Author: Alex Tinius

Despite his love for wild life and photography Alex has never caught a single anole on camera. As it turns out his study subjects avoid the cold and temperate climates that Alex calls home. Following his Ph.D. thesis under the guidance of Tony Russell (UofCalgary) his main interests lie in the form, function, and evolution of the appendicular girdles. Alex viciously exploits anole diversity to investigate causal relationships between the variation in skeletal morphology and associated differences in ecology and habitat use.

The first three paragraphs of Jane Peterson’s contribution to the Second Anolis Newsletter.

Jane Peterson’s contribution to The Second Anolis Newsletter remains one of the most comprehensive exemplars of functional-morphological research of the anoline appendicular girdles. In just a few short paragraphs Peterson (1974) outlined the key differences in pectoral girdle morphology between the Anolis ecomorphs, drawing information from both field observations and anatomical dissections of anoles from all four Greater Antillean islands. The outlined study could have formed a major contribution to our understanding of ecomorphology, had these brief observations ever been expanded into a scientific publication. Sadly, they remained as notes, confined to a brief communique on an informal basis (that continues to be formally cited). Several intriguing studies hence have examined anole appendicular morphology, but rarely allowed for implications that reach across multiple island radiations (e.g. Anzai et al. 2014, Herrel et al. 2018).

With my 2016 Ph.D. thesis, I set out to quantify what Jane Peterson had observed forty years prior, and must confess that I still fall short of reproducing the multitude of implications that Peterson’s (1974) brief descriptions alluded to. Instead of combining video-recorded movement cycles with morphological descriptions, my comparisons are solely based on three-dimensional shape analysis of the skeletal elements that comprise the breast-shoulder apparatus (BSA): the clavicle, interclavicle, presternum, and scapulocoracoid (Fig. 1). Employing the power of computed tomography scanning, and geometric morphometric analysis, I quantified the shapes of the central elements of the pectoral girdle, and compared these across anole radiations.

As with earlier work, I focused on the Jamaican ecomorph representatives, and sought out their ecomorph counterparts from Hispaniola and Puerto Rico, particularly targeting those species that are the most and least similar to the Jamaican forms. That last line of thought did not reveal any straightforward answers, as the complex structural shape of the BSA allows these anoles to be relatively distinct in some aspects, while being quite similar in others. For example, the general shape of the presternum and interclavicle are quite similar between the two trunk-ground anoles Anolis lineatopus (Jamaica) and A. gundlachi (Puerto Rico), while that of the scapulocoracoid differs quite remarkably between the two. These complex associations will take a more detailed analysis than what is warranted here, so I’ll focus on the bigger picture instead.

Fig. 1: CT-rendition of the skeletal components of the breast-shoulder apparatus of Anolis baleatus in lateromedial view, depicting all anatomical features described in the text. The gray arrow denotes anterior.

Skeletal elements of the BSA in isolation

Previous analysis of the scapulocoracoid in isolation revealed that its shape differs between Anolis habitat specialists, and resembles a particularly dorsoventrally tall shape in twig anoles (Tinius et al. 2020). The other ecomorph groups (trunk-ground, trunk-crown, and crown-giant) show obvious tendencies towards a particular structural organization, but in none of these does the scapulocoracoid resemble a truly characteristic shape.

Muscle map on scapulocoracoid of Anolis insolitus

Morphology of the Scapulocoracoid of Anolis Ecomorphs

By Alex Tinius

On September 3, 2020

In All Posts, New Research

From the onset of my scientific career I have been fascinated by the pectoral girdle. In its structural and functional diversity it is barely rivaled by any other skeletal part of the tetrapod body. Anoles, in particular, employ their forelimbs not only in locomotion, but also in various routines of display, grooming, feeding, or mating. It is likely that the different functional roles fulfilled by the pectoral limb and girdle impose varying, and potentially opposing, selective pressures onto the evolution of its structural form.

Jane Peterson briefly alluded to the structural variance displayed by the different anole ecomorphs, relating them to specific locomotor requirements by providing brief descriptions in her thesis (1973) and the First Anolis Newsletter (1974). However, beyond this initial work, and a few qualitative assessments in papers regarding phylogenetically informative characters, very little is known about the variability of the anole pectoral girdle.

right scauplocoracoid of Jamaican anoles

Right scapulocoracoid of three anole species, representative of the Jamaican lineage. The arrow denotes anterior. (via Tinius et al. 2020)

In many ways, our recent publication in the Annals of Anatomy (Tinius et al. 2020) is a dream come true (at least for me), as it allowed us to finally visualise the patterns of morphological variation that Peterson (1974) could only communicate in descriptions. Because the shoulder girdle is comprised of multiple elements that are mobile with respect to one another, this paper only investigated one of its moieties: the scapulocoracoid. This paired structure spans the entire height of the body wall, is comprised of developmentally very different compounds, and directly connects the forelimb to a midline element, the presternal plate. These attributes made it a great starting point for our investigations of the pectoral girdle.

In describing the scapulocoracoid of two non-anoline iguanids, Polychrus and Pristidactylus, we anchored our comparisons in two well-studied and closely related lizards. We then expanded on this anatomical framework by comparing all representatives of the monophyletic Jamaican anole radiation to their respective ecomorph representatives on Puerto Rico and Hispaniola. We tried to take full account of the variability of the scapulocoracoid by examining it both qualitatively, in images and comparative description, and quantitatively, through geometric morphometric analysis.

CVA of the right scapulocoracoid of Anolis ecomorphs

Canonical Variate Analysis (CVA) of the right scapulocoracoid of Greater Antillean anoles, including warp image of the scapulocoracoid denoting shape changes along CV1 and CV2. (via Tinius et al. 2020)

We found that regardless of potential phylogenetic constraints on skeletal morphology, morphospatial occupancy differs markedly between ecomorph groups. Unexpectedly, twig anoles show the most distinctive shape of the scapulocoracoid, with a relatively tall scapula and anteroposteriorly short coracoid, similar to the situation found in chameleons (Fischer et al. 2010). But despite a significant overlap in morphospatial occupancy, the other three ecomorphs examined (trunk-ground, trunk-crown, and crown-giant) also exhibit trends towards a specialized scapulocoracoid morphology, such as a relatively wide/cylindrical scapulocoracoid in trunk-ground anoles.

These variations in form likely impact the size and vectors of muscles attaching to the scapulocoracoid. One muscle group that is likely particularly impacted by the differences in scapulocoracoid form is the M. serratus anterior. This muscle group originates laterally on the cervical ribs and inserts on the medial aspect of the suprascapula. The M. serratus anterior group stabilizes the scapulocoracoid during locomotion and protracts/retracts it along the body wall. The anteroposteriorly more extensive suprascapula of crown-giant anoles likely facilitates more forceful scapular retraction, through the relatively greater attachment area for this muscle and the anterior disposition of its insertion area. Contrastingly, the relatively tall scapula of twig forms likely allows for a greater moment arm acting through this muscle group, while the anteroposteriorly short suprascapula facilitates more precise protraction/retraction of the scapulocoracoid.

Right scapulocoracoid of Anolis insolitus in a) lateral, and b) medial view, showing the attachment sites of major muscle groups that act upon the scapulocoracoid. (via Tinius et al. 2020)

My only regret about this project is the exclusion of Cuban anoles, which markedly limited our ability to compare patterns in a wider phylogenetic context. Most of the crown-giant and trunk-crown anoles examined belong to their own ecologically homogenous clade, making it impossible to discern ecological from morphological signal.

The Jamaican Anolis clade provides a glimpse into what might be achieved with a phylogenetically broader sample, as it represents four major ecomorph groups (five, if you attribute A. opalinus to the trunk group) plus two non-ecomorph species within a seven-species radiation. Despite the relatively young age of the Jamaican clade, its ecomorph representatives exhibit a push towards specialized morphologies of the scapulocoracoid, even if this level of specialization is markedly smaller than in their Puerto-Rican and Hispaniolan relatives. A future widening of our sample should allow us to answer some intriguing questions regarding the retention and diversification of ecomorphologically specialized forms within distinct phylogenetic lineages.

Literature cited

Fischer, M.S, Krause, C. & Lilje, K.E. (2010): Evolution of chameleon locomotion, or how to become arboreal as a reptile.─ Zoology, 113:67-74.

Peterson, J.A. (1973): Adaptation for arboreal locomotion in the shoulder region of lizards.─ Ph.D. thesis, University of Chicago.

Peterson, J.A. (1974) [In:] Williams, E.E. (ed.) The First Anolis Newsletter. Cambridge, Massachusetts: Museum of Comparative Zoology, Harvard University.

Tinius, A., Russell, A.P., Jamniczky, H.A. & Anderson, J.S. (2020): Ecomorphological associations of scapulocoracoid form in Greater Antillean Anolis lizards.─ Annals of Anatomy, 231; doi.org/10.1016/j.aanat.2020.151527.

Cranial Ornamentation in Anolis baleatus

By Alex Tinius

On August 28, 2019

In All Posts, New Research

When I first encountered Anolis baleatus, this Hispaniolan crown-giant was mostly an inconvenience. At the time I was gathering data for my doctoral thesis by cycling preserved anoles through a µCT-scanner. Most of the adult specimens of A. baleatus were just too large to easily fit into the scan chamber, so it took a lot of patience and creativity to acquire any decent images of the appendicular girdles, which are the body parts I was interested in.

During that process I also acquired radiographic images of the head skeleton, and found unusual patterns of crenulation in this species. The cranium of Anolis baleatus displays a great degree of seemingly asymmetrical (or at least somewhat irregular) ornamentation across its dorsal surface. This is especially pronounced on the prefrontal and frontal bones, and completely obscures all superficial distinction between them in adult lizards. In adults, cranial ornamentation is also borne by the paired nasals, maxillae, and postorbitals, and the parietal (see figure).

Both Steven Poe (1998) and Susan Evans (2008) mentioned this ossified garnish, but a thorough account of their variation among anoles remains absent from the primary literature. Richard Etheridge and Kevin de Queiroz (1988) were probably the first to report on skull ornaments in anoles (as part of a discussion of several iguanian lizards with similar cranial adornments), and remarked that the distribution patterns of dermal rugae may reflect those of the topographically associated epidermal scales.

Overall, this ornamentation appears to be relatively uncommon among anoles, especially to the degree expressed in Anolis baleatus (and several other crown-giant ecomorph anoles). Considering the osteologically robust appearance of crown-giants, even at early stages of ontogenetic development, this gives rise to questions regarding the development of these ornamental patterns. Thanks to the collection efforts of Luke Mahler (University of Toronto), and a postdoctoral position in his lab, I was able to acquire CT-image data representing an ontogenetic series of this species, ranging from very young juveniles to skeletally mature adults.

While parts of the paired frontals of juveniles are covered in modest eminences, prominent cranial ornamentation is absent from small specimens (see figure). Likely, growth of these ornaments begins very late during ontogenetic development. Ornaments on the prefrontals and parietal are only evident in specimens that, to the best of our judgement, are approaching sexual maturity. We looked at fifteen specimens per sex, representing a range of juvenile and subadult sizes, and this general pattern is consistent throughout the image data. Schwartz (1974) inferred that anoles in the ricordii group reach sexual maturity between 100 and 110 mm snout-vent length (SVL), and we observed the first prominent ornaments at sizes between 90 and 95 mm SVL. Assuming that differences in size directly represent ontogenetic growth, these findings imply that Anolis baleatus starts to grow elaborate ornamentation as it approaches sexual maturity, and that expansion and growth of these ornaments then continues into skeletal maturity. Interestingly, both males and females appear to develop them at roughly the same body size.

The function and evolutionary cause of these structures remain unknown, and these are questions we are currently investigating. Body size is an important correlate for the occurrence of cranial ornaments, but these structures may also conceivably play roles in defense, feeding, or intraspecific agonistic interactions. Stay tuned!

Videos

A. baleatus, female, 55 mm SVL

A. baleatus, female, 65 mm SVL

A. baleatus, female, 96 mm SVL

A. baleatus, female, 126 mm SVL

References

Etheridge, R. & de Queiroz, K. (1988): A phylogeny of Iguanidae.─ [In:] Estes, R.D. & Pregill, G.K. (eds.): Phylogenetic Relationships of the Lizard Families: Essays Commemorating Charles L Camp, 283-367; Stanford: Stanford University Press.

Evans, S. (2008): The skull of lizards and tuatara.─ [In:] Gans, C., Gaunt, A.S. & Adler, K. (eds.), Biology of the Reptilia, vol. 20:1-347; Society for the Study of Amphibians and Reptiles, Ithaca, New York.

Poe, S. (1998): Skull characters and the cladistic relationships of the Hispaniolan dwarf twig Anolis.─ Herpetological Monographs, 12:192-236; The Herpetologists’ League.

Schwartz, A. (1974): An analysis of variation in the Hispaniolan giant anole, Anolis ricordi Dumeril and Bibron.─ Bull. Mus. Comp. Zool., 146:89-146.

Geometric Morphometric Analysis of the Shoulder of Jamaican Anoles

By Alex Tinius

On January 15, 2015

In Lizards in an Evolutionary Tree, New Research, Research Methods

Birds are lovely animals. Our avian friends swoop through the air, defecate on field equipment, and consume lizards. What’s not to like?! Well, their shoulder region, for example. Lost interclavicle, reverted muscle pathways, and so many other anatomical adaptations that appear crucial for the modern avian life style, but that are hard to explain in a gradual-evolutionary context. Reconstructing the structural evolution of the avian shoulder remains a challenging task to students of biomechanics and kinematics. When I left my European homestead to enter the Canadian realm of biological sciences, I was hoping to solve the evolutionary mystery of the avian shoulder, at least in part. Alas, the discovery of anoles sent me on a much more convoluted journey.