Terrestrial-Style Feeding in a Very Early Aquatic Tetrapod Is Supported by Evidence from Experimental Analysis of Suture Morphology

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Terrestrial-Style Feeding in a Very Early Aquatic Tetrapod Is Supported by Evidence from Experimental Analysis of Suture Morphology Terrestrial-style feeding in a very early aquatic tetrapod is supported by evidence from experimental analysis of suture morphology Molly J. Markey*† and Charles R. Marshall*‡ *Department of Earth and Planetary Sciences and ‡Department of Organismic and Evolutionary Biology and Museum of Comparative Zoology, Harvard University, 26 Oxford Street, Cambridge, MA 02138 Communicated by Andrew H. Knoll, Harvard University, Cambridge, MA, March 6, 2007 (received for review September 25, 2006) There is no consensus on when in the fish-tetrapod transition stega, captured prey using suction or biting (15). Specifically, the suction feeding, the primary method of prey capture in the aquatic fishes Eusthenopteron, Panderichthys, and Tiktaalik, and the early realm, evolved into the direct biting on prey typical of terrestrial tetrapod Ventastega, all possess large coronoid fangs, whereas animals. Here, we show that differences in the morphology of se- these teeth are absent in the more derived Acanthostega.In lected cranial sutures between species that span the fish–tetrapod addition, Eusthenopteron and Panderichthys both exhibit an transition (the Devonian osteolepiform fish Eusthenopteron, the ossified operculum, whereas the bony gill cover is lost in aquatic Devonian tetrapod Acanthostega, and the Permian terres- Tiktaalik, Ventastega, and Acanthostega. Finally, the glenoid fossa trial tetrapod Phonerpeton) can be used to infer when terrestrial of the articular faces posteriordorsally in the fish taxa discussed feeding first appeared. Our approach consists of defining a sutural here (Eusthenopteron, Panderichthys, and Tiktaalik) whereas, in morphospace, assigning functional fields to that morphospace the tetrapods Ventastega and Acanthostega, this fossa points based on our previous measurements of suture function made dorsally, indicating that the lower jaw changed the nature of its during feeding in the living fish Polypterus, inferring the functions articulation to the skull across the fish–tetrapod transition. (See of the fossil sutures based on where they fall in the morphospace, ref. 15 for a discussion of these changes in all taxa save Tiktaalik; and then using the correlation between feeding mode and the for Tiktaalik, see refs. 5 and 6.) These changes, along with the patterns of inferred suture function across the skull roof in taxa reduction of the gill chamber, are hypothesized to indicate a where feeding mode is unambiguous to infer the feeding mode reduced reliance on suction feeding in early tetrapods compared practiced by Acanthostega. Using this procedure, we find that the with osteolepiform fishes (15). suture morphologies of Acanthostega are inconsistent with the However, it is unclear how definitive the morphological hypothesis that it captured prey primarily by means of suction, changes described above are in helping us understand when in which suggests that it may have bitten directly on prey at or near the fish–tetrapod transition taxa were no longer dependent on the water’s edge. Thus, our data strongly support the hypothesis suction feeding. For example, extant fish that capture prey by that the terrestrial mode of feeding first emerged in aquatic taxa. means of suction exhibit an incredible variety of tooth arrange- ments and jaw shapes (see ref. 16). In addition, the loss of the Acanthostega ͉ fish–tetrapod transition ͉ suction feeding ͉ operculum observed in Acanthostega is reminiscent of the con- Eusthenopteron dition seen in the extant lungfish Neoceratodus (17), which nonetheless employs suction to capture prey (18). Therefore, he origin of tetrapods and their invasion of terrestrial whereas the changes noted above certainly indicate major Tenvironments are major events in vertebrate evolution. changes in the details of the feeding mechanisms between taxa Comparing early tetrapod taxa such as the Devonian tetrapods such as Eusthenopteron and Acanthostega, and may indicate a Acanthostega (1) and Ventastega (2) with the closely related reduced ability of Acanthostega to develop a pressure drop within osteolepiform fishes Eusthenopteron (3), Panderichthys (4), and the buccal cavity compared with Eusthenopteron, these morpho- Tiktaalik (5, 6) shows that the fish–tetrapod transition was logical changes do not enable us to determine how reliant defined by a suite of anatomical changes linked to changes in Acanthostega might have been on suction feeding, per se. locomotion, respiration, reproduction, the sensory apparatus, Thus, motivated by these uncertainties, we here provide an and feeding (7–9). approach for evaluating whether transitional tetrapods, specif- Feeding in water presents organisms with different challenges ically Acanthostega, captured prey primarily using suction, or by than those experienced when feeding on land because water is biting directly on prey items. This work follows the suggestion 900 times as dense, and 80 times as viscous, as air (10). Because that the shift from suction to biting prey capture should be of these differences, suction feeding, the most widespread reflected in the morphology of the cranial sutures of taxa that method of prey capture used by aquatic vertebrates, is impossible span the fish–tetrapod transition and the tetrapod invasion of in air (10), so animals that capture prey in terrestrial settings use land (13, 14, 19). In vivo different techniques, such as overtaking prey items with the jaws experiments demonstrate that cranial sutures are important indicators of skull function (20–23). However, no and biting on them (11). Therefore, we assume that fish pre- ceding the transition, such as Eusthenopteron, captured prey using suction, whereas later, fully terrestrial tetrapods captured Author contributions: M.J.M. and C.R.M. designed research; M.J.M. performed research; prey items by biting on them (see also ref. 12). Transitional forms M.J.M. analyzed data; and M.J.M. and C.R.M. wrote the paper. such as Acanthostega are thought to have captured prey in the The authors declare no conflict of interest. water (12–14), but the exact type of prey capture (i.e., suction Abbreviations: IF, interfrontal suture; IP, interparietal suture; IPP, interpostparietal suture; versus biting) used by Acanthostega and other early tetrapods is FP, frontoparietal suture; NF, nasofrontal suture; SMNH, Swedish Museum of Natural difficult to determine. History; MCZ, Harvard Museum of Comparative Zoology; CT, computed tomography. Stepwise morphological changes in the lower jaw, dentition, †To whom correspondence should be addressed. E-mail: [email protected]. degree of ossification of the operculum, and relative size of the This article contains supporting information online at www.pnas.org/cgi/content/full/ gill chamber in taxa that span the fish–tetrapod transition 0701706104/DC1. provide clues as to whether early tetrapods, including Acantho- © 2007 by The National Academy of Sciences of the USA 7134–7138 ͉ PNAS ͉ April 24, 2007 ͉ vol. 104 ͉ no. 17 www.pnas.org͞cgi͞doi͞10.1073͞pnas.0701706104 Downloaded by guest on September 29, 2021 previous studies have documented quantitative changes in su- IF tural morphology across the fish–tetrapod transition or linked specific sutural morphologies to specific feeding modes (e.g., Fr Fr suction feeding). Here, we assess where in the transition feeding changes occurred by (i) quantifying the three-dimensional mor- phology of selected sutures in taxa that span the fish–tetrapod Fr transition and the tetrapod invasion of land; (ii) inferring the IP function of these sutures using correlations between suture morphology and deformation during feeding in the extant fish Pa Pa Polypterus (23); and (iii) associating specific fossil suture mor- Pa phologies with aquatic (suction) feeding or terrestrial feeding (biting on prey). IP Here, the fish–tetrapod transition is represented by the os- teolepiform fish Eusthenopteron (3) and the Devonian tetrapod Acanthostega, the best-known early tetrapod (14). Although Pa Pa Panderichthys and Elpistostege are more closely related to tetra- Eusthenopteron pods than Eusthenopteron is (8), we did not have access to any panderichthyid specimens so those taxa were not included. We Fig. 1. Cross-sections through the IF and IP sutures of the osteolepiform fish Phonerpeton Eusthenopteron and their approximate positions through the skull roof (see selected the Permian terrestrial tetrapod (Dissoro- Introduction for discussion of the terminology used for these bones). The phoidea) (24) to represent the invasion of terrestrial environ- cross-section drawings are modified after the original drawings in the litera- ments by tetrapods because of its terrestrial lifestyle (24), the fact ture (29). The color of the sutural label indicates the location of the slice that its small skull size falls within the range exhibited by through the skull. The dorsal reconstruction is modified from the literature Eusthenopteron and Acanthostega (24), and the excellent three- (30) and was largely based on SMNH P222, the specimen used to generate the dimensional preservation exhibited by several specimens in the grinding series and cross-sectional drawings. [Scale bars: 1 mm (sutures) and 1 Museum of Comparative Zoology, Harvard University. cm (skull).] Fr, frontal; Pa, parietal. In this study, we are not concerned with the exact homologies between the skull roof bones of these taxa. Instead, we wish to compare bones that are similar in size, proportion (compared metrics used to quantify suture morphology in Eusthenopteron, with the rest of the skull),
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