Damien Olivier

Trait decoupling promotes evolutionary diversification of the trophic and acoustic system of damselfishes

Trait decoupling, wherein evolutionary release of constraints permits specialization of formerly integrated structures, represents a major conceptual framework for interpreting patterns of organismal diversity. However, few empirical tests of this hypothesis exist. A central prediction, that the tempo of morphological evolution and ecological diversification should increase following decoupling events, remains inadequately tested. In damselfishes (Pomacentridae), a ceratomandibular ligament links the hyoid bar and lower jaws, coupling two main morphofunctional units directly involved in both feeding and sound production. Here, we test the decoupling hypothesis by examining the evolutionary consequences of the loss of the ceratomandibular ligament in multiple damselfish lineages. As predicted, we find that rates of morphological evolution of trophic structures increased following the loss of the ligament. However, this increase in evolutionary rate is not associated with an increase in trophic breadth, but rather with morphofunctional specialization for the capture of zooplanktonic prey. Lineages lacking the ceratomandibular ligament also shows different acoustic signals (i.e. higher variation of pulse periods) from others, resulting in an increase of the acoustic diversity across the family. Our results support the idea that trait decoupling can increase morphological and behavioural diversity through increased specialization rather than the generation of novel ecotypes.

The cerato-mandibular ligament: a key functional trait for grazing in damselfishes (Pomacentridae)

IntroductionThe success of a taxonomic group can be promoted by a key character that allows the group to interact with its environment in a different way and to potentially occupy new niches. The Pomacentridae possess a synapomorphic trait, the cerato-mandibular (c-md) ligament, which joins the hyoid bar to the inner part of the lower jaw. It has previously been shown that this ligament is a key trait in communication in damselfishes because it enables them to slam the oral jaws shut causing teeth collision and sound production. This specific behavior of mouth closing could, however, also be used for other tasks, such as feeding. Many territorial damselfishes are referred to as farmers, due to their ability to manage algal crops on which they feed. This study hypothesizes that the c-md ligament provides an advantage for grazing filamentous algae, and should thus be considered a key trait for farming behavior.ResultsThe kinematic patterns associated with sound production and biting filamentous algae or attached animal prey are all based on the same mechanism and are associated with a slam of the oral jaws. We observed that transection of the c-md ligaments makes the fish unable to perform such actions. We also counted biting rates on filamentous algae in fish with and without the c-md ligament and observed a drop of more than 80% in the latter.ConclusionThis study shows that the c-md ligament is a key trait both for sound production and for grazing activities in damselfishes. The buccal jaw slam enables the fish to perform accurate strikes on small filamentous algae. This kind of bite probably plays a major role in farming activity and allows grazing damselfishes to occupy distinct niches, possibly increasing their competitive evolutionary success.

A morphological novelty for feeding and sound production in the yellowtail clownfish

The yellowtail clownfish Amphiprion clarkii is able to close its mouth very quickly by means of the cerato-mandibular (c-md) ligament, a synapomorphic trait of Pomacentridae joining the hyoid bar to the medial part of the lower jaw. This fast closure induces tooth collision, thus producing sounds that the clownfish uses during agonistic behaviors. To investigate whether this rapid jaw movement is also used during feeding, we analyzed the kinematics of sound production and feeding. Sound production, feeding on live planktonic prey, and feeding on food attached to tweezers was filmed with a high-speed camera. Three kinds of kinematic patterns were detected and were associated with the two different types of food presented: one performed to catch planktonic prey (PP), and two (called B-1 and B-2) to bite attached food items. The kinematic pattern of B-2 is similar to that observed during sound production (SP) and the transection of the c-md ligament highlights that sound production and biting-2 motions are dependent on this morphological trait. Our data show that the c-md ligament in addition to its role in sound production allows duplication of the mouth-closing mechanism during feeding. This highlights the key role played by the c-md ligament in sound production and feeding on attached prey. J. Exp. Zool. 323A: 227-238, 2015.

Evolution and diversity of ram-suction feeding in damselfishes (Pomacentridae)

The cerato-mandibular (c-md) ligament is a synapomorphy within Pomacentridae that creates a tight link between the lower jaws and the hyoid bars. However, this morphological trait has been secondarily lost in multiple lineages during evolution. A previous study revealed that the loss of this trait acted as a release of evolutionary constraints, leading to a cascade of morphological changes such elongated buccal jaws and a slender body. Ecomorphological interpretations suggested the loss of the c-md ligament has ultimately led to a new adaptive peak in zooplanktivory through an optimization of the ram feeding mode associated with a specialization in pelagic feeding. Here, we tested these hypotheses by comparing functional and diet diversity between damselfish species with and without the c-md ligament. Although species lacking the c-md ligament presented a conserved kinematic pattern resulting from high ram and low suction performances, our results did not support an optimization of the ram feeding mode. Indeed, some species with the c-md ligament showed the same or exceeded the ram performance of species without the c-md ligament. The species with the c-md ligament had a more diverse kinematic pattern exploring the entire ram-suction functional range in damselfishes. Finally, our results did not show any diet variations associated with the loss of the c-md ligament. Our study furthers the understanding of how a morphological trait has shaped, by its presence or absence, the ecomorpho-functional diversification of Pomacentridae.