Independent evolution of the specialized pharyngeal jaw apparatus in cichlid and labrid fishes

Background  

Fishes in the families Cichlidae and Labridae provide good probable examples of vertebrate adaptive radiations. Their spectacular trophic radiations have been widely assumed to be due to structural key innovation in pharyngeal jaw apparatus (PJA), but this idea has never been tested based on a reliable phylogeny. For the first step of evaluating the hypothesis, we investigated the phylogenetic positions of the components of the suborder Labroidei (including Pomacentridae and Embiotocidae in addition to Cichlidae and Labridae) within the Percomorpha, the most diversified (> 15,000 spp) crown clade of teleosts. We examined those based on 78 whole mitochondrial genome sequences (including 12 newly determined sequences) through partitioned Bayesian analyses with concatenated sequences (13,933 bp).     

Functional design and evolution of the pharyngeal jaw apparatus in euteleostean fishes

Functional and structural patterns in the pharyngeal jaw apparatus of euteleostean fishes are described and analysed as a case study of the transformation of a complex biological design. The sequential acquisition of structural novelties in the pharyngeal apparatus is considered in relation to both current hypotheses of euteleostean phylogeny and patterns of pharyngeal jaw function. Several euteleostean clades are corroborated as being monophyletic, and morphologically conservative features of the pharyngeal jaw apparatus are recognized. Functional analysis, using cinematography and electromyography, reveals four distinct patterns of muscle activity during feeding in primitive euteleosts (Esox) and in derived euteleostean fishes(Perca, Micropterus, Ambloplites, Pomoxis). The initial strike, buccal manipulation, pharyngeal manipulation, and the pharyngeal transport of prey into the oesophagus all involve unique muscle activity patterns that must be distinguished in analyses of pharyngeal jaw function. During pharyngeal transport, the upper and lower pharyngeal jaws are simultaneously protracted and retracted by the action of dorsal and ventral musculoskeletal gill arch couplings. The levator externus four and retractor dorsalis muscles, anatomical antagonists, overlap for 70–90°of their activity period. Levatores externi one and two are the main protractors of the upper pharyngeal jaws in the acanthopterygian fishes studied. The major features of pharyngeal jaw movement in primitive euteleosts are retained in many derived clades in spite of a dramatic structural reorganization of the pharyngeal region. Homologous muscles have radically changed their relative activity periods while pharyngeal jaw kinematics have been modified relatively little. Patterns of transformation of activity may thus bear little direct relationship to the sequence of structural modification in the evolution of complex designs. Overall function of a structural system may be maintained, however, through co-ordinated modifications of the timing of muscle activity and anatomical reorientation of the musculoskeletal system. Deeper understanding of the principles underlying the origin and transformation of functional design in vertebrates awaits further information on the acquisition of both structural and functional novelties at successive hierarchical levels within monophyietic clades. This is suggested as a key goal of future research in functional and evolutionary morphology.     

Functional morphology of the pharyngeal jaw apparatus in perciform fishes: An experimental analysis of the haemulidae

A new mechanical model for function of the pharyngeal jaw apparatus in generalized perciform fishes is developed from work with the family Haemulidae. The model is based on anatomical observations, patterns of muscle activity during feeding (electromyography), and the actions of directly stimulated muscles. The primary working stroke of the pharyngeal apparatus involves simultaneous upper jaw depression and retraction against a stabilized and elevating lower jaw. The working stroke is characterized by overlapping activity in most branchial muscles and is resolved into three phases. Four muscles (obliquus dorsalis 3, levator posterior, levator externus 3/4, and obliquus posterior) that act to depress the upper jaws become active in the first phase. Next, the retractor dorsalis, the only upper jaw retracting muscle, becomes active. Finally, there is activity in several muscles (transversus ventrales, pharyngocleithralis externus, pharyngohyoideus, and protractor pectoralis) that attach to the lower jaws. The combined effect of these muscles is to elevate and stabilize the lower jaws against the depressing and retracting upper jaws. The model identifies a novel mechanism of upper jaw depression, here proposed to be the primary component of the perciform pharyngeal jaw bite. The key to this mechanism is the joint between the epibranchial and toothed pharyngobranchial of arches 3 and 4. Dorsal rotation of epibranchials 3 and 4 about the insertion of the obliquus posterior depresses the lateral border of pharyngobranchials 3 and 4 (upper jaw). The obliquus dorsalis 3 muscle crosses the epibranchial-pharyngo-branchial joint in arches 3 and 4, and several additional muscles effect epibranchial rotation. Five upper jaw muscles cause upper jaw depression upon electrical stimulation: the obliquus dorsalis 3, levator posterior, levator externus 3/4, obliquus posterior, and transversus dorsalis. This result directly contradicts previous interpretations of function for the first three muscles. The presence of strong depression of the upper pharyngeal jaws explains the ability of many generalized perciform fishes to crush hard prey in their pharyngeal apparatus.     

Function of a key morphological innovation: fusion of the cichlid pharyngeal jaw

The pharyngeal jaw of cichlids may represent a key innovation that facilitated their unparalleled trophic divergence. In cichlids, 'fusion' of the lower pharyngeal jaw (LPJ) results from suturing between the two lower ceratobranchials. To examine, what novel abilities a more extensively fused pharyngeal jaw may confer, the function of LPJ suturing was examined in Heroine cichlids. Greater LPJ suturing, pharyngeal jaw splitting under compression and the forces used to crush molluscs in the wild suggest increased LPJ fusion in the trophically polymorphic Herichthys minckleyi operates to strengthen the pharyngeal jaw. Among Heroine cichlid species, the presence of an external LPJ suture and feeding specialization on molluscs was evolutionarily quite variable, but greater LPJ fusion estimated from the amount of external suturing was highly correlated with molluscivory. Throughout cichlid diversification, increased pharyngeal jaw fusion via suturing has likely helped to reinforce the LPJ during pharyngeal processing thereby facilitating the ability of cichlids to exploit durable prey.     

The pharyngeal jaw apparatus of the Cichlidae and Pomacentridae: function in feeding and sound production

Reviews in Fish Biology and Fisheries - Labroid fishes (PerciformesLabroidei) possess a highly developed pharyngeal jaw apparatus (PJA). A tremendous body of literature describes the anatomy and...     

Transmission of ocular media in labrid fishes

Wrasses (Labridae) are the second largest family of fishes on the Great Barrier Reef (after the Gobiidae) and, in terms of morphology and lifestyle, one of the most diverse. They occupy all zones of the reef from the very shallow reef flats to deep slopes, feeding on a variety of fauna. Many wrasses also have elaborately patterned bodies and reflect a range of colours from ultraviolet (UV) to far red. As a first step to investigating the visual system of these fishes we measured the transmission properties of the ocular media of 36 species from the Great Barrier Reef, Australia, and Hawaii, California and the Florida Keys, USA. Transmission measurements were made of whole eyes with a window cut into the back, and also of isolated lenses and corneas. Based on the transmission properties of the corneas the species could be split into two distinct groups within which the exact wavelength of the cut-off was variable. One group had visibly yellow corneas, while the corneas of the other group appeared clear to human observers. Five species had ocular media that transmitted wavelengths below 400 nm, making a perception of UV wavelengths for those species possible. Possible functional roles for the different filter types are discussed.     

Versatility and specialization in labrid fishes: ecomorphological implications

Summary The term specialized has been used to describe species that possess unique functional attributes and/or a narrow, stereotyped range of attributes, but there are few comparative functional analyses of specialists and generalists. If species with functional morphological specializations are capable of functioning over a broad range, the link between morphology and ecology may be relaxed under certain environmental conditions. In this study, high-speed films of jaw movements during prey capture were compared statistically for three coexisting coral reef fish species in the family Labridae, one trophic specialist and two trophic generalists. The trophic specialist possessed a unique functional feature related to the movement of the hyoid in the floor of the mouth, while the trophic generalists were not observed to possess any functional specializations. All three species showed functional versatility in that they were able to adjust their prey capture mechanism in response to the evasive potential of the prey. The functional versatility of trophic specialists has implications for ecomorphological studies, since species characterized as possessing unique functional or morphological features may demonstrate marked flexibility in ecological variables such as diet or foraging behavior, decreasing the likelihood of identifying correlations between morphology and ecology.     

Integrated diversification of locomotion and feeding in labrid fishes

An organism''s performance of any ecological task involves coordination of multiple functional systems. Feeding performance is influenced by locomotor abilities which are used during search and capture of prey, as well as cranial mechanics, which affect prey capture and processing. But, does this integration of functional systems manifest itself during evolution? We asked whether the locomotor and feeding systems evolved in association in one of the most prominent and diverse reef fish radiations, the Labridae. We examined features of the pectoral fins that affect swimming performance and aspects of the skull that describe force and motion of the jaws. We applied a recent phylogeny, calculated independent contrasts for 60 nodes and performed principal components analyses separately on contrasts for fin and skull traits. The major axes of fin and skull diversification are highly correlated; modifications of the skull to amplify the speed of jaw movements are correlated with changes in the pectoral fins that increase swimming speed, and increases in force capacity of the skull are associated with changes towards fins that produce high thrust at slow speeds. These results indicate that the labrid radiation involved a strong connection between locomotion and feeding abilities.     

Projecting mechanics into morphospace: disparity in the feeding system of labrid fishes

In no group of organisms has the link between species richness, morphological disparity, disparity in mechanics and functional or ecological diversification been made explicit. As a step towards integrating these measures of diversity, we examine how the mechanics of the anterior-jaw four-bar linkages of 104 species of Great Barrier Reef (GBR) labrid fishes maps into a scale-independent morphospace. As predicted from theory, no relationship exists between overall size and the mechanics of velocity and force transmission in labrid anterior-jaw linkages. Nonetheless, mechanics associated with the anterior jaw appear to have constrained diversification of labrid anterior-jaw morphology. Furthermore, simulations depict a generally nonlinear relationship between the length of individual links and transmission of motion. In addition, no relationship was found between morphological disparity and mechanical disparity among the most species-rich labrid groups from the GBR. It is also established that regions of morphospace equivalent in morphological disparity differ over nearly an order of magnitude in mechanical disparity. These results illustrate that without an explicit interpretation of the consequences of per unit change in morphology, conclusions about diversification drawn only from morphological disparity may be misleading.     

Ecomorphology of the eyes and skull in zooplanktivorous labrid fishes

Zooplanktivory is one of the most distinct trophic niches in coral reef fishes, and a number of skull traits are widely recognized as being adaptations for feeding in midwater on small planktonic prey. Previous studies have concluded that zooplanktivores have larger eyes for sharper visual acuity, reduced mouth structures to match small prey sizes, and longer gill rakers to help retain captured prey. We tested these three traditional hypotheses plus two novel adaptive hypotheses in labrids, a clade of very diverse coral reef fishes that show multiple independent evolutionary origins of zooplanktivory. Using phylogenetic comparative methods with a data set from 21 species, we failed to find larger eyes in three independent transitions to zooplanktivory. Instead, an impression of large eyes may be caused by a size reduction of the anterior facial region. However, two zooplanktivores (Clepticus parrae and Halichoeres pictus) possess several features interpreted as adaptations to zooplankton feeding, namely large lens diameters relative to eye axial length, round pupil shape, and long gill rakers. The third zooplanktivore in our analysis, Cirrhilabrus solorensis, lacks all above features. It remains unclear whether Cirrhilabrus shows optical specializations for capturing planktonic prey. Our results support the prediction that increased visual acuity is adaptive for zooplanktivory, but in labrids increases in eye size are apparently not part of the evolutionary response.     

The jaw apparatus of the Cretaceous ammonite Reesidites

Jaws are preserved within the body chambers of three specimens of a collignoniceratid ammonite Reesidites minimus (Hayasaka and Fukada) from the Upper liuoniaq of Hokkaido, Japan. Light microscopic and SEM observations of sections indicate that both upper and lower jaws consist mainly of a thick, double-walled chitinous lamella with a beak-like anterior projection. The outer chitinous lamella of the lower jaw is covered by a thick calcareous layer. The jaw apparatus of this species morphologically resembles aptychus-type jaws of Jurassic ammonites, but is distinguished by the presence of an anterior beak-like projection with serrated ridges and grooves in the lower jaw. These observations strongly suggest a biting ability in this species.     

Comparison of laboratory-reared eggs, embryos and larvae of five labrid fishes

Eggs, embryos and larvae of five labrid fishes, Thalassoma cupido, Pteragogus flagellifer, Pseudolabrus japonicus, Halichoeres tenuispinnis, and H. poecilopterus, reared in the laboratory are described and compared. The eggs were buoyant and spherical, with a single, spherical oil globule. P. japonicus eggs were unique in lacking melanophores on the oil globule. Eggs of the remaining species closely resembled each other, except in diameter. Incubation periods were short, ranging from ca. 19 h in H. poecilopterus to ca. 31 h in P. japonicus. The newly-hatched embryos also resembled each other, having a short tail and large oval or pear-shaped yolksac, the anterior tip of which extended beyond the snout. The single oil globule was located at the anterior tip of the yolk. As the yolksac diminished with growth, its anterior tip moved posteriorly. The yolk and oil globule were completely absorbed 3 or 4 days after hatching. In all free embryos and larvae except for Pteragogus flagellifer, needle-like projections appeared on both the dorsal and anal finfold margins 12 h to 1 day after hatching. Although morphology of free embryos and larvae of all five species was very similar, differences in pigmentation, location of the anus, and the needle-like projections were apparent. Artificial keys to the newly-hatched embryos and larvae are given.     

Phylogeny and jaw ontogeny of beloniform fishes

To investigate jaw evolution in beloniform fishes, we reconstructedthe phylogeny of 54 species using fragments of two nuclear (RAG2and Tmo-4C4) and two mitochondrial (cytochrome b and 16S rRNA)genes. Our total molecular evidence topology refutes the monophylyof needlefishes (Belonidae) and halfbeaks (Hemiramphidae), butsupports the monophyly of flyingfishes (Exocoetidae) and sauries(Scomberesocidae). Flyingfishes are nested within halfbeaks,and sauries are nested within needlefishes. Optimization ofjaw characters on the tree reveals a diverse array of evolutionarychanges in ontogeny. During their development, needlefishespass through a "halfbeak" stage that closely resembles the adultcondition in the hemiramphid halfbeaks. The reconstruction ofjaw transitions falsifies the hypothesis that halfbeaks arepaedomorphic derivatives of needlefishes. Instead, halfbeaksmake up a basal paraphyletic grade within beloniforms, and theneedlefish jaw morphology is relatively derived. The parallelbetween needlefish ontogeny and beloniform phylogeny is discussed,and clades amenable to future morphological analysis are proposed.     

Phylogenetic aspects of Cetacean origins: A morphological perspective

The evolutionary steps leading up to the origin of cetaceans involved pervasive changes in the masticatory apparatus, the ear, and limb morphology. These changes bear heavily on the phylogenetic relationships of Cetacea, and are investigated here on the basis of two of its earliest members:Pakicetus andAmbulocetus. A phylogenetic analysis of cetaceans, five groups of mesonychians, and five other groups of ungulates indicates thatPakicetus is the sister group to all other cetaceans, and that Cete (mesonychians and Cetacea) is a monophyletic group.     

The interrelationships of Acanthomorph fishes: A total evidence approach using molecular and morphological data

DNA sequence and morphological data were analyzed for specimens of twenty-five species of acanthomorph fishes and two specimens representing the outgroups Aulopiformes and Myctophiformes. A 572 base-pair (bp) segment of the 12S ribosomal mitochondrial gene, 1112 bp from three regions of the 28S ribosomal nuclear gene, and 38 morphological transformation series were analyzed under the criterion of maximum parsimony. The total evidence analysis resulted in a set of four most parsimonious trees. Relationships common to all trees are largely congruent with the hypothesis articulated by Johnson and Patterson (1993. Bull. Mar. Sci. 52, 554-626).     

A morphological cline in Eucalyptus: a genetic perspective

The putative hybrid zone between Eucalyptus populnea and E. brownii is examined using morphological and molecular techniques. This species complex displays continuous morphological variation across the study area, which has been previously interpreted as the product of hybridization between allopatric species. A microsatellite analysis indicates that there was little genetic structuring across the morphological cline and only low levels of population differentiation. The nested clade analysis of the JLA+ region of the chloroplast DNA (cpDNA) indicates that the geographical distribution of cpDNA haplotypes is unlikely to be the result of historical hybridization events, and that restricted seed-mediated gene flow with isolation by distance is responsible for the phylogeographical distribution. A more plausible explanation for the origin and persistence of the morphological cline is that the process of continuous morphological diversification has been promoted by a directional selection gradient. This study addresses species status within Eucalyptus and the belief that hybridization is widespread and is an important process in the group's evolution.