A MODEL SYSTEM OF STRUCTURAL DUPLICATION: … · 2020. 6. 1. · ticularly in comparisons between...

Syst. Biol. 46(3):441^63, 1997

A MODEL SYSTEM OF STRUCTURAL DUPLICATION:HOMOLOGIES OF ADDUCTOR MANDIBULAE MUSCLES IN

TETRAODONTIFORM FISHES

JOHN P. FRIEL AND PETER C. WAINWRIGHT

Department of Biological Science, Florida State University, Tallahassee, Florida 32306-4370, USA;E-mail: [email protected] (J.P.F.), [email protected] (P.C.W.)

Abstract.—We critically reviewed the homologies of the jaw muscles in tetraodontiform fishes(Triacanthoidea, Balistoidea, Tetraodontoidea), as first described in Winterbottom's phylogeneticmonograph (1974, Smithson. Contrib. Zool. 155:1-201), as a case study in structural duplication.Within this order of teleost fishes, the two main adductor mandibulae muscles, Al and A2, areduplicated one or more times in some subclades. The number of descendant Al and A2 musclesranges from as few as the original two muscles in triplespines to as many as eight muscles insome filefishes. As first pointed out by Winterbottom, the homologies of some muscles are unclear,particularly in comparisons between the superfamilies Balistoidea (boxfishes, triggerfishes, file-fishes) and Tetraodontoidea (pursefishes, molas, puffers, porcupinefishes). We reassessed the ho-mologies (orthologs and paralogs) of these Al and A2 muscles based on their origins, insertions,and relative masses in representative taxa and their congruence with a phylogeny for these taxa.New names that reflect the homologies of these muscles are presented. Ten muscle duplicationsby subdivision and three phylogenetic losses of muscles have occurred in this system. No rela-tionship was found between the number of separate muscles and the relative masses of the Alor A2 muscles, suggesting that muscle duplication events essentially repackage existing muscletissue. However, both Al and A2 muscle masses are correlated with each other and with thefeeding ecology of these fishes. Durophagous taxa have relatively larger Al and A2 muscles,whereas planktivores and benthic grazers have relatively smaller A2 muscles. [Homology; mor-phological duplications; muscle evolution; orthology; paralogy; Tetraodontiformes.]

The concept of structural duplicationhas played a central role in the search forgeneral patterns and repeating themes indie evolution of organismal design (Ver-meij, 1973a, 1973b; Liem, 1980b; Lauder,1981, 1990; Liem and Wake, 1985; Schaeferand Lauder, 1986; Emerson, 1988; Lauderand Liem, 1989). The central idea is thatphylogenetic increases in the number ofstructural units with the same primitivefunction promote functional diversificationby several routes. Repeated elements in-crease the overall complexity of design,which may underlie an increase in mor-phological and functional diversity withina clade (Vermeij, 1973a; Liem, 1980b;Schaefer and Lauder, 1986, 1996). Thefunctional redundancy created by dupli-cation of morphology or molecules mayalso release constraints on one of the prim-itive elements, permitting it to evolve anew form or function (Lauder, 1981). Forexample, redundancy is thought to be aprimary mechanism in the evolution ofgene function (Ohno, 1970; Ohta, 1989), the

evolution of the protein structural diversi-ty (Chothia, 1994), and the evolution ofsome developmental mechanisms in ver-tebrates (Holland et al., 1994; Holland andGarcia-Fernandez, 1996).

Although numerous examples exist ofrepeated elements in animals and plants(e.g., appendages, blood vessels, body seg-ments, hairs, leaves, muscles, scales), rela-tively few cases have been developed tothe point that specific consequences ofstructural duplication can be tested withina rigorous phylogenetic framework (Laud-er, 1990). Here, we describe a system ofstructural duplication in the jaw muscula-ture of tetraodontiform fishes. Within thisclade, the Al and A2 adductor mandibulaemuscles have been duplicated repeatedlyin different subclades and extant taxa maypossess from two to eight separate Al andA2 muscles. Our primary purpose here isto review the homology and phylogenetichistory of these tetraodontiform jaw mus-cles and present a nomenclature that re-flects our hypotheses of homologies. We

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442 SYSTEMATIC BIOLOGY VOL. 46

Triacanthoids Balistoids Tetraodontoids

11 genera20 species

4 genera7 species

331 genera 11 genera 14 genera95 spedes 40 spedes 33 spedes

1 genus 3 genera1 spedes 3 spedes

20 genera 6 genera147 spedes 19 spedes

Triacanthodidae Triacanthidae Monacanthidae Balistidae Ostraciidae Triodontidae MoNdae Tetraodontidae Diodontidae

FIGURE 1. Phylogeny of extant tetraodontiform families based on the work of Winterbottom (1974b), Mat-suura (1979), Tyler (1981), Lauder and Liem (1983), and Winterbottom and Tyler (1983). Images represent thegeneral body form of fishes in these families. The number of genera and spedes are from Nelson (1994).

also present initial data on the functionalconsequences of muscle duplicationthrough an analysis of muscle sizes.

Adductor Mandibulae Muscles ofTetraodontiform Fishes

The teleost order Tetraodontiformes is adiverse group of primarily marine fishesbroadly distributed throughout the tropi-cal and temperate regions of the world.This order is represented today by ninefamilies containing approximately 101genera with 365 species (Fig. 1; Nelson,1994). The tetraodontiform phylogenyused in this study was proposed by Win-terbottom (1974b), was corroborated byLauder and Liem (1983), and is supportedby additional data provided by Matsuura(1979), Tyler (1980), and Winterbottomand Tyler (1983). Tetraodontiforms are di-vided into three large clades. The relative-ly basal superfamily Triacanthoidea con-tains the Triacanthodidae (spikefishes) andTriacanthidae (triplespines). These triacan-thoids are the sister taxon to the more fa-

miliar tetraodontiform fishes placed in theother two superfamilies. The superfamilyBalistoidea contains the Ostraciidae (box-fishes, cowfishes), Balistidae (triggerfish-es), and Monacanthidae (filefishes). Theirsister group, the superfamily Tetraodon-toidea, contains the Triodontidae (purse-fishes), Molidae (ocean sunfishes), Tetra-odontidae (puffers), and Diodontidae(porcupinefishes).

One of the most distinctive features ofmost tetraodontiforms are their robustteeth and powerful oral jaws. Unlike mostother bony fishes, tetraodontiform fishesuse their oral jaws not only to capture butalso to process prey (Turingan and Wain-wright, 1993; Wainwright and Turingan,1993; Turingan, 1994). As in other fishes,the muscles responsible for closing andgenerating the biting forces of the oral jawsare those of the adductor mandibulae com-plex (Lauder, 1985). In most teleost fishes,this muscle complex consists of at leastfour muscles, Al, A2, A3, and Aw, whichare distinguished based on their relative

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1997 FRIEL AND WAINWRIGHT—HOMOLOGIES OF TETRAODONTIFORM JAW MUSCLES 443

origins and insertions on the jaws (Winter-bottom, 1974a). All of these muscles orig-inate on the palatal arch and are innervat-ed by branches of the fifth cranial nerve.Winterbottom (1974a) hypothesized thatall adductor mandibulae muscles of teleostfishes plesiomorphically inserted solely onthe lower jaw and Al has arisen phyloge-netically by encroachment of muscle fibersupon the maxilla-mandibular ligament,which connects the upper and lower jaws.Thus, all adductor mandibulae muscles ex-cept Al retain this plesiomorphic insertionon the lower jaw, and Al may retain aclose connection with A2 in basal tetra-odontiforms such as triacanthoids. In mostteleost fishes including all tetraodonti-forms, Al and A2 are the most easily ob-served jaw muscles given their large sizeand relatively superficial positions. A3 andAw lie deep to both Al and A2 and alwaysinsert on the lower jaw.

Within tetraodontiforms, the number ofAl and A2 muscles has increased in someclades, whereas the A3 and Aw muscleswhen present are always singular (Winter-bottom, 1974b). The number of Al musclesranges from a single undivided Al in alltriacanthoids and triodontids to as manyas six separate Al muscles in some mon-acanthids. Similarly, the number of A2muscles varies from a single A2 in triacan-thids to as many as three separate A2 mus-cles in balistids and tetraodontids. Thisduplication of adductor mandibulae mus-cles, along with variation in their originsand insertions, has made identifying ho-mologous muscles between families andparticularly superfamilies difficult. Win-terbottom's (1974b) classic monograph onthe myology of tetraodontiform fishes doc-uments the diversity of adductor mandib-ulae muscles in this clade and providedthe first nomenclature for these muscles.During initial research on a representativebalistoid (the gray triggerfish, Batistes ca-priscus) and a tetraodontoid (the southernpuffer, Sphoeroides nephalus), we identifiedmuscles following Winterbottom (1974b).However, like Winterbottom, we had dif-ficulty identifying some muscles in Sphoe-roides and in comprehending the transfor-

mations necessary to explain apparentmorphological differences between "ho-mologous" muscles in both taxa. Thus, webegan to question these homologies, par-ticularly in comparisons between balis-toids and tetraodontoids.

In addition to reviewing the morpholo-gy described by Winterbottom (1974b), weexamined additional taxa and here providedata on the relative masses of the Al andA2 muscles in representatives of six of thenine tetraodontiform families. Mass is gen-erally reflective of the force-producing ca-pacity of skeletal muscles (Powell et al.,1984), and we analyzed the general pat-terns of adductor mass in light of thisfunctional interpretation. We asked twospecific questions. First, as the adductormuscles are duplicated, does the overallmass of the adductor muscle complex in-crease or are new muscles essentiallycarved out of existing tissue? Second, arepatterns of diversity in adductor musclesize reflective of differences among speciesin feeding habits?

Homobgies of Duplicated Muscles

Our review and new hypotheses of mus-cle homologies are based on the assump-tion that all the duplicated Al and A2muscles in this clade of fishes have beenproduced by physical subdivision of pre-existing muscles. Specifically, all Al andA2 muscles have arisen in a phylogeneticsense by repeated subdivision of singularAl and A2 muscles present in the commonancestor of all tetraodontiforms and in anontogenetic sense by repeated subdivisionof singular Al and A2 muscles presentduring the development of an individualfish. We favor this model of muscle evolu-tion over a de novo model in which a newjaw muscle could arise from a novel con-densation of myogenic tissue. Although wedo not regard the de novo origin of mus-cles as an impossibility, a subdivisionmodel is consistent with the repeated ob-servations of incompletely divided musclesin some taxa (e.g., Al muscles of ostraciidsand A2 muscles of monacanthids). Suchintermediate morphologies would not beproduced by a de novo model but might

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be expected with a subdivision model. Al-though no ontogenetic data on tetraodon-tiforms is available, study of the adductormandibulae complex in other teleost fishesdoes support a subdivision model (Ad-riaens and Verraes, 1996).

Another important aspect of the subdi-vision model is that it produces a hierar-chical pattern of ancestral and duplicateddescendant muscles. Such a phylogeneticframework for muscles, like a phylogenyfor taxa, allows for explicit predictionsabout the descendant muscles based onpleisiomorphic features (i.e., functions, mo-tor patterns, physiology, etc.) inheritedfrom the ancestral muscle. Muscles that ap-pear de novo, by definition, have no clearhomology to any preexisting muscle andthus no predictable pleisiomorphic fea-tures when they first appear.

We concur with Lauder (1990) that du-plication of morphological structures suchas jaw muscles of tetraodontiforms is anal-ogous to the more familiar phenomenon ofgene duplication. Granted, this analogy isnot exact because duplication of genes isexplained only by phylogeny and dupli-cation of morphological structures is ex-plained by both phylogeny and ontogeny(Patterson, 1987). Nevertheless, duplicationof structures (i.e., genes or morphology)should require the recognition of both par-alogs and orthologs if possible (Fitch, 1970;Patterson, 1987, 1988). Simply put, para-logs are different copies of a structure,derived from a single ancestral structure,that are present in the same or differentindividuals (e.g., a and p hemoglobingenes, Ala and Alp muscles; Fig. 2a),whereas orthologs are the same particularcopy in different individuals (e.g., a he-moglobin genes, Ala muscles; Fig. 2a).Properly identifying orthologs in differenttaxa is critically important in any compar-ative or phylogenetic study involving du-plicated structures (Patterson, 1987; Doyle,1992; Hillis, 1994).

In practice, the identification of paralogsand orthologs of morphological structuresis often not possible. Problems in homolo-gizing duplicated structures both betweenindividuals (i.e., orthology) and within in-

A1ab' A1ab" A1ab"' |Aipb'm Aipb"m

^^4

A2g"b| |A2p1

(C) A2a A2p

VA2

FIGURE 2. Muscle duplication by subdivision, (a)Muscle duplication events mapped onto a phylogenyof three hypothetical taxa. An ancestral muscle, Al, issubdivided into two descendant muscles, Ala andAlp, in the common ancestor of taxa X, Y, and Z. Aipis later subdivided into two additional descendantmuscles, Aip' and Aip", in the ancestor of taxon Z.Different copies of a duplicated muscle in the sameindividual or in different taxa are paralogous muscles(e.g., Ala and Aip in taxa X and Y). The same copyof a duplicated muscle in different taxa are ortholo-gous muscles (e.g., Ala in taxa X, Y, and Z; Aip intaxa X and Y). (b). Subdivision pattern of Al musclesin tetraodontiform fishes. Muscle names reflect thehistorical relationships between duplicated muscles.Boxes at the same level in the figure and suffixes b(balistoids or balistids), m (monacanthids), o (ostra-ciids), and t (tetraodontoids or tetraodontids) denotemuscles produced by parallel subdivision events indifferent clades. (c) Subdivision pattern of A2 musclesin tetraodontiform fishes.

dividuals (i.e., paralogy) have been point-ed out by Bateson (1892, 1894), Danforth(1930), Van Valen (1982), Roth (1984), Wag-ner (1989a, 1989b), Mabee (1993), and oth-ers. For example, it may be difficult if notimpossible to identify orthologs when oneparticular copy of a duplicated structure isnot morphologically distinct relative to

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others in different individuals (e.g., a scaleon the body of a fish vs. another scale ona different fish) or when the total numberof duplicated structures and thus the rel-ative position or identity of any one copydiffers between individuals (e.gv vertebra15 in a fish with 50 total vertebrae vs. ver-tebra 15 in another fish with 55 total ver-tebrae). Furthermore, in most cases of se-rial homology (e.g., body segments,vertebrae, fin rays, teeth), homonomy (e.g.,hairs, scales, blood cells), and redundantfunctional linkages (e.g., jaw opening lig-aments in teleost fishes; Lauder and Liem,1989), the duplicated structures cannot behomologized with a single structure in ahypothetical ancestor or outgroup taxon(McKitrick, 1994).

In contrast, the duplicated jaw musclesdescribed in this study can be homolo-gized with single ancestral muscles justlike duplicated genes can be homologizedwith single ancestral genes. The generalconcepts of homology between muscleswithin an individual and the evolution ofmuscles via subdivision have previouslybeen suggested by McKitrick (1994). Here,we build upon these concepts and presentthe first attempt to explicitly distinguishorthologs and paralogs for duplicatedmorphological structures.

MATERIALS AND METHODS

This review is based in part on mor-phology described by Winterbottom(1974b). In addition, we examined the jawmusculature of 24 species from seven ofthe nine families. Taxa examined, taxon ab-breviations used in figures, number of in-dividuals examined, and standard lengthare as follows: one triacanthodid, Parahol-lardia lineata (1, 120 mm); two triacanthids,Triacanthus biaculeatus (TB, 2, 174-225 mm)and Trixiphichthys zveberi (TW, 2, 124-143mm); two ostraciids, Acanthostracion quad-ricornis (AQ, 2, 51-141 mm) and A. poly-gonius (AP, 1, 128 mm); three balistids,Balistes capriscus (BC, 2, 124-256 mm), B.vetula (BV, 2, 155-187 mm), and Xanthich-thys ringens (XR, 2, 147-168 mm); fourmonacanthids, Aluterus schoepfi (AS, 2,127-169 mm), Cantherhines pullus (CPU, 1,

143 mm), C. macrocerus (CM, 1, 325 mm),and Monacanthus hispidus (MH, 2, 93-215mm); eight tetraodontids, Arothron mani-lensis (AM, 1,185 mm), Canthigaster rostrata(CR, 1, 61 mm), Chelonodon patoca (CPA, 1,115 mm), Torquigener hicksi (TH, 1, 83 mm),Lagocephalus lagocephalus (LL, 1, 506 mm),Sphoeroides maculatus (SM, 2, 130-172 mm),S. nephalus (SN, 3, 205-235 mm), and S. tes-tudineus (ST, 1, 164 mm); and four diodon-tids, Chilomycterus antennatus (CA, 1, 130mm), C. schoepfi (CS, 1, 96 mm), Diodon hol-ocanthus (DHQ 1, 107 mm), and D. hystrix(DHY, 1, 235 mm). Fishes were initiallyfixed in 10% formalin and then transferredto 70% ethanol prior to dissection. Allspecimens except Parahollardia lineata(FMNH 46686) are from the laboratory col-lection of P. C. Wainwright at Florida StateUniversity. One or two individuals of eachspecies were dissected along with an ad-ditional size series of 10 striped burrfish,Chilomycterus schoepfi (41-166 mm). Theseadditional burrfish were included to ob-tain preliminary data on the allometry ofthe Al and A2 muscles in tetraodontiformfishes. Fishes were weighed to the nearestgram prior to dissection, and all Al andA2 muscles were carefully dissected andremoved from one side of the head fromall specimens except Parahollardia lineata.Individual muscles were gently patted dryto remove excess fluid and weighed to thenearest 0.01 g. Most of the anatomical il-lustrations that supplement our descrip-tions were produced from camera lucidadrawings of representative specimens dis-sected in this study.

All mass data were log transformed be-fore statistical analyses were performed.The effect of body size was removed byregressing muscle mass on body mass andcalculating residuals. Any apparent corre-lations between the raw data points or re-siduals could be due to the confoundingeffects of phylogeny because species arenot statistically independent data points(Felsenstein, 1985; Garland et al., 1992). Todetermine whether such correlated char-acter evolution was real, we also calculatedphylogenetically independent contrastswith the computer program CAIC (Purvis

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and Rambaut, 1995). Using an incomplete-ly resolved phylogeny and an assumptionof equal branch lengths, 19 standardizedcontrasts were generated. All regressionsinvolving contrasts were forced throughthe origin as required (Garland et al.,1992).

To reflect our hypotheses of muscle ho-mologies, we produced a new nomencla-ture for the Al and A2 muscles of tetra-odontiform fishes. We tried to maintaincurrent names when possible. Orthologousmuscles have the same unique name in alltaxa possessing them, and cases of parallelmuscle evolution are always clearly iden-tified (Figs. 2b, 2c). To preserve the histor-ical relationships among adductor man-dibulae muscles, each subdivision eventrequires new names for all descendantmuscles. There has been a tendency to re-tain the ancestral muscle name for the onedescendant muscle that diverges least fromthe ancestral muscle morphology. Al-though this practice reduces the number ofnew names needed, it obscures the ho-mologies between the descendant musclesand their ancestral muscle.

In our new nomenclature, muscle namesbegin with either Al or A2 followed bysuffixes to reflect the transformational his-tories of these muscles. The descendantmuscles of a primary subdivision event aredesignated by a and (3, those of a subse-quent secondary subdivision event by sin-gle, double, or triple primes if necessary(as in monacanthids), and those of a sub-sequent tertiary subdivision event by aand p again. In addition, the suffixes b, m,o, and t, for balistoids or balistids, mona-canthids, ostraciids, and tetraodontoids ortetraodontids, respectively, are used to dis-tinguish descendant muscles produced byparallel (i.e., nonhomologous) subdivisionevents in different clades. This nomencla-ture and hierarchy of muscles is summa-rized in Figures 2b and 2c. The correspon-dence between old and new muscle namesis summarized in the Appendix. Abbrevi-ations are used in figures for nonadductormandibulae muscles and other elements:adductor arcus palatini (AAP), dentary(DEN), dilatator operculi (DO), erectores

dorsalis (ERD), hypertrophied branchios-tegal ray (HBR), levator arcus palatini(LAP), levator operculi (LO), maxilla (MX),palatine (PAL), premaxilla (PMX), protrac-tor hyoidei (PHY), ramus mandibularis(RMD), and retractor arcus palatini (RAP).All osteological terms follow Tyler (1980).

Because the ultimate test of any hypoth-esis of homology is that of congruencewith the homologies of other characters(Patterson, 1982,1988), we used a variationof this test to argue for our new set of ho-mologies. We compared transformation se-ries for the Al and A2 muscles, one basedon current homologies and the other basedon our new homologies, for the same phy-logeny of tetraodontiform families (Fig. 1).Although this phylogeny was originallybased in part on Winterbottom's homolo-gies of Al and A2 muscles, it is supportedby other characters presented by Winter-bottom (1974b), Matsuura (1979), Tyler(1980), and Winterbottom and Tyler(1983). The same phylogeny was producedby parsimony analysis of all available dataminus any Al and A2 characters, so therewas no circularity in optimizing thesemuscle homologies on this phylogeny.

Transformation series were optimizedusing assumptions of both accelerated(ACCTRAN) and delayed (DELTRAN)transformation in MacClade (Maddisonand Maddison, 1992). These options do notchange the number of character steps butcan reveal equally parsimonious transfor-mation series. The ACCTRAN option max-imizes reversals by favoring early gains ofmuscles near the root of the phylogenyand later losses of muscles. In contrast, theDELTRAN option maximizes parallelismsby favoring independent gains of musclesnear the tips of the phylogeny. This pro-cedure allowed us to determine the mini-mum number of evolutionary steps neces-sary to explain the observed morphologyin the terminal taxa given a particular setof muscle homologies and to comparecompeting hypotheses of homologies. Thepreferred set of homologies was the onethat required the fewest steps and leastamount of homoplasy.

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RESULTS

This review is divided into four sections:homologies of Al muscles within balis-toids, homologies of Al muscles betweenbalistoids and tetraodontoids, homologiesof A2 muscles between balistoids and tet-raodontoids, and comparisons of the rela-tive masses of Al and A2 muscles in rep-resentative taxa. Because the first threesections deal with competing hypothesesof homologies, it is necessary to use thetwo different nomenclatures. By conven-tion, in the morphological descriptions themore familiar names of Winterbottom(1974b) are listed first and are immediatelyfollowed by the new names in parentheses,e.g., Ala (=Alab'). In all other sectionsand in all figures, muscle names follow thenew nomenclature, which is summarizedin Figures 2b and 2c and the Appendix.

Homologies of Al Muscles in Balistoids

Most triacanthoids retain the plesiomor-phic Al condition for all tetraodontiforms.There is a single superficial Al, dorsal toA2, which originates beneath the eye andinserts on both the upper and lower jaws(Fig. 3a). The only exceptions to this pat-tern are the long-snouted triacanthodidgenera Macrorhamphosodes and Halimochi-rurgus, in which Al shares a tendon withA2 and inserts solely on the lower jaw(Winterbottom, 1974b). In all triacan-thoids, Al is separated anteriorly from A2by the path of the ramus mandibularis ofthe trigeminal nerve (Fig. 3a). However intriacanthids, Al is not completely separat-ed from A2 posteriorly (Fig. 3a) as it is intriacanthodids.

In contrast to the condition in triacan-thoids, Al is duplicated one or more timesin all balistoids and all tetraodontoids ex-cept triodontids. Some of these Al musclesin both balistoids and tetraodontoids wereconsidered orthologs by Winterbottom(1974b).

In ostraciids, Al is superficially coveredby A2 muscles and is incompletely subdi-vided into three sections: a large dorsal di-vision, A1B" (=Alab), and two smallerventral divisions, Alp (=Aipb'o) and

Alp' (=Alpb"o) (Fig. 3d). The separationbetween these two ventral muscles is slightin some taxa (including the Acanthostracionexamined here) but is well developed inother ostraciids examined by Winterbot-tom (1974b). All three Al sections insertvia a common tendon on the distal portionof the maxilla.

In balistids, most of Al is superficiallycovered by A2 muscles and Al is subdi-vided once into a superficial muscle, Ala(=Alab) and a deeper muscle, Alp(=Alpb) (Figs. 3e, 3f). Ala (=Alab) orig-inates in front of the eye along the ethmoidregion and narrowly inserts on the distalend of the maxilla. Alp (=Aipb), in con-trast, originates relatively ventrally, on themetapterygoid, and inserts narrowly onthe distal end of the maxilla. Both Al mus-cles insert on the upper jaw via a commontendon.

This balistid pattern is modified in mon-acanthids by further duplication of Almuscles. Most monacanthids have at leasttwo superficial and three deep Al muscles(Figs. 3g, 3h). The superficial Al musclesinclude Ala (=Alab;), which inserts onthe maxilla, and Ala ' (=Alab"), which in-serts on both the maxilla and upper lip.The deep Al muscles include Alp(=Aipb'm) and Alp' (=Aipb"m), whichboth insert on the maxilla, and AI7(=Alab'"), which uniquely inserts on thepalatine. Variations of this monacanthidpattern occur in a few genera. Ala '(=Alab") is absent in Aluterus, and Alp'(=Aipb"m) is absent in Anacanthus. Ala"(=Alab'P) is uniquely present in Oxymon-acanthus dorsal to Ala ' (=Alab'a) and in-serts on the maxilla. Alp" (=Aipb"mp) isuniquely present in Paraluteres dorsomedi-al to Alp' (=Aipb"ma) and inserts on themaxilla.

Based on the pattern of Al muscles inbalistoids, Winterbottom (1974b) hypothe-sized that Al was subdivided into a su-perficial Ala (=Alab) and a deep Alp(=Aipb) in the common ancestor of allbalistoids. In addition, his recognition ofAlp' in both ostraciids (=Aipb"o) andmonacanthids (=Aipb"m) could be con-strued as indicating that these muscles are

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DO

A1pb"oA1ocb Alpb'o

A1

1 cm (f) (g) 1 cm (h)FIGURE 3. Jaw musculature of representative balistoids. See text for muscle and other element abbreviations,

(a) Triacanthus biacukatus, superficial view; Al does not overlie A2, and both muscles are incompletely subdi-vided posteriorly, (b) T. biacukatus, deep view of jaw musculature with Al and A2 removed, (c) Acanthostracionquadricornis, superficial view; A2 is subdivided into A2a and A2|3, and these two muscles lie superficial to theAl muscles, (d) A. quadricornis, deep view with A2a and A2|J removed; Al is subdivided into Alab, Al($b"o,and Aipb'o. (e) Batistes capriscus, superficial view; A2 is subdivided into A2a, A2(3'b, and A2|3"b, and thesethree muscles lie superficial to the Al muscles, (f) B. capriscus, deep view with A2a and A2p'b removed; Alis subdivided into Alab and AlfJb. (g) Monacanthus hispidus, superficial view; A2 is subdivided into A2a andA2p, and these two muscles lie superficial to all Al muscles except Alab' and Alab". (h) M. hispidus, deepview with Alab', Alab", A2a, and A2(3 removed; note the three deep Al muscles, Alab'", Alfib'm, andAipb"m.

orthologs and that AlfJ' was present in thecommon ancestor of all balistoids. This Alpattern for the common ancestor of balis-toids requires the following transforma-tions to explain the morphology observedin extant taxa. Subsequently in the lineageleading to ostraciids, Ala (=Alab) waslost and Alp' (=Al|Sb"o) was subdividedto form Alp" (=Alab). Apparently, Alp'was lost in the lineage leading to balistids.In the lineage leading to monacanthids

and within this clade, Ala ' (=Alab") andAla" (=Alab'P) have subdivided fromAla, Alp" (=Al(Jb"m|S) has subdividedfrom Alp, and Al-y (=Alab'") has arisenwith uncertain affinities to any other Almuscles. This transformation series for Almuscles in balistoids, using Winterbot-tom's homologies and nomenclature, ismapped on a phylogeny of tetraodonti-forms in Figure 4a.

Our reexamination of adductor mandib-

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Triacanthoids

1 1

A1 A1

Triacanthodidae Triacanthidae\ > -

X

•ITA1a'A1y

J^V

A1PA1P'

Balistoids

A1a

A1p

"s • -to ij 1

Monacanthidae Balistidae

A1a'AIY

^#A1|3' lost^

1A1PAIP'

AIP"^—-0^

Ostraciidae

^A IP "^ ^ ^ ^ 1 a lost

Tetraodontoids

1AIO

Aip/iAl / ^ ^ v

Triodontidae Molidae

Reversal ^ ^ ^ ^ ^(loss or fusion) ^ ^

1

A1a A1aA1P Alfl

Tetraodontidae Diodontidae

^ t ^ A1 a shifts origin^ ^ A i p shifts origin

A1P'

(a)F A1a&A1p


1 \A1ab' Aipb'm A1abA1ab" Aipb"mA1ab'"

A1cct

A1atA1atAipt

TriacanthodidaeTriacanthidae Monacanthidae Balistidae Ostraciidae Triodontidae Molidae Tetraodontidae Diodontidae

A1ot&A1pt

Aipb'm&Aipb"m1ab',A1ab"&A1ctb'

(b)FIGURE 4. Competing hypotheses of the evolution of Al muscles in tetraodontiform fishes, (a) Transfor-

mation series (ACCTRAN) based on muscle names and homologies proposed by Winterbottom (1974b). Thisseries requires a minimum of 10 steps (five gains, two shifts in the relative position of muscles, three reversalsby loss or fusion), (b) Alternative transformation series (ACCTRAN and DELTAN) based on new muscle namesand homologies described here. This series requires a minimum of five steps (all muscle duplications by sub-division). Note the parallel evolution of Ala and Aip in balistoids and tetraodontoids and Aip' and Alp" inostraciids and monacanthids.

ulae muscles suggests an alternative sce-nario of evolution of Al muscles withinbalistoids. We hypothesize that the ances-tral Al condition for balistoids was notlike that of balistids but was instead a par-tially subdivided Al like that of ostraciids.We consider Winterbottom's (1974b) A1(Tof ostraciids and Ala of balistids andmonacanthids to be orthologs, which werename Alab. This hypothesis of homol-ogy is suggested by the relative positionand mass of this Al muscle as compared

with other Al muscles. In all balistoids,Alab is the dorsalmost Al muscle and al-ways lies anterodorsal to the path of theramus mandibularis branch of the trigem-inal nerve. In addition, new data on the rel-ative masses of adductor mandibulae mus-cles reveal that Alab is consistently thelargest Al muscle in all balistoids.

In our scenario of Al evolution withinbalistoids, we hypothesize that Alab com-pletely separated from the ventral portionof Al, AlfJb, and shifted more anterodor-

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sally to a superficial position in the com-mon ancestor of balistids and monacan-thids. We do not consider Winterbottom's(1974b) Alp or Alp' of ostraciids andmonacanthids to be orthologs. Instead, wehypothesize these muscles have arisen in-dependently through separate subdivisionevents in both clades and thus have re-named them Aip'o and Aip"o in ostra-ciids and Aip'm and Aip"m in monacan-thids, respectively.

Several additional duplication eventsand losses of muscles have produced acomplex pattern of Al muscles in mona-canthids. It is unclear whether Alab',Alab", and Alab'" have been produced bya single subdivision event or by two se-quential subdivision events because allthree muscles appear simultaneously onthe phylogeny. Although other subdivisionevents in tetraodontiforms have producedonly two descendant muscles, it is moreparsimonious to assume that a single sub-division event of Alab produced thesethree muscles. The absence of Alab' inAluterus and of Aipb"m in Anacanthus isinterpreted as reversal by loss or fusion.Both genera are relatively derived mona-canthids and these muscles are present intheir sister taxa (Matsuura, 1979). Alab"aand Alab"p in Oxymonacanthus andAipb"ma and Aipb"mp in Paraluteres haveclearly arisen through two additional du-plication events within these genera. Thistransformation series for Al muscles forbalistoids, using the new homologies andnomenclature, is mapped on a phylogenyof tetraodontiforms in Figure 4b.

Homologies of Al Muscles between Balistoidsand Tetraodontoids

In triodontids, the sister group to allother tetraodontoids, Al is an undividedsuperficial muscle that originates beneaththe eye and inserts broadly on the proxi-mal portion of the maxilla (Fig. 5a). In con-trast, Al in molids, tetraodontids, and di-odontids is subdivided into a superficialventral muscle, Ala (=Aipt), and a super-ficial dorsal muscle, Alp (=Alat) (Figs.5b-e). These muscles are not covered byA2 muscles, and the relative dorsoventral

positions of the Al muscles is reversed ascompared with balistoids. Ala (=Aipt)originates superficially over the A2 mus-cles and inserts broadly on the distal endof the maxilla. Alp (=Alat) originates infront of the eye and inserts broadly on theproximal portion of the maxilla.

Winterbottom (1974b) did not explicitlystate whether the undivided Al of triodon-tids is a plesiomorphic condition as in tria-canthoids or a derived condition (i.e., a re-versal by either loss of one muscle orfusion of both). He did however explicitlyhomologize Ala (=Alab) in balistoids(Figs. 3e, 3f) and Ala (=Alpt) in tetra-odontoids (Figs. 3b, 3d) (Winterbottom,1974b:74). This interpretation of Al ho-mologies implies that Al was subdividedinto Ala (=Alab and Alpt) and Alp(=Aipb and Alat) in the common ances-tor of balistoids and tetraodontoids. How-ever, Winterbottom (1974b:74) went on tostate that Alp (=Aipb) of balistoids andAlp (=Alat) of tetraodontoids were prob-ably not homologous. These statementscreate a paradox because any subdivisionevent produces at least two pairs of or-thologous muscles in descendant taxa.There are only two alternatives; either bothAla and Alp are orthologs in balistoidsand tetraodontoids or neither of them are.

If one were to accept that Ala (=Alab)in balistoids and Ala (=Aipt) in tetra-odontoids are orthologs, then Al musthave been subdivided in the common an-cestor of balistoids and tetraodontoids.This hypothesis then requires the loss of amuscle or fusion of both muscles to ex-plain the undivided Al in triodontids andapparent absence of Ala (=Alab) in os-traciids. Such a scenario for Al evolution,using Winterbottom's (1974b) names andhomologies, is optimized (ACCTRAN) ona phylogeny of tetraodontiforms in Figure4a. Based on this set of homologies, at least10 steps are required (five gains of mus-cles, two shifts of muscle origins, and threereversals via loss or fusion of muscles) toexplain the origin of the Al muscles in thecommon ancestors of each tetraodontiformfamily. The only difference under DEL-TRAN is that Alp' is gained independent-

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A1A2oc

PALMX

PMX

RMD

1 cm (e)FIGURE 5. Jaw musculature of representative tetraodontoids. See text for muscle and other element abbre-

viations, (a) Triodon macropterus, superficial jaw musculature (adapted from original; Winterbottom, 1974b); Alis undivided and A2 is subdivided into A2a and A2|3. A23 passes medial to the path of the ramus mandibular-is. (b) Sphoeroides nephalus, superficial view; Al is subdivided into Alat and Aipt, AlfJt lies superficial to someA2 muscles, and A2 is subdivided into A2a, A2(3't, and A20"t. A23"t passes lateral to the path of the ramusmandibularis. (c) 5. nephalus, deep view with AlJ3t and A20't removed; A2a inserts on the maxilla, (d) Chilo-mycterus schoepfi, superficial view; Al is subdivided into a small Alat and a large Aipt. A13t lies superficialto some A2 muscles, (e) C. schoepfi, deep view with Alpt and part of the maxilla removed. The ramus man-dibularis passes entirely within A2f$ from the neurocranium to the lower jaw.

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ly in both monacanthids and ostraciidsrather than being gained in the commonancestor of balistoids and later lost in bal-istids.

Alternatively, we hypothesize that theundivided Al of triodontids is the plesio-morphic condition for tetraodontids be-cause Al was undivided in the commonancestor of both balistoids and tetraodon-toids. Therefore no duplicated Al musclesof tetraodontoids are orthologs of any du-plicated Al muscles of baslistoids. This hy-pothesis is completely consistent with ourscenario for Al evolution within balistids.Subsequently, Al was subdivided in thecommon ancestor of molids, tetraodontids,and diodontids to form Alat and Al(3t.Alat has remained in the relatively dorsalposition of Al in triodontids while Aipthas expanded ventrally over the A2 mus-cles. A transformation series for Al evo-lution, using our nomenclature and ho-mologies, is optimized on a phylogeny oftetraodontiforms in Figure 4b. Our scenar-io requires only five steps (all gains bymuscle duplication by subdivision) to ex-plain the origin of these Al muscles in thecommon ancestors of each tetraodontiformfamily. This transformation series is thesame under ACCTRAN or DELTRAN.

Homologies of Al Muscles in Balistoids andTetraodontoids

As in other teleost fishes, A2 is the mainsection of the adductor mandibulae mus-culature, which plesiomorphically insertson the lower jaw. In tetraodontiforms, thismuscle may be undivided or may consistof up to three separate muscles. To identifyorthologous muscles in taxa with morethan a single A2 muscle, Winterbottom(1974b) proposed using their positions rel-ative to the path of the ramus mandibular-is of the trigeminal nerve to the lower jaw.

In most triacanthodids, A2 is represent-ed by two muscles, a posterodorsal A2aand an anteroventral A2(3, which lies me-dial to the RMD (Winterbottom, 1974b).Gosline (1986) suggested that A2a in tria-canthodids may in fact be a portion of Al.However, this is not the case in the tria-canthid examined in this study (Parahollar-

dia), and we followed Winterbottom's pro-posal. Exceptions to this triacanthodidpattern are the long-snouted genera, Mac-rorhamphosodes and Halimochirurgus, whichhave an undivided A2 (Winterbottom,1974b). The path of the RMD in these twogenera is unknown. As in these specializedtriacanthodids, all triacanthids have an un-divided A2 muscle, which lies medial tothe path of the RMD (Fig. 3a).

In balistoids, A2 is always representedby at least two muscles. In ostraciids, botha dorsal A2a and a ventral A2p are pres-ent, and both muscles pass lateral to thepath of the RMD (Fig. 3c). Plesiomor-phically, these muscles are completely sep-arated in ostraciids but are fused posteri-orly in one ostraciid subclade, the tribeAracanini (Winterbottom and Tyler, 1983).In balistids, there are three A2 muscles ina dorsoventral sequence, A2a, A2(3(=A2p'b), and A2T (=A2(3"b), respectively(Fig. 3e). In most balistids, A2a passes lat-eral to the path of the RMD, whereas bothA2(3 (=A2p'b) and A2^ (=A2(Tb) are me-dial to the path of this nerve. Variation isfound in the balistid Balistipus undulatus,where the RMD passes through A2a be-fore passing lateral to A2£ (=A2(3'b) (Win-terbottom, 1974b). In monacanthids, onlytwo A2 muscles, A2a and A2(3, are present(Fig. 3g). In some genera (e.g., Chaetoderma,Monacanthus, Paramonacanthus, Paraluteres,Pervagor, Stephanolepis), the ventral portionof A2(3 may be slightly differentiated (Fig.3g) but is never completely separated as isA27 (=A2p"b) in balistids (Figs. 3e, 3f). Inall monacanthids, A2a passes lateral andA2p passes medial to the path of the RMD(Fig- 3g).

Like balistoids, all tetraodontoids alsohave at least two A2 muscles. In triodon-tids, A2 is represented by a dorsal A2aand a ventral A2(3, and the RMD passesmedial to A2a and lateral to A2fi muchlike it does in most balistids and all mon-acanthids (Winterbottom, 1974b) (Fig. 5a).This triodontid A2 pattern differs howeverfrom that of all other tetraodontids. Inmolids, tetraodontids, and diodontids,A2a (=A2p or A2p't and A2^"t) and A2(3(=A2a) are present but the relative origins

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of these muscles have apparently shifted ifA2p is identified as the A2 muscle medialto the path of the RMD (Figs. 5b-e). Inthese three families, A2a (=A20 or A2p'tand A2p"t) now lies ventral to A2p (=A2a)and is in the same relative position as A2fiin triodontids.

In tetraodontids, A2a (=A2(3) has twodistinct heads (=A2(3't and A2J3"t) (Win-terbottom, 1974b). The ventral head(=A2P"t) is present in all tetraodontid gen-era examined here, but its separation fromthe dorsal head (=A2£'t) may be partiallyobscured in superficial view by Ala(=Aipt). Furthermore, the insertion ofA2S (=A2a) has shifted from the lowerjaw to the maxilla in the three species ofSphoeroides examined.

The path of the RMD varies in tetra-odontids and diodontids and differs fromthe clear pattern in balistids, monacan-thids, and triodontids. The RMD may startmedial to A2a (=A2p't and A2(Tt) butpasses through the anteroventral portion(A2f$"t) just before it reaches the lower jaw(e.g., Arothron, Canthigaster, Chelonodon,Sphoeroides) or it may travel entirely withinA2a (=A2S) before reaching the lower jaw(e.g., Chibmycterus, Diodon).

Based on the pattern of A2 muscles,Winterbottom (1974b) hypothesized thatA2 was subdivided in the common ances-tor of all tetraodontiforms and the undi-vided A2 of some triacanthoids had arisenthrough two separate character reversalsby loss or fusion, once in triacanthids andonce in the common ancestor of Macro-rhamphosodes and Halimochirurgus. Winter-bottom used the path of the RMD to dis-tinguish A2a and A2(3 in most balistoidsand all tetraodontoids. This hypothesis re-quires at least one shift of the RMD in os-traciids and a relative shift of the originsof both A2 muscles in the ancestor of mo-lids, triodontids, and diodontids to main-tain these homologies. A separate A2-y(=A2B"b) has arisen in the lineage leadingto balistids by subdivision of A2B. Winter-bottom however did not provide a separatename for an analogous subdivision of A2fJ,which occurs in tetraodontids. A transfor-mation series for A2 muscles, using Win-

terbottom's names and homologies, is op-timized (ACCTRAN) on a phylogeny oftetraodontiforms in Figure 6a. This scenar-io requires a minimum of six steps (twogains, one shift in the path of the RMD,two shifts of muscle origins, and one re-versal by loss or fusion) to explain the or-igin of A2 muscles in the common ances-tors of each tetraodontiform family. Theonly difference under DELTRAN is thatsubdivision of A2 into A2a and A2B hasoccurred independently in triacanthidsand in the common ancestor of balistoidsand tetraodontoids.

We also consider A2 to have been sub-divided in the common ancestor of all tet-raodontiforms and the undivided A2 insome triacanthodids and all triacanthids tobe independent reversals. However, thishypothesis is tentative because under DEL-TRAN it is equally parsimonious to as-sume that the undivided A2 of triacan-thids is plesiomorphic and the divided A2of most triacanthodids is independentlyderived from that of balistoids and tetra-odontoids. In either case, the A2 homolo-gies we propose for balistoids and tetrao-dontoids are unaffected.

Our scenario of A2 evolution differsfrom Winterbottom's (1974b) mainly be-cause we hypothesize that A2a and A2Bhave retained their relative positions in alltetraodontiforms while the path of theRMD has shifted at least twice. Based onour observations, variation in the path ofthe RMD between species is greater thanoriginally suggested by Winterbottom.Thus, we consider the path of the RMD anunreliable landmark for identifying de-scendant A2 muscles. Use of this criterionleads to the misidentification of the orthol-ogous A2 muscles in molids, tetraodon-tids, and diodontids.

A transformation series for the evolutionof A2 muscles based on our names and ho-mologies is optimized (ACCTRAN) on aphylogeny of tetraodontiforms in Figure6b. As with Winterbottom's (1974b) ho-mologies, the only difference under DEL-TRAN is that the subdivision of A2 intoA2a and A2(3 has occurred independentlyin triacanthids and the common ancestor

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TriacanthodidaeTriacanthidae Monacanthidae Balistidae Ostraciidae Triodontidae

Reversal(loss or fusion)

MdkJae

A2p A2PA2a A2a

Tetraodonttdao Diodontidae

A2a shifts originA2p shifts origin

(a) A2a&A2P


TriacanthodidaeTriacanthidae Monacanthidae Balistidae Ostraciidae Triodontidae Molidae Tetraodontidae Diodontidae

Reversal ^ ^ ^ ^ P **sion) ^ S ^ ^ " mandibularis shifts ^ ^

Path of ramusmandibularis shifts

(b) A2O&A2P

FIGURE 6. Competing hypotheses of the evolution of A2 muscles in tetraodontiform fishes, (a) Transfor-mation series (ACCTRAN) based on muscle names and homologies proposed by Winterbottom (1974b). Thisseries requires a minimum of six steps (two gains, one shift of the ramus mandibularis, two shifts in the relativepositions of muscles, one reversal by loss or fusion), (b) Alternative transformation series (ACCTRAN) basedon new muscle names and homologies described here. This series requires a minimum of six steps (threeduplications by muscle subdivision, two shifts in the path of the ramus mandibularis, one reversal by loss orfusion). This series is more parsimonious than that based on the homologies proposed by Winterbottom (1974b)because it explains the origin of additional muscles not previously recognized in tetraodontids.

of balistoids and tetraodontoids. We hy-pothesize that the ancestor of balistoidsand tetraodontoids had a dorsal A2a andventral A2(3 with the RMD passing lateralto A2a. In the lineage leading to balistidsand monacanthids, A2|3 had a slightly dif-ferentiated ventral section. This ventralsection completely subdivided to formA2p'b and A2p"b in the common ancestorof balistids. In the ostraciid lineage, the

path of the RMD shifted to pass medial toboth A2a and A2p. Triodontids retain therelatively plesiomorphic A2 pattern for tet-raodontiforms. This pattern was modifiedin the common ancestor of molids, tetra-odontids, and diodontids when the pathof the RMD again shifted to pass medialto A2p. In the tetraodontid lineage, A2pindependently subdivided to form A2p'tand A2(3"t. In total, our scenario requires

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six steps (three gains, two shifts in thepath of the RMD, and one reversal by lossor fusion) to explain the origin of A2 mus-cles in the common ancestors of each tetra-odontiform family and includes a step forthe origin of A20't and A2p"t in tetraodon-tids, which were not recognized as sepa-rate muscles by Winterbottom. Thus, thescenario based on our new homologies ismore parsimonious than that based onWinterbottom's homologies.

Relative Masses of Al and Al Muscles

Based on an ontogenetic series of 10burrfish, Chilomycterus schoepfi (41-166 mmstandard length), most Al and A2 musclesshowed slight positive allometry (slopes ofleast squares regressions of log musclemass on log body mass: Alat = 0.936;Al(3t = 1.126; A2a = 1.169; A2{* = 1.126).Only Alat differs from other Al and A2muscles by having slight negative allome-try. This muscle is extremely atrophied inall diodontids examined (e.g., Figs. 5d, 5e).Interspecifically, the Al and A2 muscles of22 other tetraodontiform species alsoshowed slight positive allometry. An ex-ample of this relationship is shown in Fig-ure 7a, where the log of the mass of all Almuscles is plotted against the log of bodymass for 10 C. schoepfi along with singlerepresentatives of 22 other species. A leastsquares regression fitted to the log-trans-formed data of all species has a slope of1.04, a y-intercept of -2.51, and an r2 of0.80. The only clear outliers to this trendare the ostraciids, Acanthostracion polygoni-us and A. quadricornis, and one triacanthid,Trixiphichthys xveberi. Standardized inde-pendent contrasts of Al mass and bodymass also show a strong positive correla-tion (slope = 1.06; r2 = 0.89) (Fig. 7b).

The percentage of adductor muscle masscomprised by the Al muscle varies consid-erably among tetraodontiforms, rangingfrom 23% in one tetraodontid, Sphoeroidesnephalus, to 61% in one balistid, Xanthich-thys ringens. Thus, there is considerablevariation in the amount of muscle tissuedevoted to moving the upper or lowerjaws. There is also considerable overlap invariation between most families, with the

1.00

-1.750.75 1.25 1.75 2.25 2.75

log(body mass)3.25

0.80

O

0.00

-0.10 0.00 0.10 0.20 0.30 0.40 0.50 0.60 0.70 0.80Contrast in log(body mass)

FIGURE 7. Slight positive allometry of Al musclemass for most tetraodontiform fishes, (a) Plot oflog(Al mass) and log(body mass) for 10 individualsof Chilomycterus schoepfi (x ) plus single individuals of22 tetraodontiform species (•). See text for species ab-breviations, (b) Plot of contrasts in log(Al mass) andcontrasts in log(body mass) for 19 independent con-trasts. A line fitted to these contrasts and forcedthrough the origin has a slope of 1.06 and an r2 of0.89.

greatest intrafamilial variation in tetra-odontids and balistids.

A pattern does emerge when the resid-uals of log Al mass and log A2 mass re-gressed against log body mass were plot-ted against each other (Fig. 8a). There wasa strong tendency for species with relative-ly large Al muscles to also have relativelylarge A2 muscles and for species with rel-

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0.50 -0.40 -0.30 -0.20 -0.10 -0.00 -

-0.10 --0.20 --0.30 --0.40 --0.50 --0.60 --0.70 --0.80 --0.90 -

-1.00 -

(a)

XR. AM

TB* *BC

AS* # #CPU CM

LL

•TW

•AP # A Q

CPA # C R

BV pHY.ST S N

TH CA* -

*DHO

-0.6 -0.5 -0.4 -0.3 -0.2 -0.1 0.0 0.1 0.2 0.3 0.4 0.5 0.6Residual of log(A2 mass)

0.40

0.30

(b)•

•

K % ••

O 0.20

g 0.10

ou"5 o.oo

-0.10 -

-0.20-0.15 -0.10 -0.05 0.00 0.05 0.10 0.15 0.20

Residual of contrast in log(A2 mass)

FIGURE 8. Positive correlation between Al massand A2 mass in tetraodontiform fishes, (a) Plot of re-siduals of log(total Al mass) and the residuals oflog(total A2 mass) both regressed against log(bodymass) for single individuals of 23 tetraodontiform spe-cies. An individual located at the intersection of bothaxes would represent a fish with average Al and A2masses for all tetraodontiforms of that body size. Seetext for species abbreviations, (b) Plot of residuals ofcontrasts in log(Al mass) and log(A2 mass) both re-gressed against contrast in log(body mass) for 19 in-dependent contrasts. A line fitted to these contrastsand forced through the origin has a slope of 1.12 andan r2 of 0.55.

atively small Al muscles to have relativelysmall A2 muscles. This positive correlationis supported by residuals of standardizedcontrasts for Al and A2 mass regressedagainst standardized contrasts of body

mass (slope = 1.12; r2 = 0.55) (Fig. 8b).Those taxa that have relatively large ad-ductor muscles (most tetraodontids, di-odontids, and Balistes vetula) are duropha-gous and feed on prey such as molluscs,echinoderms, and crabs (Randall, 1967).Species with relatively small Al and A2muscles (ostraciids, several monacanthids,one triacanthid) tend to be grazers thatfeed on algae and relatively soft-bodied in-vertebrates (Randall, 1967). Morphologicaloutliers tend to be trophic outliers as well.For example, the tetraodontid Lagocephalusis a pelagic puffer that feeds largely on softprey such as squid (Wheeler, 1969). Thetriggerfish Xanthichthys is a zooplanktivoreand has a relatively small A2 muscle (Tur-ingan, 1994).

No relationship was seen between thenumber of adductor mandibulae musclespossessed by a species and the relative sizeof the adductor mandibulae complex (Fig.9a). Many taxa with only four or five Aland A2 muscles, such as balistids, tetra-odontids, or diodontids, have much largerresiduals than some monacanthids, withas many as seven Al and A2 muscles. Thislack of correlation is also supported whenresiduals (standardized contrasts of log[Aland A2 mass] regressed against standard-ized contrasts in log[body mass]) are plot-ted against standardized contrast in thenumber of Al and A2 muscles (slope =0.03; r2 = 0.01) (Fig. 9b).

The relative contributions of individualAl descendant muscles to total Al massfor eight representative species are shownin Figure 10a. In all balistoids examined(ostraciids, balistids, monacanthids), Alabis the largest Al descendant muscle, andthis relationship is maintained if its de-scendant muscles, e.g., Alab', Alab", andAlab'" in monacanthids such as Monacan-thus, are pooled together. This observationthat Alab is the largest Al muscle in bal-istoids is also consistent with our hypoth-esis that Winterbottom's (1974b) Alp" ofostraciids (e.g., Acanthostracion) is the or-tholog to Alab of balistids and monacan-thids.

Unlike balistoids, the relative masses ofAl descendant muscles in tetraodontoids

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0.50-

0.30-

0.10-

-0.10 -

-0.30-

-0.50-

-0.70-

(a)

•TB

•TW

S N «

C R »ST

DHY»CS «CPA

. XR! A M

DHO BC

•LL

•AQ

•AP

•CM

•AS

# MH

•CPU

2 3 4 5 6 7

Number of A1 & A2 muscles

^ 0.25

s

-0.15-0.80 -0.40 0.00 0.40 0.80 1.20

Contrast in number of A1 & A2 muscles

FIGURE 9. No correlation between muscle massand number of jaw muscles in tetraodontiform fishes,(a) Plot of residuals of log(Al mass + A2 mass) re-gressed against log(body mass) and total number ofAl and A2 muscles for single individuals of 23 tetra-odontiform species. Data points for Diodon hystrix(DHY) and Chilomycterus schoepfi (CS) overlap on thisplot. See text for other species abbreviations, (b) Plotof residuals of contrasts in log(Al mass + A2 mass)regressed against contrasts in log(body mass) and to-tal number of Al and A2 muscles for 19 independentcontrasts. A line fitted to these contrasts and forcedthrough the origin has a slope of 0.025 and an r2 of0.01.

examined (tetraodontids, diodontids) varyconsiderably between taxa, which is con-sistent with our hypothesis that the Al de-scendant muscles of tetraodontoids havearisen independently in this clade and arenot orthologs of any Al muscles of balis-

toids. At one extreme is the tetraodontidLagocephalus with a large Alat and a smallAipt, and at the other extreme are diodon-tids such as Chilomycterus, which have aminute Alat and an enormous AlfJt. Oth-er tetraodontids examined in this studyhave relatively equal-size Al descendantmuscles such as those of Sphoeroides (Fig.10a).

The relative contributions of individualA2 descendant muscles to total A2 massfor the same eight species are shown inFigure 10b. In most balistoids and tetra-odontoids, A2p is larger than A2a. Thispattern is reversed in all monacanthidssuch as Monacanthus and in a single balis-tid, Xanthichthys, where A2a is larger thanA2(3. This reversal is more likely due to areduction in A2(3 rather than to an increasein A2a because these same taxa have neg-ative A2 residuals as compared with othertetraodontiforms (Fig. 8). One other nota-ble difference is the relatively small A2aand large A2p't and A2f*"t of Sphoeroidesas compared with other tetraodontids.This pattern may be associated with thefact that A2a uniquely inserts on the upperjaw in this genus.

DISCUSSION

The adductor mandibulae system of tet-raodontiform fishes provides a clear ex-ample of phylogenetic repetition of mor-phological elements. This system is wellsuited to an analysis of the functional con-sequences of structural duplication for sev-eral key reasons. First, there is a well-cor-roborated phylogeny of the major lineagesof tetraodontiform fishes. Second, the newmuscle nomenclature presented here willpermit specific comparisons to be madebetween the functional attributes of an an-cestral muscle and the descendants that re-sult from a splitting event. Third, includingmuscle evolution within tetraodontiformfamilies, we recognize a total of 10 casesof muscle subdivision and 4 cases of re-versals by either loss or fusion of musclesubdivisions in this system. This largenumber of independent changes in musclenumber makes it possible to repeatedlytest specific hypotheses about the conse-

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Triacanthus biaculeatus Xanthichthys ringens Acanthostracion quadhcomis Sphoeroides nephalusTriacanthidae Balistidae Ostraciidae Tetraodontidae

Batistes caphscusBalistidae

Monacanthus hispidus Lagocephalus lagocephalus Chilomycterus schoepfiMonacanthidae Tetraodontidae Diodontide

(b)

Triacanthus biaculeatusTriacanthidae

Xanthichthys ringens Acanthostracion quadricomisBalistidae Ostraciidae

Sphoeroides nephalusTetraodontidae

Batistes capriscusBalistidae

Monacanthus hispidus Lagocephalus lagocephalus Chilomycterus schoepfiMonacanthidae Tetraodontidae Diodontidae

FIGURE 10. Pie charts of muscle masses for individuals of eight species from six tetraodontiform families,(a) Al muscles. All descendant Ala muscles in balistoids are shaded the same. The Ala and AlfJ muscleshave arisen independently in both balistoids and tetraodontoids. (b) A2 muscles. The A2(3' and A2fJ" muscleshave arisen independently in both balistids and tetraodontids.

quences of subdivision. Because musclesubdivision is not a phylogenetically orontogenetically unique event, it is possibleto generate statistically useful samplesizes, thus addressing a problem that hasplagued comparative studies (Garland etal., 1992).

Muscle Homologies

This review of the Al and A2 musclesof tetraodontiforms revealed that severalmuscles currently identified by the samename in different subclades are not or-thologs and thus require new names to re-

flect new hypotheses of homology. Trans-formation series based on these newhomologies are more parsimonious forboth Al and A2 muscles than are thosebased on homologies proposed by Winter-bottom (1974b).

We hypothesize that a minimum of 10separate duplication events have producedthe diversity of Al and A2 muscles inthese fishes. This review revealed twotrends in the evolution of jaw muscles intetraodontiforms. First, the origins of Aland A2 muscles and the relative positionsof descendant muscles to each other are

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conservative features in this clade. Forthese fishes, position is a more reliable cri-terion for identifying muscles than is thepath of the RMD, which has been used inother studies (Winterbottom, 1974b; Gos-line, 1986). The path of this nerve is a re-liable landmark for Al muscles in balis-toids but not for A2 muscles intetraodontoids.

Second, duplication of muscles by sub-division is more common whereas second-ary loss of duplicated muscles is less com-mon than previous studies have suggested.A similar trend in phylogenetic increasesin muscle number was reported by Gosline(1986), who surveyed higher groups of te-leost fishes and found mat muscles pro-duced by primary subdivision of the ad-ductor mandibulae were seldomsecondarily lost. Some of the differences inthe muscle gain versus loss ratio for thetransformations series examined in thisstudy are expected because homoplasythat was originally due to secondary lossesof "homologous" muscles is now ex-plained instead by parallel gains of "non-homologous" muscles through additionalsubdivision events. We recognize at leastthree such cases of parallel muscle evolu-tion: Alab and Al|3b of balistoids versusAlat and Alpt of tetraodontoids, AlfJb'oand Al(3b"o of ostraciids versus Aipb'mand AlfJb"m of monacanthids, and A2|3'band A2|3"b of balistids versus A2|3't andA2B"t of tetraodontids.

Duplication of jaw muscles by subdivi-sion has undoubtedly occurred severaltimes within teleost fishes. According toGosline (1989) "Al" and "A2" muscleshave arisen once in ostariophysan fishes(Cypriniformes, Characiformes, Silurifor-mes, Gymnotiformes) and again indepe-nently in higher teleost fishes (Beryciformes,Zeiformes, Perriformes, Scorpaeniformes,Tetraodontiformes). Other more complexadductor mandibulae subdivisions similarto those described here for tetraodonti-forms have occurred in loricarioid catfishes(Trichomycteridae, Nematogenyidae, Cal-lichthyidae, Scoloplacidae, Astroblepidae,Loricariidae) (Howes, 1983; Schaefer andLauder, 1986, 1996) and parrotfishes (Scar-

idae) (Bellwood and Choat, 1990; Bell-wood, 1994). Loricarioids and scaridscould potentially serve as other modelcases of duplication because phylogeniesare available for both groups (Howes, 1983;Schaefer, 1987; Bellwood, 1994). Complexpatterns of duplicated jaw muscles occurin clades of fishes that have highly derivedoral jaw morphologies and novel feedingmodes. Most bony fishes are ram or suc-tion feeders and use their oral jaws forprey capture but not processing (Liem,1980a; Lauder, 1985). In contrast, tetra-odontiform fishes and parrotfishes usetheir robust oral jaws to both capture andprocess food items, which are often quitehard (e.g., molluscs, corals) (Bellwood andChoat, 1990; Turingan and Wainwright,1993; Wainwright and Turingan, 1993;Turingan, 1994). In loricarioid catfishes,the oral jaws are highly modified to scrapefood items such as algae off objects or torasp plant material (Schaefer and Lauder,1986, 1996).

Our recognition of homologies differentfrom those of Winterbottom (1974b) is dueto two main factors. First, our homologiesare based on an explicit model of muscleevolution by subdivision. This model pro-duces paralogs, which we distinguishedfrom their common ancestral muscle andeach other. Although Winterbottom alsosuggested that new muscles are producedby subdivision, he often retained an ances-tral muscle name for the one descendantmuscle that resembled the ancestral mus-cle in outgroup taxa. This practice ulti-mately obscured the homologies betweenthese muscles.

Second, Winterbottom's (1974b) analysispredates the widespread availability ofcomputer programs for analyzing data andinvestigating alternative optimizations ofcharacters. As Winterbottom stated (1974b:73), his analysis methods precluded thepossibility of any explanations based onparallel or convergent evolution. Althoughthe topology of his "hand generated" phy-logeny is identical to one produced usinga computer algorithm and the same data,it lacked explicit character transformationssuch as those investigated in this study. A

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posteriori analysis of the transformationsseries for homoplastic characters can some-times reveal alternative and possibly moreparsimoniously interpreted homologies.Although these new homologies may notchange the phylogeny itself, they may rad-ically affect any hypotheses based on therefuted homologies.

Masses of Al and Al Muscles

A correlation between adductor musclemass and diet has been previously report-ed for other fishes. Bellwood and Choat(1990) found that parrotfishes that bite andexcavate pieces of hard coral skeletonswhile feeding had relatively larger jawbones and greater total adductor mandibu-lae mass than did parrotfishes that onlyscrape the algae-encrusted surfaces of oldcoral skeletons while feeding. Similarly,Turingan (1994) found that durophagoustetraodontiforms such as balistids, tetra-odontids, and diodontids had relativelymassive A2 muscles, jaws, and suspensionelements as compared with a single graz-ing monacanthid examined. However, hedid not find any significant differences inAl mass between taxa, as we have foundhere with the larger number of nondu-rophagous taxa (i.e., triacanthids, ostra-ciids, and several monacanthids) exam-ined. Although some monacanthids hadAl residuals similar to those of balistids,tetraodontids, and diodontids, most didnot.

Our sample of 23 tetraodontiform spe-cies from six families shows no support forthe idea that overall adductor mass will in-crease as new muscles evolve (Figs. 9a, 9b).During phylogenetic increases in the num-ber of muscles, the existing muscle tissueapparently is subdivided not only in aqualitative sense, as our model states, butalso in a quantitative sense. One interpre-tation of this pattern could be that con-structional constraints (Barel, 1983) on thespace available to adductor muscle tissuelimit increases in total adductor musclemass. However, this factor is probably notlimiting the ability of the adductor muscleto change in overall size, as indicated bythe existing diversity in overall adductor

mass that clearly varies with trophic habits(Fig. 8a). Constructional constraints willundoubtedly place some upper boundaryon the size of the adductor mandibulaemusculature, but the flexibility that is in-dicated by ecomorphological patterns sug-gests that increases in the number of ad-ductor muscles could theoreticallyinfluence the amount of muscular tissue.

Although there have been numerousmuscle duplications in this system, mostdescendant muscles retain their primitiveattachment to a particular jaw element (i.e.,Al muscles insert on the maxilla, and A2muscles insert on the mandible). Only twoexamples were found where muscle inser-tions had changed to different bony ele-ments. In monacanthids, the insertion ofAlab'" has shifted from the maxilla to thepalatine bone (Fig. 3g) (Winterbottom,1974b). In tetraodontids of the genusSphoeroides, A2a insertion has shifted fromthe mandible to the maxilla (Fig. 5c). Inmonacanthids, this shift is associated witha subdivision event, whereas in Sphoeroides,the shift clearly occurred after the subdi-vision event.

Currently, we are further exploring theanalogy drawn in this study between du-plications of genes and duplications ofmorphological elements. A major para-digm in molecular evolution is that geneduplication leads to divergence in nucleo-tide sequence and ultimately divergence inthe function of paralogous genes (Ohno,1970; Ohta, 1989; Chothia, 1994; Hollandet al., 1994; Holland and Garcia-Fernandez,1996). Thus, is duplication of muscles alsoassociated with divergence in function,and if so, are there general patterns inmuscle evolution? To address these ques-tions, we are using electromyography toquantify one aspect of muscle function, theindividual activity patterns of musclesduring feeding events. Because paralogousmuscles are derived from the same ances-tral muscle, they should have the same ple-siomorphic function (i.e., activity pattern)unless functional divergence has occurred.If one or more of the duplicated musclesexamined in this study have functionallydiverged, we should find differences in the

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relative timing (i.e., onset and duration)and/or intensity of muscular activity be-tween paralogous muscles. Such differ-ences in activity patterns should havefunctional consequences for the feedingmechanisms in these fishes.

ACKNOWLEDGMENTS

We thank J. Grubich, K. Ralston, and T. Thys forthoughtful comments on a draft of this manuscriptand R. Winterbottom for his feedback on several as-pects of this research. We also thank R. Turingan forproviding some of the specimens used in this studyand M. Westneat for the loan of specimens from theField Museum of Natural History. Support for this re-search was provided by NSF grant IBN 9306672 to P.C. Wainwright.

REFERENCES

ADRIAENS, D., AND W. VERRAES. 1996. Ontogeny ofcranial musculature in Clarias gariepinus (Siluroidei:Clariidae): The adductor mandibulae complex. J.Morphol. 229:255-269.

BAREL, C. D. N. 1983. Towards a constructional mor-phology of the cichlid fishes (Teleostei, Perciformes).Neth. J. Zool. 33:357-^24.

BATESON, W. 1892. On the numerical variation inteeth, with a discussion of the concept of homology.Proc. Zool. Soc. Lond. 1892:102-115.

BATESON, W. 1894. Materials for the study of variationtreated with especial regard to discontinuity in theorigin of species. Macmillan, New York.

BELLWOOD, D. R. 1994. A phylogenetic study of theparrotfishes family Scaridae (Pisces: Labroidei),with a revision of genera. Rec. Aust. Mus. Suppl.20:1-86.

BELLWOOD, D. R., AND R. CHOAT. 1990. A functionalanalysis of grazing in parrotfishes (family Scaridae):The ecological implications. Environ. Biol. Fishes 28:189-214.

CHOTHIA, C. 1994. Protein families in the metazoangenome. Development (Suppl.) 1994:27-33.

DANFORTH, C. H. 1930. Numerical variation and ho-mologies in vertebrae. Am. J. Phys. Anthropol. 14:463^81.

DOYLE, J. J. 1992. Gene trees and species trees: Mo-lecular systematics as one-character taxonomy. Syst.Bot. 17:144-163.

EMERSON, S. 1988. Testing for historical patterns ofchange: A case study with frog pectoral girdles. Pa-leobiology 14:174-186.

FELSENSTEIN, J. 1985. Phytogenies and the compara-tive method. Am. Nat. 125:1-15.

FITCH, W. M. 1970. Distinguishing homologous fromanalogous proteins. Syst. Zool. 19:99-113.

GARLAND, T., JR., P. H. HARVEY, AND A. R. IVES. 1992.Procedures for the analysis of comparative data us-ing phylogenetically independent contrasts. Syst.Biol. 41:18-32.

GOSLINE, W. A. 1986. Jaw muscle configuration insome higher teleostean fishes. Copeia 1986:705-713.

GOSLINE, W. A. 1989. Two patterns of differentiationin the jaw musculature of teleostean fishes. J. Zool.Lond. 218:649-661.

HILLIS, D. M. 1994. Homology in molecular biology.Pages 339-368 in Homology: The hierarchical basisof comparative biology (B. K. Hall, ed.). AcademicPress, San Diego.

HOLLAND, P. W. H., AND J. GARCIA-FERNANDEZ. 1996.Hox genes and chordate evolution. Dev. Biol. 173:382-395.

HOLLAND, P. W. H., N. A. WILLIAMS, AND A. SIDOW.1994. Gene duplication and the origins of vertebratedevelopment. Development (Suppl.) 1994:125-133.

HOWES, G. J. 1983. The cranial muscles of loricarioidcatfishes, their homologies and value as taxonomiccharacters (Teleostei: Siluroidei). Bull. Br. Mus. Nat.Hist. 45:309-345.

LAUDER, G. V. 1981. Form and function: Structuralanalysis in evolutionary morphology. Paleobiology7:430-̂ 142.

LAUDER, G. V. 1985. Aquatic feeding in lower verte-brates. Pages 210-229 in Functional vertebrate mor-phology (M. Hildebrand, D. M. Bramble, K. F. Liem,and D. B. Wake, eds.). Harvard Univ. Press, Cam-bridge, Massachusetts.

LAUDER, G. V. 1990. Functional morphology and sys-tematics: Studying functional morphology in a his-torical context. Annu. Rev. Ecol. Syst. 21:317-340.

LAUDER, G. V, AND K. F. LIEM. 1983. The evolutionand interrelationships of the actinopterygian fishes.Bull. Mus. Comp. Zool. 150:95-197.

LAUDER, G. V., AND K. F. LIEM. 1989. The role of his-torical factors in the evolution of complex organis-mal functions. Pages 63-78 in Complex organismalfunctions: Integration and evolution of vertebrates(D. B. Wake and G. Roth, eds.). Wiley and Sons,New York.

LIEM, K. F. 1980a. Acquisition of energy by teleosts:Adaptive mechanisms and evolutionary patterns.Pages 299-334 in Environmental physiology of fish-es (M. A. Ali, ed.). Plenum, New York.

LIEM, K. F. 1980b. Adaptive significance of intra- andinterspecific differences in the feeding repertoires ofcichlid fishes. Am. Zool. 20:295-314.

LIEM, K. F., AND D. B. WAKE. 1985. Morphology: Cur-rent approaches and concepts. Pages 366-377 inFunctional vertebrate morphology (M. Hildebrand,D. M. Bramble, K. F. Liem, D. B. Wake, eds.). Har-vard Univ. Press, Cambridge, Massachusetts.

MABEE, P. M. 1993. Phylogenetic interpretations ofontogenetic change: Sorting out the actual and ar-tefactual in an empirical case study of centrarchidfishes. Zool. J. Linn. Soc. 107:175-291.

MADDISON, W. P., AND D. R. MADDISON. 1992.MacClade: Analysis of phylogeny and characterevolution, version 3.05. Sinauer, Sunderland, Mas-sachusetts.

MATSUURA, K. 1979. Phylogeny of the superfamilyBalistoidea (Pisces: Tetraodontiformes). Mem. Fac.Fish. Hokkaido Univ. 26:49-169.

MCKITRICK, M. C. 1994. On homology and the on-tological relationship of parts. Syst. Biol. 43:1-10.

Dow




NELSON, J. S. 1994. Fishes of the world, 3rd edition.Wiley and Sons, New York.

OHNO, S. 1970. Evolution by gene duplication.Springer-Verlag, Heidelberg, Germany.

OHTA, T. 1989. Role of gene duplication in evolution.Genome 31:304-310.

PATTERSON, C. 1982. Morphological characters andhomology. Pages 21-74 in Problems of phylogeneticreconstruction (K. A. Joysey and A. E. Friday, eds.).Academic Press, New York.

PATTERSON, C. 1987. Introduction. Pages 1-22 in Mor-phology and molecules in evolution: Conflict orcompromise (C. Patterson, ed.). Cambridge Univ.Press, New York.

PATTERSON, C. 1988. Homology in classical and mo-lecular biology. Mol. Biol. Evol. 5:603-625.

POWELL, P., R. R. ROY, P. KANIM, M. A. BELLO, AND V.EDGERTON. 1984. Predictability of skeletal muscletension from architectural determinations in guineapig hind limbs. J. Appl. Physiol. 57:1715-1721.

PURVIS, A., AND A. RAMBAUT. 1995. Comparativeanalysis by independent contrasts (CAIC): An Ap-ple Macintosh application for analysing compara-tive data. Comp. Appl. Biosci. 11:247-251.

RANDALL, J. E. 1967. Food habits of reef fishes of theWest Indes. Stud. Trop. Oceanogr. 5:655-847.

ROTH, V. L. 1984. On homology. Biol. J. Linn. Soc. 22:13-29.

SCHAEFER, S. A. 1987. Osteology of Hypostomus ple-costomus (Linnaeus), with a phylogenetic analysis ofthe loricariid subfamilies (Pisces: Siluroidei). Con-trib. Sci. (Los Angel.) 394:1-31.

SCHAEFER, S. A., AND G. V. LAUDER. 1986. Historicaltransformation of functional design: Evolutionarymorphology of the feeding mechanisms of loricari-oid catfishes. Syst. Zool. 35:489-508.

SCHAEFER, S. A., AND G. V. LAUDER. 1996. Testing his-torical hypotheses of morphological change: Bio-mechanical decoupling in loricarioid catfishes. Evo-lution 50:1661-1675.

TURINGAN, R. G. 1994. Ecomorphological relation-

ships among Caribbean tetraodontiform fishes. J.Zool. Lond. 233:493-521.

TURINGAN, R. G., AND P. C. WAINWRIGHT. 1993. Mor-phological and functional bases of durophagy in thequeen triggerfish, Batistes vetula (Pisces, Tetraodon-tiformes). J. Morphol. 215:101-118.

TYLER, J. C. 1980. Osteology, phylogeny, and higherclassification of the fishes of the order Plectognathi(Tetraodontiformes). NOAA Tech. Rep., NMFS Circ.434:1-422.

VAN VALEN, L. M. 1982. Homology and causes. J.Morphol. 173:305-312.

VERMEIJ, G. 1973a. Adaptation, versatility and evolu-tion. Syst. Zool. 22:466-477.

VERMEIJ, G. 1973b. Biological versatility and earthhistory. Proc. Natl. Acad. Sci. USA 70:1936-1938.

WAGNER, G. P. 1989a. The biological homology con-cept. Annu. Rev. Ecol. Syst. 20:51-69.

WAGNER, G. P. 1989b. The origin of morphologicalcharacters and the biological basis of homology.Evolution 43:1157-1171.

WAINWRIGHT, P. C, AND R. G. TURINGAN. 1993. Cou-pled versus uncoupled functional systems: Motorplasticity in the queen triggerfish Balistes vetula. J.Exp. Biol. 180:209-227.

WHEELER, A. 1969. The fishes of the British Isles &N. W. Europe. Michigan State Univ. Press, East Lan-sing.

WINTERBOTTOM, R. 1974a. A descriptive synonymy ofthe striated muscles of the Teleostei. Proc. Acad.Nat. Sci. Phila. 125:225-317.

WINTERBOTTOM, R. 1974b. The familial phylogeny ofthe Tetraodontiformes (Acanthopterygii: Pisces) asevidenced by their comparative myology. Smithson.Contrib. Zool. 155:1-201.

WINTERBOTTOM, R., AND J. C. TYLER. 1983. Phyloge-netic relationships of aracanin genera of boxfishes(Ostraciidae: Tetraodontiformes). Copeia 1983:902-917.

Received 16 July 1996; accepted 20 February 1997Associate Editor: Paula Mabee

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APPENDIX. Correspondence between the jaw mus-cle names used by Winterbottom (1974b) and the newnames used in this study of tetraodontiform fishes.

FamilyWinterbot-tom (1974b) This study

Triacanthodidae

Triacanthidae

Ostraciidae

Balistidae

Monacanthidae

Triodontidae

Molidae

Tetraodontidae

Diodontidae

AlA2aA2pAlA2AlpAip'Aip"A2aA2pA l aAipA2aA2pA27A l aAla'Ala"Al-yAlpAlp'Aip"A2aA2pAlA2aA2PA l aAipA2aA2pA l aAlpA2aA2pA l aAipA2aA2p

AlA2aA2PAlA2Alpb'oAipb"oAlabA2aA2pAlabAlpbA2aA2p'bA2p"bAlab'Alab" or Alab"aa

Alab"pAlab'"Alpb'mAipb"m or Aipb"ma<Aipb"mpA2aA2pAlA2aA2PAlptAlatA2pA2a

AlptAlatA2p't and A2p"tA2aAlptAla tA2pA2a

* Muscle duplications unique to some genera within thisfamily.

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