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Figure 4. CT reconstruction of the breast-shoulder apparatus of Norops lineatopus. (a) Ventrolateral view with the scapulocoracoid in unadjusted (unrotated) position. (b–d) Configuration following rotation of the scapulocoracoid into the standardized position (see text for details) and showing the position of the 43 landmarks (Table 1) used in the geometric morphometric analyses. (b) Ventrolateral view, (c) anterior view, (d) dorsolateral view.

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Figure 5. CT reconstructions of the components of the breast-shoulder apparatus of Cophosaurus texanus (far left column) and all five species of Norops examined in this study. Each species of Norops examined is represented by a column of reconstructions, in the sequence N. lineatopus, N. valencienni, N. grahami, N. garmani, and N. opalinus. Elements are represented as follows: (a) vertebral column in lateral view, (b) presternum in dorsal view, (c) interclavicle in dorsal view, (d) clavicle in anterolateral view, (e) scapulocoracoid in lateral view, (f) scapulocoracoid in posterior view.

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Figure 6. CT reconstruction of the left scapulocoracoid of Cophosaurus texanus in (a) lateral and (b) ventral view, showing the anatomical features of this element (nomenclature after Russell and Bauer, 2008). (c) Interclavicle of Cophosaurus texanus and (d) Norops lineatopus in anterolateral view, indicating the morphological difference in the form of the anterior process. (e) Presternum of Norops valencienni in anterolateral view showing the coracosternal groove and the long dorsolateral processes that are characteristic of N. valencienni.

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In C. texanus there is a single large fontanelle in the posterior half of the presternal plate (that in some specimens is paired and divided in the midline, Fig. 5b). I. iguana lacks this fontanelle. Siebenrock (1895) and Skinner (1959) both noted that the extent of the fontanelle can vary between different developmental stages. Both the existence and the extent of this fontanelle probably reflect limitations of the imaging technique rather than actual skeletal features, and are, therefore not examined here.

Cophosaurus texanus and Norops lineatopus

In Norops lineatopus the dorsal lip of the sulcus spans the entire anterior half of the presternal plate, as is also seen I. iguana, but not in C. texanus (Fig. 5b). The presternum of N. lineatopus is narrower and relatively longer than that of C. texanus (Fig. 5b). The posterior extremity of the presternal plate carries a shallow, anteriorly-directed indentation, to either side of which attach the mesosternal rods. The latter, in many instances, are fused together in their anterior portions, carrying the above-mentioned indentation further posteriorly. This results in a gradual, rather than an abrupt, transition from presternum to mesosternum (Fig. 5b).

Variation among Jamaican Norops

In comparison to that of the other species of Norops investigated, the presternum of N. lineatopus is most similar to that of N. grahami in overall form and configuration. In contrast, the presternum of the other three species appears more attenuated (Fig. 5b). The paired dorsolateral processes of the dorsal sulcus are, in a relative sense, about three times as long in N. valencienni as they are in the other species (Fig. 6). In N. valencienni the third sternal rib uniquely articulates with the mesosternum (Fig. 5b).

Interclavicle
Iguana iguana and Cophosaurus texanus

The interclavicle is T-shaped (Fig. 5c). In C. texanus it is strongly depressed, whereas in I. iguana it is cylindrical, and only its posterior process is depressed. The interclavicle makes contact with the presternum via a wide longitudinal groove in the ventral face of the latter, which occupies the anterior half of the presternum.

The lateral processes are very short (about one sixth of the total width of the BSA) in I. iguana, whereas in C. texanus they span almost one half of the total width of the BSA. The anteroventral edge of the interclavicle forms a short, shovel-like process (Fig. 6), which is relatively longer in C. texanus than it is in I. iguana. The lateral processes meet the posterior process at an angle of about 85° in both species.

Cophosaurus texanus and Norops lineatopus

Although generally cruciform, the very short anterior process of the interclavicle gives this element a T-shaped appearance in N. lineatopus (Fig. 5c). The body of the interclavicle is depressed. The lateral processes form an angle of about 55° to 60° with the posterior process, which is considerably less than that in C. texanus. A longitudinal groove in the lateral process divides its medial half into dorsally and posteriorly oriented components, a separation that is absent from I. iguana and C. texanus (Fig. 5c). The medial third of the clavicle articulates directly with this groove. The very short anterior-medial process is cylindrical and forms a proboscis-like extension. The equivalent process in I. iguana and C. texanus is strongly depressed (Fig. 6).

Variation among Jamaican Norops

In its general form the interclavicle is very similar in all examined Norops species (Fig. 5c). The angle between the lateral processes and the posterior process varies from 45° to 65° in N. opalinus, 55° to 60° in N. grahami and N. garmani, to 55° to 65° in N. valencienni (Fig. 5c).

Clavicle
Iguana iguana and Cophosaurus texanus

In both species the shaft of the clavicle is cylindrical and the primary curvature is very smooth, the element forming an almost halfmoon-shape in anterior view (Fig. 5d). In comparison to C. texanus, the clavicular shaft is relatively thicker in I. iguana. In C. texanus a short portion (10 to 20% of the total length of the clavicle) of the dorsal quarter of the shaft is anteroposteriorly compressed (Fig. 5d), a feature that is barely noticeable in I. iguana. The dorsal articulatory surface of the clavicle tapers into a mediolaterally compressed process that forms a shallow articulatory groove.

Cophosaurus texanus and Norops lineatopus

In N. lineatopus the shaft of the clavicle is lateromedially compressed, and the apex of the primary curvature segregates it into dorsal and medial portions (Fig. 5d). Both of these are almost straight, and at the midpoint of the shaft both meet at an angle of about 120°. The shaft is asymmetrically flattened (it is thickest dorsomedially and strongly compressed ventrolaterally), contrasting with the smooth curvature of the cylindrical shaft of C. texanus and I. iguana (Fig. 5d). The surfaces of the acromio-clavicular joint are shaped similarly in N. lineatopus, C. texanus and I. iguana.

Variation among Jamaican Norops

In N. lineatopus the medioventral and dorsal portions of the shaft constitute about three fifths and two fifths of the total length of the clavicle, respectively (Fig. 5d). The same is so for N. garmani. In N. opalinus the ventral aspect of the clavicle is relatively longer, and the apex of the primary curvature is displaced farther towards the dorsal extremity of the clavicle. The form of the clavicle in N. grahami is intermediate between that of N. lineatopus and N. opalinus. In N. valencienni the dorsal and medioventral portions each constitute about half the length of the clavicle (Fig. 5d).

Scapulocoracoid
Iguana iguana and Cophosaurus texanus

The scapulocoracoid of lizards forms a single functional and structural unit. However, it is divisible into four distinct topographical elements: the suprascapula, scapula, coracoid and epicoracoid (Fig. 6a,b). With its four fenestrae the scapulocoracoid of I. iguana is assignable to type 6 of Lécuru's (1968a) scheme, whereas C. texanus lacks the secondary coracoid fenestra (Fig. 6b), and is assignable to type 5. In I. iguana the secondary coracoid ray lies almost in the frontal plane, and is only slightly angled in an anteroventral direction. Medioposterior to that ray lies the circular secondary coracoid fenestra, which is absent from C. texanus.

In I. iguana the epicoracoid borders about one quarter to one half of the total circumference of each scapulocoracoid fenestra, whereas in C. texanus it borders only about 10% of their total circumference (Fig. 6b), resulting in the epicoracoid being relatively more extensive in I. iguana.

Cophosaurus texanus and Norops lineatopus

The free edges of the suprascapula and epicoracoid are not precisely discernible in CT images, because the density contrast between these two elements and the surrounding soft tissue varies greatly in C. texanus (and also in Norops). Thus, the anterior border of the scapulocoracoid fenestra is unresolved in most of our reconstructions. The scapulocoracoid of N. lineatopus is assignable to type 3 of Lécuru (1968a), with only the scapulocoracoid and primary coracoid fenestrae present (Fig. 5e). The position and orientation of the fenestrae that are present are almost identical to said openings in I. iguana and C. texanus (Fig. 5e). However, the scapular ray is oriented directly anteriorly in N. lineatopus, although it sometimes has a small anteroventral inclination. The rays are relatively narrower and the primary coracoid fenestra and the scapulocoracoid fenestra are relatively wider and longer in N. lineatopus in comparison to C. texanus (Fig. 5e). Medially the epicoracoid constitutes a band-like continuation of the coracoid in N. lineatopus. It articulates with the presternum for about three fifths of its anteroposterior extent, whereas its anterior portion lies dorsal to the interclavicle (Fig. 4).

Variation among Jamaican Norops

In N. valencienni the anteroposterior extent of the scapula, and, to a lesser degree, that of the suprascapula, is markedly shorter than it is in N. lineatopus (Fig. 5e). The scapulocoracoid of N. grahami and N. garmani are qualitatively indistinguishable from that of N. lineatopus (Fig. 5e,f). The form of the curvature between the lateral and ventromedial portion of the coracoid, as well as the extent of the scapula and suprascapula, vary equally both within and between these species (Fig. 5f).

In comparison with N. lineatopus the reconstructed dorsal edge of the suprascapula is strongly emarginated in both C. texanus and N. opalinus (Fig. 5e). In the latter, the true extent of the suprascapula reaches further dorsally than is evident in the reconstruction based on CT images.

Morphological Variation Within Norops

The vertebral column of N. lineatopus is qualitatively indistinguishable from that of all other species of Norops examined (Fig. 5a). The first three sternal ribs articulate with the presternal plate, and the following two ribs contact the mesosternum. This pattern is deviated from only by N. valencienni, in which the articulatory facet for the third sternal rib is borne by the mesosternum (Fig. 5b). The rhomboidal presternal plate is lateromedially narrow in N. valencienni, relatively wider in N. garmani and N. opalinus, and widest in N. lineatopus and N. grahami (Fig. 5b). The presternum bears a pair of dorsolateral processes that are relatively elongated in N. valencienni when compared with the other Norops species (Fig. 6).

The interclavicle is very similar in all examined Norops species. The angle between the lateral processes and the posterior process increases from N. opalinus, to N. lineatopus, N. grahami, and N. garmani, and then to N. valencienni (Fig. 5c). The clavicle is divisible into a ventromedial and a dorsal portion at the apex of its primary curvature. The length of the ventromedial portion increases, proportionally to the dorsal portion, from N. valencienni to N. garmani and N. lineatopus, to N. grahami, and is greatest in N. opalinus (Fig. 5d).

The scapulocoracoid is a complex three-dimensional structure (Fig. 5e,f), which makes it difficult to qualitatively assess its morphological variation within and between species. In N. valencienni the anteroposterior extent of the scapula, and, to a lesser degree that of the suprascapula, is markedly shorter than that of the other species of Norops examined (Fig. 5e). The dorsal extent of the suprascapula of N. opalinus is relatively short in comparison to that of the other species of Norops, which is probably reflective of low density contrast between the material of the suprascapula and the surrounding soft tissue in this, the smallest species examined.

Geometric Morphometric Quantitative Comparison

We divided the BSA into four moieties (Table 2), the components of which are generally stably and immovably linked to each other. The vertebral column poses the only exception in that regard, since we could not correct for displacement at the intervertebral joints. When examining landmarks 1 through 5, we thus focus on anteroposterior disposition. The eigenvalues and variance explained by the PCs of the dataset for each of the moieties are provided in Table 3. Only the PCs that are deemed informative after application of the broken-stick model are shown and discussed.

Table 3. Eigenvalues and variance of the explored PC scores for each data set
Data setPC1PC2PC3PC4PC5PC6 
  1. We show only PCs that are informative according to the broken-stick model (broken stick calculated using PAST, V2.17, Hammer, 2012).

Complete BSA0.001812330.000915430.000599480.000531990.000446470.00036288Eigenvalue
25.11812.6878.3087.3736.1885.029Variance [%]
Vertebrae0.001186610.000477700.000395500.00019832  Eigenvalue
44.40717.87714.8017.422  Variance [%]
Presternum-interclavicle0.001830760.001481100.000695340.00053999  Eigenvalue
27.82022.50610.5668.205  Variance [%]
Clavicle0.001362590.00063359    Eigenvalue
82.72519.025    Variance [%]
Scapulocoracoid0.004394700.002046650.001377510.001044790.000952480.00073888Eigenvalue
30.11614.0269.4407.1606.5275.063Variance [%]

Testing for size-dependence of the principal components

The Pearson-correlation between log-transformed snout-vent length and centroid size (logCS) indicates that the latter closely models the former (Table 4). We, therefore, used only logCS to test for size-dependence of the shape data.

Table 4. Correlation coefficients of a two-sided Pearson correlation of log-transformed SVL with log-transformed centroid size
Test groupVertebraePresternum-interclavicleClavicleScapulocoracoid
r0.8740.8880.8840.881
P<0.001<0.001<0.001<0.001

All PCs that are accounted for in Table 3 were regressed against logCS. Doing so revealed only a very weak association between size and shape (Table 5). The vertebral column exhibits the strongest size correlation, with both PC1 and PC4 showing a statistically significant size signal. Size shows the strongest predictive value for PC4 of the vertebral column (29%, Table 5). Few additional size-shape correlations are evident for the other moieties, and they are all lower than those for the vertebral column.

Table 5. Single-variable regression of principal components over log-transformed centroid síze: variation predicted by logCS, and probability thereof
MoietyVertebraePresternum-interclavicle
PC1PC2PC3PC4PC1PC2PC3PC4
Predicted by logCS (%)11.638.492.5628.680.993.0111.610.96
P0.0200.0640.314< 0.0010.4780.1850.0290.449
MoietyClavicleScapulocoracoid
PC1PC2PC1PC2PC3PC4PC5PC6
  1. Bold-faced correlations are statistically significant for an error interval of 0.05.

Predicted by logCS (%)11.638.492.5628.680.993.0111.610.96
P0.0200.0640.314< 0.0010.4780.1850.0290.449
Predicted by logCS (%)1.3010.628.086.5614.209.290.183.96
p0.3600.0310.0800.0450.0020.0490.7780.235

Testing for the presence of sexual dimorphism in the data

Our qualitative assessment revealed morphological differences between species, but not between sexes. Although locomotor habitat exploitation by male and female anoles in a given species may be similar, the complex social signaling practiced by males may influence BSA structure in subtle ways (Wataru et al., 2013). The exploration of external morphometric features by Powell and Russell (1991) showed that the scaling relationship of limb length to snout-vent length differs between sexes of both N. garmani and N. grahami. Our PCA of the data subsets for the clavicle of N. lineatopus reveals no difference in the mean shapes of this skeletal moiety between males and females (Fig. 7, Table 6). During cross-validation of the data sets of the presternum-interclavicle moiety, and the scapulocoracoid, a great number of specimens were misclassified (Table 6). The discriminant function analysis successfully assigns the specimens of N. lineatopus to the correct sex with a success rate from 42% to 78%, and, according to the canonical correlation analysis, the two data subsets of males and females are fairly similar (Table 7). If a morphological difference between the BSA elements of male and female Norops exists, it is too subtle to be recognized using our methods. Males potentially have a shorter medioventral portion of the clavicle (Fig. 7b), but the overall morphospace that is encompassed by all male specimens completely engulfs the female morphospace (Fig. 7a).

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Figure 7. (a) PC2 plotted against PC1 for all specimens of N. lineatopus for the clavicle data set. (b) Mean shape resulting from a discriminant function analysis of the clavicle data set representing the difference between male and female N. lineatopus. Numbered points represent landmarks. Males in black, females in grey.

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Table 6. “Leave-one-out” cross-validation scores for the discriminant function analysis for the sexes of N. lineatopus for all data subsets, using the Procrustes coordinates as predictors
Data subsetWrongly assigned to
FemaleMale
Vertebrae5/26%5/42%
Presternum-interclavicle7/33%4/39%
Clavicle6/22%5/42%
Scapulocoracoid9/47%7/58%
Table 7. Canonical correlation analysis using the relevant PCs of the four datasets (broken stick model, see Table 3), to predict sexes in N. lineatopus
Test groupVertebraeIcl-sternClavScapcor
  1. Given are the canonical correlation for the first canonical variate; Wilk's Lambda, χ2, degrees of freedom, and significance of F for all canonical variates combined.

Canonical correlation0.4870.4780.5060.678
Wilk's Lambda0.7630.7720.7440.540
χ27.1666.6027.82615.705
df5537
P0.2090.2520.0500.028
Between-species discrimination

The PCA reveals no distinctive morphometrically-discernible group that uniquely corresponds to one species (Fig. 8). Even so, each species occupies a particular zone within the PC plots. For example the scapulocoracoid data set reveals that N. grahami shares its morphospace with N. garmani and N. opalinus (Fig. 8d), and all three are relatively well segregated from the other species.

image

Figure 8. PC scores for the four structural moieties of the BSA. Species are identified by symbols and shading as follows: inverted triangles (▾) Norops lineatopus, squares (▪) N. valencienni, diamonds (♦) N. grahami, left-pointing triangles (◂) N. garmani, triangles (▴) N. opalinus. - - a) vertebrae, b) presternum-interclavicle, c) clavicle, d) scapulocoracoid. Ellipses indicate limits of distribution of the data pertaining to each species.

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The CVA (Tables 8 to 11) revealed the best discrimination for the scapulocoracoid data set, which assigned at least 50% of the members of each species to the correct groups (Table 11). In the following section we explore the differences that are indicated by the discriminant function analysis.

Table 8. Between-species discrimination as revealed by the canonical variate analysis (CVA) in the vertebrae data set, using all principal components as predictors
 LineatopusGrahamiValencienniGarmaniOpalinus
N. lineatopus6/19.4%3/9.7%2/6.5%8/25.8%12/38.7%
N. grahami2/16.7%6/50%2/16.7%2/16.7%0
N. valencienni003/75%01/25%
N. garmani01/33.3%02/66.7%0
N. opalinus4/33.3%1/8.3%01/8.3%6/50%
Vertebral column

The geometric morphometric analysis of the vertebral column moiety reveals only subtle differences between some of the species (Figs. 8a and 9; Table 8). Because the vertebrae are mobile with respect to each other, and since we were not able to correct for this variation, only anteroposterior displacement of the landmarks is considered here.

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Figure 9. Mean shape changes as revealed by the discriminant function analysis for the vertebral data set depicting the difference between Norops lineatopus and a) N. valencienni, b) N. grahami, c) N. garmani, and d) N. opalinus. Numbered points represent landmarks (see Table 1).

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N. valencienni and N. grahami exhibit relatively longer thoracic vertebrae (landmarks 2 and 3 are displaced slightly posteriorly, Fig. 9), when compared with the other Norops species examined.

Presternum-interclavicle

The presternum and interclavicle are analysed as a unit, because they are immovably linked. Our DF reveals the smallest coracosternal angle in N. valencienni, a medium angle in N. lineatopus and N. garmani, and the greatest angle in N. grahami and N. opalinus (Fig. 10). This angle directly relates to a lateromedially wider or narrower presternal plate (Fig. 10). N. garmani, N.opalinus and N. grahami exhibit relatively the shortest presternum. In these three species landmarks 16 and 17 are both displaced posteriorly, indicating a shorter posterior half of the presternum relative to that of N. lineatopus. The presternum of N. valencienni is relatively very narrow, and the anterior half of the presternal plate is longer relative to that of the other species (Fig. 10; Table 9).

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Figure 10. Mean shape changes as revealed by the discriminant function analysis for the presternum-interclavicle moiety depicting the difference between Norops lineatopus and a) N. valencienni, b) N. grahami, c) N. garmani, and d) N. opalinus. Numbered points represent landmarks (see Table 1).

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Table 9. Between-species discrimination as revealed by the canonical variate analysis (CVA) in the interclavicle and presternum data set, using all principal components as predictors
 LineatopusGrahamiValencienniGarmaniOpalinus
Lineatopus20/66.7%3/10%1/3.3%1/3.3%5/16.7%
Grahami1/9.1%5/45.5%1/9.1%3/27.3%1/9.1%
Valencienni1/16.7%04/66.7%1/16.7%0
Garmani0003/100%0
Opalinus1/9.1%2/18.2%01/9.1%7/63.6%

The position of the articulatory facets of the sternal ribs varies greatly between specimens. PC2, which emphasizes this positional change, exhibits a continuum of PC scores (Fig. 8b) from a relatively anteriorly-disposed position of the sternal ribs in N. opalinus and N. garmani to a relatively posteriorly-disposed position, and a migration of the third sternal rib onto the mesosternum, in N. valencienni (Fig. 10; Table 9).

Our discriminant function analysis reveals a species-specific range of variation in the angle between the posterior and lateral processes of the interclavicle, with the angle trending from being smallest in N. opalinus, and increasing through N. garmani, N. grahami and N. lineatopus, to being greatest in N. valencienni (Fig. 10).

The length of the posterior process of the interclavicle also varies relative to that of the presternum and the paired lateral processes. The mean shape of the interclavicle of N. valencienni displays the shortest posterior process (Fig. 10), and the longest interclavicle is found in N. grahami, N. opalinus and N. garmani. A relatively long posterior process always coincides with a greater distance between the anterior extremity of the interclavicle and that of the presternum, whereas the lateral extremity of the lateral process (landmark 37) is barely displaced in any of the mean shapes (Fig. 10). Thus, the variation in the angle between the lateral and posterior processes of the interclavicle is, at least in part, associated with variation in the distance between the sternum and the anterior extremity of the interclavicle.

Clavicle

The mean shape of the clavicle is very similar in N. garmani and N. grahami (Fig. 11; Table 10). In N. opalinus the apex of the primary curvature lies relatively closer to the dorsal extremity, thus reciprocally elongating the ventral aspect of the clavicular shaft. In N. lineatopus this apex lies relatively closer to the medial extremity than it does in N. garmani and N. grahami (Fig. 11). In N. valencienni the apex is only slightly more medial than it is in N. lineatopus.

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Figure 11. Mean shape changes as revealed by the discriminant function analysis for the clavicle data set depicting the difference between Norops lineatopus and a) N. valencienni, b) N. grahami, c) N. garmani, and d) N. opalinus. Numbered points represent landmarks (see Table 1).

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Table 10. Between-species discrimination as revealed by the canonical variate analysis (CVA) in the clavicle data set, using all principal components as predictors
 LineatopusGrahamiValencienniGarmaniOpalinus
N. lineatopus11/36.7%09/30%4/13.3%6/20%
N. grahami08/66.7%1/8.3%1/8.3%2/16.7
N. valencienni1/16.7%04/66.7%01/16.7
N. garmani1/25%003/75%0
N. opalinus3/21.4%004/28.6%7/50%
Table 11. Between-species discrimination as revealed by the canonical variate analysis (CVA) in the scapulocoracoid data set, using all principal components as predictors
 LineatopusGrahamiValencienniGarmaniOpalinus
N. lineatopus26/83.9%1/3.2%2/6.5%02/6.5%
N. grahami08/66.7%004/33.3%
N. valencienni1/16.7%04/66.7%1/16.7%0
N. garmani001/25%2/50%1/25%
N. opalinus2/14.3%4/28.6%01/7.1%7/50%
Scapulocoracoid

Our DF revealed that in N. valencienni the dorsal and ventral edges of the suprascapula are displaced relative to that of the other species (Fig. 12), making it relatively taller. The epicoracoid, the secondary coracoid ray and the scapular ray all terminate relatively closer to the glenoid fossa in N. valencienni than they do in the other species examined (Figs. 5e and 12; Table 11). In N. grahami the anterior extremity of the scapular ray is displaced anterolaterally, together with the scapula-suprascapular border, relative to the organization in N. lineatopus. Compared with the latter, the dorsal extremity of the suprascapula is displaced posteromedially in N. grahami (Fig. 12). Thus, the scapulocoracoid of N. lineatopus appears to be dorsoventrally straighter and mediolaterally narrower than it is in N. grahami. Relatively the narrowest lateromedial extent of the scapulocoracoid is encountered in N. valencienni and N. lineatopus, followed by a slightly wider scapulocoracoid in N. opalinus, with the relatively widest one being possessed by N. grahami and N. garmani (Fig. 12).

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Figure 12. Mean shape changes as revealed by the discriminant function analysis for the scapulocoracoid data set depicting the difference between Norops lineatopus and a) N. valencienni, b) N. grahami, c) N. garmani, and d) N. opalinus. Numbered points represent landmarks (see Table 1). Left lateral view on the left, posterior view on the right.

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Lateromedially the scapulocoracoid is relatively wider in N. garmani and N. grahami in comparison to that of N. valencienni and N. lineatopus (Fig. 12). The suprascapula and coracoid form a greater angle relative to the scapula in N. garmani and N. grahami when compared with the situation in N. lineatopus (Figs. 5f and 12). In N. opalinus the scapula and coracoid appear lateromedially wider in anterior view, which can only be the result of a rotation of the scapula relative to the coracoid.

The anterior portion of the epicoracoid (anterior to the coracosternal groove, landmarks 20 and 21, Table 1) is relatively anteroposteriorly shorter in N. grahami, N. garmani and N. valencienni, when compared with N. lineatopus and N. opalinus (Fig. 12).

Lastly, the glenoid fossa is displaced dorsally in N. garmani when compared with the other Norops species examined (Fig. 12). This shift coincides with a relative ventral displacement of the anteroventral extremity of the coracoid and epicoracoid, and with a relatively ventral shift of the anterior aspect of the border between the epicoracoid and coracoid. We therefore conclude that the glenoid fossa is positioned relatively more dorsally on the body in N. garmani compared with the condition in the other Norops species examined.

Canonical variates

A CVA that uses ecomorph categories as grouping criteria revealed the best scores for the scapulocoracoid, and relatively high numbers of misclassification for the vertebrae (Tables 12 to 15). The twig ecomorph is relatively well discriminated from the other ecomorphs, except for the scapulocoracoid data set, where it scores lowest (Table 15). The four ecomorphs differ greatly in the relative amount of morphospace occupied, rendering the results of the CVA questionable (Fig. 13).

Table 12. Between-ecomorph discrimination as revealed by the canonical variate analysis (CVA) in the vertebrae data set, using all principal components as predictors
 Trunk-groundTrunk-crownCrown-giantTwig giant
Trunk-ground11/35.5%9/29%2/6.5%9/29%
Trunk-crown6/25%9/37.5%3/12.5%6/25
Crown-giant01/25%3/75%0
Twig giant01/33.3%02/66.7%
image

Figure 13. Diagrams of the first two Canonical variates as revealed by the CVA of the Procrustes shape data of the four structural moieties of the BSA. Ecomorphs are identified by symbols and shading as follows: inverted triangles (▾) trunk-ground, squares (▪) twig giant, diamonds (♦)trunk-crown, left-pointing triangles (◂) crown-giant. - - a) vertebrae, b) presternum-interclavicle, c) clavicle, d) scapulocoracoid. Ellipses indicate limits of distribution of the data pertaining to each ecomorph.

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CVA of the vertebral data set does not allow for discrimination of trunk-crown or trunk-ground representatives reactive to any other ecomorph, although the other two ecomorphs are relatively distinct from one another (Table 12). Twig anoles appear to feature dorsally displaced articulations for the sternal ribs (Fig. 13a).

The interclavicle-presternum moiety reveals a relatively good discrimination between ecomorphs, except for trunk-crown forms (Table 13). Twig anoles can be distinguished by a relatively short distance between the anterior extremity of the interclavicle and presternum; a lateromedially narrow presternum; and relatively long paired lateral processes (Fig. 13b).

Table 13. Between-ecomorph discrimination as revealed by the canonical variate analysis (CVA) in the interclavicle and presternum data set, using all principal components as predictors
 Trunk-groundTrunk-crownCrown-giantTwig giant
Trunk-ground24/80%4/13.3%1/3.3%1/3.3%
Trunk-crown4/18.2%11/50%2/9.1%5/22.7%
Crown-giant1/16.7%04/66.7%1/16.7%
Twig giant0003/100%

The clavicle moiety has little discriminatory power (Table 14), and all ecomorphs share considerable morphospace with each other (Fig. 13c).

Table 14. Between-ecomorph discrimination as revealed by the canonical variate analysis (CVA) in the clavicle data set, using all principal components as predictors
 Trunk-groundTrunk-crownCrown-giantTwig giant
Trunk-ground11/36.7%5/16.7%9/30%5/16.7%
Trunk-crown5/19.2%13/50%1/3.8%7/26.9%
Crown-giant2/33.3%04/66.7%0
Twig giant1/25%003/75%
Table 15. Between-ecomorph discrimination as revealed by the canonical variate analysis (CVA) in the scapulocoracoid data set, using all principal components as predictors
 Trunk-groundTrunk-crownCrown-giantTwig giant
Trunk-ground26/83.9%3/9.7%2/6.5%0
Trunk-crown2/7.7%23/88.5%01/3.8%
Crown-giant1/16.7%04/66.7%1/16.7%
Twig giant01/25%1/25%2/50%

The scapulocoracoid data set has probably the greatest discriminatory power (Table 15). Twig anoles exhibit a relatively dorsoventrally taller suprascapula, and anteroposteriorly shorter scapulocoracoid and coracoid fenestra, and a shorter epicoracoid (Fig. 13d). The scapulocoracoid of trunk-crown and crown giant representatives is dorsoventrally shorter, and the angle between the posterior edge of the scapula and suprascapula is smaller than that of the other two ecomorphs (resulting in more strongly curved posterior edge of the scapulocoracoid).

Correlation with phylogeny

Mapping average PC shapes of each moiety onto the two phylogenies, the shape variation in the vertebral column and presternum-interclavicle appear to reflect no phylogenetic signal (Table 16). Some phylogenetic signal may be present in the clavicle and scapulocoracoid moieties.

Table 16. P value of permutation test against the null hypothesis of no phylogenetic signal
Phylogenetic hypothesisVertebraeIcl-sternClavScapcor
Nicholson et al. (2012)0.76840.66220.09510.1642
Alföldi et al. (2011)0.59970.19970.14690.0480

The phylogenetic hypothesis of Alföldi et al. (2011) generally yields smaller p-values compared with that of Nicholson et al. (2012), except for the clavicle data set (Table 16). However, only shape changes in the scapulocoracoid appear to be at all related to the phylogeny.

DISCUSSION

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGEMENTS
  8. LITERATURE CITED

Morphological Patterns in the BSA of Jamaican Anoles

To ground our study we employed Iguana iguana and Cophosaurus texanus as outgroups to establish a comparative framework that could be explored qualitatively and quantitatively. Comparing the mounted skeleton of I. iguana with the three-dimensional renditions of C. texanus, it becomes apparent that in the scans only the extent of the suprascapula and epicoracoid exhibit noticeable variability in their rendition between different specimens. All other skeletal features of the BSA are readily observable to their full extent in the virtual reconstructions.

Among the species of Norops examined we were able to determine, through qualitative and quantitative comparison, that the components of the BSA of all species examined differ in their morphology from those of the other species, but that few of these differences are actually discriminatory (Fig. 5, Tables 8-11).

Our analysis also revealed that sexes differ in their morphospatial distribution, although a clear discrimination between sexes is not possible (Fig. 7, Tables 6 and 7). If a morphological difference between the BSA elements of male and female Norops exists, it is too subtle to recognize employing our methods. Because our focus is on the exploration of morphological differences between Jamaican anoles, we do not further explore sexual dimorphism at this time.

Since our data are based only on adult specimens, allometric effects should play only a minor role on the perceived size differences. However, it is still possible that one species merely represents an upscaled form of another, so the data needed to be tested for size-correlation. A regression of the PCs against logCS revealed only a very weak association between size and shape (Table 5). The strong size correlation that is evident in the vertebral column is not unexpected, since the landmarks that make up this moiety are aligned along the body long axis. This structural correlation with body length makes a size-based prediction of 12% for PC1 (Table 5) appear very low.

Powell and Russell (1991) examined external morphometric features of N. garmani, N. opalinus and N. grahami, and showed that the features that they investigated scale differently among these species. Our analysis results in a similar conclusion. Although they are similar in habitat preference, N. garmani and N. grahami differ morphologically from N. opalinus, and not merely in the scaling of their skeletal elements (Table 5, Fig. 8). Without further data relating to allometric growth of the species and skeletal elements examined, we are unable to argue conclusively whether the correlation between size and PCA is driven by phylogeny, ontogeny or absolute size. Furthermore, the covariation between size and shape that is evident in our analysis is relatively small (Table 5). Adopting a conservative definition of “significance” (Higgs, 2013), and recognizing the relatively small correlation between shape and absolute size, we decided not to “correct” for size in our data. Instead, we used the Procrustes data and principal components as represented by their respective analyses.

The PCA reveals that all species occupy distinctive regions of morphospace (Fig. 8). Although the analysis through principal components does not allow for clear-cut discrimination between these groups, the differential morphospatial distribution allows us to test whether distinctive areas of the morphospace are preferentially occupied by distinct species or ecomorphs. CVA reveals that the means of most species differ from each other (Tables 8-11. However, the data for the vertebrae have only very little discriminatory power, and only N. valencienni can be distinguished from the other species with some certainty (Table 8). The interclavicle-presternum moiety of N. grahami is barely distinguishable from that of any other species examined, but representatives of all other species differentiate relatively well (Table 9). N. grahami performs relatively well in the CVA of the clavicle data set, but all other species, including N. valencienni, appear to be less differentiable (Table 10). Relatively the best CVA scores are achieved for the scapulocoracoid, where at least 50% of every species group is correctly classified, and N. grahami can be distinguished from all species but N. opalinus (Table 11).

The ecomorph-based CVA revealed discriminatory power in the shape changes of the four moieties (Fig. 13, Tables 12-15 that are similar to those retrieved from the species-based CVA (Fig. 8, Tables 8-11. The strongest discrimination is achieved for the scapulocoracoid dataset, and the relatively weakest correlation values are found for the vertebral moiety, regardless of whether the data are classified by species or ecomorph designation (Tables 11 and 15). When N. grahami and N. opalinus are grouped together as a single trunk-crown ecomorph, the latter becomes comparable in sample size (Fig. 3) and disparity (Fig. 13) to the trunk-ground ecomorph (N. lineatopus), which makes these two groups more readily comparable as ecomorphs than they are as species. The morphometric differences revealed by the PCA and CVA are very similar (Figs. 8 and 13). However, since the morphometric disparity varies between ecomorph groups (Fig. 13), it is also easy to overinterpret the canonical variation.

Combining the data of N. opalinus and N. grahami into a trunk-crown ecomorph group results in a greater discriminatory power for the scapulocoracoid data set (Tables 11 and 15), but not for the vertebral moiety (Tables 8 and 12). This shows that ecomorph groups do not necessarily have greater explanatory power for the morphological diversity that is evident in our data than do species groups. There appear to be species-specific differences between N. opalinus and N. grahami that prevent a more effective discrimination of these two species from all others. The clavicle of N. grahami appears to be distinctly different from that of N. opalinus (Table 10), and their combination as trunk-crown ecomorph results in less discrimination from the other species (Table 14). The form of the clavicle is very variable among lizards, and characters related to its morphological diversity have featured repeatedly in phylogenetic analyses (Sukhanov, 1961; Lécuru, 1968b; Russell, 1988). However, little is known of the functional implications of these differences in clavicular form (Peterson, 1973; Russell, 1988; Russell and Bauer, 2008). We posit that the form of the clavicle is more variable within small radiations (such as the monophyletic radiation of Jamaican Norops) than is that of any of the other elements of the BSA, which makes it more susceptible to microecological adaptation than the other skeletal elements. This remains to be tested.

The major findings from the DF are that (i) the relative distance between the anterior extremity of the interclavicle and that of the presternum increases from N. valencienni, to N. opalinus, to N. grahami and N. garmani, and is greatest in N. lineatopus (Figs. 10 and 13b), and that this distance covaries with the angle between the lateral processes and the posterior process of this element. (ii) The relative length of the medioventral portion of the clavicle increases from N. valencienni, to N. lineatopus, to N. grahami and N. garmani, and is longest in N. opalinus (Fig. 11). (iii) The scapulocoracoid is lateromedially relatively the narrowest in N. valencienni and N. lineatopus, is slightly wider in N. opalinus, and is widest in N. grahami and N. garmani (Figs. 12 and 13d). (iv) The coracoid, scapulocoracoid and scapular rays are anteroposteriorly short in N. valencienni, relatively longer in N. garmani, N. grahami and N. lineatopus, and are longest in N. opalinus. No two patterns in any of these four major findings describe the same trajectory in terms of sequential change between the species, and the four patterns are distinct from one another, meaning that every element of the BSA conveys different information in relation to the differentiation between species and ecomorphs of Jamaican Norops.

In attempting to summarize our findings, and seek features that potentially discriminate N. valencienni, N. grahami, N. garmani and N. opalinus from N. lineatopus, and from each other, we note the following differences in comparison with N. lineatopus.

Norops valencienni (twig giant) is characterized by relatively long thoracic vertebrae; a lateromedially narrow and anteroposteriorly lengthened presternum; the dorsolateral process of the presternum is relatively long; its mesosternum articulates with the third sternal rib; the posterior process of the interclavicle is relatively short and there is a large angle between the lateral and posterior process; the apex of the primary curvature of the clavicle is ventrally shifted; the scapula and suprascapula are dorsoventrally tall; the scapula, coracoid and epicoracoid are anteroposteriorly short.

N. grahami (trunk-crown) exhibits anteroventrally shifted articulatory facets of the sternal ribs; a relatively lateromedially wide and anteroposteriorly short presternum; a slightly lengthened posterior process of the interclavicle; a relatively small dorsal shift of the apex of the clavicle; an anterolateral displacement of the anterior extremity of the scapular ray and of the scapula-suprascapular boundary; and a smaller angle between the ventral and dorsal portion of the coracoid.

N. garmani (crown giant) is characterized by a slightly lateromedially narrower and anteroposteriorly elongated presternum (relatively the second-longest presternum after that of N. valencienni); a slightly elongated posterior process of the interclavicle; a relatively small dorsal displacement of the apex of the clavicle (as also seen in N. grahami); an anterior and medial elongation of the epicoracoid; a dorsal displacement of the glenoid fossa; a relatively dorsoventrally taller scapula; and a lateromedially wider scapulocoracoid.

N. opalinus (trunk-crown) is characterized by a relatively dorsally displaced apex of the clavicle; a dorsoventrally short suprascapula; and torsion around the dorsoventral axis of the scapulocoracoid.

Placing this understanding of variation in structure of the BSA into the context of the ecology of these species, we note that differences between the taxa considered are subtle and relatively slight, except for the situation revealed for the twig ecomorph Norops valencienni. This twig anole exhibits some unusual traits within this radiation, such as the very narrow and elongated presternum (Figs. 10 and 13b), the elongated paired dorsolateral processes of the presternum (Fig. 6e), articulation of the third sternal rib with the mesosternum instead of the presternum (Figs. 5b and 6), the short posterior process of the interclavicle (Fig. 10), and the anteroposteriorly short scapulocoracoid (Figs. 12 and 13d).

Although N. valencienni is absolutely larger than most of the other examined species, the specimens of N. garmani are of about the same size, or larger (Fig. 3), without showing a morphology as distinctive as that of N. valencienni. Thus, the unique shape of the skeletal elements of the BSA of N. valencienni cannot be attributed to its size alone. According to recent phylogenetic studies, N. valencienni is a relatively basal member of the Jamaican anole radiation (Fig. 2, Alföldi et al., 2011; Nicholson et al., 2012), and according to our analysis there exists little phylogenetic signal in the data (Table 16). It is rather unlikely, although not impossible, that its distinctive morphology evolved at or near the phylogenetic node that it shares with the other species of Norops examined.

An alternate explanation for the discrete morphology of the BSA of N. valencienni is that it has deviated from its Jamaican congeners in relation to its adaptations relating to locomotor and habitat occupancy characteristics that differ markedly from those of the other examined species. Indeed, N. valencienni is unusual in that it forages widely (contrasting with the sit-and-wait foraging mode of the other Norops species examined; Losos, 1990b). In comparison to other Jamaican Norops, it moves for relatively long periods of time, but moves relatively slowly (Hicks and Trivers, 1983). Like other twig anoles it exhibits a great range of motion at the shoulder joint (Peterson 1974). Peterson's observations (1974) described twig anoles as being able to markedly extend their stride length via excursion at the coracosternal joint. This contradicts the findings of Higham et al. (2001), who reported a relatively short stride length for N. valencienni as compared with N. lineatopus and N. garmani. However, the latter authors studied anoles running at their maximum speed, and thus their results are not directly comparable with those reported by Peterson (1973, 1974), who studied the locomotion of these anoles in their natural environment. Since twig anoles manoeuvre on relatively the narrowest branches, in comparison to other ecomorphs (Butler and Losos, 2002), they profit from increased limb mobility in exchange for a relative reduction in locomotor speed.

Our data agree with the findings of Mahler et al. (2013) who showed that many island species of anoles are represented on other islands by almost perfect morphological copies, whereas other species exhibit distinct character sets that set them apart. Such gross morphological deviation between closely related lizards is not limited to anoles, but also occurs, for example, in geckos (Higham and Russell, 2010). The external morphology of the desert-dwelling Rhoptropus afer differs greatly from that of its sister species R. bradfieldi, whereas the latter is morphologically very similar to its other congeners (Bauer et al., 1996). Higham and Russell (2010) associated this great deviation in morphology, that occurred over a relatively short evolutionary time span, with a suite of locomotor adaptations peculiar to R. afer. We posit that morphometric changes along the branch leading to N. valencienni do not represent changes at the ancestral node, but instead bear evidence that the morphology of N. valencienni is uniquely highly divergent. We thus infer that the remainder of the Jamaican anole radiation has remained more conservative in the structure of the BSA, and that they exhibit more subtle changes with respect to each other.

The degree of mobility of the scapulocoracoid varies with the magnitude of the angle between the sagittal plane and the coracosternal groove, it being greatest when the angle is low (Peterson, 1973; Russell and Bauer, 2008). Peterson (1973) reported a relatively narrow presternum in the crown-giant Anolis richardi, and a decrease in said coracosternal angle with species occupying perches of smaller diameter. We encountered the greatest angle in the crown-giant N. garmani (Figs. 5b, 10, and 13b), which contrasts with Peterson's findings of a low angle in the crown-giant A. richardi. However, in the Jamaican radiation N. garmani occupies the widest perches, and the other four species occupy successively narrower perches (the perch diameter decreases from N. opalinus to N. grahami, to N. lineatopus, to N. valencienni; Butler and Losos, 2002). Thus, the increase in the coracosternal angle is directly reflected in an increase of the average perch diameter from N. valencienni to N. garmani. The greater mobility of the scapulocoracoid in the sagittal plane allows for a greater range of motion of the arms, thus increasing stability of the gait, especially on narrow branches (Peterson, 1973). However, the great excursion of the shoulder also leads to a decrease in relative locomotor speed (Peterson, 1973; Higham et al., 2001).

The length of the posterior process of the interclavicle is relatively the shortest in the twig anole N. valencienni (Figs. 10 and 13b), and the anteroposteriorly longest interclavicle is found in N. grahami, N. opalinus and N. garmani. The relative length of the interclavicle correlates with the distance between the anterior extremity of the interclavicle and the presternum (Figs. 10 and 13b). The length of the interclavicle has played a prominent role in anoline systematics (Guyer and Savage, 1986, 1992), but little functional interpretation has been attempted. Peterson (1973) found a relatively short posterior process of the interclavicle in the trunk-ground form Anolis cybotes and the trunk anole A. distichus. This contrasts with our findings, in which the trunk-ground form (N. lineatopus) shows an interclavicle of intermediate length between the other species. Additional data are required to determine whether there are any ecomorphological patterns that are reflective of variations in the shape of the interclavicle.

Both the posterior process of the interclavicle and the mediolateral portion of the clavicle are relatively long in the trunk-crown species N. grahami and N. opalinus, and in the crown-giant N. garmani (Figs. 10 and 13). The relatively great distance between the anterior tips of the presternum and the interclavicle relates to a more tapered appearance of the anterior portion of the BSA, reflecting a more acute angle between the lateral processes and the posterior process of the interclavicle, and a lengthened ventromedial portion of the clavicle (Fig. 5). Higham et al. (2001) studied sprinting performance in Jamaican anoles, and found that N. grahami runs faster on a strongly inclined surface than does N. lineatopus, which, in turn, is faster than N. valencienni. This makes it plausible, although only suggestive at present, that the anteriorly lengthened and more tapered BSA of crown anoles directly relates to their ability to climb on vertical surfaces. One possible reason for such a relationship is a greater muscle mass of the M. clavodeltoideus and M. pectoralis. Both of these muscles originate from the lateral and posterior processes of the interclavicle, and play important roles during the swing phase of locomotion (Fürbringer, 1900; Jenkins and Goslow, 1983). Wataru et al. (2013) compared the extent of the appendicular muscles of various anoles, and found differences that relate to variation in habitat occupation and signalling behaviour.

The relative width of the ventromedial portion of the coracoid and epicoracoid increases from N. lineatopus and N. valencienni, to N. garmani and N. grahami, and is greatest in N. opalinus. The ventromedial portion of the clavicle lengthens following a similar sequence, except that N. valencienni exhibits relatively the shortest ventromedial portion of the five species of Norops examined. This is probably not reflective of a wider chest in N. garmani, N. grahami and N. opalinus, because the lateral processes of the interclavicle and the width of the presternum are both relatively narrow in N. garmani, N. opalinus and N. valencienni (Figs. 10 and 13b). Peterson (1973, 1974) hypothesized that a correlative relationship exists between the form of the clavicle and that of other elements of the shoulder girdle. We did not observe such a relationship in our data, and examination of additional anoline radiations is necessary to determine whether more consistent patterns of variation in the form of the elements of the BSA are evident among anoles.

The shape variation in the vertebral column and presternum-interclavicle appear to carry no phylogenetic signal (Table 16). Only the distribution of the mean shapes of the scapulocoracoid appears to be related to phylogenetic history, and the topology of Alföldi et al. (2011) yields a P value of 0.048. However, the phylogenetic hypothesis of Nicholson et al. (2012) yields a P value of 0.164 (Table 16). The relatively small difference in the P values indicates that the topology of the phylogenetic tree does not have much influence on the outcome of the analysis.

Previous authors have found morphological characters of the clavicle that are useful indicators of phylogenetic relationships at the genus or family level (Sukhanov, 1961; Lécuru, 1968b; Russell, 1988). We argue that the form of the clavicle is more malleable in its adaptability to microecological differences relating to habitat occupation and exploitation than is the form of the vertebrae, presternum-interclavicle, and scapulocoracoid moieties.

From our results it is difficult to determine whether the differentiation in shape of the components of the BSA is reflective of ecomorph designation. More investigations are needed to determine whether similar ecomorphs to those comprising the Jamaican radiation, but occupying different Caribbean islands, exhibit similar patterns of configuration of the BSA. By so doing it will be possible to further investigate whether ecomorphs are structurally recognizable according to skeletal patterns that reflect their occupancy of their particular sector of the physical resource space.

This exploratory study, and the literature sources that relate to anole ecology, provide a solid foundation for designing additional studies that may further our understanding of covarying morphological and ecological patterns, and the ability to place these into a functional-morphological context that assists in explaining processes of adaptive radiation of anoline island populations. Renous and Gasc (1977) outlined an integrated approach that would yield a holistic picture of the morphology and locomotor behaviour of a focal lizard taxon, and this was reiterated by Russell and Bels (2001) for designing a research program that aims at a comprehensive understanding of locomotor kinematics among lizards. Similar studies have been conducted on the forelimb of Tupinambis (Renous and Gasc, 1977), and on the limbs and girdles of Chameleo (Fischer et al., 2010), and we designate Anolis as a next logical step in this series of kinematic and locomotor studies.

Possible Methodological Problems

Our geometric morphometric findings were mostly consistent with our qualitative observations, but were also able to reveal many additional, more subtle differences between and within the species of Norops that we examined. Both the qualitative and the quantitative approaches, however, have their own limitations. A purely descriptive approach likely will not reveal form changes that are subtle (such as the relatively longer thoracic vertebrae of N. valencienni, Fig. 9) or that are highly variable within one species.

In contrast, geometric morphometrics is limited by the landmarks selected. These are assumed to represent a meaningful approximation of the form of the examined object. Any such analysis shows only the relative displacement of distinct landmarks, and since we were only able to identify a relatively small number of reference points for each skeletal element of the BSA (Tables 1 and 2), these landmarks bear only a limited relationship to the detailed three-dimensional form of each element. For example, any variability in the relative size and orientation of the scapulocoracoid fenestrae remain undetectable in our data. More elaborate methods can be utilized to compare the geometric shape of complex three-dimensional objects that exhibit a small number of type I and II landmarks (Bernhard, 2003; Gunz et al., 2005; Souter et al., 2010; Cornette et al., 2013), and this possibility will be explored elsewhere.

For both the PCA (Fig. 8) and the CVA (Fig. 13) the morphology of one specimen of N. valencienni (twig giant) is in some respects more similar to that of other ecomorph representatives than it is to members of its own species. With only six specimens of this species it is not possible to determine whether this case constitutes an outlier or indeed lies within the regular morhological spectrum of N. valencienni. Except for this one individual, N. valencienni appears to exhibit morphological disparity that is less extensive than that of the representatives of the trunk-ground (N. lineatopus) and trunk-crown ecomorphs (N. grahami and N. opalinus). The morphological variability in the BSA of N. garmani (crown giant), similarly, is relatively small. This makes interpretation of the canonical variate analysis difficult, as the assumption of equal disparity is violated. Furthermore, the sample sizes differ greatly between the species examined (Fig. 3), so that the outcome of the CVA can only be taken as being suggestive, and not confirmatory, of structural differences between the ecomorphs.

ACKNOWLEDGEMENTS

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGEMENTS
  8. LITERATURE CITED

All CT scans were conducted in the lab of Jason Anderson (University of Calgary, Faculty of Veterinary Medicine), and the authors thank Jason Pardo for technical support with the scanning procedures. The authors are also grateful to Larry Powell (University of Calgary) for his comments on statistical analysis.

LITERATURE CITED

  1. Top of page
  2. ABSTRACT
  3. INTRODUCTION
  4. MATERIALS AND METHODS
  5. RESULTS
  6. DISCUSSION
  7. ACKNOWLEDGEMENTS
  8. LITERATURE CITED
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