Phylogeny and Jaw Ontogeny of Beloniform Fishes1

Integrative and Comparative Biology, Nov 2004 by Lovejoy, Nathan R, Iranpour, Mahmood, Collette, Bruce B

Evolution of jaw ontogeny

The optimization of jaw characters on the total molecular evidence beloniform tree clearly falsifies the scenario proposed by Nichols and Breder (1928) and supported by de Beer (1940). These authors hypothesized that needlefishes are the basal members of Beloniformes, and that halfbeaks represent a more derived paedomorphic lineage. Instead, our hypothesis suggests that halfbeaks are relatively basal members of Beloniformes, and the needlefish morphology is relatively derived. The presence of elongate lower jaws in both juveniles and adults is relatively plesiomorphic, whereas the evolution of an elongate upper jaw in adults is a relatively derived condition. Collette et al. (1984) also supported this scenario, based on a phylogeny in which each of the traditional beloniform families was monophyletic. In the topology presented here, the basal paraphyletic position of the halfbeaks provides additional confidence in the optimization of the elongate lower jaw in juvenile and adult as the relatively plesiomorphic states.

The increased number of taxa and the more detailed presentation of jaw condition (Fig. 2) compared to Lovejoy (2000), makes possible a more complete compilation of evolutionary changes in beloniform jaw ontogeny. Figure 4 is a schematic summary of these transitions. The story of beloniform jaws is clearly not limited to the simple transition between the "halfbeaked" and "needle-jawed." The hypothesized patterns of transformation are complex. The generalized halfbeak ontogeny leads independently to ontogenies in which adults lose the elongate lower jaw (e.g., Oxyporhamphus, Arrhamphus). In most fiyingfishes, the elongate lower jaw is absent in juveniles. The generalized needlefish ontogeny leads to ontogenies in which juveniles have elongate upper and lower jaws (e.g., Tylosurus crocodilus), and others in which the elongate upper jaw is absent in adults (Belonion). In sauries the transitions are particularly striking. CoIolabis and Elassichthys have short upper and lower jaws as adults and juveniles, while Scomberesox has elongate upper and lower jaws in adults (Collette et al, 1984). Thus, the placement and relationships of sauries requires the loss of elongate upper and lower jaws, followed by their reappearance in Scomberesox.

What drives the evolution of jaw ontogeny? Boughton et al. (1991) summarized evidence for the importance of jaw shape for the feeding ecology of needlefishes. Needlefishes in the "halfbeak" stage often consume prey such as shrimp, mysids, amphipods, and phytoplankton, but after developing the elongate upper jaw, shift to a fish diet. The forceps-like adult needlefish morphology is well-suited to piscivory. Taxa such as Tylosurus crocodilus and Xenentodon cancila, which have no "halfbeak" juvenile stage, feed almost exclusively on fishes (Breder, 1932; Foster, 1974). Thus, it seems likely that changes in jaw ontogeny may be at least partially related to diet and food availability. Our phylogenetic approach suggests an additional consideration. While most needlefishes are marine, there are a number of freshwater taxa, including several freshwater endemic genera: Xenentodon from Southeast Asia, and Pseudotylosurus, Potamorrhaphis, and Belonion from South America. Most of these taxa display notable changes in ontogenetic patterns; however, not all are in the same direction. Xenentodon, and Potamorrhaphis have lost the "halfbeak" stage as juveniles, while Belonion maintains the halfbeak stage as an adult. The concentration of evolutionary change in ontogeny along freshwater lineages may be related to high diversity of food types in tropical freshwater habitats. For example, in South America, Belonion feeds mainly on Zooplankton, insect larvae, and bryozoans, Potamorrhaphis on terrestrial insects (particularly ants), and Pseudotylosurus on fishes (Goulding and Carvalho, 1984). Specialization on alternative food resources might drive evolutionary shifts in jaw ontogeny and morphology. Several species of Strongylura are also freshwater inhabitants (S. krefftii, S. hubbsi, and 5. fluviatilis), but data for the juvenile condition are not available for these taxa. The relationship between ecology and jaw ontogeny will remain speculative until more detailed studies of diet, broader surveys of ontogeny, and functional investigations of morphology are completed.