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Phylogeny and Jaw Ontogeny of Beloniform Fishes1 INTEGR.COMP.BIOL., 44:366±377 (2004) Phylogeny and Jaw Ontogeny of Beloniform Fishes1 NATHAN R. LOVEJOY,2,*MAHMOOD IRANPOUR,* AND BRUCE B. COLLETTE² *Department of Zoology, University of Manitoba, Z320 Duff Roblin Building, Winnipeg, MB, R3T 2N2, Canada ²National Marine Fisheries Service Systematics Laboratory, Smithsonian Institution, P.O. Box 37012, NMNH Rm. WC-57, MRC 0153, Washington, D.C. 20013-7012 SYNOPSIS. To investigate jaw evolution in beloniform ®shes, we reconstructed the phylogeny 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 needle®shes (Belonidae) and half- beaks (Hemiramphidae), but supports the monophyly of ¯ying®shes (Exocoetidae) and sauries (Scombere- socidae). Flying®shes are nested within halfbeaks, and sauries are nested within needle®shes. Optimization of jaw characters on the tree reveals a diverse array of evolutionary changes in ontogeny. During their development, needle®shes pass through a ``halfbeak'' stage that closely resembles the adult condition in the hemiramphid halfbeaks. The reconstruction of jaw transitions falsi®es the hypothesis that halfbeaks are paedomorphic derivatives of needle®shes. Instead, halfbeaks make up a basal paraphyletic grade within beloniforms, and the needle®sh jaw morphology is relatively derived. The parallel between needle®sh on- togeny and beloniform phylogeny is discussed, and clades amenable to future morphological analysis are proposed. INTRODUCTION and Parenti, 1981; Collette et al., 1984) is a good mod- Phylogeny is integral to understanding the evolution el system for investigating the evolution of ontogeny. of ontogeny. Without a ®rm understanding of a group's Beloniform species exhibit striking variation in jaw evolutionary relationships, the polarities of ontogenet- structure that varies both ontogenetically and phylo- ic transformations are irretrievable. In particular, de- genetically, and appears related to feeding. The most termining the role of heterochrony (changes in devel- spectacular ontogenetic changes occur in belonid nee- opmental timing during evolution) depends on phylo- dle®shes. Larval needle®shes have short jaws of equal genetic patterns. Gould (1977) emphasized this point, length. However, in juveniles, the lower jaw elongates which was further developed by Alberch et al. (1979), ®rst, producing a morphology that is distinctly remi- and rephrased in a cladistic context by Fink (1982). niscent of a related family, the halfbeaks (Hemiram- Two broad heterochronic patterns have been identi®ed, phidae)Ðindeed, needle®shes in this juvenile ``half- paedomorphosis and peramorphosis. In taxa that ex- beak'' form have been mistakenly described as new hibit paedomorphosis, descendant adults exhibit mor- species of hemiramphids (Collette and Parin, 1970). phological features of the juveniles of their putative Later, the upper jaw elongates as well, giving rise to ancestors. In peramorphosis, descendant taxa extend the nearly equal length jaws of most adult needle®shes. the ontogeny of ancestors, so that adult features of the These transformations appear linked to ecological ancestor appear in the juveniles of descendants. In both shifts: juvenile needle®shes in the ``halfbeak'' mor- cases, alterations of developmental timing produce phology feed primarily on plankton, while most adult parallels between ontogeny and phylogeny. Numerous needle®shes are piscivorous (Boughton et al., 1991). studies have implicated heterochrony in the evolution The similarity in jaw morphology between juvenile of morphology in ®shes (e.g., Bemis, 1984; Winter- needle®shes and the closely related Hemiramphidae bottom, 1990; Boughton et al., 1991; Johnson and has provoked alternative interpretations. Severtsov Brothers, 1993; Zelditch et al., 2000). Gould (1977) (1927; summarized in Gould, 1977) thought that the points out that the endeavour to assess the relative fre- ontogeny of needle®shes paralleled the phylogeny of quencies of peramorphosis versus paeodomorphosis beloniforms. He hypothesized that short-jawed ances- may be misplaced in a ®eld with nearly limitless em- tral ¯ying®shes gave rise to descendant halfbeaks, pirical potential. However, the examination of speci®c which in turn gave rise to the more advanced needle- cases may still yield valuable insight into the relation- ®shes. Needle®sh ontogeny would thus be an example ship between phylogeny, ontogeny and ecology. of the phenomenon of recapitulation or peramorphosis. The order Beloniformes, a group that currently in- Nichols and Breder (1928), on the other hand, building cludes the needle®shes (Belonidae), halfbeaks (Hemi- on the work of Schlesinger (1909) and Regan (1911) ramphidae), ¯ying®shes (Exocoetidae), sauries (Scom- proposed an alternative beloniform phylogeny. In their beresocidae) and rice®shes (Adrianichthyidae) (Rosen scheme, needle®shes are the most basal family, and gave rise to hemiramphids, which in turn gave rise to 1 From the Symposium Patterns and Processes in the Evolution ¯ying®shes. They hypothesized that hemiramphids are of Fishes presented at the Annual Meeting of the Society for Inte- ``®xed larval'' (or paedomorphic) needle®shes (Nich- grative and Comparative Biology, 4±8 January 2003, at Toronto, Canada. ols and Breder, 1928, p. 435). de Beer (1940) reported 2 E-mail: [email protected] this ®nding in his book ``Embryos and Ancestors'' 366 EVOLUTION OF BELONIFORM JAW ONTOGENY 367 which emphasized the importance of paedomorphosis provide phylogenetic information that spanned a as an evolutionary pattern. broader range of taxonomic divergence. The nuclear Clearly, differentiating between the paedomorphosis gene, Tmo-4C4 (Tmo) is an anonymous, putative pro- and recapitulation scenarios for beloniforms is only tein-coding locus identi®ed and used for phylogeny by possible with a robust phylogenetic hypothesis for the Streelman and Karl (1997). It provided resolution of group. Lovejoy (2000) presented a phylogenetic anal- families and genera within labroids, and was thus ex- ysis based on 2 mitochondrial genes, a nuclear gene, pected to provide useful information for deeper parts and morphology for representatives of all 5 beloniform of the beloniform tree. Recombination Activating families. The result falsi®ed Nichols and Breder's Gene 2 (RAG2) is a nuclear gene that appears to (1928) paedomorphic hemiramphid origin hypothesis, evolve slightly faster than Tmo-4C4 (Lovejoy and which predicted a basal position for needle®shes. In- Collette, 2001), and has proven useful for species-level stead, hemiramphids were found to represent a basal phylogenetic analyses (Sullivan et al., 2000; Lovejoy paraphyletic grade, with needle®shes and ¯ying®shes and Collette, 2001). relatively derived. The phylogenetic position of nee- For each sample, approximately 25 mg of tissue was dle®shes therefore matched the prediction of Severt- rinsed brie¯y in water, then DNA puri®ed using Qia- sov's (1927) recapitulation hypothesis. gen's spin-column tissue kit. Cells were lysed at 558 Here, we present an extension and test of Lovejoy's in 20 ml of Proteinase K (20 mg/ml) for three to six (2000) ®ndings. We have expanded the matrix by add- hours. Lysate was bound to the spin column mem- ing 14 ingroup taxa to the previous 39, which signif- brane, and washed twice by centrifugation. DNA was icantly improves taxonomic coverage of hemiramphids then eluted by centrifugation twice with 200 ml of low and ¯ying®shes. We have also added a novel source salt buffer. of character data, by sequencing a 1 kilobase fragment In the case of cyt b, 16S, and Tmo, template for of the nuclear gene, Recombination Activating Gene sequencing was initially ampli®ed using published 2, or RAG2. Our analysis is based on the nuclear PCR primers. For RAG2, primers were developed by RAG2 and Tmo-4C4 genes, and the mitochondrial cy- comparing available vertebrate sequences. New prim- tochrome-b and 16S rRNA genes. We use the resultant ers were then designed for sequencing and additional phylogenetic hypothesis to explore the evolution of ampli®cations (for details and primer lists, see Love- jaw ontogeny. joy, 2000 and Lovejoy and Collette, 2001). Generally, DNA was ampli®ed in 50 ml reactions containing 1 ml METHODS of DNA, 3 mM MgCl2, 20 mM Tris HCl pH 8.4, 50 Fishes were collected in the ®eld by ourselves or mM KCl, 200 mM dNTPs, 0.4 mM of each primer, and colleagues. Gill tissue was either frozen immediately one unit of Gibco Taq polymerase. PCR ampli®cations in liquid nitrogen or preserved in 95±100% ethanol or were performed using the following conditions: 30 buffer of 20% DMSO, 0.25 M EDTA at pH 8, satu- second denaturation at 958 to start, followed by 35 rated with NaCl (Seutin et al., 1991). Tissue preserved cycles of denaturation at 958 for 30 seconds, annealing in buffer and stored at room temperature reliably at 488±558 for 60 seconds, and 728 extension for 90 yields ampli®able DNA (after storage for up to four seconds, followed by a ®nal extension of 728 for 5 years). Voucher specimens were preserved in 10% minutes. In cases where faint secondary bands were buffered formalin, transferred to 70% ethanol or 50± detected, template was run in 1% agarose gels, then 55% isopropanol and deposited in museum collections cut out and cleaned using PCR puri®cation spin col- (catalogue numbers for voucher specimens are listed umns (Qiagen). with sequences in GenBank). PCR products were cleaned
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