Cranial joint histology in the mallard duck (Anas platyrhynchos): new insights on avian cranial kinesis

Abstract

The evolution of avian cranial kinesis is a phenomenon in part responsible for the remarkable diversity of avian feeding adaptations observable today. Although osteological, developmental and behavioral features of the feeding system are frequently studied, comparatively little is known about cranial joint skeletal tissue composition and morphology from a microscopic perspective. These data are key to understanding the developmental, biomechanical and evolutionary underpinnings of kinesis. Therefore, here we investigated joint microstructure in juvenile and adult mallard ducks (Anas platyrhynchos; Anseriformes). Ducks belong to a diverse clade of galloanseriform birds, have derived adaptations for herbivory and kinesis, and are model organisms in developmental biology. Thus, new insights into their cranial functional morphology will refine our understanding of avian cranial evolution. A total of five specimens (two ducklings and three adults) were histologically sampled, and two additional specimens (a duckling and an adult) were subjected to micro-computed tomographic scanning. Five intracranial joints were sampled: the jaw joint (quadrate-articular); otic joint (quadrate-squamosal); palatobasal joint (parasphenoid-pterygoid); the mandibular symphysis (dentary-dentary); and the craniofacial hinge (a complex flexion zone involving four different pairs of skeletal elements). In both the ducklings and adults, the jaw, otic and palatobasal joints are all synovial, with a synovial cavity and articular cartilage on each surface (i.e. bichondral joints) ensheathed in a fibrous capsule. The craniofacial hinge begins as an ensemble of patent sutures in the duckling, but in the adult it becomes more complex: laterally it is synovial; whereas medially, it is synostosed by a bridge of chondroid bone. We hypothesize that it is chondroid bone that provides some of the flexible properties of this joint. The heavily innervated mandibular symphysis is already fused in the ducklings and remains as such in the adult. The results of this study will serve as reference for documenting avian cranial kinesis from a microanatomical perspective. The formation of: (i) secondary articular cartilage on the membrane bones of extant birds; and (ii) their unique ability to form movable synovial joints within two or more membrane bones (i.e. within their dermatocranium) might have played a role in the origin and evolution of modern avian cranial kinesis during dinosaur evolution.

Joint histology inAlligator mississippiensischallenges the identification of synovial joints in fossil archosaurs and inferences of cranial kinesis

“…We recently proposed that secondary cartilage played an important role in the evolution of avian cranial kinesis, by allowing the formation of kinetic synovial joints not only within chondrocranial elements, but also within the dermatocranium, as well as mediating novel, derived articulations between elements (i.e. 'secondary articulations' sensu [17,41]). In extant crocodylians, when novel articulations appear, such as the pterygomandibular joint (a putative second jaw joint, [42]), they do not form secondary cartilage but are instead covered by a thick pad of dense irregular connective tissue [42], identical to the connective tissue layers described here on the quadrate ( figure 2h,l ).…”

“…in the chick or mallard ducks; [17,18]). The presence of a cartilage cap on the quadrate but dense connective tissue on the opposing side of the joint could be classified as a mix of a syndesmosis and synchondrosis depending on the investigator's frame of reference.…”

Dinosaur paleohistology: review, trends and new avenues of investigation

“…The skull of vertebrates is composed of two main types of bones: membrane bones that arise directly within the mesenchyme as bone blastemas, and endochondral bones, which first arise as primary cartilage models before being (fully or partially) replaced by bone (Hall, 2005; Couly, Coltey & Le Douarin, 1993). To avoid any confusion, we will refer to these two types of “bones” as “membranous elements” and “endochondral elements.” In modern birds, secondary cartilage is found exclusively on membranous elements, either as articular cartilage (e.g., in ducks, secondary cartilage is found on the squamosal, within the socket that articulates with the quadrate; Bailleul, Witmer & Holliday, 2017) or at muscle or ligamentous insertions (e.g., on the surangular underlying the ligamentum squamosomandibulare in the chick; Hall, 1968). Note that mammals also have secondary cartilage, but based on parsimony and different mechanisms of tissue initiation, it has been determined that avian and mammalian secondary cartilages are not homologous and arose independently during evolution (i.e., in birds, mechanical stimulation is required for both the initiation and maintenance of secondary cartilage, whereas in mammals it is only required for its maintenance; Hall, 2000; also see Supplemental Material in Bailleul, Hall & Horner, 2012).…”

“…Avian secondary cartilage arises from the periosteum of membranous elements, and in comparison, the articular cartilage found on the ends of endochondral elements (e.g., the quadrate, and elements of the chondrocranium) is a type of primary cartilage ( because it originated from the primary cartilage model; Hall, 1967, 1968, 2000; Bailleul, Hall & Horner, 2012). Secondary cartilage may differ slightly microstructurally from the more common primary cartilage (i.e., it may have less extracellular matrix, at least very early in ontogeny, or it may be more fibrous later in ontogeny, e.g., see Bailleul, Hall & Horner, 2012; Bailleul, Witmer & Holliday, 2017) but the identification of this tissue is mostly based on its location (i.e., on a membranous element) and not purely on histological differences (Bailleul, Hall & Horner, 2012). The presence of this “avian” tissue in non-avian dinosaurs suggests that birds inherited this tissue from their non-avian dinosaur ancestors (Bailleul, Hall & Horner, 2012), and provides further phylogenetic evidence at the microscopic scale for the close evolutionary relationship of these groups.…”

The lacrimal/ectethmoid region of waterfowl (Aves, Anseriformes): Phylogenetic signal and major evolutionary patterns

“…The lacrimal bone (os lacrimale) of waterfowl is a small bilateral element lying on the anterolateral edge of the orbit, which usually articulates with the skull at the level of the craniofacial hinge or the lateral margin of the frontal alone (Bailleul, Witmer, & Holliday, 2016; Baumel & Witmer, 1993; Cracraft, 1968). It is a flat bone, variable in shape and mediolateral thickness that in many birds often forms a nearly immobile joint to the ectethmoid, although the latter bone is absent in most anatids.…”