Phylogeny and Jaw Ontogeny of Beloniform Fishes1

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

SYNOPSIS. To investigate jaw evolution in beloniform fishes, we reconstructed the phytogeny of 54 species using fragments of two nuclear (RAG2 and Tmo-4C4) and two mitochondrial (cytochrome b and 16S rRNA) genes. Our total molecular evidence topology refutes the monophyly of needlefishes (Belonidae) and halfbeaks (Hemiramphidae), but supports the monophyly of flyingfishes (Exocoetidae) and sauries (Scomberesocidae). Flyingfishes are nested within halfbeaks, and sauries are nested within needlefishes. Optimization of jaw characters on the tree reveals a diverse array of evolutionary changes in ontogeny. During their development, needlefishes pass through a "halfbeak" stage that closely resembles the adult condition in the hemiramphid halfbeaks. The reconstruction of jaw transitions falsifies the hypothesis that halfbeaks are paedomorphic derivatives of needlefishes. Instead, halfbeaks make up a basal paraphyletic grade within beloniforms, and the needlefish jaw morphology is relatively derived. The parallel between needlefish ontogeny and beloniform phylogeny is discussed, and clades amenable to future morphological analysis are proposed.

INTRODUCTION

Phylogeny is integral to understanding the evolution of ontogeny. Without a firm understanding of a group's evolutionary relationships, the polarities of ontogenetic transformations are irretrievable. In particular, determining the role of heterochrony (changes in developmental timing during evolution) depends on phylogenetic patterns. Gould (1977) emphasized this point, which was further developed by Alberch et al. (1979), and rephrased in a cladistic context by Fink (1982). Two broad heterochronic patterns have been identified, paedomorphosis and peramorphosis. In taxa that ex- ' hibit paedomorphosis, descendant adults exhibit morphological features of the juveniles of their putative ancestors. In peramorphosis, descendant taxa extend the ontogeny of ancestors, so that adult features of the ancestor appear in the juveniles of descendants. In both cases, alterations of developmental timing produce parallels between ontogeny and phylogeny. Numerous studies have implicated heterochrony in the evolution of morphology in fishes (e.g., Bemis, 1984; Winterbottom, 1990; Boughton et α/., 1991; Johnson and Brothers, 1993; Zelditch et al., 2000). Gould (1977) points out that the endeavour to assess the relative frequencies of peramorphosis versus paeodomorphosis may be misplaced in a field with nearly limitless empirical potential. However, the examination of specific cases may still yield valuable insight into the relationship between phylogeny, ontogeny and ecology.

The order Beloniformes, a group that currently includes the needlefishes (Belonidae), halfbeaks (Hemiramphidae), flyingfishes (Exocoetidae), sauries (Scomberesocidae) and ricefishes (Adrianichthyidae) (Rosen and Parenti, 1981; Collette et al, 1984) is a good model system for investigating the evolution of ontogeny. Beloniform species exhibit striking variation in jaw structure that varies both ontogenetically and phylogenetically, and appears related to feeding. The most spectacular ontogenetic changes occur in belonid needlefishes. Larval needlefishes have short jaws of equal length. However, in juveniles, the lower jaw elongates first, producing a morphology that is distinctly reminiscent of a related family, the halfbeaks (Hemiramphidae)-indeed, needlefishes in this juvenile "halfbeak" form have been mistakenly described as new species of hemiramphids (Collette and Parin, 1970). Later, the upper jaw elongates as well, giving rise to the nearly equal length jaws of most adult needlefishes. These transformations appear linked to ecological shifts: juvenile needlefishes in the "halfbeak" morphology feed primarily on plankton, while most adult needlefishes are piscivorous (Boughton el αι., 1991).

The similarity in jaw morphology between juvenile needlefishes and the closely related Hemiramphidae has provoked alternative interpretations. Severtsov (1927; summarized in Gould, 1977) thought that the ontogeny of needlefishes paralleled the phylogeny of beloniforms. He hypothesized that short-jawed ancestral flyingfishes gave rise to descendant halfbeaks, which in turn gave rise to the more advanced needlefishes. Needlefish ontogeny would thus be an example of the phenomenon of recapitulation or peramorphosis. Nichols and Breder (1928), on the other hand, building on the work of Schlesinger (1909) and Regan (191 1) proposed an alternative beloniform phylogeny. In their scheme, needlefishes are the most basal family, and gave rise to hemiramphids, which in turn gave rise to flyingfishes. They hypothesized that hemiramphids are "fixed larval" (or paedomorphic) needlefishes (Nichols and Breder, 1928, p. 435). de Beer (1940) reported this finding in his book "Embryos and Ancestors" which emphasized the importance of paedomorphosis as an evolutionary pattern.

Clearly, differentiating between the paedomorphosis and recapitulation scenarios for beloniforms is only possible with a robust phylogenetic hypothesis for the group. Lovejoy (2000) presented a phylogenetic analysis based on 2 mitochondria! genes, a nuclear gene, and morphology for representatives of all 5 beloniform families. The result falsified Nichols and Breder's (1928) paedomorphic hemiramphid origin hypothesis, which predicted a basal position for needlefishes. Instead, hemiramphids were found to represent a basal paraphyletic grade, with needlefishes and flyingfishes relatively derived. The phylogenetic position of needlefishes therefore matched the prediction of Severtsov's (1927) recapitulation hypothesis.