Form and function of damselfish skulls: rapid and repeated evolution into a limited number of trophic niches

Abstract

Background: Damselfishes (Perciformes, Pomacentridae) are a major component of coral reef communities, and the functional diversity of their trophic anatomy is an important constituent of the ecological morphology of these systems. Using shape analyses, biomechanical modelling, and phylogenetically based comparative methods, we examined the anatomy of damselfish feeding among all genera and trophic groups. Coordinate based shape analyses of anatomical landmarks were used to describe patterns of morphological diversity and determine positions of functional groups in a skull morphospace. These landmarks define the lever and linkage structures of the damselfish feeding system, and biomechanical analyses of this data were performed using the software program JawsModel4 in order to calculate the simple mechanical advantage (MA) employed by different skull elements during feeding, and to compute kinematic transmission coefficients (KT) that describe the efficiency with which angular motion is transferred through the complex linkages of damselfish skulls.

Results: Our results indicate that pomacentrid planktivores are significantly different from other damselfishes, that biting MA values and protrusion KT ratios are correlated with pomacentrid trophic groups more tightly than KT scores associated with maxillary rotation and gape angle, and that the MAs employed by their three biting muscles have evolved independently. Most of the biomechanical parameters examined have experienced low levels of phylogenetic constraint, which suggests that they have evolved quickly.

Conclusion: Joint morphological and biomechanical analyses of the same anatomical data provided two reciprocally illuminating arrays of information. Both analyses showed that the evolution of planktivory has involved important changes in pomacentrid functional morphology, and that the mechanics of upper jaw kinesis have been of great importance to the evolution of damselfish feeding. Our data support a tight and biomechanically defined link between structure and the functional ecology of fish skulls, and indicate that certain mechanisms for transmitting motion through their jaw linkages may require particular anatomical configurations, a conclusion that contravenes the concept of "many-to-one mapping" for fish jaw mechanics. Damselfish trophic evolution is characterized by rapid and repeated shifts between a small number of eco-morphological states, an evolutionary pattern that we describe as reticulate adaptive radiation.

Figure 1

Anatomical landmarks and biomechanical linkages of functional importance for damselfish feeding. A. Landmarks used in morphological and biomechanical analyses: 1 = Tip of the anterior-most tooth on the premaxilla; 2 = Tip of the anterior-most tooth on the dentary; 3 = Maxillary-palatine joint (upper rotation point of the maxilla); 4 = Insertion of the A1 division of the adductor mandibulae on the maxilla; 5 = Maxillary-articular joint (lower point of rotation of the maxilla); 6 = Insertion of the A2 division of the adductor mandibulae on the articular process; 7 = Insertion of the A3 division of the adductor mandibulae on the anterior, medial surface of the articular; 8 = Posterior tip of the ascending process of the premaxilla; 9 = Joint between the nasal bone and the neurocranium; 10 = The most anterio-ventral point of the eye socket; 11 = Articular-quadrate joint (lower jaw joint); 12 = Insertion of the interopercular ligament on the articular (point at which moth opening forces are applied); 13 = Most posterio-ventral point of the eye socket; 14 = Dorsal-most tip of the supraoccipital crest on the neurocranium; 15 = Most dorsal point on the origin of the A3 division of the adductor mandibulae on the preopercular; 16 = Most dorsal point on the origin of the A1 division of the adductor mandibulae on the preopercular; 17 = Most dorsal point on the origin of the A2 division of the adductor mandibulae on the preopercular; 18 = Posterio-ventral corner of the preopercular; 19 = Corner of the mouth. B. Levers and linkages in damselfish skulls, with schematics of the three divisions of the adductor mandibulae.

Figure 2

The damselfish phylogeny used in the phylogenetic comparative analyses in this study. Numbers indicate branch lengths. This tree is derived from a Bayesian consensus tree computed from nuclear and mitochondrial genetic data from 104 damselfish species and all 29 damselfish genera [68,69]. Abudefduf vaigiensis, Amphiprion peridarion and Stegastes partitus are used to estimate the positions of their cogeners: Abudefduf saxatilis, Amphiprion akindynos and Stegastes flavilatus. Planktivores (red), Herbivores (green), Omnivores (blue)

Figure 3

Canonical variates (CV) score plot for CV axes 1 and 2. Herbivores in green, Omnivores in blue, planktivores in red, and Cheiloprion labiatus, which eats coral polyps, in black. The location for C. labiatus was based on the results of relative warps analyses. The number key for individual fishes is: Abudefduf vagiensis (1), Acanthochromis polyacanthus (2), Altrichthys curatus (3), Amblyglyphidodon curacao (4), Amblypomacentrus clarus (5), Amphiprion akindynos (6), Cheiloprion labiatus (7), Chromis amboinensis (8), Chromis hirundo (9), Chromis punctipinnis (10), Chrysiptera cyanea (11), Dascyllus melanurus (12), Dischistodus melanotus (13), Hemiglyphidodon plagiometopon (14), Hypsypops rubicundus (15), Lepidozygus tapeinosoma (16), Mecaenichthys immaculatus (17), Microspathodon dorsalis (18), Neoglyphidodon nigroris (19), Neopomacentrus azysron (20), Nexilosus latifrons (21), Parma microlepis (22), Plectroglyphidodon lacrymatus (23), Pomacentrus alexanderae (24), Pomachromis richardsoni (25), Premnas biaculeatus (26), Pristotis obtusirostris (27), Similiparma hermani (28), Stegastes flavilatus (29), Teixeirichthys jordani (30).

Figure 4

Pictorial descriptions of relative warps axes and the morphological extremes in each damselfish trophic class. Plates A-H display pairwise comparisons of damselfishes whose head shapes are strongly separated along one RW axis, but which are otherwise very similar (they have similar scores on other axes). Plate A: Teixeirichthys jordani (RW1-). Plate B: Hypsypops rubicundus (RW1+). Plate C: Dischistodus melanotus (RW2-). Plate D: Microspathodon dorsalis (RW2+). Plate E: Plectroglyphidodon lacrymatus (RW3-). Plate F: Amphiprion akindynos (RW3+). Plate G. Chromis amboinensis (RW4-). Plate H: Neopomacentrus cyanomos (RW4+). Plate I: Azurina hirundo. Plate J: Chrysiptera cyanea. Plates B and J depict the range of variation in the head shapes of damselfish omnivores. Plates C and D depict the range of variation in the head shapes of damselfish herbivores. Plates G and I depict the range of variation in the head shapes of damselfish planktivores. _* = the posterio-dorsal tip of the ascending process of the premaxilla. + = the dorsal edge of the origin of the A2 division of the adductor mandibulae on the preopercular bone. ‡ = the dorsal edge of the origin of the A1 division of the adductor mandibulae on the preopercular bone. All scale bars = 1.0 cm.

Figure 5

Regression plots (27 data points) for those phylogenetically independent contrasts (PIC) that were statistically significant. Maxillary KT = MKT. Gape KT = GKT. Protrusion KT = PKT