Heterochrony and developmental modularity of cranial osteogenesis in lipotyphlan mammals

Abstract

BackgroundHere we provide the most comprehensive study to date on the cranial ossification sequence in Lipotyphla, the group which includes shrews, moles and hedgehogs. This unique group, which encapsulates diverse ecological modes, such as terrestrial, subterranean, and aquatic lifestyles, is used to examine the evolutionary lability of cranial osteogenesis and to investigate the modularity of development.ResultsAn acceleration of developmental timing of the vomeronasal complex has occurred in the common ancestor of moles. However, ossification of the nasal bone has shifted late in the more terrestrial shrew mole. Among the lipotyphlans, sequence heterochrony shows no significant association with modules derived from developmental origins (that is, neural crest cells vs. mesoderm derived parts) or with those derived from ossification modes (that is, dermal vs. endochondral ossification).ConclusionsThe drastic acceleration of vomeronasal development in moles is most likely coupled with the increased importance of the rostrum for digging and its use as a specialized tactile surface, both fossorial adaptations. The late development of the nasal in shrew moles, a condition also displayed by hedgehogs and shrews, is suggested to be the result of an ecological reversal to terrestrial lifestyle and reduced functional importance of the rostrum. As an overall pattern in lipotyphlans, our results reject the hypothesis that ossification sequence heterochrony occurs in modular fashion when considering the developmental patterns of the skull. We suggest that shifts in the cranial ossification sequence are not evolutionarily constrained by developmental origins or mode of ossification.

Sexual Dimorphism of Craniodental Morphology in the Raccoon Dog <i>Nyctereutes procyonoides</i> from South Korea

“…One explanation for this variability is that the selective forces acting upon the craniodental morphology of each sex may be different between populations. However, it should be noted that many craniodental traits are often associated with one another [11,18,19]. If quantitative aspects of such traits are significantly integrated in a likewise manner, the apparent sexual dimorphism observed in some traits might be a byproduct of true sexual dimorphism.…”

Bony skull development in the Argus monitor (Squamata, Varanidae, Varanus panoptes) with comments on developmental timing and adult anatomy

“…As a methodological problem, the stage resolution among the studied species has an important influence when reconstructing ancestral sequences and may disguise actual developmental patterns (discussed by Germain and Laurin, 2009;Werneburg andSánchez-Villagra, 2009, 2011;Koyabu et al, 2011;Laurin and Germain, 2011;Werneburg et al, 2013b). Small sample sizes for particular embryological ages inevitably provide reduced resolution for the timing of any given developmental event.…”

“…Although the onset of ossification only represents a minute excerpt of a long process of bone differentiation, recent comparative studies of the sequence of developmental events in skeleton formation have suggested general patterns of developmental similarity across a range of vertebrate groups (Sánchez-Villagra, 2002;Schoch, 2006;Maxwell, 2008;Weisbecker et al, 2008;Germain and Laurin, 2009;Weisbecker and Mitgutsch, 2010;Koyabu et al, 2011Koyabu et al, , 2014Werneburg and Sánchez-Villagra, 2015). As a rule of thumb, the earlier an element appears during development, the more prominent it becomes in the adult because it has more time to grow (Mehnert, 1897(Mehnert, , 1898Huxley, 1932;Sánchez-Villagra et al, 2008;Maxwell, 2009;Maxwell and Larsson, 2009;Werneburg and Sánchez-Villagra, 2015).…”

“…For developing bones, different mesenchymal anlagen might be connected in an ontogenetic and evolutionary sense. Consequently, evolutionary, developmental, and modular considerations should be applied where possible and tested (Koyabu et al, 2011). Finally, the accelerated or decelerated development and expansion of one particular element may prevent or allow two or more other elements to come in contact and to form sutures or attachments in adult anatomy (see Section 4.3.…”

The fossil record of phenotypic integration and modularity: A deep-time perspective on developmental and evolutionary dynamics

“…Many layers of developmental patterning may obscure each other, termed the "palimpsest" problem (42). Indeed, there seems to be little to no relationship between cranial phenotypic modules and coordination of skeletal heterochronies (25,(43)(44)(45), unlike in the postcranial skeleton. Nonetheless, quantitative approaches can estimate the developmental contribution to phenotypic integration in fossil taxa, even without identifying a specific developmental driver, by measuring fluctuating asymmetry (FA).…”