Skull ontogeny: developmental patterns of fishes conserved across major tetrapod clades

EVOLUTION & DEVELOPMENT

8:6, 524 –536 (2006)

Skull ontogeny: developmental patterns of fishes conserved across major tetrapod clades Rainer R. Schoch Staatliches Museum fu¨r Naturkunde Stuttgart, Rosenstein 1, D-70191 Stuttgart, Germany Correspondence (email: [email protected])

SUMMARY In vertebrates, the ontogeny of the bony skull forms a particularly complex part of embryonic development. Although this area used to be restricted to neontology, recent discoveries of fossil ontogenies provide an additional source of data. One of the most detailed ossification sequences is known from Permo-Carboniferous amphibians, the branchiosaurids. These temnospondyls form a near-perfect link between the piscine osteichthyans and the various clades of extant tetrapods, retaining a full complement of dermal bones in the skull. For the first time, the broader evolutionary significance of these event sequences is analyzed, focusing on the identification of sequence heterochronies. A set of 120 event pairs was analyzed by event pair cracking, which helped identify active movers. A cladistic analysis of the

event pair data was also carried out, highlighting some shared patterns between widely divergent clades of tetrapods. The analyses revealed an unexpected degree of similarity between the widely divergent taxa. Most interesting is the apparently modular composition of the cranial sequence: five clusters of bones were discovered in each of which the elements form in the same time window: (1) jaw bones, (2) marginal palatal elements, (3) circumorbital bones, (4) skull roof elements, and (5) neurocranial ossifications. In the studied taxa, these ‘‘modules’’ have in most cases been shifted fore and back on the trajectory relative to the Amia sequence, but did not disintegrate. Such ‘‘modules’’ might indicate a high degree of evolutionary limitation (constraint).

INTRODUCTION

ontogeny of the skull may contribute critically to bridge these gaps. Although the underlying mechanisms cannot be studied directly, patterns of heterochronic change derived from an analysis of the actual changes of developmental events on the trajectory will help to form a framework of developmental patterns whose mechanistic basis (e.g., neural crest evolution) may then be studied in crown groups. In recent time, paleontological evidence on sequences of bone formation and growth patterns in extinct vertebrates has accumulated (Boy 1974; Sander 1989; Caldwell 1994; Carroll et al. 1999; O’Keefe et al. 1999). Among these finds, the discovery of early larval stages of an extinct amphibian clade, the branchiosaurid temnospondyls, has revealed detailed ossification sequences for the skull (Boy 1974; Schoch 1992, 2004). Recently, one of these sequences was compared with that of a primitive salamander, the hynobiid Ranodon, which yielded a vast degree of similarity in the timing of ossification of single bones (Schoch 2002). From a morphological point of view, this was not expected because (i) extant salamanders and fossil temnospondyls differ substantially in the structure and morphology of the skull, and (ii) other lissamphibians such as anurans and caecilians depart boldly from this sequence. The actual bearing of these sequence similarities on tetrapod evolution is yet to be evaluated within a phylogenetic framework. This forms the focus of the present study, which uses recently

The declared aim of evolutionary developmental biology is to understand the reprogramming of developmental mechanisms and its bearing on macroevolution (Raff and Raff 2000; Hall 2002; Wilkins 2002; Arthur 2002a, b, 2004). The embryonic formation of the vertebrate skull should be an ideal focus for such studies, because even minor changes in this multidimensional system may have a significant effect on the phenotype. Although vertebrate skulls vary enormously in architecture, function, and modes of growth, a surprising degree of evolutionary conservation at the level of developmental mechanisms has been uncovered in the last decade (Francis-West et al. 1998; Hall 1999a, b). On the other hand, it seems obvious that functional demands, such as early larval feeding, should have an impact on the developmental patterning of the skull (Adriaens and Verraes 1998). Today, the embryonic formation of cranial bones can be traced in great detail through development. Cranial ossification sequences may be crucial for the understanding of skull formation, because in contrast to soft tissue data they can be derived from both extant and fossil taxa. In the preceding decades, wide morphological gaps between crown groups have left room for much speculation about the mechanisms and history of skull remodeling. Fossil evidence on the early 524

& 2006 The Author(s) Journal compilation & 2006 Blackwell Publishing Ltd.

Schoch developed analytical techniques for the comparison of developmental sequences. Among the relatively few well-known cranial ossification sequences in osteichthyans, that of branchiosaurids forms a near-perfect link between bony ‘‘fishes’’ and the various clades of crown-tetrapods, because unlike all living tetrapods, they retained a full complement of dermal bones in the skull. The present study concentrates on the following questions: (1) in which points do the trajectories of branchiosaurids and extant tetrapods depart from the (supposedly primitive) trajectory of basal actinopterygians, (2) have these evolutionary changes of the developmental sequence been disassociated or are there coherent patterns, and (3) are there any patterns that have been conserved across the transition to amniotes, and are there differences in the degree of conservation or evolutionary change among amniotes?

METHODS Techniques for analyzing developmental sequences have been developed by Smith (1996, 1997, 2002) and Velhagen (1997). More recently, Jeffery et al. (2002) have focused on a procedure that identifies active evolutionary shifts of events on a developmental trajectory. A particular strength of this procedure is that it may distinguish events that have actively shifted on the trajectory (‘‘active movers’’) from those that have only apparently moved (‘‘hitchhikers’’) because of their relation to other actively moving events and that show no movement in relation to fix events. The main focus of this method are the significant movements (identified shifts above a certain threshold) of events within an evolving ontogeny, a procedure termed event pair cracking (Jeffery et al. 2002). Event pairing methods have recently been criticized and have shown to lead to erroneous results (Schulmeister and Wheeler 2004). However, these problems are of a more general nature, affecting any reconstruction of ancestral states (Maddison 1995). Here, I have performed three kinds of analyses: (1) using event pairs as a primary character source in order to elucidate their potential bearing on tetrapod phylogeny, (2) identifying active movers by event-pair cracking of 120 event pairs, and (3) optimizing the identified active movers on a preexisting consensus phylogeny to identify consistent evolutionary change of cranial development in tetrapods. Analyses (2) and (3) form the major focus of this study, comparing whole event sequences of tetrapods with a supposedly primitive sequence, that of the actinopterygian Amia calva. The main questions of these comparisons are (i) which are the major sequence heterochronies (active movers) in each taxon as compared with the Amia sequence, and (ii) how large was the amount of evolutionary conservation among cranial ossification sequences in tetrapods. The focus of interest is thus not primarily the search for phylogenetic signals, but rather analyzing patterns of developmental constraints and evolutionary pathways along which cranial ossification sequences were altered in tetrapods. Herein, event pairing and event-pair cracking were applied to compare the one (supposedly ancestral) fish sequence (Amia calva) with those of tetrapods. This comparison followed the procedure

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outlined in Jeffery et al. (2002); see Appendix A for raw data. First, a set of 120 event pairs were derived from a sequence of 16 developmental events: the ossification of the premaxilla, maxilla, denatry, parasphenoid, vomer, palatine, parietal, supratemporal, postorbital, exoccipital, sphenethmoid, frontal, nasal, squamosal, prefrontal, and jugal (Appendix A, Table A1). Then, a matrix of these 120 event pairs was generated with coding as suggested by Smith (1997): 0 5 row event occurring before a column event, 1 5 simultaneous occurrence, and 2 5 row event occurring after a column event. (1) Phylogenetic inference (Fig. 1): As summarized by BinindaEmonds et al. (2002), event pairs derived from developmental sequences are nonindependent for two reasons: first, because they may be ontogenetically linked (causal sequences) and second for the way they are coded, in that each event is compared with every other event, with the consequence that each event is involved in many characters. Nevertheless, analyzing event pairs by using parsimony may shed light on shared developmental patterns of widely divergent clades. Therefore, each of the 120 event pairs was coded as a separate character and was analyzed for a total of 13 taxa, one out-group (Amia calva, Grande and Bemis 1998), and 12 in-groups (the extinct branchiosaurid Apateon caducus (Schoch 2002), the salamanders Ranodon sibiricus, Salamandrella keyserlingii, and Ambystoma maculatum (Lebedkina 1979), the basal anuran Ascaphus truei (Yeh 2003), the caecilian Gegeneophis ramaswamii (Mu¨ller et al. 2005), as well as the following amniotes: the sauropsids Chelydra serpentina (Rieppel 1993b), Lacerta agilis (Rieppel 1992), Alligator mississippiensis (Rieppel 1993a), and Gallus gallus (Erdmann 1939) and two mammal ‘‘taxa,’’ one consensus sequence

Fig. 1. Comparison of currently held consensus phylogeny (based on Laurin and Reisz 1997; Rieppel and Reisz 1999; Zardoya and Meyer 2001; Ruta et al. 2003) with the cladistic analysis based on 120 event-pair characters and 13 taxa as performed in the present study. Dotted nodes show unorthodox or controversial relationships. Rather than indicating true phylogenetic relationships, the results indicate shared aspects of developmental sequences, most of which are likely to have occurred in parallel, such as the postdisplacement of jaw elements (Ascaphus and Chelydra) or the predisplacement of the nasal (Gegeneophis and Lacerta).

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of marsupials (Smith 1997) and the placental Mus musculus (Erdmann 1939). The parsimony analysis was carried out using the branch-and-bound mode of Paup 3.1 (Swofford 1991), with all characters unordered and those events that did not occur in a particular taxon coded as uncertain (‘‘?’’). (2) Identification of active movers (Appendix A, Tables A2 and A3): Event-pair cracking was carried out in all 12 tetrapod sequences, based on the procedure outlined by Jeffery et al. (2002). Significant movements were identified by the following three steps: (1) the total relative change (TRC) for each event was calculated, (2) actively moving events were filtered out to retain only those with the largest relative change, and (3) relative changes of these active movers were corrected for changes involving other selected events (see Jeffery et al. 2002 for details). In step 2, the median of the absolute values of the TRCs was chosen as a threshold to separate significant movers from other events (see Appendix A, Table A3). (3) Optimization of active movers on a consensus phylogeny of tetrapods (Fig. 2): Character evolution was mapped using MacClade 3.0 (Maddison and Maddison 1992). The phylogenetic topology is a consensus of the following cladistic analyses: Laurin and Reisz (1997) and Ruta et al. (2003) for basal tetrapods as well as Laurin and Reisz (1995), deBraga and Rieppel (1997), Rieppel and Reisz (1999), and Zardoya and Meyer (2001) for relationships among amniotes. Throughout this article, the terms ‘‘time’’ and ‘‘time window’’ are used in a relative sense, as absolute age data are not relevant for the performed analyses. ‘‘Step’’ refers to the number of

positions an evolutionary shift has taken, for instance a postdisplacement by four steps means that a particular developmental event has moved by four positions into a later part of the developmental sequence. The terms ‘‘sequence heterochrony,’’ ‘‘predisplacement,’’ and ‘‘postdisplacement’’ refer to patterns of heterochrony, without any implication on the evolutionary causation that produced these patterns.

CRANIAL OSSIFICATION SEQUENCES The present study refers to published ossification sequences of well-known taxa from representative clades of bony gnathostome vertebrates (osteichthyans), with the emphasis on extant lissamphibians (salamanders, frogs, caecilians) and amniotes (turtles, squamates, crocodiles, birds, marsupials, and placentals). The study of skull morphology across major tetrapod taxa is made difficult by the fact that all extant lissamphibians and most amniotes lack a range of dermal bones primitively present in fossil tetrapods as well as fossil and extant outgroups, the fish-like sarcopterygians and actinopterygians. Among those taxa whose ossification sequences are available, Permo-Carboniferous branchiosaurids are the only tetrapod clade that retained a full complement of bones in the skull. From these mostly larval specimens, detailed ossification sequences are known (Boy 1974; Schoch 1992, 2002,

Fig. 2. Hypothesis of major evolutionary changes in the cranial ossification sequences of tetrapods. Data based on event-pair cracking sensu Jeffery et al. (2002), here mapped onto a tetrapod consensus phylogeny. Only apomorphic active movers are mapped, with predisplacements represented by ‘‘ ’’ and postdisplacements by ‘‘1.’’

Schoch 2004; Schoch and Carroll 2003). By this, they form a keystone in the comparison of developmental trajectories across the fish–tetrapod transition, still spanning a time window of at least 60 myr between their appearance as a clade (Westphalian D) and the supposed time window of the fish–tetrapod transition (Frasnian). A problem arising specifically in the analysis between ‘‘fishes’’ and tetrapods is the homology of the cranial bones whose relative appearance is to be compared. In both extant dipnoans and actinistians, many cranial elements are either lacking or cannot be readily homologized with actinopterygians and tetrapods (Janvier 1996). Thus, comparison of ossification sequences of cranial bones is largely confined to the palate. Therefore, basal crown-actinopterygians such as Polypterus or Amia are those extant fish-like osteichthyans that approach the tetrapod condition most closely (Schultze 1993).

Actinopterygians Among extant actinopterygians, basal clades such as cladistians (polypterids), paddlefishes (polyodontids), sturgeons (acipenseriforms), gars (ginglymods), and halecomorphs (amiids) come significantly closer to the primitive osteichthyan condition than extant teleosts, actinistians, or dipnoans (Lauder and Liem 1983; Janvier 1996). Polypterids and amiids in particular retain a large complement of dermal bones in the skull (Jarvik 1980; Grande and Bemis 1998), which is reduced in other taxa. The maxilla is firmly integrated into the skull and the gape is long, which has not only conserved plesiomorphic developmental pathways of bone formation but also serves as a model for the feeding mechanism of primitive osteichthyans (Lauder 1980). Ossification sequences have been published by Pehrson (1958) and Wacker et al. (2001) on Polypterus and Sewertzoff (1925), Pehrson (1940), and Grande and Bemis (1998) on Amia calva, whereas deBeer (1937) has added further observations to these and commented on ossification sequences of other actinopterygians. Among the listed extant taxa, the Polypteridae is generally conceived the basalmost clade, while the position of the Amiidae is far more crownwards, being the sister taxon of the Teleostei (Lauder and Liem 1983; Janvier 1996). Yet, the ossification sequence of Amia calva is the most detailed known and based on numerous specimens (Grande and Bemis 1998), whereas the sequence in Polypterus senegalus has been studied in depth only in the earliest (apterolarval) phase (Wacker et al. 2001). In Amia calva, the first bones to form are the tooth-bearing elements of the jaws and palate (Sewertzoff 1925; Pehrson 1940). As in other groups, teeth form before bone (deBeer 1937), and extensive sampling has revealed a detailed ossification sequence (Grande and Bemis 1998). According to the latter study, the sequence of those ossifications relevant

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to the present analysis reads: premaxilla–maxilla–dentary– parasphenoid–vomer–anterior dermopalatine (palatine)– ectopterygoid–dermopterotic (supratemporal)–entopterygoid (pterygoid)–postorbital–exoccipital–orbitosphenoid. In order to compare this sequence with those of tetrapods, the homology of some of these bones had to be clarified first. The homologies of the anterior dermopalatine, entopterygoid, and dermopterotic with the palatine, pterygoid, and supratemporal of tetrapods have been discussed by Arratia and Schultze (1991) and Janvier (1996). In the present analysis of ossification sequences, Amia served as the single outgroup. For this reason, all those bones only present in tetrapods were given the final rank in the Amia sequence, which resulted in the identification of apparent evolutionary shifts of these elements in all tetrapods; these shifts are all artifacts of coding, which was throughout considered in the event-pair cracking analyses. The known ossification sequence in Polypterus senegalus (Wacker et al. 2001) is similar to that of Amia calva in most aspects, especially the early appearance of maxilla, dentary, and palate bones as well as the later formation of the parietal and supratemporal; it departs only significantly by the postponed formation of the premaxilla. Acipenser ruthenus, which was studied by deBeer (1937), agrees more with Amia calva than with Polypterus senegalus in that the premaxilla is among the first bones to ossify.

Sarcopterygians In the few extant fish-like sarcopterygians, only palate and jaw elements can be readily homologized, and their ontogenetic formation has been studied only in the Australian lungfish Neoceratodus forsteri (Kemp 1977, 1999; Bartsch 1994). In this taxon, the first bones to form in the skull are the vomer, pterygoid, and parasphenoid almost at the same time, followed by opercular elements and the skull roofing elements EQ, JLM, ABC, and YZ (Kemp 1999). The early primordia of the dermal palatal and mandible bones grossly resemble those of actinopterygians and urodele larvae, especially the spatial patterning of the parasphenoid. The available fossil material of sarcopterygians does not reveal definitive data on the sequence of formation of dermal skull bones. The smallest specimens of Eusthenopteron foordi have already fully formed crania (Schultze 1984), despite poorly ossified postcranial skeletons (Carroll 2001).

Temnospondyls (Fig. 3A) The Temnospondyli form a large clade that includes taxa from which different ontogenetic stages have been found. In a few of these, more detailed patterns of ossification could be traced through size classes of specimens, and cranial ossification sequences have been particularly detected in branchiosaurids and related dissorophoid taxa. Boy (1974), Schoch (1992,

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Fig. 3. Phylogeny of tetrapods with the major taxa analyzed in this study (A–F). Three arbitrary stages exemplify the successive formation of skull bones in representative tetrapods. The underlying phylogeny is a consensus of recent results (see Fig. 1). Sources: Apateon caducus from Schoch (2002, 2004), Ranodon sibiricus from Lebedkina (1979, 2004), Cheyldra serpentina from Rieppel (1993a), Lacerta vivipara from Rieppel (1992), Alligator mississippiensis from Rieppel (1993b), and Homo sapiens from Augier (1931) and Drews (1993). Skeletal elements that ossify in the same relative time window are given the same color (red: jaws; blue: palate; green: skull roof; orange: circumorbitals; gray: bones with unclear homology).

2002, 2003), and Witzmann and Pfretzschner (2003) analyzed sequences of cranial ossification. Within branchiosaurids, such patterns have already been compared among closely related species that revealed slight variation in the sequence of later ontogenetic events particularly (Schoch 2004). The most complete cranial ossification sequence of temnospondyls is that of Apateon caducus, which has recently been found to be similar in numerous aspects to that of hynobiid salamanders (Schoch 2002). However, the branchiosaurid sequences are remarkably similar not only to salamanders but also to that of primitive actinopterygians such as Amia in that the jaw and palate bones formed early, followed by the skull roof, and finally involving circumorbital and braincase elements (Fig. 3A).

Lissamphibians (Fig. 3B) The main reference sequences taken here for salamanders are those of Ranodon sibiricus (Fig. 3B) and Salamandrella keyserlingii, two primitive urodeles belonging to the hynobiids studied extensively by Lebedkina (1979, 2004) and Schmalhausen (1968). Further, I included Ambystoma mexicanum of

Lebedkina (1979) and Yeh (2003). In salamanders, the ossification sequence is particularly similar to branchiosaurids, only in that in the braincase ossification starts relatively earlier and the maxilla generally forms very late in development. In anurans, Trueb (1985), Haas (1999), and Yeh (2003) have summarized evidence on cranial ossification sequences, and from the latter source the sequence of Ascaphus truei was taken. Yeh (2003) highlighted that the group as a whole shows very late formation of jaws as contrasted by an early formation of the exoccipital and frontoparietal. In caecilians, Wake and Hanken (1982) studied a sample of Dermophis mexicanus and Mu¨ller et al. (2005) analyzed the cranial ossification sequence in Gegeneophis ramaswamii. The latter, more detailed sequence reveals early formation of jaws and palate followed by the skull roof and braincase.

Reptiles (Fig. 3C–E) Studies focusing on reptile skull formation are relatively few in number and a range of articles have appeared only recently (Rieppel 1992, 1993a–c; Rieppel and Zaher 2001). Among

Schoch turtles, cranial ossification was reviewed by Bellairs and Kamal (1981) and Rieppel (1993b). The few available data suggest that in chelonians the jaw, palate, and circumorbital bones come first, followed by the cheek elements and frontal, and finally the parietal, parasphenoid, and neurocranium (Fig. 3C). Schauinsland (1900) and Howes and Swinnerton (1901) studied aspects of cranial development in Sphenodon punctatum, finding a pattern quite simliar to turtles, especially the early formation of jaws and most of the dermatocranium and the late appearance of the parietal and parasphenoid. Squamates have been covered more extensively, which includes lizards (Rieppel 1987, 1992), chamaeleons (Fineman 1941; Rieppel 1993c), amphisbaenians (Montero et al. 1999), and snakes (Rieppel and Zaher 2001). Again, these taxa develop jaw and circumorbital elements early and neurocranium late, exemplified by Lacerta vivipara in Fig. 3D. Crocodiles have been studied by Parker (1883), deBeer (1937), and Rieppel (1993a), who found that at first the jaws form, followed by the circumorbitals, then the palatal elements, and finally all other skull bones including the braincase (Fig. 3E). In birds, Erdmann (1939) has worked on cranial ossifications of Gallus gallus, where he found the nasal, squamosal, maxilla, jugal, dentary, and premaxilla to form rather early, whereas the braincase and some skull roofing bones make a later appearance.

Mammals (Fig. 3F) Cranial ossification of mammals has most recently been studied by Smith (1997), who analyzed various sequences of marsupials and placentals, calculating consensus sequences for each group. Smith found a broad resemblance between the studied sequences, with both sharing an early formation of jaw bones and a late formation of skull roofing elements. Marsupials and placentals differ particularly in the timing of palate and braincase ossifications.

PHYLOGENETIC IMPLICATIONS OF SEQUENCE DATA The cladistic analysis of 120 event pairs derived from the studied 16 ossification events gave some rather perplexing results. Within tetrapods, the extinct branchiosaurid Apateon was grouped as the basalmost taxon, whereas the three salamanders form a clade just above this node. This is consistent with Laurin and Reisz’s (1997) hypothesis, who suggested that temnospondyls may fall outside crown tetrapods. It is at odds with other recent hypotheses (Ruta et al. 2003; Schoch and Milner 2004), and particularly contradicts Schoch and Carroll’s (2003) suggestion that cranial ossification sequences shared between salamanders and branchiosaurids may be apomorphic. However, mapping active movers onto tetrapod phylogeny gave different results reported below.

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More importantly, in the present cladistic analysis both Ascaphus and Gegeneophis were not found to nest with salamanders to form a monophyletic Lissamphibia, but instead within the amniote clade. For that assemblage, the strict consensus of the three most parsimonious topologies reads as follows: Gegeneophis and Lacerta form a basal ‘‘clade,’’ followed by Ascaphus and Chelydra, and finally a ‘‘clade’’ formed by marsupials, placentals, Alligator, and Gallus. This result is clearly at odds with all major phylogenetic studies of the last decades, and there is little doubt that the signalFif anyFemerging from this analysis does not have an immediate bearing on phylogeny. Quite obvious is the delay in the ossification of jaw elements shared by Ascaphus and Chelydra, a feature well known to be convergent, involving very different adaptational contexts: in tadpoles teeth do not form before metamorphosis, and turtles fail to form teeth altogether. A representative of another edentulous clade, Gallus, shows only a postdisplacement of the premaxilla, while the maxilla and dentary have not moved significantly; however, this has no impact on the cladistic analysis of event pairs. The most significant event sequence change shared between Gegeneophis and reptiles is the extreme postdisplacement of the parasphenoid, whereas the particular feature shared between Gegeneophis and Lacerta is the predisplacement of the nasal. Finally, the sequences of Gallus and Alligator share a lack of the supratemporal (recorded as a ‘‘postdisplacement’’ in the analysis), whereas the nesting of crocodiles and birds with mammals is largely obtained by the early formation of the jugal in both groups. The latter is certainly a derived feature, as indicated by branchiosaurids and other extinct early tetrapods (Schoch 2003). In a variant of this analysis, Amia was omitted and Apateon defined as an outgroup. In the heuristic search mode, this gave three trees (247 steps; CI: 0.74; RI: 0.538; RC: 0.379), with a quite similar result to that of the more inclusive variant just described. The only difference is that Gallus falls outside the group that includes Alligator and the two mammal sequences, nested below Ascaphus and Chelydra. In the branchand-bound search mode, the tree collapsed entirely, with only Lacerta plus Gegeneophis and Chelydra plus Ascaphus retained as groupsFapparently, the divergence of these sequences from those of all other tetrapods is profound. In sum, this cladistic analysis of event sequence data gives highly unorthodox results that must not be ‘‘translated’’ into a phylogeny of development without careful consideration. Rather than reflecting true relationships, these results highlight some major evolutionary changes in cranial ossification that are likely to have happened repeatedly, and quite obviously for entirely different adaptational reasons. By this, the obtained pattern may be a means to detect homoplasy in the evolution of early embryonic development. A further problem are all those elements for which there is no homologue in the

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out-group, such as the frontal, nasal, squamosal, and jugal; major shifts in their developmental timing can only be identified when compared with a more proximate out-group, such as the branchiosaurids, which also had these bones. Likewise, bones that were lost in evolution (supratemporal, jugal, postorbital) may come out as postdisplacement, event though a true heterochronic postdisplacement need not have been involved in their loss. At this stage, it is impossible to conclude from the patterns emerging from cladistic analysis to the underlying evolutionary processes.

MAJOR EVOLUTIONARY SHIFTS IN CRANIAL DEVELOPMENT The identification of active movers in cranial ossification sequences revealed various interesting patterns. The most general ones involve shifts that probably occurred at the fish– tetrapod transition or, equally likely, somewhere within the lineage of fish-like sarcopterygians. The relationships between the crown groups focused at in this study are generally well understood. The critical phylogenetic framework is formed by (i) the basal osteichthyan dichotomy between actinopterygians and sarcopterygians, (ii) the monophyly of the tetrapods, and (iii) the monophyly of amniotes. All of these major nodes are supported by a broad consensus (Lauder and Liem 1983; Benton 1988; Janvier 1996; Schultze and Cumbaa 2001). As there are relatively few ossification sequences available across clades, there is no necessity to refer to in-group relationships of sarcopterygians.

Fish--tetrapod transition If viewed from the crown-group perspective, the main innovation in the tetrapod skull is the de novo formation of skull roof bones (a single pair of nasals, frontals, jugals, prefrontals, and postfrontals) and the loss of others (extrascapluars, branchiostegals, opercular elements). Today, there are numerous finds of fossil sarcopterygians to bridge this crown-group gap (Schultze and Arsenault 1985; Ahlberg 1991; Vorobyeva and Schultze 1991; Janvier 1996; Clack 2000; Schultze and Cumbaa 2001; Zhu and Schultze 2001; Daeschler et al. 2006). However, these finds have revealed no data on ossification sequences and thus are of no help to the present problem. At best, they provide indirect evidence for the hypothesis that the cranial morphology of basal crown-actinopterygians is plesiomorphic and that there is a continuity in the composition of skull bones from primitive osteichthyans through lower tetrapods. The numerous symplesiomorphies shared by stem-actinopterygians and stem-sarcopterygians support this (Nielsen 1942, 1949; Moy-Thomas and Miles 1971; Gardiner 1984; Janvier 1996). Apart from the rather obvious morphological changes that make the skulls of extant tetrapods and osteichthyan fishes look so different, it is surprising to find that the developmen-

tal trajectory has conserved many features in the relative timing of bone forming events. This does not only involve the early formation of tooth-bearing elements (which, from a functional aspect, seems easily explained in these early actively feeding aquatic larvae) but also concerns the timing of appearance of (i) the parasphenoid, (ii) the ectopterygoid (when present), (iii) the parietal ( 5 frontal of piscine Osteichthyes), and (iv) the exoccipital and orbitosphenoid in the braincase. All these events have, according to the event-pair cracking analyses, not moved actively in the evolution of the trajectory across the fish–tetrapod transition. This agrees with the detailed morphological similarity between the bone primordia of amiids, branchiosaurids, and urodeles as described before.

Early tetrapod evolution The position of the extinct Branchiosauridae is equivocal with respect to crown-tetrapods; whereas Milner (1988, 1993), Trueb and Cloutier (1991), and Ruta et al. (2003) consider the Temnospondyli as forming part of the lissamphibian stem group, Laurin and Reisz (1997) suggested that temnospondyls might fall entirely outside crown-tetrapods. Mapping the major shifts in cranial ossification reveals that branchiosaurids share mostly plesiomorphic traits with salamanders, such as the early formation of jaws and palate bones, as well as the clustering of parietal, frontal, and squamosal in early development or the circumorbital elements in late development. Yet, there are other, shared patterns of branchiosaurids and salamanders, especially the morphogenesis of palate and medial skull roof elements that may well be apomorphic when compared with other tetrapods and piscine outgroups (see Schoch 2002 for details of these spatial patterns). One unique feature of branchiosaurids and the two most primitive salamanders studied here, Ranodon and Salamandrella, is the delayed ossification of braincase elements, which appear to have been moved into later phases with respect to Amia and all other studied tetrapods. If this indicates a close relationship between salamanders and branchiosaurids, it was reversed in more advanced urodeles such as Ambystoma. In the fish–tetrapod transition, the most conspicuous movement among the studied events is the postdisplacement of the postorbital, which, in branchiosaurids, formed in a later phase than it does in Amia. The squamosal and frontal, on the other hand, appear to have moved into an earlier phase, but this is a result of coding these elements in Amia, where they are absent and consequently ranked among the latest events. Thus, the squamosal and frontal may not have moved at all.

Lissamphibians Among lissamphibians, extant salamanders have conserved a remarkably ancestral developmental trajectory. Compared with Amia, the three studied salamander sequences differ only in minor points. The most conspicuous shift found here is that

Schoch of the maxilla, which is postponed in all salamanders, Ascaphus, and GegeneophisFa potential synapomorphy of all examined lissamphibians. This recalls the situation in branchiosaurids, which develop the maxilla early, but at least share a similar morphology with salamanders in which the element is short and does not contact the cheek elements (Schoch 2002). Some of the studied salamanders share the postdisplacement of the premaxilla (here: with Ascaphus) and the predisplacement of the palatine. Ascaphus is unique in having predisplaced the parietal and exoccipital by three event steps each, and this pattern is common, probably apomorphic for anurans (Yeh 2003). Among lissamphibians, Gegeneophis is unique in the postdisplacement of the parasphenoid, but as reported above this is also recorded in all studied reptiles. There are no shared patterns exclusive to frogs and caecilians or salamanders and caecilians, but some salamanders share the postdisplacement of the premaxilla with frogs, which might be a derived condition.

Amniote origin All analyzed amniote sequences have one active mover in common that lies markedly above the threshold: the predisplacement of the jugal. This reveals a further interesting pattern, when compared with the results in branchiosaurids and lissamphibians. Whereas in branchiosaurids the postorbital is moved into late phases to form within the same time window as the jugal (and other circumorbitals), amniotes show a predisplacement of the jugal into the same phase wherein the postorbital (and other circumorbitals) form. It is unclear which pattern is primitive for tetrapods, as only these two larger clades survive today, and the absence of the jugal (and prefrontal) in Amia provides no out-group data for this question. In lissamphibians, only primitive salamanders retain some circumorbital bones, and these form very late in development, exactly as in branchiosaurids (Lebedkina 1979; Schoch 2002). These results may be interpreted in two ways, depending on the underlying phylogeny (see Schoch and Milner 2004 for a recent summary of lissamphibian theories). (1) In the Temnospondyl hypothesis of lissamphibian origins, branchiosaurids nest as close relatives within the lissamphibian stem; this would favor the ‘‘circumorbitals-late’’ pattern to be derived for that clade. (2) In the Lepospondyl hypothesis, branchiosaurids fall outside the tetrapod crown, thus indicating the primitive condition for tetrapods, and this would instead indicate the branchiosaurid pattern to be plesiomorphic.

Reptiles and birds Chelydra, Lacerta, Alligator, and Gallus represent the largest extant clade of tetrapods: the Reptilia. The ossification sequence shows a range of active movers, some of them having shifted by large numbers of steps (see Appendix A). In this respect, reptiles have the most derived cranial ossification se-

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quences of all studied tetrapods. The most outstanding active mover of reptiles is the postdisplacement of the parasphenoid, which is only paralleled in the caecilian Gegeneophis. The nasal is markedly predisplaced in Lacerta and Gallus, but in Alligator and Chelydra this predisplacement is much smaller in amount and falls well below the threshold. Finally, an obvious feature that has an impact on the ossification sequence is the failure of the supratemporal to form, a reduction character that is probably homoplastic in the phylogeny of reptiles and other tetrapods.

Mammals In extant mammals, the cranial sequence is much less divergent from that of Amia and lower tetrapods than that of reptiles. The jaw, braincase, and skull roofing elements are mostly unaffected by sequence heterochronies. Marsupials and placentals share the postdisplacement of the vomer into a later phase in cranial development, whereas a significant postdisplacement of the palatine is only recorded in marsupials. On the other hand, placentals show a postdisplacing shift of the exoccipital slightly above the threshold, which is also present in placentals but falls below the threshold.

SHARED ACTIVE MOVERS---CONSTRAINTS IN CRANIAL DEVELOPMENT? The preceding analyses suggest that in the majority of the vertebrates studied here, small groups of bones apparently shifted together as active movers along the ontogenetic trajectory. The following consistencies among such active movers have been identified. 1. Dermal jaw bones (premaxilla, maxilla, dentary): Whether tooth bearing or not, these bones mostly form at about the same time across the studied sample of vertebrates. Even in the single outstanding example of salamanders (where the maxilla is shifted into very late stages close to metamorphosis), the premaxilla has also moved, as event-pair cracking revealed. In actinopterygians, branchiosaurids, and salamanders, these bones are attached to teeth already in the earliest stages, whereas in reptiles, teeth form somewhat later, but usually well within the embryonic period (Rieppel 1992). That jaws form early in vertebrate development was hinted at by Erdmann (1939) and Yeh (2003), but never has this been shown in such a broad range of taxa. 2. Marginal palate bones (ectopterygoid, palatine, vomer): In actinopterygians, branchiosaurids, and salamanders, these bones (when present) bear teeth already in early stages. This type of dentition differs from that of the jaw bones in covering larger areas and the single teeth are mostly smaller. In extant reptiles, this type of palatal dentition is largely reduced and forms long after the first appearance of the bony primordia. The palatine and vomer probably shifted

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in concert from an early phase of cranial development in Amia, branchiosaurids, lissamphibians, and most reptiles to a later phase in mammals. 3. Circumorbital bones (prefrontal, postfrontal, postorbital, jugal): Dermal bones surrounding the eye form at about the same time in Amia and Polypterus, but their homology with the circumorbital elements of tetrapods is mostly unclear. In tetrapods, circumorbital bones form(ed) at about the same relative time in branchiosaurids and primitive salamanders, and they do so in all extant reptiles analyzed. In mammals, only the jugal is retained, which was predisplaced by a similar number of steps as compared with reptiles, and in the latter it forms within the same time window as other circumorbital elements. These data suggest that in tetrapod evolution, the eye-surrounding bones have been moved in concert in the evolution of cranial development. 4. Braincase ossifications: The exoccipital, sphenethmoid (orbitosphenoid), and prootic are the most widespread braincase ossifications in both actinopterygians and tetrapods, and they form generally long after most of the dermatocranium has started to ossify (actinopterygians, branchiosaurids, salamanders). Among reptiles, all extant taxa studied form the neurocranial bones in the latest phase of cranial development. The only exception are anuran tadpoles; in these braincase elements form much earlier and at least the exoccipital and prootic appear to have been predisplaced into the earliest phase of skull formation. 5. Skull roof: Less apparent, but still consistent in timing, the three most important and evolutionary conservative bones in the skull roofFthe parietal, frontal, and squamosalFform within the same developmental phase in many tetrapods. This is suggested by simple comparison of sequences, as well as event-pair cracking, indicating the consistent relative predisplacement of the frontal and squamosal of tetrapods relative to Amia, where these elements were ranked last in the sequence. This ‘‘predisplacement’’ consistently ‘‘shifts’’ the bones into the phase when the parietal ossifies. The coherent formation of sets of bonesFjaw, palate, roof, circumorbital, and braincaseFis a consistent pattern detected both by simple comparison of sequences and more subtle analyses such as event-pair cracking. The major question arising here is whether these sets of bones form true ‘‘modules’’ as defined in Schlosser and Wagner (2004). Such modules could either be caused by shared mechanisms in development or they might form functionally integrated units.

on ossification sequences have been reported by Mabee and Trendler (1996), Adriaens and Verraes (1998), and Wagemans and Vandervalle (2001) in extant actinopterygians. The shared moving of dentigerous jaw elements may therefore not be surprising in these clades. Consistent with this is the early ossification of jaws, palatal elements, and the early onset of tooth formation in Amia and Polypterus, branchiosaurids, and all those salamanders having aquatic larvae. In these, the parasphenoid forms relatively early as well, which probably protects the ventral side of the brain against pressures generated during suction feeding and prey capture. Rather unexpected, however, is the evolutionary conservation of early jaw formation in reptiles and mammals, indicating that there may be additional constraints not confined to immediate functional requirements.

Developmental constraints The coherent ossification of jaw elements, whether occurring early in dentigerous or later in edentulous tetrapods, may exemplify a shared developmental cascade that controls early skull formation. Hall (1999a) reported the dependence of jaw bones from the prior formation of cartilages and their role in epithelial–mesenchymous interactions (EMIs). As the cartilages of the first arch form before any other primordial skull structure, the early induction of jaw bones may not be surprising. Indeed, Cassin and Capuron (1977) found these cartilages to induce jaw and palate bones in the salamander Pleurodeles. This does not mean that there must be a causal relation between skull bones or, more realistically, between tissues inducing different sets of skull bones. Rather, the finding that sets of cranial bones may shift rather independently fore and back the developmental trajectory contradicts such a simplistic view. Instead, the most general pattern may be that different sets of bones may be induced by different EMIs, whereas bones from the same developmentally linked set of bones may be induced by similar or identical signaling cascades. In our current example of tetrapod cranial ossification, this general hypothesis is consistent with three different observations: (1) the jaw and palate elements are induced by first arch cartilages and trabecles (Cassin and Capuron 1977), (2) the roofing elements (parietal, frontal, squamosal) are induced by EMIs involving the midbrain and hindbrain (Hall 1999b), and (3) the braincase elements are influenced by a signaling cascade that involves a particular gene family, Otx (FrancisWest et al. 1998). These three examples would also fulfill some of the criteria for a developmental module as defined by various authors in Schlosser and Wagner (2004).

Functional constraints The results obtained provide some interesting evolutionary patterns correlating with changes in feeding, such as evolutionary tooth loss in birds and turtles and tooth and jaw bone postdisplacement in anurans. Similar functional constraints

Modules Once identified, modules in development and evolution could greatly deepen our understanding of the evolution of skull architecture. For example, the evolutionary postdisplacement

Schoch of the formation of circumorbitals in salamanders (and other lissamphibians) probably resulted in the reduction or absence of some elements (jugal, postfrontal, postorbital) and thus established an open cheek region in which the jaw-closing muscles attach in a novel fashion (Schoch 2002). It is to be noted that this pattern does not imply that the bones were initially lost for purely ‘‘developmental’’ reasons. To be consistent with evolutionary theory, it will always need a functional-adaptive explanation on top of it. Conversely, in amniotes, the retention of most dermal bones inherited from early tetrapods is remarkable, whereas their adult morphology differs boldly from early tetrapods. This is most obvious in the cheek region, which is fenestrated in all extant lepidosaurs and archosaurs (diapsid condition) as well as mammals (synapsid condition). The spatial patterns of ossification in these bones depart markedly from their homologues in actinopterygians, branchiosaurids, and salamanders, which is already established in the initial primordia. Thus, although the circumorbitals have obviously been retained as a developmentally linked set of bonesFperhaps a developmentally integrated functional module involving the jaw-closing musculatureFthe context in which they form differs from that in early tetrapods. It remains unclear whether this is a result of the shift of circumorbitals into a much earlier phase of cranial development, but this is at least conceivable. Unlike the completely open postorbital skulls of extant amphibians, the diapsid skull architecture involves well-defined temporal bars that serve as an attachment site for jaw-closing musculature quite different from that of salamanders. This example highlights the difficulty not only in identifying a module sensu Schlosser and Wagner (2004) but also in deciding whether it involves functional or developmental constraints, or both. Paleontology and descriptive embryology may provide intriguing and stimulating raw data here, but without precise knowledge of the underlying developmental mechanisms there will not be any substantial progress in this field. Acknowledgments I am grateful to Sergey Smirnov and the late Natalya Lebedkina for stimulating discussions and their hospitality. Andrew Milner and Ju¨rgen Boy have encouraged this and related projects in many ways. Hans-Peter Schultze, Gloria Arratia, Wolfgang Maier, Hendrik Mu¨ller, Lennart Olsson, Wolf-Ernst Reif, and Florian Witzmann have been helpful in discussions and by providing literature. Peter Bartsch and Gloria Arratia kindly provided material of Amia calva. The two reviewers, Olaf Bininda-Emonds and Hans Larson, were extremely helpful in making me rethink numerous points, and this manuscript has benefited from further comments by Mike Coates. The Deutsche Forschungsgemeinschaft supported a related project on metamorphosis in Palaeozoic amphibians (DFG-grant SCHO-02, 1/1).

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APPENDIX A

Table A1. Cranial ossification sequences analyzed

Amia Apateon Salamandrella Ranodon Ambystoma Ascaphus Gegeneophis Chelydra Lacerta Alligator Gallus Marsupialia Mus

pm A

m B

d C

ps D

v E

pl F

p G

st H

po I

eo J

se K

f L

n M

sq N

pf O

ju P

1 1 2 2 2 5 1 3 1 2 5 1 1

2 1 6 6 6 8 2 3 1 1 2 1 1

3 1 1 1 1 6 1 3 1 1 4 1 1

4 3 3 2 3 3 3 5 6 10 10 6 6

5 2 1 2 2 4 1 3 1 5 8 4 3

6 2 1 2 2 11 2 3 1 5 3 1 3

7 4 4 2 4 2 2 2 2 7 7 2 2

8 5 9 8 9 11 4 6 2 11 11 6 6

9 8 9 8 9 11 4 1 3 3 11 6 6

10 10 5 4 5 1 2 4 4 8 6 2 4

11 11 8 7 7 9 2 5 5 9 9 6 6

12 4 4 2 4 2 2 2 2 3 5 2 2

12 6 6 5 8 10 2 6 2 6 1 5 5

12 4 4 3 4 7 3 2 2 4 1 3 2

12 7 7 7 9 11 4 3 2 3 5 6 6

12 9 9 8 9 11 4 3 2 3 3 3 2

See text for sources. pm, premaxilla; m, maxilla; d, dentary; ps, parasphenoid; v, vomer; pl, palatine; p, parietal; st, supratemporal; po, postorbital; eo, exoccipital; f, frontal; n, nasal; sq, squamosal; pf, prefrontal; ju, jugal.

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EVOLUTION & DEVELOPMENT

Vol. 8, No. 6, November^December 2006

Table A2. Total relative changes (TRCs) of events relative to plesiomorphic sequence (Amia)

Apateon Salamandrella Ranodon Ambystoma Ascaphus Gegeneophis Chelydra Lacerta Alligator Gallus Marsupialia Mus

pm A

m B

1 3 6 3 5 2 10 4 2 8 2 2

0 9 9 8 7 9 8 2 0 1 0 0

d C 2 0 2 2 0 1 6 0 2 3 2 2

ps D

v E

2 1 3 1 0 8 10 12 11 10 F F

0 3 1 2 0 4 3 3 5 7 7 5

pl F 2 5 1 4 F 4 2 5 3 1 5 3

p G 2 1 3 1 3 2 3 5 5 4 2 1

st H

po I

2 F F F F F 8 3 8 8 F F

4 F F F F F 8 4 2 6 F F

eo J 5 1 1 1 6 0 2 4 3 0 2 3

se K 5 4 4 2 2 2 2 4 3 2 F F

f L

n M

4 6 9 3 9 6 13 2 10 4 7 5

sq N

4 0 3 1 1 7 4 6 1 14 1 2

8 4 11 5 2 5 13 6 5 14 3 3

pf O

ju P

1 3 F F F F 8 6 10 7 F F

2 F F F F F 8 6 10 10 3 5

Movers falling above the threshold ( 5 mean) are in bold.

Table A3. Corrected total relative changes (TRCs) of events relative to plesiomorphic sequence (Amia), with only the recalculated active movers listed

Apateon Salamandrella Ranodon Ambystoma Ascaphus Gegeneophis Chelydra Lacerta Alligator Gallus Marsupialia Mus

pm A

m B

5 2 2

6 7 6 4 6

8

5

d C

ps D

v E

pl F

p G

st H

po I

eo J

se K

1

2

2 2 2

4

f L

n M 2 4 5

sq N

H!

2 3 5 8 8 8 7

See text and Jeffery et al. (2002) for procedure.

5

3

1 5 5

4 3

4

4 4 11

4

ju P

2 2 5 4

4

3 11 4

10

10

8 4 3

pf O

4 7

4 7 8 2 4