Integration of Morphological Data Sets for Phylogenetic Analysis of Amniota: The Importance of Integumentary Characters and Increased Taxonomic Sampling

Abstract

Several mutually exclusive hypotheses have been advanced to explain the phylogenetic position of turtles among amniotes. Traditional morphology-based analyses place turtles among extinct anapsids (reptiles with a solid skull roof), whereas more recent studies of both morphological and molecular data support an origin of turtles from within Diapsida (reptiles with a doubly fenestrated skull roof). Evaluation of these conflicting hypotheses has been hampered by nonoverlapping taxonomic samples and the exclusion of significant taxa from published analyses. Furthermore, although data from soft tissues and anatomical systems such as the integument may be particularly relevant to this problem, they are often excluded from large-scale analyses of morphological systematics. Here, conflicting hypotheses of turtle relationships are tested by (1) combining published data into a supermatrix of morphological characters to address issues of character conflict and missing data; (2) increasing taxonomic sampling by more than doubling the number of operational taxonomic units to test internal relationships within suprageneric ingroup taxa; and (3) increasing character sampling by approximately 25% by adding new data on the osteology and histology of the integument, an anatomical system that has been historically underrepresented in morphological systematics. The morphological data set assembled here represents the largest yet compiled for Amniota. Reevaluation of character data from prior studies of amniote phylogeny favors the hypothesis that turtles indeed have diapsid affinities. Addition of new ingroup taxa alone leads to a decrease in overall phylogenetic resolution, indicating that existing characters used for amniote phylogeny are insufficient to explain the evolution of more highly nested taxa. Incorporation of new data from the soft and osseous components of the integument, however, helps resolve relationships among both basal and highly nested amniote taxa. Analysis of a data set compiled from published sources and data original to this study supports monophyly of Amniota, Synapsida, Reptilia, Parareptilia, Eureptilia, Eosuchia, Diapsida, Neodiapsida, Sauria, Lepidosauria, and Archosauriformes, as well as several more highly nested divisions within the latter two clades. Turtles are here resolved as the sister taxon to a monophyletic Lepidosauria (squamates + Sphenodon), a novel phylogenetic position that nevertheless is consistent with recent molecular and morphological studies that have hypothesized diapsid affinities for this clade.

Sauropod dinosaur osteoderms from the Late Cretaceous of Madagascar

“…The structural organization (compact cortex, cancellous core) and bone histology of the juvenile specimen (UA 9331) are broadly comparable with those of other archosaurs [1][2][3][4]7 . In contrast, the gross anatomical and microscopic structure of the adult-sized specimen (FMNH PR 2342) is unique.…”

“…The shape and surface texture of Rapetosaurus osteoderms indicates that these elements were low in relief and embedded in the integument as in other vertebrates [1][2][3]14,16 . As evidenced from extant taxa, all osteoderms form and reside within the dermis, either adjacent to the interface between the strata superficiale and compactum, or exclusively within the stratum superficiale, and are overlain by the epidermis [1][2][3][14][15][16][17] . The surface texture of Rapetosaurus osteoderms is consistent with the hypothesis that, as in crown group archosaurs, these structures were overlain by epidermal scales [1][2][3] .…”

“…Instead, we hypothesize that Rapetosaurus (and probably most titanosaurs) was characterized by a small number of osteoderms. Furthermore, unlike many osteoderm-bearing archosaurs [1][2][3] , these elements did not develop pervasively throughout the dermis but were probably restricted to the isolated regions of the integument. Whereas previous descriptions had reported the presence of articulating mosaics of osteoderms from the Maevarano formation 5 , we reinterpret these 'mosaics' as the fragmentary remains of individual adult-sized cavitied elements that were crushed post-mortem.…”

“…As evidenced from extant taxa, all osteoderms form and reside within the dermis, either adjacent to the interface between the strata superficiale and compactum, or exclusively within the stratum superficiale, and are overlain by the epidermis [1][2][3][14][15][16][17] . The surface texture of Rapetosaurus osteoderms is consistent with the hypothesis that, as in crown group archosaurs, these structures were overlain by epidermal scales [1][2][3] . The hollow nature of the adult specimen is unique, and we speculate that the juvenile morph remodels to achieve the adult form.…”

“…1c-e). Computed tomographic (CT) scans demonstrate that the pristinely preserved outer cortex of dense, compact bone is underlain by a cancellous core of bony trabeculae similar to that of other amniote osteoderms [1][2][3][4] ( Fig. 1e).…”