Review Article |
Corresponding author: Eduardo Ascarrunz ( eascarrunz@mailfence.com ) Corresponding author: Marcelo R. Sánchez-Villagra ( m.sanchez@pim.uzh.ch ) Academic editor: Ingmar Werneburg
© 2022 Eduardo Ascarrunz, Marcelo R. Sánchez-Villagra.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Ascarrunz E, Sánchez-Villagra MR (2022) The macroevolutionary and developmental evolution of the turtle carapacial scutes. Vertebrate Zoology 72: 29-46. https://doi.org/10.3897/vz.72.e76256
|
The scutes of the carapace of extant turtles exhibit common elements in a narrow range of topographical arrangements. The typical arrangement has remained constant since its origin in the clade Mesochelydia (Early Jurassic), after a period of apparent greater diversity in the Triassic. This contribution is a review of the development and evolutionary history of the scute patterns of the carapace, seen through the lens of recent developmental models. This yields insights on pattern variations in the fossil record. We reinterpret the “supracaudal” scute and propose that Proganochelys had five vertebral scutes. We discuss the relationship between supramarginal scutes and Turing processes, and we show how a simple change during embryogenesis could account for origin of the configuration of the caudal region of the carapace in mesochelydians. We also discuss the nature of the decrease in number of scutes over the course of evolution, and whether macroevolutionary trends can be discerned. We argue that turtles with complete loss of scutes (e.g., softshells) follow clade-specific macroevolutionary regimes, which are distinct from the majority of other turtles. Finally, we draw a parallel between the variation of scute patterns on the carapace of turtles and the scale patterns in the pileus region (roof of the head) of squamates. The size and numbers of scales in the pileus region can evolve over a wide range, but we recognized tentative evidence of convergence towards a typical configuration when the scales become larger and fewer. Thus, typical patterns could be a more general property of similar systems of integumentary appendages.
canalization, ontogeny, pholidosis, scales, Squamata, Testudines, variation
A conspicuous feature of amniotes is the diversity of skin appendages that cover their bodies, such as hair in mammals, feathers in birds, and scales in reptiles (including the legs of birds). These appendages have been found to develop in the embryo from specialized plate-like patches of thickened epidermis, called placodes (Oliveira-Martinez et al. 2003;
Here, we review different aspects of an outstanding example of evolutionarily conserved pholidosis: the mosaic of scutes of the carapace of the dorsal shell of turtles (carapace). It is a rare opportunity to be able to study the evolutionary history of patterns of epidermal appendages in deep time with abundant palaeontological data, and the turtle shell probably provides the best material of this kind.
The first known turtles with a carapace (turtles with a carapace = clade Testudinata; crown turtles = clade Testudines) are from the Late Triassic (Norian, 227-208 Ma) (
In this contribution we integrate a series of recent studies in palaeontology and developmental biology, including a model based on reaction-diffusion processes (
We focus our discussion in the carapace, as the development of the plastron (ventral portion of the shell) has not been studied in similar detail. The developmental systems of scute patterning on the carapace and plastron are considered independent (
Both carapace and plastron are made up of an internal layer of bone plates with contributions of the ribs, and an external layer of scutes. Secondarily, the leatherback sea turtle Dermochelys coriacea, the soft-shelled turtles (Trionychidae) and Carettochelys insculpta do not have scales on the carapace. Soft-shelled turtles are particularly divergent in their shell and its mode of development (
Excepting the hawksbill sea turtle Eretmochelys imbricata, there is little or no overlap between scutes. The limits between adjacent scutes form epidermal furrows termed seams, following the terminology proposed by
The bone plates and scute mosaic of the carapace of the vast majority of modern turtles conform to a basic plan that appeared in the clade Mesochelydia (
Synthetic phylogeny of testudinatans highlighting many of the species and clades mentioned in the text. Based mainly on
The external anatomy of the bony carapace of testudinatans. Pholidosis is shown by the imprints (sulci) left by the borders of the corneous scutes. Kayentachelys aprix is the oldest known testudinatan that displays the complete mesochelydian plan: the general layout of bone plates and scutes that is preserved in the majority of living turtles, such as the emydid Malaclemys terrapin. Earlier testudinatans like Proganochelys quendstedti and Proterochersis porebensis (reconstructions) had more capacial scutes, and the series of marginal scutes did not meet in the posterior part of the carapace. Proterochersis also shows evidence of numerous irregular bone plates that are not present in mesochelydians; see Szczygielski & Sulej (2019) for details. Labelled elements are bone plates. Scute homologies are colour-coded. Thin lines represent bone plate sutures; thick lines represent sulci. The sutures in Proganochelys are unknown. Proganochelys after
The underlying bone plates follow a similar arrangement that is however non-congruent with the scute pattern (Fig.
The following account synthesizes findings from
The major feature in the early development of the carapace are the “carapacial ridges”: two nearly parallel longitudinal bulges between the anterior and posterior limb buds, in the flanks of the dorsal region of the embryo (
In subsequent stages of turtle carapace development, a series of six pairs of placodes appears along the midline, on the dorsum of the trunk of the embryo. The five posterior pairs of placodes are the primordia of the five vertebral scutes, and the anterior pair are the primordia of the cervical scute (
The formation of the seams between the scutes has been described in detail by
The identities of all the carapacial scutes are thus settled, and their subsequent development is mostly concerned with changes in their proportions and further maturation of the epithelium (
The turtle carapace provided one of the many examples that D’Arcy
Over the course of the last few decades, Cherepanov and colleagues (
A causal model to explain the generation of scute patterns based on Turing patterns was introduced by
The model of
This relatively simple model is highly successful in reproducing key features of the scute mosaic. The first reaction-diffusion process originating from the twelve pairs of marginal placodes induce the formation of two rows of four or five “pleural” placodes, and a medial row of six pairs of placodes representing the cervical and the five vertebrals. The second reaction-diffusion process mimics the growth of the primordia and the appearance of the scute seams. The result is most satisfactory in the middle region of the trunk, even reproducing the fusion of the pairs of primordia of vertebrals II, III, and IV (Fig.
Simulations of pholidosis of the carapace with a reaction-diffusion model. Darker colours indicate higher concentrations of activator of the first reaction diffusion-process (A1) or the inhibitor of the second reaction-diffusion process (I2). A, The beginning (t=0) and end (t=250000 iterations) of the simulation with the original parameters of
The model was also successful in replicating abnormal scute patterns of actual turtles (
The reaction-diffusion model provides a causal complement to the general thrust of the segment-dependent model. This is particularly relevant because, beyond the pre-pattern of twelve marginal placodes along the carapacial ridges, the reaction-diffusion model involves no concept of body segmentation. Still, it has not been explored to what extent the reaction-diffusion model can reproduce the range of intraspecific supernumerary scale variations that are strongly suggestive of the strict correspondence between myosepta and scute placodes (
There are only eight known and undisputed species of non-mesochelydian turtles, most of them from the Norian (Late Triassic, 227–208.5 Ma; except Australochelys africanus from the Hettangian) (Fig.
The most complex pholidosis is seen in Proganochelys quendstedtii (Fig.
The almost complete scutation pattern can also be observed in Proterochersis porebensis and Proterochersis robusta, where there are typically one cervical, five vertebrals, four pairs of pleurals, 14 marginals (at least 12 in Proterochersis porebensis), and three supramarginals (
The left and right series of marginal scutes do not meet at the midline in the caudal region of the carapace in any of the earliest testudinatans where this condition can be ascertained: Proganochelys quendstedti, Proterochersis spp., Waluchelys cavitesta, and Palaeochersis talampayensis (
We propose, first, that the fundamental difference in the development of the caudal region of the carapace of basal testudinatans was the failure of the lateral marginal scute series to meet at the midline, posterior to the primordium of vertebral V. It is easy to derive this inference from the fact that in extant turtles the series of marginal scute primordia develop early along the carapacial ridges, when the ridges are roughly parallel to each other, on the flanks of the embryo. Thus, vertebral V remains at the postero-medial edge of the carapace, preserving the relative position of the scute primordia from the early stages of development. This leads us directly to a second proposition: that it might not be necessary to retain the notion of a distinct kind of scute called “supracaudal”, unique to basal testudinatans. Instead, we propose that the “supracaudal” attributed to Proganochelys and Waluchelys might be a very short vertebral V, with the same topological relations as seen in Proterochersis, except with respect to the supramarginals. Embryological observations and the reaction-diffusion model show that the all scutes along the midline of the carapace (the cervical and the vertebrals) have the same initial mode of development from paired placodes (
Thus, in our new interpretation, Proganochelys has five vertebral scutes, just as Proterochersis and the vast majority of mesochelydians. The pholidosis of the central region of the carapace of other basal testudinatans is unknown, and in the absence of contradictory evidence, it is reasonable to presume that they also had five vertebral scutes in total.
Another possible interpretation of the nature of the “supracaudal” of basal testudinatans, is that it is the result of the fusion of multiple marginal scutes, and therefore the marginal series meet in the caudal region of the carapace in Proganochelys and Waluchelys. A fusion of the XIIth pair of scutes occurs in tortoises (Testudinidae), which results in a single scute occupying the posteromedial edge of the carapace (see above) (
Comparison of the carapace pholidosis of several testudinatans. Waluchelys cavitesta after
Apart from the caudal notch, another distinctive feature of basal testudinatans is the presence of supramarginal scutes. This is the most difficult series of scutes to characterize, as their numbers and anatomical location vary widely across species. In addition to basal testudinatans, supramarginal scutes also occur in the alligator snapping turtle Macrochelys temminckii (
The evolution of the testudinatan shell from the Triassic to the present has resulted in a net reduction in the average number of its constituent elements. Various authors have thus recognized this as a macroevolutionary trend towards simplification of both the numbers of bony plates and epidermal scutes (
Here we take a closer look at the history of gains and losses of carapacial scutes. We will first consider the majority of turtles that retain the epidermal scutes. We will address turtles with complete loss of scutes separately.
The modern turtle shell displays a distinctive pholidotic pattern in that a large surface of the body is covered with a mosaic of few scales (typically 38 in the carapace; Fig.
Gains and losses of scutes. Minimal (most parsimonious) independently accumulated gains and losses of carapacial scutes apomorphic for selected species or clades of testudinatans. The “nuchal scute” (
Clade or species | Cervicals | Vertebrals | Pleurals (pairs) | Marginals (pairs) | Other (pairs) | Reference |
Mesochelydia | 0 | 0 | 0 | –2 to –4 | –2 to –12 |
|
Elseya | –1 | 0 | 0 | 0 | 0 | Ascarrunz, unpublished |
Kinosternidae | 0 | 0 | 0 | –1 | 0 |
|
Lepidochelys olivacea (Carettinae) | 0 | 0 to +2 | +1 to +2 | +1 | 0 |
|
Macrochelys | 0 | 0 | 0 | 0 | +3 to +4 |
|
Notochelys platynota | 0 | +1 | 0 | 0 | 0 |
|
Pelomedusoides | –1 | 0 | 0 | 0 | 0 | Ascarrunz, unpublished |
Testudo graeca (Testudinidae) | –1 | 0 | 0 | –1 | 0 |
|
Boremys grandis † (Eubaeninae) | +2 | +1 | 0 | 0? | +9? |
|
Clemmydopsis mehelyi † | 0 | 0 | –2 | 0 | 0 |
|
Kallokibotion † | –1 | 0 | 0 | 0 | 0 |
|
Naomichelys speciosa † | 0 | 0 | 0 | 0 | +1 |
|
Platychelys oberndorferi † | 0 | 0 | 0 | 0 | +3 |
|
Pleurosternidae † | –1 | 0 | 0 | 0 | 0 |
|
Sakya riabinini † | 0 | +5 | +6 | +2 | 0 |
|
Tropidemys seebachi † (Thalassochelydia) | +1 | +3? | 0? | 0? | +3? |
|
Total gains – losses | –2 | +10 to +12 | +5 to +6 | –1 to –3 | +7 to +18 |
Cordero & Vlachos (2021) presented the first quantitative analyses of the evolution of the numbers of shell elements with comparative methods. But they too acknowledge that scute gains and losses represent fairly rare events over the course of the evolutionary history of testudinatans, and that it is difficult to sample the relevant species in an unbiased manner. For this reason, the overall rate of change in scute number is bound to be small. If there are statistically identifiable trends in the dominant macroevolutionary regime, they are subtle. Properly characterizing them will require extensive scute number variation data, and a comprehensive time-scaled phylogeny of testudinatans. Neither are available at the moment.
Finally, we note that it is difficult to conceive a distinct and plausible mechanism for between-lineage downward trends in scute number. Between-lineage dynamics have been attributed to species selection (
It has been suggested that groups of species in a new “Bauplan” have more variability (i.e., more capacity to generate variation) than subsequent clades, which are less prone to vary (
The evolutionary history of testudinatan carapacial scutes involved different macroevolutionary regimes. We examine in the following subsections the clades that feature complete loss of shell scutes: Trionychia, and the marine turtles Dermochelyidae and Protostegidae. The developmental processes that produce total loss of scutes (see below) are quite different from the ones that produce the loss of individual scutes, where the total corneous coverage of the shell is preserved by fusions or compensatory expansions of other scutes in a space-filling manner (reviewed in
The clade Trionychia includes the Trionychidae (softshell turtles) and Pan-Carettochelys (the scute-less pig-nosed turtle Carettochelys insculpta and numerous extinct relatives;
We infer that in early trionychids and the ancestors of Carettochelys, scute loss was driven by the adaptive value in the decornification of the skin covering the shell, and a relaxation of the strength of natural selection for the maintenance the developmental system of periodic patterning that determines the scute mosaics. Similar hypotheses have been put forward by previous authors (
It is more difficult to hypothesize about the drivers for scute loss in the marine turtle clades Protostegidae and Dermochelyidae. Only the latter is represented by an extant species, the leatherback turtle Dermochelys coriacea. The Protostegidae might be stem-chelonioids or the sister clade of Dermochelyidae (
It is illuminating to seek parallels between character systems in different clades. For the pholidosis of the turtle carapace, though, is difficult to come by with analogous (or homologous) character systems that display relevant similarities in the morphological, developmental, and evolutionary characteristics that we have discussed in this paper. For instance, the large scales on the body of pangolins do not grow in a surface-filling fashion forming a mosaic, as they are arranged in numerous overlapping rows (
We identified a more satisfactory analogue in a different anatomical region. There is great diversity in the pholidotic patterns of the head in squamates, including mosaics of scales of a wide range of sizes, from proper scutes to small “granular” scales. In squamates excluding gekkotans and dibamids, scutes are fairly common in the “pileus region”: the dorsal surface of the head extending from the tip of the rostrum to the occiput. Notably, when scutes are found in the pileus, they have a tendency to be form similar arrangements, and individual scutes can be recognized between species (
Pileus scalation patterns in squamates. Left: Traditionally hypothesized homologies of scales between different squamate clades. Identities become clear only when the scales are large, forming scutes. Diagrams after
In a manner roughly analogous to the mesochelydian plan, a stereotypical pileus scute pattern has been considered ancestral for squamates (
Based on photographic data collected for a previous study (
The head is a complex anatomical structure that tightly accommodates and supports diverse sense organs and mechanical feeding specializations, among other functions. Turtle shells, in contrast, provide a vessel for a large body cavity where organs are arranged more freely, and are routinely displaced due to head and limb tucking, food intake, and gravidity. Unlike bones, most specific scales are not intimately associated with other critical components of the head (except the interoccipital scale with the pineal eye in lizards, and scales surrounding eyes and nares), and therefore the topography of the scutes should be more prone to vary with respect to the geometric and mechanical diversity of the vertebrate head. A worthy avenue of research would be to examine if the evolution of pholidotic patterns and scale size reflect the parallel ecological adaptations seen in the gross head geometry of pythons and boas (
We infer that the scale systems of the turtle carapace and the pileus of squamates are subject to similar kinds of developmental biases (
In turtles, a release from the bias towards the mesochelydian plan occurs in trionychians and Dermochelys, where the lack of scutes obviates the need for preserving a patterning morphogenetic process (
Unfortunately, the fossil record is unlikely to shed light in the matter. Unlike the bony shell (
Developmental models aid palaeontologists to assess problems about character change in explicit causal frameworks. Even if the models do not suffice to explain all the relevant variation, they can shed light on matters previously only understood as far as the traditional approach of pattern-matching can reveal. In the carapace, the recent discoveries highlight the relationship between body segmentation and scute patterning, and how the same structures in the flanks of the carapace, –the carapacial ridges–, contribute to the formation of the outer ring of the carapace while possibly inducing its internal integumental patterning, as suggested by the temporal and causal priority of the marginals over the pleurals and vertebrals. We showed how the origin of the mesochelydian plan can be understood in these terms.
For the vast majority of turtles that retain their scutes, the macroevolutionary patterns are more complex and subtle than what might be conveyed by the “trend toward scute loss” that is traditionally suggested in the literature. Still, the reasons why scute number evolution remains highly constrained remain unknown, especially in contrast with what it is possible to induce in the developmental models, and also with what is seen in the diversity resulting from a similar developmental system in squamates.
On a more general note, we hope that this paper is an example of how considerations of ontogeny offer a deeper and necessary understanding of morphological transformations that occur in macroevolutionary time (
We are deeply indebted to Damien Esquerré for sharing his photographic data of boas and pythons. We thank Julien Claude, Serjoscha Evers, Torsten Scheyer, and Walter Joyce for discussions and bibliographic material, as well as Gerardo Cordero and an anonymous reviewer for fruitful suggestions and critiques. We thank Ingmar Werneburg and Irina Ruf for the chance to publish this work in honour of Wolfgang Maier and their leadership in this noble task.
MRSV thanks Roland Zimm and Isaac Salazar-Ciudad for the opportunity to participate in Roland’s doctoral thesis evaluation committee and thus become acquainted with this important and beautiful work.
MRSV expresses his deep gratitude to Wolfgang Maier for the exceptional professional opportunities he created to him and the mentorship over the many years, including of course countless discussions and teachings on comparative anatomy and developmental evolution.
Control files for simulations
Data type: .zip
Explanation note: Control files for simulations with the reaction-diffusion model.