Linking form and function of the fibrous joints in the skull: A new quantification scheme for cranial sutures using the extant fish Polypterus endlicherii

Abstract

The aim of this study is to connect specific sutural morphologies with the specific types of deformation they experience. To meet this goal, we quantified the morphologies of the interfrontal (IF), interparietal (IP), and frontoparietal (FP) sutures in the extant fish Polypterus endlicherii, and used our published measurements of in vivo deformation of these sutures during feeding to infer how suture morphology and function are connected. Specifically, we found that three relatively simple measures of cross-sectional suture complexity (i.e., the ratio of total sutural length to its shortest end-to-end length; amount of sutural overlap; and size of the largest interdigitation) can be used to distinguish between the IF, FP, and IP sutures, which exhibit very different cross-sectional shapes and responses to loading. Interestingly, these differences in cross-sectional morphology are not reflected by the linear traces of these sutures on the surface of the skull, implying that cross-sectional shape of a suture must be known to infer the loading conditions it experiences. Plotting the three cross-sectional metrics against one another to yield a sutural morphospace shows that the IF, IP, and FP sutures define regions that are largely distinct from one another. Our previous measurements of strain across these sutures suggested that the FP region would lie between the IF and IP regions; instead, the FP region is largely set apart from the other two fields. Based on this discovery, and on the locations of cranial muscles, we propose a new model of deformation in the skull of P. endlicherii during feeding, in which rotation parallel to the skull roof is combined with bending, subjecting the FP suture to complex shearing. Finally, although the sutures of P. endlicherii appear to be significantly less complex than those of mammals, these fish sutures show a similar range of morphologies and perform similar functions as do mammalian sutures. J. Morphol. 268:89-102, 2007 KEY WORDS: cranial sutures; suture morphology; morphospace; PolypterusWithout knowing the what, the how, and the why, one may stand, not for hours or days, but for weeks before a fish's skull, and our contemplation will be little more than a vacant stare at its complex stalictitic form.German anatomist L. Oken, quoted by R. Owen, 1854 The mechanical role of cranial sutures has been the focus of much research over the past 30 years

Terrestrial-style feeding in a very early aquatic tetrapod is supported by evidence from experimental analysis of suture morphology

“…Specifically, we found that the IF suture in Polypterus is tensed, whereas the IP suture is compressed during feeding (23). The FP suture of Polypterus may experience tension or compression (23), which probably indicates shearing or bending (27). Based on these correlations between suture form and function, we assume the following: that fossil sutures that plot in the morphospace volume defined by the Polypterus IF suture measurements (pink) experienced tension; that sutures that lie in the Polypterus IP volume (blue) experienced compression; and that fossil suture morphologies that fall in the Polyperus FP volume (green) of the morphospace experienced more complex loading conditions that would have been manifested as a combination of tension and compression (Fig.…”

“…Five metrics (27) were used to quantify the surface traces and cross-sectional morphologies of the interfrontal (IF), interparietal (IP), frontoparietal (FP), and nasofrontal (NF) sutures in Eusthenopteron, Acanthostega, and Phonerpeton: (i) interdigitation index: the length of the suture in cross-section divided by the distance between its ends (21); (ii) amount of overlap (ϭ beveling) in cross-section (19); (iii) size of the largest interdigitation in the suture's cross-section; (iv) bone thickness at the suture; and (v) the index of sinuousity: length of the suture on the surface of the skull divided by the distance between its ends (equals the index of interdigitation in ref. 28).…”

“…To fully describe the suture morphologies exhibited by the fossil taxa, we used a sutural morphospace, rather than considering each metric individually. We used three of the four cross-sectional sutural metrics to make the morphospace, omitting bone thickness because prior analysis of suture form and function during feeding in the extant fish Polypterus showed that bone thickness does not affect the deformation pattern exhibited by a suture (27). Therefore, we plotted only the index of interdigitation, beveling amount, and largest interdigitation size measured in the fossil sutures together with values from positionally comparable sutures in the extant fish Polypterus to create the sutural morphospace (Fig.…”

“…Therefore, we plotted only the index of interdigitation, beveling amount, and largest interdigitation size measured in the fossil sutures together with values from positionally comparable sutures in the extant fish Polypterus to create the sutural morphospace (Fig. 4) (27). Assigning Functions to the Sutural Morphospace.…”

Ontogeny of the Early Triassic Cynodont Thrinaxodon liorhinus (Therapsida): Cranial Morphology

“…Gross observation of the skulls only allowed the surface (ectocranial) trace of the sutures to be examined, a common practice done in many comparative studies (e.g., van Heerden, 1972;Wang et al, 2006); however this may not always indicate the internal structure of the suture (Markey and Marshall, 2007). The internal structure of only a few skulls could be observed, either through serial sections or micro-CT (see below).…”