Development of the cypriniform protrusible jaw complex in Danio rerio: Constructional insights for evolution

Abstract

Studies on the evolution of complex biological systems are difficult because the construction of these traits cannot be observed during the course of evolution. Complex traits are defined as consisting of multiple elements, often of differing embryological origins, with multiple linkages integrated to form a single functional unit. An example of a complex system is the cypriniform oral jaw apparatus. Cypriniform fishes possess an upper jaw characterized by premaxillary protrusion during feeding. Cypriniforms effect protrusion via the kinethmoid, a synapomorphy for the order. The kinethmoid is a sesamoid ossification suspended by ligaments attaching to the premaxillae, maxillae, palatines, and neurocranium. Upon mouth opening, the kinethmoid rotates as the premaxillae move anteriorly. Along with bony and ligamentous elements, there are three divisions of the adductor mandibulae that render this system functional. It is unclear how cypriniform jaws evolved because although the evolution of sesamoid elements is common, the incorporation of the kinethmoid into the protrusible jaw results in a function that is atypical for sesamoids. Developmental studies can show how biological systems are assembled within individuals and offer clues about how traits might have been constructed during evolution. We investigated the development of the protrusible upper jaw in zebrafish to generate hypotheses regarding the evolution of this character. Early in development, the adductor mandibulae arises as a single unit. The muscle divides after ossification of the maxillae, on which the A1 division will ultimately insert. A cartilaginous kinethmoid first develops within the intermaxillary ligament; it later ossifies at points of ligamentous attachment. We combine our structural developmental data with published kinematic data at key developmental stages and discuss potential functional advantages in possessing even the earliest stages of a system for protrusion.

Flexibility in starting posture drives flexibility in kinematic behavior of the kinethmoid-mediated premaxillary protrusion mechanism in a cyprinid fish,Cyprinus carpio

“…Rotation of the kinethmoid moves its dorsal end rostrally, and it pushes via a ligament on the premaxilla, causing protrusion; the same result can be accomplished via manual manipulation of anesthetized or freshly killed animals. The ligamentous attachment between these bones is histologically suited to act in compression, as it is enriched with hyaline cell cartilage and low in fibrous tissue (Benjamin, 1989), and the ontogenetic onset of protrusion coincides with kinethmoid ossification (Staab and Hernandez, 2010). We have not attempted to investigate the forces imposed in vivo on the premaxilla by protrusion or tested the material properties of this ligament, though this could be a fruitful approach.…”

“…The kinethmoid is a cypriniform synapomorphy and is ubiquitous across this clade of nearly 3500 species (Simons and Gidmark, 2010), with the exception of one highly miniaturized species (Britz et al, 2009). The kinethmoid is an unpaired, midline sesamoid bone or cartilage that develops within the intermaxillary ligament (Staab and Hernandez, 2010). In adult fishes it is suspended within a ligamentous network, with connections to the premaxillae, maxillae, palatines and neurocranium (Fig.2).…”

The development of zebrafish tendon and ligament progenitors

“…However, the tendon and ligament populations have never been characterized in this context. Head tendons and ligaments have been described in teleosts in terms of comparative morphology and feeding mechanics (Cubbage and Mabee, 1996;Diogo et al, 2008;Liem, 1967;Staab and Hernandez, 2010;Westneat, 1990). Most developmental studies have focused on the formation of the jaw joint (Miller et al, 2003;Nichols et al, 2013;Talbot et al, 2010) and have described the regions where muscles attach to cartilage as muscle insertion sites (Schilling and Kimmel, 1997).…”

Independently evolved upper jaw protrusion mechanisms show convergent hydrodynamic function in teleost fishes

“…This is because the rapid advancement of the mouth towards the prey increases the acceleration of the fluid around the prey, a major component of force when prey resist the flow by clinging to a holdfast or swimming away from the predator upper and lower jaws, these fishes have an additional bone involved in the jaw protrusion mechanism. The kinethmoid, a synapomorphy uniting cypriniforms, is a novel median bone that is suspended by ligaments linking the upper jaws to the neurocranium (Hernandez et al, 2007;Staab and Hernandez, 2010). As the mouth opens, the kinethmoid rotates anteriorly, and the premaxillae are protruded by forces acting at the posterior end of the premaxilla ascending process.…”