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Session Schedule & Abstracts

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Saturday 2nd July, 2016

Symposium: Life Underground: Morphological Consequences of Fossoriality 1

Room: Salon F   9:30 am–11:00 am

Moderator(s): C. A. Hipsley, E. Sherratt, & H. C. Maddin
FOS1-1  9:30 am  Introduction to the Symposium. Maddin HC*, Carleton University

FOS1-2  9:45 am  The influence of fossoriality on cranial architecture in caecilian amphibians (Gymnophiona). Brenning M.*, Carleton University; Kleinteich T., Kiel University; Wake M., University of California Berkeley; Maddin H., Carleton University
Abstract: Fossoriality, wherein the head is employed as the primary locomotor organ (i.e., head-first burrowing), has evolved multiple times independently within Tetrapoda. Among these, caecilians have been shown to exert some of the greatest forces against the substrate during burrowing, and this has been attributed to their unique mode of hydrostatic locomotion. In order to gain a clearer understanding of the features associated with their forceful mode of fossoriality, the skulls of caecilians were examined from both morphological and mechanical perspectives. Examination of cranial architecture reveals elements of the dermal skull form extensive lap joints with adjacent elements in the anteroposterior direction, whereas overlap between elements in the mediolateral direction is minimal or absent. Dense networks of collagen fibres span the joint surfaces. In addition, nostrils are rimmed with cartilage throughout life, and joints between certain elements (e. g., maxillopalatine and braincase) are filled with cartilaginous plugs, also predominantly oriented in the anteroposterior direction. Results of finite element analysis support the hypothesis that cranial joints together with strategically placed cartilages form a complex dampening system, capable of reducing the transmission of compressive forces to the braincase and throughout the dermal skull produced during head-first burrowing. These features contrast somewhat with those known for other fossorial tetrapods, and may thus represent important adaptations associated with the style of burrowing observed within the caecilian lineage.

FOS1-3  10:00 am  Eyes underground: The degradation of vision genes in subterranean environments. Emerling CA*, University of California Berkeley; Springer MS, University of California Riverside
Abstract: Vertebrates that have adapted to a subterranean niche experience various extreme conditions, which include a drastic reduction in light exposure. Evolutionary theory predicts that commitment to life underground for millions of years should relax selection on, or select against, traits involved in detecting light, resulting in the degradation of photosensory systems and their underlying genes. Here we test this hypothesis by examining the functionality of 65 vision genes in three fossorial mammals with varying commitments to underground life: the star-nosed mole (Condylura cristata), naked mole-rat (Heterocephalus glaber), and Cape golden mole (Chrysochloris asiatica). We show that the highly subterranean naked mole-rat and golden mole have a greater abundance of visual pseudogenes than the facultatively subaerial star nosed-mole, and the loss of genes is mostly restricted to those that function in bright-light. We provide evidence of complete loss of cone photoreceptors in the golden mole, the first genomic confirmation of pure-rod retinas in a terrestrial vertebrate. We then estimated the timing of vision gene loss and found that it largely postdates inferred adaptations for fossoriality. This suggests that vision pseudogenes can be used to estimate the minimum age of adaptation to a subterranean environment in vertebrates with a limited or absent fossil record. We then show that the loss of bright-light visual genes also occurred early in the history of xenarthrans (sloths, armadillos, anteaters) potentially suggesting an early subterranean bottleneck in this clade. We further demonstrate that genes related to melatonin production and reception also have degraded in xenarthrans, providing further support for this hypothesis.

FOS1-4  10:15 am  Ontogenetic allometry constrains cranial shape of the head-first burrowing worm lizard Cynisca leucura (Reptilia: Squamata: Amphisbaenidae). Hipsley CA*, University of Melbourne; Rentinck MN, Museum für Naturkunde Berlin; Roedel MO, Museum für Naturkunde Berlin; Mueller J, Museum für Naturkunde Berlin
Abstract: Amphisbaenians are fossorial, predominantly limbless squamates with distinct cranial shapes corresponding to specific burrowing behaviors. Little is known of their cranial osteology, which represents a critical loss of information as the majority of morphological investigations of squamate relationships are based on cranial characters. We investigated cranial variation in the West African Coast Worm Lizard Cynisca leucura, a round-headed member of the family Amphisbaenidae. Using geometric morphometric analyses of three-dimensional computed tomographic scans, we found that cranial osteology of C. leucura is highly conserved, with the majority of shape changes occurring during growth as the cranium becomes more slender and elongate, with increasing interdigitation among the dermal roofing bones. The ventral cranium, however, remain loosely connected in adults, likely as a protective mechanism against repeated compression and torsion during burrow excavation. Intraspecific variation was strongly correlated with size from juveniles to adults, indicating a dominant role of ontogenetic allometry in determining cranial shape. Given the fossorial habits of C. leucura, we hypothesize that cranial allometry is under strong stabilizing selection to maintain optimal proportions for head-first digging, thus constraining the ability of individuals to respond to differing selection pressures including sexual selection and variation in diet or microhabitat. For species in which digging performance is less important (e.g., in softer sand), allometric associations during growth may be weakened, allowing changes to the ontogenetic trajectory and subsequent morphological traits. Such developmental dissociation between size and shape, known as heterochrony, may be implicit in the evolution of the other amphisbaenian cranial shapes (shovel, spade and keel), which may themselves be functionally optimized for their respective burrowing techniques.

FOS1-5  10:30 am  Cranial and postcranial specializations for fossoriality in the Permian dicynodont family Cistecephalidae. Kammerer CF*, Museum fuer Naturkunde Berlin; Froebisch J, Museum fuer Naturkunde Berlin
Abstract: Burrowing was a common behavior in small-bodied Permo-Triassic synapsids, as evidenced by an extensive ichnological record and the preservation of in situ skeletons in burrows. However, while some form of den construction may have been prevalent among early synapsids, only a single clade, Cistecephalidae, is currently thought to include obligately fossorial taxa. Evidence for obligate fossoriality in cistecephalids is based on their limb anatomy, which is convergent on that of modern fossorial mammals in the possession of a massive olecranon process, flattened phalanges, and a robust humerus with well-developed supinator process. Here, we present new data on fossorial adaptations in cistecephalids. Cranial adaptations for fossoriality in cistecephalids have received little study, other than general recognition of their broad, flattened skull. However, cistecephalids exhibit significantly more complex cranial sutures than other dicynodonts. The naso-frontal suture of Cistecephalus has a mean degree of interdigitation (measured as path/point length) of 3.61 vs. 1.89 in Diictodon (a taxon found in burrows) and 1.26 in Dicynodon (not found in burrows), and other cistecephalid snout sutures show similar values. We argue this high sutural complexity is related to strain from the surrounding substrate, as in extant head-based fossors such as amphisbaenians. Although some derived cistecephalid taxa mirror extant fossors in reduced orbit size, others retain large orbits and show evidence of binocular vision, indicating significant diversity in behavior within this family. Placing cistecephalid burrowing specializations in a phylogenetic context highlights their uniqueness among dicynodonts: a new specimen of Myosaurus (the sister-taxon of Cistecephalidae), including the first skeleton known for this taxon, shows almost none of their peculiarities, with the only possible exception being a shared reduction in the number of cervical vertebrae to 5.

FOS1-6  10:45 am  Morphological specialization and kinematic flexibility in mole burrowing (Mammalia: Talpidae). Lin YF*, UMass, Amherst; Konow N, Brown University; Dumont ER, UMass, Amherst
Abstract: The interplay between morphological specialization and kinematic flexibility is important for organisms that move between habitats with different substrates. Burrowing is energetically expensive and requires substantial interaction with soil to both break it apart and move it. Moles (Talpidae) have evolved extraordinary forelimb morphologies including an extremely enlarged teres major (75% of total forelimb muscle mass) that spans the shoulder joint, and an unusually long olecranon process on the ulna for attachment of the elbow extensors. Enlarged elbow extensor moment arms have been hypothesized as being important during scratching in other digging mammals. Despite these apparent specializations, moles exhibit different digging behaviors depending upon the compactness of the soil. In loose soil they perform lateral strokes to move the soil aside, but in very compact soil they scratch the soil to loosen it. Using marker-based X-ray Reconstruction of Moving Morphology (XROMM), we tested the hypotheses that in Eastern moles (Scalopus aquaticus) the shoulder is the primary joint involved in lateral strokes, while the elbow joint plays the larger role in scratching. Unexpectedly, we found that both lateral strokes and scratching are primarily driven by movement at shoulder joint. This suggests that the massive teres major is the primary source of muscle force during both lateral strokes and scratching. We also found that the end of the lateral strokes has an additional increment of elbow extension compared to scratching. This enables moles to move and compress soil to open a tunnel with a single stroke. Burrowing by scratching in compact soil requires the moles to clear the tunnel by moving soil to the surface. Our work provides an example of how kinematic flexibility of a very specialized forelimb allows an animal to make use of very different substrates.

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