rspb.royalsocietypublishing.org
Is there an exemplar taxon for modelling the evolution of early tetrapod hearing? J. S. Anderson1, J. D. Pardo1, H. C. Maddin2, M. Szostakiwskyj3 and A. Tinius3
Comment Cite this article: Anderson JS, Pardo JD, Maddin HC, Szostakiwskyj M, Tinius A. 2016 Is there an exemplar taxon for modelling the evolution of early tetrapod hearing? Proc. R. Soc. B 283: 20160027. http://dx.doi.org/10.1098/rspb.2016.0027
Received: 5 January 2016 Accepted: 14 March 2016
Author for correspondence: J. S. Anderson e-mail: [email protected]
1 Department of Comparative Biology and Experimental Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada T2N 4N1 2 Department of Earth Sciences, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario, Canada K1S 5B6 3 Department of Biological Sciences, University of Calgary, 2300 University Drive NW, Calgary, Alberta, Canada T2N 1N4
Christensen et al. recently published a study of hearing in neotenic and experimentally metamorphosed axolotls (Ambystoma mexicanum) and a larval and adult tiger salamander (A. tigrinum), which contributes greatly to our understanding of salamander sound perception in water and air [1]. They demonstrate that premetamorphic, atympanic aquatic salamanders are capable of perceiving high frequency airborne sounds similar to terrestrial adults, demonstrating an interesting capacity for an atympanic ear to function for sound perception in a variety of media. This important research, in combination with other recent studies on the sound perception capabilities of lungfish [2], is helping to better clarify issues related to the water-to-land transition. However, the implication of their experimental design demands a consideration of the evolutionary history of their selected exemplar taxa so these valuable data can be interpreted in a broader context. Our criticisms focus on two major points: the use of salamanders as a proxy for hearing ability intermediate between aquatic and terrestrial vertebrates, and the use of microsaurs as exemplars of the early tetrapod condition. The currently accepted hypothesis for the origin of a tympanic ear is as a derivation from the spiracle of sarcopterygian fish [3]. In ‘fish’ the spiracle is associated with gill breathing: water passes through the spiracular notch in the rear of the skull, past the braincase and the bracing hyomandibula, to the oropharynx and gill arches [4]. With the loss of gills, the persisting spiracular lumen is co-opted into a middle ear chamber, and the cranial support role of the hyomandibula (now termed stapes) is eliminated, leaving this bone to extend freely into the middle ear chamber (figure 1). In derived tetrapods, the spiracular opening is expanded and covered by a membrane (the tympanum) that collects sound. Vibrations are transmitted to the inner ear via the stapes, which becomes more delicate and better able to propagate fine vibrations [7–10].
1. Salamanders are not evolutionary intermediates
The accompanying reply can be viewed at http://dx.doi.org/10.1098/rspb.2016.0716.
Christensen et al. state ([1], p. 2), ‘Equally important, [the urodele auditory system] can be regarded as a potential model for the intermediate evolutionary developmental stage’ between lungfish and frogs. However, there is strong evidence that salamanders have secondarily lost a tympanic ear, which dramatically changes the interpretation of the results of this study. Most palaeontologists agree that modern amphibians (Lissamphibia) are a monophyletic group with origins among a group of temnospondyls, the Amphibamidae [5,11 –17] (but see [18] for an alternative view). Amphibamids are considered to have had a tympanic hearing system identical to that of frogs [9,10,19] (figure 1). This hearing system was probably present in the first temnospondyls [20], dating well into the Carboniferous. Interestingly, a middle ear similar to salamanders is also seen in some secondarily atympanic frogs [21]. This secondary loss of tympanic hearing is also evident physiologically. All lissamphibians possess two epithelia: one associated with low-frequency
& 2016 The Author(s) Published by the Royal Society. All rights reserved.
(a)
2
tympanum hyomandibula/stapes operculum ossicle
Carrolla
amniote total group
Protorothyris
(b)
rspb.royalsocietypublishing.org
temporal embayment present
spiracle
Amniota Microsauria
temporal embayment absent
(c) Seymouria
amphibian total group
Tersomius
(g)
Dissorophoidea
( f)
Amphibamidae
Gastrotheca origin of amphibian TE
Batrachia
Ambystoma
(e)
Broiliellus
(h)
water–land transition
Dendrerpeton
(i)
( j)
Archeria
Kyrinion
(k)
fin to limb transition
(l)
Crassigyrinus
Pederpes
(m)
Ventastega
(n)
Eusthenopteron
Figure 1. Phylogenetic context of middle ear evolution in early tetrapods. Phylogeny modified from [5,6]. TE, tympanic ear. Illustrations not to scale.
environmental stimulations and one with high-frequency aerial sound. Salamanders show a phylogenetically correlated reduction in innervation of the epithelium associated with high frequency sound perception [22], indicating the presence of a tympanic hearing system in their evolutionary past. A similar trend is found in the atympanic caecilians
[23,24]. This point is critical because Christensen et al. tested sensitivity to sound vibrations at the auditory nerve, which directly reflects the innervation of the sensory epithelia detecting the stimulus. Because salamanders have remnants of the greater innervation of the fully tympanic ear, it is expected that they can perceive sound better than animals
Proc. R. Soc. B 283: 20160027
(d)
2. Microsaurs are not representative of early tetrapods
3. Conclusion and recommendations Experimental studies of modern taxa have the potential to inform our understanding of major transitions in evolutionary history otherwise preserved only in the fossil record, but the selection of exemplary taxa for such studies is nontrivial to their applicability. Researchers must consider the evolutionary histories of taxa to ensure that the model organisms are appropriate analogues so that conclusions can be drawn with confidence. The middle ear of Polypterus is more anatomically similar to that seen in stem tetrapods and lungfish near the tetrapodomorph divergence and could be an appropriate analogue to test in future studies of this question. Given the above, we assert that the conclusion that ‘early tetrapods also may have been able to detect aerial sound before the appearance of the tympanic middle ear’ ([1], p. 8) drawn from observations of salamanders and microsaurs is unfounded. Instead, the results of this study provide interesting insights into the strength of the conservation of an auditory apparatus adapted to terrestrial hearing in a group of aquatic salamanders. Authors’ contributions. All authors contributed equally. Competing interests. We have no competing interests. Funding. This study was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to J.S.A.
Acknowledgements. We thank Jennifer Clack and Eric Lombard for previous discussions on these subjects, which does not imply their agreement with our comment. This manuscript was further improved by comments from two anonymous reviewers, Dr Jakob ChristensenDalsgaard and the editorial staff.
References 1.
2.
3.
4.
5.
Christensen CB, Lauridsen H, Christensen-Dalsgaard J, Pedersen M, Madsen PT. 2015 Better than fish on land? Hearing across metamorphosis in salamanders. Proc. R. Soc. B 282, 20141943. (doi:10.1098/rspb.2014.1943) Christensen-Dalsgaard J, Brandt C, Wilson M, Wahlberg M, Madsen PT. 2010 Hearing in the African lungfish (Protopterus annectens): preadaptation to pressure hearing in tetrapods? Biol. Lett. 7, 139–141. (doi:10.1098/rsbl.2010.0636) Clack JA. 2015 Evolutionary biology: the origin of terrestrial hearing. Nature 519, 168 –169. (doi:10. 1038/519168a) Graham JB, Wegner NC, Miller LA, Jew CJ, Lai NC, Berquist RM, Frank LR, Long JA. 2014 Spiracular air breathing in polypterid fishes and its implications for aerial respiration in stem tetrapods. Nat. Commun. 5, 1 –6. (doi:10.1038/ncomms4022) Maddin HC, Jenkins Jr FA, Anderson JS. 2012 The braincase of Eocaecilia micropodia (Lissamphibia, Gymnophiona) and the origin of caecilians. PLoS ONE 7, e50743. (doi:10.1371/journal.pone.0050743)
6.
Clack JA, Ahlberg PE, Blom H, Finney SM. 2012 A new genus of Devonian tetrapod from North-East Greenland, with new information on the lower jaw of Ichthyostega. Palaeontology 55, 73 –86. (doi:10. 1111/j.1475-4983.2011.01117.x) 7. Clack J. 2002 Patterns and processes in the early evolution of the tetrapod ear. J. Neurobiol. 53, 251 –264. (doi:10.1002/neu.10129) 8. Bolt JR, Lombard RE. 1985 Evolution of the amphibian tympanic ear and the origin of frogs. Biol. J. Linn. Soc. 24, 83 –99. (doi:10.1111/j.10958312.1985.tb00162.x) 9. Lombard RE, Bolt JR. 1979 Evolution of the tetrapod ear: an analysis and reinterpretation. Biol. J. Linn. Soc. 11, 19–76. (doi:10.1111/j.1095-8312.1979.tb00027.x) 10. Lombard RE, Bolt JR. 1988 Evolution of the stapes in Paleozoic tetrapods: conservative and radical hypotheses. In The evolution of the amphibian auditory system (ed. B Fritzsch). New York, NY: John Wiley and Sons, Inc. 11. Ruta M, Coates MI. 2007 Dates, nodes and character conflict: addressing the lissamphibian origin
12.
13.
14.
15.
problem. J. Syst. Paleontol. 5, 69– 122. (doi:10. 1017/S1477201906002008) Trueb L, Cloutier R. 1991 A phylogenetic investigation of the inter- and intrarelationships of the Lissamphibia (Amphibia: Temnospondyli). In Origins of the higher groups of tetrapods: controversy and consensus (eds H-P Schultze, L Trueb), pp. 174–193. London, UK: Comstock Publishing Associates. Bolt JR. 1969 Lissamphibian origins: possible protolissamphibian from the Lower Permian of Oklahoma. Science 166, 888–891. (doi:10.1126/ science.166.3907.888) Bolt JR. 1991 Lissamphibian origins. In Origins of the higher groups of tetrapods: controversy and consensus (eds H-P Schultze, L Trueb), pp. 194–222. London, UK: Comstock Publishing Associates. Sigurdsen T, Bolt JR. 2009 The lissamphibian humerus and elbow joint, and the origins of modern amphibians. J. Morphol. 270, 1443–1453. (doi:10.1002/Jmor.10769)
3
Proc. R. Soc. B 283: 20160027
Christensen et al. [1] assert that microsaurs are morphological exemplars for the early tetrapod condition (a rationale for this was not provided) and that similarities of the middle ear can be used to associate the functional data derived from salamanders with the early evolution of frog-like hearing. This is problematic for two reasons. First, phylogenetically microsaurs are more closely related to the amniote crown group than any early tetrapod [5,11,24,25]. They are derived in both lacking a spiracular embayment and in possessing a short, robust stapes, unlike all taxa that span the water-toland transition up to, and including, frogs (figure 1). Rather than representing a transition between aquatic and terrestrial living, microsaurs are highly specialized terrestrial species adapted to burrowing. Second, whereas Christensen et al. are correct in recognizing superficial similarities between salamanders and microsaurs, including the lack of an otic notch and stapes with broad footplates and short columellae, microsaurs differ in several important anatomical details [26–28]. For example, microsaurs have the stapes completely filling the fenestra vestibularis, whereas salamanders also have an operculum [22]. All lissamphibians [24,29] and some temnospondyls [19] possess a posterior pressure relief pathway via the perilymphatic foramen, whereas microsaurs possess an ossified crista interfenestralis that prevents this posterior
perilymphatic flow, strongly suggesting they possess a more amniote-like anterior pattern [26,30].
rspb.royalsocietypublishing.org
without any evolutionary history of terrestrial hearing. The fact that secondarily aquatic salamanders, such as axolotl, do not differ in their ability to hear aerial sound from terrestrial salamanders reflects the conservation of a degree of terrestrial hearing capability. Even under the heterodox ‘lepospondyl hypothesis’ [18] this loss is recognized.
22.
23.
25.
26.
27.
28.
29.
30.
two new genera. PLoS ONE 10, e0127307. (doi: 10. 1371/journal.pone.0127307) Pardo JD, Szostakiwskyj M, Anderson JS. 2015 Cranial morphology of the brachystelechid ‘microsaur’ Quasicaecilia texana Carroll provides new insights into the diversity and evolution of braincase morphology in recumbirostran ‘microsaurs’. PLoS ONE 10, e0130359. (doi:10.1371/journal.pone. 0130359) Maddin HC, Olori JC, Anderson JS. 2011 A redescription of Carrolla craddocki (Lepospondyli: Brachystelechidae) based on high-resolution CT, and the impacts of miniaturization and fossoriality on morphology. J. Morphol. 272, 722–743. (doi:10. 1002/jmor.10946) Maddin HC. 2011 Deciphering morphological variation in the braincase of caecilian amphibians (Gymnophiona). J. Morphol. 272, 850–871. (doi:10. 1002/jmor.10953) Pardo JD, Anderson JS. In review Cranial morphology of the Carboniferous –Permian tetrapod Brachydectes newberryi (Lepospondyli, Lysorophia): new data from micro-CT. PLoS ONE.
4
Proc. R. Soc. B 283: 20160027
24.
198 –210. (doi:10.1655/HERPETOLOGICA-D-1300082R1) Lombard RE. 1977 Comparative morphology of the inner ear in salamanders (Caudata: Amphibia). Contrib. Vert. Evol. 2, 1–143. Fritzsch B, Wake MH. 1988 The inner ear of gymnophione amphibians and its nerve supply: a comparative study of regressive events in a complex sensory system (Amphibia, Gymnophiona). Zoomorphology 108, 201– 217. (doi:10.1007/ bf00312221) Maddin HC, Anderson JS. 2012 The evolution of the amphibian ear with implications for lissamphibian phylogeny: insight gained from the caecilian inner ear. Fieldiana Life and Earth Sci. 5, 59 – 76. (doi:10. 3158/2158-5520-5.1.59) Maddin HC, Russell AP, Anderson JS. 2012 Phylogenetic implications of the morphology of the braincase of caecilian amphibians (Gymnophiona). Zool. J. Linn. Soc. 166, 160–201. (doi:10.1111/j. 1096-3642.2012.00838.x) Szostakiwskyj M, Pardo JD, Anderson JS. 2015 Micro-CT study of Rhynchonkos stovalli (Lepospondyli, Recumbirostra), with description of
rspb.royalsocietypublishing.org
16. Sigurdsen T, Bolt JR. 2010 The Lower Permian amphibamid Doleserpeton (Temnospondyli: Dissorophoidea), the interrelationships of amphibamids, and the origin of modern amphibians. J. Vertebr. Paleontol. 30, 1360– 1377. (doi:10.1080/02724634.2010.501445) 17. Sigurdsen T, Green DM. 2011 The origin of modern amphibians: a re-evaluation. Zool. J. Linn. Soc. 162, 457–469. (doi:10.1111/j.1096-3642.2010.00683.x) 18. Marjanovic´ D, Laurin M. 2013 The origin(s) of extant amphibians: a review with emphasis on the ‘lepospondyl hypothesis’. Geodiversitas 35, 207 – 272. (doi:10.5252/g2013n1a8) 19. Sigurdsen T. 2008 The otic region of Doleserpeton (Temnospondyli) and its implications for the evolutionary origin of frogs. Zool. J. Linn. Soc. 154, 738–751. (doi:10.1111/j.1096-3642.2008.00459.x) 20. Robinson J, Ahlberg PE, Koentges G. 2005 The braincase and middle ear region of Dendrerpeton acadianum (Tetrapoda: Temnospondyli). Zool. J. Linn. Soc. 143, 577–597. (doi:10.1111/j.1096-3642.2005.00156.x) 21. Grant T, Bolı´var-G W. 2014 A new species of semiarboreal toad with a salamander-like ear (Anura: Bufonidae: Rhinella). Herpetologica 70,
Is there an exemplar taxon for modelling the evolution of early tetrapod hearing? J. S. Anderson1, J. D. Pardo1, H. C. Maddin2, M. Szostakiwskyj3 and A. Tinius3
Comment Cite this article: Anderson JS, Pardo JD, Maddin HC, Szostakiwskyj M, Tinius A. 2016 Is there an exemplar taxon for modelling the evolution of early tetrapod hearing? Proc. R. Soc. B 283: 20160027. http://dx.doi.org/10.1098/rspb.2016.0027
Received: 5 January 2016 Accepted: 14 March 2016
Author for correspondence: J. S. Anderson e-mail: [email protected]
1 Department of Comparative Biology and Experimental Medicine, University of Calgary, 3330 Hospital Drive NW, Calgary, Alberta, Canada T2N 4N1 2 Department of Earth Sciences, Carleton University, 1125 Colonel By Drive, Ottawa, Ontario, Canada K1S 5B6 3 Department of Biological Sciences, University of Calgary, 2300 University Drive NW, Calgary, Alberta, Canada T2N 1N4
Christensen et al. recently published a study of hearing in neotenic and experimentally metamorphosed axolotls (Ambystoma mexicanum) and a larval and adult tiger salamander (A. tigrinum), which contributes greatly to our understanding of salamander sound perception in water and air [1]. They demonstrate that premetamorphic, atympanic aquatic salamanders are capable of perceiving high frequency airborne sounds similar to terrestrial adults, demonstrating an interesting capacity for an atympanic ear to function for sound perception in a variety of media. This important research, in combination with other recent studies on the sound perception capabilities of lungfish [2], is helping to better clarify issues related to the water-to-land transition. However, the implication of their experimental design demands a consideration of the evolutionary history of their selected exemplar taxa so these valuable data can be interpreted in a broader context. Our criticisms focus on two major points: the use of salamanders as a proxy for hearing ability intermediate between aquatic and terrestrial vertebrates, and the use of microsaurs as exemplars of the early tetrapod condition. The currently accepted hypothesis for the origin of a tympanic ear is as a derivation from the spiracle of sarcopterygian fish [3]. In ‘fish’ the spiracle is associated with gill breathing: water passes through the spiracular notch in the rear of the skull, past the braincase and the bracing hyomandibula, to the oropharynx and gill arches [4]. With the loss of gills, the persisting spiracular lumen is co-opted into a middle ear chamber, and the cranial support role of the hyomandibula (now termed stapes) is eliminated, leaving this bone to extend freely into the middle ear chamber (figure 1). In derived tetrapods, the spiracular opening is expanded and covered by a membrane (the tympanum) that collects sound. Vibrations are transmitted to the inner ear via the stapes, which becomes more delicate and better able to propagate fine vibrations [7–10].
1. Salamanders are not evolutionary intermediates
The accompanying reply can be viewed at http://dx.doi.org/10.1098/rspb.2016.0716.
Christensen et al. state ([1], p. 2), ‘Equally important, [the urodele auditory system] can be regarded as a potential model for the intermediate evolutionary developmental stage’ between lungfish and frogs. However, there is strong evidence that salamanders have secondarily lost a tympanic ear, which dramatically changes the interpretation of the results of this study. Most palaeontologists agree that modern amphibians (Lissamphibia) are a monophyletic group with origins among a group of temnospondyls, the Amphibamidae [5,11 –17] (but see [18] for an alternative view). Amphibamids are considered to have had a tympanic hearing system identical to that of frogs [9,10,19] (figure 1). This hearing system was probably present in the first temnospondyls [20], dating well into the Carboniferous. Interestingly, a middle ear similar to salamanders is also seen in some secondarily atympanic frogs [21]. This secondary loss of tympanic hearing is also evident physiologically. All lissamphibians possess two epithelia: one associated with low-frequency
& 2016 The Author(s) Published by the Royal Society. All rights reserved.
(a)
2
tympanum hyomandibula/stapes operculum ossicle
Carrolla
amniote total group
Protorothyris
(b)
rspb.royalsocietypublishing.org
temporal embayment present
spiracle
Amniota Microsauria
temporal embayment absent
(c) Seymouria
amphibian total group
Tersomius
(g)
Dissorophoidea
( f)
Amphibamidae
Gastrotheca origin of amphibian TE
Batrachia
Ambystoma
(e)
Broiliellus
(h)
water–land transition
Dendrerpeton
(i)
( j)
Archeria
Kyrinion
(k)
fin to limb transition
(l)
Crassigyrinus
Pederpes
(m)
Ventastega
(n)
Eusthenopteron
Figure 1. Phylogenetic context of middle ear evolution in early tetrapods. Phylogeny modified from [5,6]. TE, tympanic ear. Illustrations not to scale.
environmental stimulations and one with high-frequency aerial sound. Salamanders show a phylogenetically correlated reduction in innervation of the epithelium associated with high frequency sound perception [22], indicating the presence of a tympanic hearing system in their evolutionary past. A similar trend is found in the atympanic caecilians
[23,24]. This point is critical because Christensen et al. tested sensitivity to sound vibrations at the auditory nerve, which directly reflects the innervation of the sensory epithelia detecting the stimulus. Because salamanders have remnants of the greater innervation of the fully tympanic ear, it is expected that they can perceive sound better than animals
Proc. R. Soc. B 283: 20160027
(d)
2. Microsaurs are not representative of early tetrapods
3. Conclusion and recommendations Experimental studies of modern taxa have the potential to inform our understanding of major transitions in evolutionary history otherwise preserved only in the fossil record, but the selection of exemplary taxa for such studies is nontrivial to their applicability. Researchers must consider the evolutionary histories of taxa to ensure that the model organisms are appropriate analogues so that conclusions can be drawn with confidence. The middle ear of Polypterus is more anatomically similar to that seen in stem tetrapods and lungfish near the tetrapodomorph divergence and could be an appropriate analogue to test in future studies of this question. Given the above, we assert that the conclusion that ‘early tetrapods also may have been able to detect aerial sound before the appearance of the tympanic middle ear’ ([1], p. 8) drawn from observations of salamanders and microsaurs is unfounded. Instead, the results of this study provide interesting insights into the strength of the conservation of an auditory apparatus adapted to terrestrial hearing in a group of aquatic salamanders. Authors’ contributions. All authors contributed equally. Competing interests. We have no competing interests. Funding. This study was supported by a Discovery Grant from the Natural Sciences and Engineering Research Council of Canada to J.S.A.
Acknowledgements. We thank Jennifer Clack and Eric Lombard for previous discussions on these subjects, which does not imply their agreement with our comment. This manuscript was further improved by comments from two anonymous reviewers, Dr Jakob ChristensenDalsgaard and the editorial staff.
References 1.
2.
3.
4.
5.
Christensen CB, Lauridsen H, Christensen-Dalsgaard J, Pedersen M, Madsen PT. 2015 Better than fish on land? Hearing across metamorphosis in salamanders. Proc. R. Soc. B 282, 20141943. (doi:10.1098/rspb.2014.1943) Christensen-Dalsgaard J, Brandt C, Wilson M, Wahlberg M, Madsen PT. 2010 Hearing in the African lungfish (Protopterus annectens): preadaptation to pressure hearing in tetrapods? Biol. Lett. 7, 139–141. (doi:10.1098/rsbl.2010.0636) Clack JA. 2015 Evolutionary biology: the origin of terrestrial hearing. Nature 519, 168 –169. (doi:10. 1038/519168a) Graham JB, Wegner NC, Miller LA, Jew CJ, Lai NC, Berquist RM, Frank LR, Long JA. 2014 Spiracular air breathing in polypterid fishes and its implications for aerial respiration in stem tetrapods. Nat. Commun. 5, 1 –6. (doi:10.1038/ncomms4022) Maddin HC, Jenkins Jr FA, Anderson JS. 2012 The braincase of Eocaecilia micropodia (Lissamphibia, Gymnophiona) and the origin of caecilians. PLoS ONE 7, e50743. (doi:10.1371/journal.pone.0050743)
6.
Clack JA, Ahlberg PE, Blom H, Finney SM. 2012 A new genus of Devonian tetrapod from North-East Greenland, with new information on the lower jaw of Ichthyostega. Palaeontology 55, 73 –86. (doi:10. 1111/j.1475-4983.2011.01117.x) 7. Clack J. 2002 Patterns and processes in the early evolution of the tetrapod ear. J. Neurobiol. 53, 251 –264. (doi:10.1002/neu.10129) 8. Bolt JR, Lombard RE. 1985 Evolution of the amphibian tympanic ear and the origin of frogs. Biol. J. Linn. Soc. 24, 83 –99. (doi:10.1111/j.10958312.1985.tb00162.x) 9. Lombard RE, Bolt JR. 1979 Evolution of the tetrapod ear: an analysis and reinterpretation. Biol. J. Linn. Soc. 11, 19–76. (doi:10.1111/j.1095-8312.1979.tb00027.x) 10. Lombard RE, Bolt JR. 1988 Evolution of the stapes in Paleozoic tetrapods: conservative and radical hypotheses. In The evolution of the amphibian auditory system (ed. B Fritzsch). New York, NY: John Wiley and Sons, Inc. 11. Ruta M, Coates MI. 2007 Dates, nodes and character conflict: addressing the lissamphibian origin
12.
13.
14.
15.
problem. J. Syst. Paleontol. 5, 69– 122. (doi:10. 1017/S1477201906002008) Trueb L, Cloutier R. 1991 A phylogenetic investigation of the inter- and intrarelationships of the Lissamphibia (Amphibia: Temnospondyli). In Origins of the higher groups of tetrapods: controversy and consensus (eds H-P Schultze, L Trueb), pp. 174–193. London, UK: Comstock Publishing Associates. Bolt JR. 1969 Lissamphibian origins: possible protolissamphibian from the Lower Permian of Oklahoma. Science 166, 888–891. (doi:10.1126/ science.166.3907.888) Bolt JR. 1991 Lissamphibian origins. In Origins of the higher groups of tetrapods: controversy and consensus (eds H-P Schultze, L Trueb), pp. 194–222. London, UK: Comstock Publishing Associates. Sigurdsen T, Bolt JR. 2009 The lissamphibian humerus and elbow joint, and the origins of modern amphibians. J. Morphol. 270, 1443–1453. (doi:10.1002/Jmor.10769)
3
Proc. R. Soc. B 283: 20160027
Christensen et al. [1] assert that microsaurs are morphological exemplars for the early tetrapod condition (a rationale for this was not provided) and that similarities of the middle ear can be used to associate the functional data derived from salamanders with the early evolution of frog-like hearing. This is problematic for two reasons. First, phylogenetically microsaurs are more closely related to the amniote crown group than any early tetrapod [5,11,24,25]. They are derived in both lacking a spiracular embayment and in possessing a short, robust stapes, unlike all taxa that span the water-toland transition up to, and including, frogs (figure 1). Rather than representing a transition between aquatic and terrestrial living, microsaurs are highly specialized terrestrial species adapted to burrowing. Second, whereas Christensen et al. are correct in recognizing superficial similarities between salamanders and microsaurs, including the lack of an otic notch and stapes with broad footplates and short columellae, microsaurs differ in several important anatomical details [26–28]. For example, microsaurs have the stapes completely filling the fenestra vestibularis, whereas salamanders also have an operculum [22]. All lissamphibians [24,29] and some temnospondyls [19] possess a posterior pressure relief pathway via the perilymphatic foramen, whereas microsaurs possess an ossified crista interfenestralis that prevents this posterior
perilymphatic flow, strongly suggesting they possess a more amniote-like anterior pattern [26,30].
rspb.royalsocietypublishing.org
without any evolutionary history of terrestrial hearing. The fact that secondarily aquatic salamanders, such as axolotl, do not differ in their ability to hear aerial sound from terrestrial salamanders reflects the conservation of a degree of terrestrial hearing capability. Even under the heterodox ‘lepospondyl hypothesis’ [18] this loss is recognized.
22.
23.
25.
26.
27.
28.
29.
30.
two new genera. PLoS ONE 10, e0127307. (doi: 10. 1371/journal.pone.0127307) Pardo JD, Szostakiwskyj M, Anderson JS. 2015 Cranial morphology of the brachystelechid ‘microsaur’ Quasicaecilia texana Carroll provides new insights into the diversity and evolution of braincase morphology in recumbirostran ‘microsaurs’. PLoS ONE 10, e0130359. (doi:10.1371/journal.pone. 0130359) Maddin HC, Olori JC, Anderson JS. 2011 A redescription of Carrolla craddocki (Lepospondyli: Brachystelechidae) based on high-resolution CT, and the impacts of miniaturization and fossoriality on morphology. J. Morphol. 272, 722–743. (doi:10. 1002/jmor.10946) Maddin HC. 2011 Deciphering morphological variation in the braincase of caecilian amphibians (Gymnophiona). J. Morphol. 272, 850–871. (doi:10. 1002/jmor.10953) Pardo JD, Anderson JS. In review Cranial morphology of the Carboniferous –Permian tetrapod Brachydectes newberryi (Lepospondyli, Lysorophia): new data from micro-CT. PLoS ONE.
4
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24.
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