The field of palaeoneurology was founded a century ago and is a long-established branch of inquiry into fossil vertebrates (Edinger, 1921). However relatively little attention has been given to investigation into the evolution of the brain in fossil fishes, most likely due to the fact that the brain-braincase relationship is generally not as close as in “higher” vertebrates such as birds and mammals (Jerison, 1973). Nevertheless, there were some pioneering early works specifically investigating fossil fishes which laid the foundation for further palaeoneurological research in early vertebrates (Chang, 1982; Janvier, 1974; Jarvik, 1942; Jarvik, 1972; Stensiö, 1963; Stensiö, 1927). These days modern advances in imaging technologies are transforming the palaeoneurological landscape, enabling more in-depth investigations of structure-function relationships (Bruner et al., 2018; Walsh and Knoll, 2011), including in early vertebrates.

Lungfish represent a unique evolutionary lineage, which has persisted for over 400 million years. Their crania differ quite remarkably from other sarcopterygian fishes in having lost the intracranial joint, possession of an autostylic jaw suspension, unique dentition and differences in the number and arrangement of dermal skull bones (Schultze, 1986). Homologues of skull roofing bones across sarcopterygians were difficult to identify, leading to the adoption of an alternate (and unique) labelling scheme that continues to be used today (Forster-Cooper, 1937), with additions and updates from Ahlberg, 1991; Cloutier, 1997; Miles, 1977. Furthermore, lungfish skulls have undergone considerable reduction in the degree of ossification and the fusion and/or loss of bone, leading to a massive (~10-fold) reduction in the number of dermal skull bones present in extant Dipnoi compared to some Devonian forms (Criswell, 2015). However, there has been relatively little attention paid to examining brain evolution in early lungfish (Dipnoi), despite the crania of a large number of fossils having been described since early in the 19th Century (Sedgwick and Murchison, 1828), more than 100 fossil lungfish taxa described, and renewed taxonomic interest in lungfish as the extant sister group of the tetrapods.

While aspects of the anatomy of the central nervous system in extant lungfish have been known for close to 150 years (Collin, 2007; Huxley, 1876; Northcutt, 1986), it was only recently that the specific spatial relationship between the brain and the endocranial cavity was investigated. This was examined first in the Australian lungfish, Neoceratodus (Clement et al., 2015), and later in the lepidosirenid lungfish (Lepidosiren and Protopterus) and other piscine sarcopterygians (Challands et al., 2020). It was found that contrary to earlier reports of the lungfish brain filling just a fraction (10%) of its brain cavity (Jerison, 1973), values in fact ranged between 40% and 80% (Challands et al., 2020; Clement et al., 2021; Clement et al., 2015). Moreover, these studies highlighted that the forebrain and labyrinth regions in particular had a close correspondance between brain and endocast, in comparison with the mid and hindbrain regions with a looser association.

Currently, only eight species of fossil lungfish have had the endocast (the negative space within the cranium) described or illustrated in any considerable manner (either full or partial), and are all of Devonian age. These include Dipnorhynchus sussmilchi (Campbell and Barwick, 1982; Clement et al., 2016a), Chirodipterus wildungensis (Säve-Söderbergh, 1952), ‘Chirodipterus’ australis (Henderson and Challands, 2018; Miles, 1977), Griphognathus whitei and Holodipterus gogoensis (Miles, 1977), Dipnorhynchus kurikae (Campbell and Barwick, 2000), Rhinodipterus kimberleyensis (Clement and Ahlberg, 2014), and Dipterus valenciennesi (Challands, 2015). Additional fragmentary neurocranial information is also known in Scaumenacia curta (Boirot and Challands, 2021).

Some early investigations into fossil lungfish endocranial morphology led Stensiö, 1963 to suggest that the dipnoan brain 'type' had developed by the beginning of the Devonian and has not undergone any significant changes since that time. However, recent work has shown that the endocasts of some Devonian lungfish continued to change in morphology with the acquisition of new characters certainly into the Upper Devonian period, while also retaining other primitive characteristics (Challands, 2015; Clement and Ahlberg, 2014; Clement et al., 2016a).

The polarity of such characters in the cranial endocasts of fossil lungfish has largely been determined by reference to brains of extant taxa; the Lepidosireniformes (Protopterus and Lepidosiren) and the Ceratodontiformes (Neoceratodus). For example, Northcutt, 1986; Northcutt, 2011 stated that pedunculate olfactory bulbs are the likely primitive state in the Dipnoi as this characteristic is observed in Neoceratodus, (considered the most morphologically conservative of the extant dipnoan taxa), and also in the extant coelacanth Latimeria (Dutel et al., 2019). Furthermore, pedunculate olfactory bulbs are also seen in stem osteichthyans (Clement et al., 2018), as well as several more basal outgroups such as placoderms (Zhu et al., 2021).

Determining the polarity of endocast characters is important at this juncture in dipnoan palaeoneurological research as we are now in a position to recognise and apply more neurocranial characters to phylogenetic analyses. Following on from Friedman’s detailed analysis of lungfish interrelationships based on neurocranial evidence (Friedman, 2007), Clement et al., 2016a conducted the first phylogenetic analysis of Palaeozoic lungfish based entirely on endocast characters, further emphasising their use for such studies. Despite the problematic homology of dermal bones, endocranial anatomy tends to be far more conserved in vertebrates and thus highly valuable for comparative analysis.

Here, we investigate the endocranial morphology of six Devonian dipnoans (Iowadipterus halli, Gogodipterus paddyensis, Pillararhynchus longi, Griphognathus whitei, Orlovichthys limnatis, and Rhinodipterus ulrichi) from synchrotron and computed tomography (CT), and compare them with those taxa already known (fossil and extant) using multivariate morphometric analyses (Figure 1). We hypothesise that, just as cranial elongation manifests in numerous ways by lengthening of either the snout, jaw or cheek regions, the neurocranium (and by consequence, the endocasts) of Devonian lungfish will have also accommodated elongation by modifying different regions to varying extents.

Figure 1

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Lungfish first appear in the fossil record in the Early Devonian as robust marine animals, many with hyper-mineralised tooth plates, heavily-ossified dermal skulls and neurocrania (Cui et al., 2022). However, from the Late Devonian-Carboniferous onwards, many undergo a decline in the degree of ossification as their skeleton becomes more cartilaginous. This reduction in the dipnoan cranial dermal skeleton was likely accompanied by some changes in the cranial cavity form, but this level of increasingly poor ossification of the neurocranium in those taxa limits our possible comparisons to between the more heavily ossified Devonian forms and extant taxa only. Consequently, some of the oldest lungfish taxa are the most completely known, especially with respect to neurocranial morphology. With the exception of the Permian lungfish Persephonichthys chthonica (Pardo et al., 2014), no post-Devonian fossil taxa have had their cranial endocasts described. We acknowledge that our investigation of lungfish brain evolution as elucidated from morphometric analysis of cranial endocasts is still preliminary in several respects. Due to the extreme age and rarity of 3D preserved lungfish endocrania, we used all material available to us. Admittedly we cannot hope to control for many factors, including ontogeny, so our interpretations must naturally take that into consideration. However, we hope that our study inspires future work on the neural evolution of both fossil and extant lungfish.

Implications for sensory abilities in early lungfish

Overall, there is considerable variation in the shape and relative proportions of the endocasts examined. Griphognathus whitei stands out as the most extreme case of elongation of the olfactory region, whereas other taxa, such as Iowadipterus halli, appear to elongate the midbrain region, whilst retaining very short olfactory canals and more conventionally-shaped nasal capsules (rounded to slightly oval). Although only a partial endocast, Gogodipterus paddyensis is nearly indistinguishable from Pillararhynchus longi in labyrinth morphology. All ‘chirodipterid’ taxa (sensu Friedman, 2007) appear to share mediolaterally-oriented nasal capsules, close to equidimensional circular arcs of their semicircular canals and a broad angle of bifurcation between the olfactory canals. Despite this, the ‘chirodipterid’ taxa do not consistently cluster together in the analyses, giving further weight to the proposition that these taxa form a paraphyletic group (Friedman, 2007).

Rhinodipterus ulrichi and ‘Chirodipterus’ australis have endocasts with strongly anteroventrally-directed fore/midbrain portions in comparison with the hindbrain, while presumed close relatives R. kimberleyensis and other ‘chirodipterid’ taxa do not display this character. Aside from this, the endocasts of the two Rhinodipterus species are broadly similar to each other – the absence of an eminence for the pineal organ in R. kimberleyensis is likely simply a preservational artefact (Clement and Ahlberg, 2014). The hypophyseal recess varies from being directed ventrally (R. kimberleyensis, Orlovichthys limnatis, P. longi) or posteroventrally (Dipnorhynchus spp., Dipterus valenciennesi, R. ulrichi).

The length of the olfactory canals (usually incorporating olfactory nerve, bulb and tract) and their angle of bifurcation are one of the largest sources of variation among endocasts of different lungfish taxa (Figure 8), and unsurprisingly, these two features are strongly linked. The shape of the olfactory capsules appears highly variable in Devonian lungfish endocasts (Figure 12). These are most commonly oval-shaped, although the orientation can vary. Others are highly elongate as in Griphognathus whitei, to triangular in ‘Chirodipterus’ australis. Our study simply captured length but future work on shape and orientation may prove pertinent to the overall plasticity of the olfactory region. The other strongest signals from our data concern the labyrinths, specifically the size and shape of the sacculus, utriculus and the semicircular canals. The semicircular canals (arc height, length, and width) tend to covary as an integrated module, whereas the utriculus and sacculus vary independently of each other. The sacculus is better integrated with the semicircular canals than the utriculus (Figure 11), suggesting a modular dissociation.

Figure 12

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Taken together, our analyses suggest that the olfactory and labyrinth regions are more plastic and may reflect species differences in chemosensory and vestibular sensitivity (and potentially auditory) abilities, whereas the hindbrain remains more conserved. These findings are of note as the olfactory region seems to be changing independently from all other endocast variables, despite elongated dermal crania being modified in different ways (e.g. elongation of the dermal snout, cheek, or jaws). A similar finding has been established for extant cartilaginous fishes, where the olfactory bulbs maintain a substantial level of allometric independence from the rest of the brain in more than 100 species, reflecting differences in ecological niche, particularly habitat (Yopak et al., 2015; Yopak et al., 2019), a relationship which is common to other vertebrates (Yopak et al., 2010). This suggests that these species of lungfish may have had different olfactory abilities for various survival tasks including localizing prey, avoiding predators, and chemosensory communication with conspecifics.

The inner ears are comprised of a superior division containing the semicircular canals, which are predominantly involved in balance perception, and whose morphology is considered closely correlated with an animal’s orientation within the water column, sensitivity to movement and even visual acuity (Kemp and Christopher Kirk, 2014; Malinzak et al., 2012; Spoor et al., 2002; Spoor et al., 2007), although the generality of this relationship is being challenged in some more recent works (Bronzati et al., 2021). In contrast, the inferior division, or vestibule, contains the sacculus and utriculus, which are sensitive to mechanical acceleration, but also play an auditory role in discriminating and localising sound. Inner ear morphology in fishes tends to be relatively conserved, and when there is variation it is more commonly seen in this inferior division rather than the semicircular canals (Ladich and Schulz-Mirbach, 2016). The sacculus (combined with the lagena in lungfish), is most sensitive to movements in the vertical plane, whereas the utriculus detects angular and linear acceleration predominantly in the horizontal plane (Platt et al., 2004). Similar bioimaging techniques and consequent morphometric analyses have been used to successfully predict both auditory and vestibular abilities in other aquatic vertebrates (Lauridsen et al., 2011; Ramcharitar et al., 2004), thus lending support to our functional interpretations in lungfish contained herein.

With soft tissues, such as brains, typically not fossilising, there is a need to use endocasts as proxies to infer or reconstruct gross neural morphology in extinct taxa (Clement et al., 2016b). With respect to making meaningful biological inferences from lungfish endocasts, evidence from extant lungfish show a moderate-high correspondence between brain and endocast in life (Challands et al., 2020; Clement et al., 2015). Interestingly, there tends to be considerably higher correspondence in the forebrain and labyrinth regions (Clement et al., 2015), and we thus can take more confidence in potential functional interpretations relating to those regions in extinct taxa. Intriguingly, it is in those regions where we see the largest variations in our analyses, highlighting the potential to elucidate significant functional insights into an animal’s sensory capabilities.

Thus, guided by our findings and the Principle of Proper Mass (Jerison, 1973), we believe we can draw some reasonable conclusions about brain evolution in lungfish. The hindbrain region appears to have remained relatively conserved throughout lungfish evolution, and there is no evidence of hypertrophy as is seen in some other lineages, that is within the Chondrichthyes and Actinopterygii (Nieuwenhuys et al., 1998; Striedter and Northcutt, 2020). The midbrain similarly seems to have remained relatively small and it seems unlikely that vision has ever been a dominant sense in lungfish (in contrast to many actinopterygians).

In contrast, the forebrain underwent early expansion in some of the oldest members of the lineage and appears to have continued to present day, suggesting an ongoing and increasing reliance in the role of olfaction. Relatedly, the high variability in this region throughout their evolutionary history highlights continuing modification of and importance in the role of olfaction in lungfish.

And finally, the changes seen in the labyrinth region, particularly the expansion of the utriculus, suggests increasing sensitivity to movements in the horizontal plane, perhaps reflecting changing sensory requirements from one niche to another. For example, we consider that animals living in a shallow, near-shore environment would have less requirement for sensitivity to large changes in the vertical plane compared to nektonic animals living in deeper, open environments throughout the water column. Thus, the modular dissociation between the sacculus +semicircular canals compared to the expansion of the utriculus may potentially be capturing a change from deeper water marine (nektonic) environments (as per some of the earliest lungfish, e.g. Dipnorhynchus), to gradually more near-shore/terrestrial ecosystems (a trend seen among Mid-Late Devonian members to present day taxa). However, we acknowledge that it is difficult to determine if increased relative utricular size results from greater reliance of sensitivity in the horizontal plane alone, or if it expands to compensate for example relative stagnation of the sacculus + semicircular canals in some way. Further studies, such as investigation of neuronal densities in extant lungfish labyrinths, may potentially help to clarify this uncertainty in future.

All data generated or analysed during this study are included in the manuscript, supporting files (5 figures and 5 spreadsheets), or online as follows: Scan data from Chirodipterus wildungensis, Gogodipterus paddyensis, Iowadipterus halli, Pillararhynchus longi and Rhinodipterus ulrichi can be found on MorphoSource at: https://www.morphosource.org/projects/000381944?locale=en. Griphognathus whitei and Orlovichthys limnatis have been deposited on Dryad: https://doi.org/10.5061/dryad.2rbnzs7p8.

1. 1. Clement AM

   (2022) Dryad Digital Repository

   Data from: Morphometric Analysis of Lungfish Endocasts Elucidates Early Dipnoan Palaeoneurological Evolution.

   https://doi.org/10.5061/dryad.2rbnzs7p8
2. 1. Clement AM

   (2021) Morphosource

   ID 000381944. Morphometric Analysis of Lungfish Endocasts Elucidates Early Dipnoan Palaeoneurological Evolution.

   https://www.morphosource.org/projects/000381944?locale=en

1. 1. Ahlberg PE

   (1991) A re-examination of sarcopterygian interrelationships, with special reference to the Porolepiformes

   Zoological Journal of the Linnean Society 103:241–287.

   https://doi.org/10.1111/j.1096-3642.1991.tb00905.x

   • Google Scholar
2. 1. Barwick RE
   2. Campbell KSW

   (1996) A Late Devonian Dipnoan, Pillararhynchus, from Gogo, Western Australia, and its relationships

   Palaeontographica Abteilung A 239:1–42.

   https://doi.org/10.1127/pala/239/1996/1

   • Google Scholar
3. Book

   1. Boirot M
   2. Challands T

   (2021)

   Paedomorphic Trait Related to Neurocranial Ossification in Two Devonian Lungfishes (Givetian Pentlandia Macroptera and Frasnian Scaumenacia Curta

   Acta Palaeontologica Polonica.

   • Google Scholar
4. 1. Bronzati M
   2. Benson RBJ
   3. Evers SW
   4. Ezcurra MD
   5. Cabreira SF
   6. Choiniere J
   7. Dollman KN
   8. Paulina-Carabajal A
   9. Radermacher VJ
   10. Roberto-da-Silva L
   11. Sobral G
   12. Stocker MR
   13. Witmer LM
   14. Langer MC
   15. Nesbitt SJ

   (2021) Deep evolutionary diversification of semicircular canals in archosaurs

   Current Biology 31:2520–2529.

   https://doi.org/10.1016/j.cub.2021.03.086

   • PubMed
   • Google Scholar
5. Book

   1. Bruner E
   2. Ogihara N
   3. Tanabe HC

   (2018) Digital Endocasts: From Skulls to Brains

   Tokyo: Springer.

   https://doi.org/10.1007/978-4-431-56582-6

   • Google Scholar
6. 1. Campbell KSW
   2. Barwick RE

   (1982) The neurocranium of the primitive dipnoan Dipnorhynchus sussmilchi (Etheridge

   Journal of Vertebrate Paleontology 2:286–327.

   https://doi.org/10.1080/02724634.1982.10011936

   • Google Scholar
7. 1. Campbell KSW
   2. Barwick RE

   (1986) Paleozoic lungfishes?a review

   Journal of Morphology 190:93–131.

   https://doi.org/10.1002/jmor.1051900409

   • Google Scholar
8. 1. Campbell KSW
   2. Barwick RE

   (2000) The braincase, mandible and dental structures of the Early Devonian lungfish Dipnorhynchus kurikae from Wee Jasper, New South Wales

   Records of the Australian Museum 52:103–128.

   https://doi.org/10.3853/j.0067-1975.52.2000.1309

   • Google Scholar
9. 1. Challands TJ

   (2015) The cranial endocast of the Middle Devonian dipnoan Dipterus valenciennesi and a fossilized dipnoan otoconial mass

   Papers in Palaeontology 1:289–317.

   https://doi.org/10.1002/spp2.1016

   • Google Scholar
10. 1. Challands TJ
    2. Smithson TR
    3. Clack JA
    4. Bennett CE
    5. Marshall JEA
    6. Wallace-Johnson SM
    7. Hill H

    (2019) A lungfish survivor of the end-Devonian extinction and an Early Carboniferous dipnoan radiation

    Journal of Systematic Palaeontology 17:1825–1846.

    https://doi.org/10.1080/14772019.2019.1572234

    • Google Scholar
11. 1. Challands TJ
    2. Pardo JD
    3. Clement AM

    (2020) Mandibular musculature constrains brain-endocast disparity between sarcopterygians

    Royal Society Open Science 7:200933.

    https://doi.org/10.1098/rsos.200933

    • PubMed
    • Google Scholar
12. Book

    1. Chang MM.

    (1982)

    The braincase of Youngolepis, a Lower Devonian crossopterygian from Yunnan, south-western China PhD

    University of Stockholm and Section of Palaeozoology, Swedish Museum of Natural History.

    • Google Scholar
13. 1. Clement AM

    (2012) A new species of long-snouted lungfish from the Late Devonian of Australia, and its functional and biogeographical implications

    Palaeontology 55:51–71.

    https://doi.org/10.1111/j.1475-4983.2011.01118.x

    • Google Scholar
14. 1. Clement AM
    2. Ahlberg PE

    (2014) The first virtual cranial endocast of a lungfish (sarcopterygii: dipnoi

    PLOS ONE 9:e113898.

    https://doi.org/10.1371/journal.pone.0113898

    • PubMed
    • Google Scholar
15. 1. Clement AM
    2. Nysjö J
    3. Strand R
    4. Ahlberg PE

    (2015) Brain - Endocast Relationship in the Australian Lungfish, Neoceratodus forsteri, Elucidated from Tomographic Data (Sarcopterygii: Dipnoi

    PLOS ONE 10:e0141277.

    https://doi.org/10.1371/journal.pone.0141277

    • PubMed
    • Google Scholar
16. 1. Clement AM
    2. Challands TJ
    3. Long JA
    4. Ahlberg PE

    (2016a) The cranial endocast of Dipnorhynchus sussmilchi (Sarcopterygii: Dipnoi) and the interrelationships of stem-group lungfishes

    PeerJ 4:e2539.

    https://doi.org/10.7717/peerj.2539

    • PubMed
    • Google Scholar
17. 1. Clement AM
    2. Strand R
    3. Nysjö J
    4. Long JA
    5. Ahlberg PE

    (2016b) A new method for reconstructing brain morphology: applying the brain-neurocranial spatial relationship in an extant lungfish to A fossil endocast

    Royal Society Open Science 3:160307.

    https://doi.org/10.1098/rsos.160307

    • PubMed
    • Google Scholar
18. 1. Clement AM
    2. King B
    3. Giles S
    4. Choo B
    5. Ahlberg PE
    6. Young GC
    7. Long JA

    (2018) Neurocranial anatomy of an enigmatic Early Devonian fish sheds light on early osteichthyan evolution

    eLife 7:e34349.

    https://doi.org/10.7554/eLife.34349

    • PubMed
    • Google Scholar
19. 1. Clement AM
    2. Mensforth CL
    3. Challands TJ
    4. Collin SP
    5. Long JA

    (2021) Brain Reconstruction Across the Fish-Tetrapod Transition; Insights From Modern Amphibians

    Frontiers in Ecology and Evolution 9:60.

    https://doi.org/10.3389/fevo.2021.640345

    • Google Scholar
20. 1. Cloutier R

    (1997)

    Morphologie et variations du toit crânien du Dipneuste Scaumenacia curta (Whiteaves) (Sarcopterygii), du Dévonien supérieur du Québec

    Geodiversitas 19:61–105.

    • Google Scholar
21. Book

    1. Collin SP

    (2007) Nervous and sensory systems

    In: Mckenzie DJ, Farrell AP, Brauner CJ, editors. Primitive Fishes, Fish Physiology. Springer. pp. 121–179.

    https://doi.org/10.1016/S1546-5098(07)26003-0

    • Google Scholar
22. 1. Criswell KE

    (2015) The comparative osteology and phylogenetic relationships of African and South American lungfishes (Sarcopterygii: Dipnoi

    Zoological Journal of the Linnean Society 174:801–858.

    https://doi.org/10.1111/zoj.12255

    • Google Scholar
23. 1. Cui X
    2. Friedman M
    3. Qiao T
    4. Yu Y
    5. Zhu M

    (2022) The rapid evolution of lungfish durophagy

    Nature Communications 13:2390.

    https://doi.org/10.1038/s41467-022-30091-3

    • PubMed
    • Google Scholar
24. 1. Dutel H
    2. Galland M
    3. Tafforeau P
    4. Long JA
    5. Fagan MJ
    6. Janvier P
    7. Herrel A
    8. Santin MD
    9. Clément G
    10. Herbin M

    (2019) Neurocranial development of the coelacanth and the evolution of the sarcopterygian head

    Nature 569:556–559.

    https://doi.org/10.1038/s41586-019-1117-3

    • PubMed
    • Google Scholar
25. 1. Edinger T

    (1921) Über Nothosaurus, Ein Steinkern der Schädelhöhle

    Senckenbergiana 3:121–129.

    https://doi.org/10.1002/ajmg.a.30539

    • Google Scholar
26. 1. Forster-Cooper C

    (1937) VII.—The Middle Devonian Fish Fauna of Achanarras

    Transactions of the Royal Society of Edinburgh 59:223–239.

    https://doi.org/10.1017/S0080456800004737

    • Google Scholar
27. 1. Friedman M

    (2007) The interrelationships of Devonian lungfishes (Sarcopterygii: Dipnoi) as inferred from neurocranial evidence and new data from the genus Soederberghia Lehman, 1959

    Zoological Journal of the Linnean Society 151:115–171.

    https://doi.org/10.1111/j.1096-3642.2007.00320.x

    • Google Scholar
28. 1. Gess RW
    2. Clement AM

    (2019) A high latitude Devonian lungfish, from the Famennian of South Africa

    PeerJ 7:e8073.

    https://doi.org/10.7717/peerj.8073

    • PubMed
    • Google Scholar
29. 1. Gross W

    (1933)

    Die Agnathen und Fische des rheinischen Devons

    Abhandlungen Der Preussischen Geologischen Landesanstalt 154:1–83.

    • Google Scholar
30. 1. Henderson SAC
    2. Challands TJ

    (2018) The cranial endocast of the Upper Devonian dipnoan “Chirodipterus” australis

    PeerJ 6:e5148.

    https://doi.org/10.7717/peerj.5148

    • PubMed
    • Google Scholar
31. 1. Huxley TH

    (1876) On Ceratodus forsteri, with observations on the classification of Fishes

    Philosophical Transactions 2:e541.

    https://doi.org/10.1111/j.1096-3642.1876.tb02541.x

    • Google Scholar
32. 1. Janvier P

    (1974) The Sensory Line System and Its Innervation in the Osteostraci (Agnatha, Cephalaspidomorphi

    Zoologica Scripta 3:91–99.

    https://doi.org/10.1111/j.1463-6409.1974.tb00807.x

    • Google Scholar
33. 1. Jarvik E

    (1942)

    On the structure of the snout of Crossopterygians and Lower Gnathostomes in general

    Zoologiska Bidrag Från Uppsala 21:235–675.

    • Google Scholar
34. 1. Jarvik E

    (1972) Middle and Upper Devonian Porolepiformes from East Greenland with Special Reference to Glyptolepis groenlandica

    Meddelelser Om Gronland 187:1–307.

    https://doi.org/10.5194/fr-3-99-2000

    • Google Scholar
35. Book

    1. Jerison HJ

    (1973)

    Evolution of the Brain and Intelligence

    Academic Press, Inc.

    • PubMed
    • Google Scholar
36. 1. Kemp A

    (2000) Chirodipterus potteri, a new Devonian lungfish from New South Wales, Australia: and the ontogeny of chirodipterid tooth plates

    Journal of Vertebrate Paleontology 20:665–674.

    https://doi.org/10.1671/0272-4634(2000)020[0665:CPANDL]2.0.CO;2

    • Google Scholar
37. 1. Kemp AD
    2. Christopher Kirk E

    (2014) Eye size and visual acuity influence vestibular anatomy in mammals

    Anatomical Record (Hoboken, N.J 297:781–790.

    https://doi.org/10.1002/ar.22892

    • PubMed
    • Google Scholar
38. 1. Ladich F
    2. Schulz-Mirbach T

    (2016) Diversity in Fish Auditory Systems: One of the Riddles of Sensory Biology

    Frontiers in Ecology and Evolution 4:1–26.

    https://doi.org/10.3389/fevo.2016.00028

    • Google Scholar
39. 1. Lauridsen H
    2. Hansen K
    3. Wang T
    4. Agger P
    5. Andersen JL
    6. Knudsen PS
    7. Rasmussen AS
    8. Uhrenholt L
    9. Pedersen M

    (2011) Inside out: modern imaging techniques to reveal animal anatomy

    PLOS ONE 6:e17879.

    https://doi.org/10.1371/journal.pone.0017879

    • PubMed
    • Google Scholar
40. 1. Long JA

    (1992) Gogodipterus paddyensis (Miles), gen nov, a new chirodipterid lungfish from the late Devonian Gogo formation, Western Australia

    The Beagle 9:11–20.

    https://doi.org/10.5962/p.263113

    • Google Scholar
41. 1. Malinzak MD
    2. Kay RF
    3. Hullar TE

    (2012) Locomotor head movements and semicircular canal morphology in primates

    PNAS 109:17914–17919.

    https://doi.org/10.1073/pnas.1206139109

    • PubMed
    • Google Scholar
42. 1. Marshall CR

    (1986) Lungfish: Phylogeny and parsimony

    Journal of Morphology 190:151–162.

    https://doi.org/10.1002/jmor.1051900411

    • Google Scholar
43. 1. Miles RS

    (1977) Dipnoan (lungfish) skulls and the relationships of the group: a study based on new species from the Devonian of Australia

    Zoological Journal of the Linnean Society 61:1–328.

    https://doi.org/10.1111/j.1096-3642.1977.tb01031.x

    • Google Scholar
44. 1. Mörs T

    (1991) An unusual large lungfish tooth plate (Dipnoi, Chirodipteridae) from the Middle Devonian of the Rhenish Massif (Bergisches Land, Germany

    Neues Jahrbuch Für Geologie Und Paläontologie - Monatshefte 1991:654–662.

    https://doi.org/10.1127/njgpm/1991/1991/654

    • Google Scholar
45. Book

    1. Nieuwenhuys R
    2. ten Donkelaar HJ
    3. Nicholson C

    (1998) The Central Nervous System of Vertebrates

    Berlin, Heidelberg: Springer.

    https://doi.org/10.1007/978-3-642-18262-4

    • Google Scholar
46. 1. Northcutt RG

    (1986) Lungfish neural characters and their bearing on sarcopterygian phylogeny

    Journal of Morphology 190:277–297.

    https://doi.org/10.1002/jmor.1051900418

    • Google Scholar
47. Book

    1. Northcutt RG

    (2011) The Central Nervous System of Lungfishes

    In: Jørgensen JM, Joss J, editors. The Biology of Lungfishes. Enfield, USA: Science Publishers. pp. 393–445.

    https://doi.org/10.1016/B978-0-12-804042-3.00006-3

    • Google Scholar
48. 1. Oba S
    2. Sato M
    3. Takemasa I
    4. Monden M
    5. Matsubara K
    6. Ishii S

    (2003) A Bayesian missing value estimation method for gene expression profile data

    Bioinformatics (Oxford, England) 19:2088–2096.

    https://doi.org/10.1093/bioinformatics/btg287

    • PubMed
    • Google Scholar
49. 1. Pardo JD
    2. Huttenlocker AK
    3. Small BJ

    (2014) An exceptionally preserved transitional lungfish from the lower permian of Nebraska, USA, and the origin of modern lungfishes

    PLOS ONE 9:e108542.

    https://doi.org/10.1371/journal.pone.0108542

    • PubMed
    • Google Scholar
50. 1. Platt C
    2. Jørgensen JM
    3. Popper AN

    (2004) The inner ear of the lungfish Protopterus

    The Journal of Comparative Neurology 471:277–288.

    https://doi.org/10.1002/cne.20038

    • PubMed
    • Google Scholar
51. 1. Podani J
    2. Kalapos T
    3. Barta B
    4. Schmera D

    (2021) Principal component analysis of incomplete data – A simple solution to an old problem

    Ecological Informatics 61:101235.

    https://doi.org/10.1016/j.ecoinf.2021.101235

    • Google Scholar
52. 1. Qiao T
    2. Zhu M

    (2009) A new tooth-plated lungfish from the Middle Devonian of Yunnan, China, and its phylogenetic relationships

    Acta Zoologica 90:236–252.

    https://doi.org/10.1111/j.1463-6395.2008.00381.x

    • Google Scholar
53. 1. Ramcharitar JU
    2. Deng X
    3. Ketten DR
    4. Popper AN

    (2004) Form and function in the unique inner ear of a teleost: the silver perch (Bairdiella chrysoura

    The Journal of Comparative Neurology 475:531–539.

    https://doi.org/10.1002/cne.20192

    • PubMed
    • Google Scholar
54. 1. Sanchez S
    2. Fernandez V
    3. Pierce SE
    4. Tafforeau P

    (2013) Homogenization of sample absorption for the imaging of large and dense fossils with synchrotron microtomography

    Nature Protocols 8:1708–1717.

    https://doi.org/10.1038/nprot.2013.098

    • PubMed
    • Google Scholar
55. 1. Säve-Söderbergh G

    (1952) On the skull of Chirodipterus wildungensis Gross, an Upper Devonian dipnoan from Wildungen

    Kunglinga Svenska Vetenskapsakademiens Handlingar 6:1–29.

    https://doi.org/10.7717/peerj.5149

    • Google Scholar
56. 1. Schultze HP

    (1986) Dipnoans as sarcopterygians

    Journal of Morphology 190:39–74.

    https://doi.org/10.1002/jmor.1051900407

    • Google Scholar
57. 1. Schultze HP

    (1992) A new long-headed dipnoan (Osteichthyes) from the middle Devonian of Iowa, USA

    Journal of Vertebrate Paleontology 12:42–58.

    https://doi.org/10.1080/02724634.1992.10011430

    • Google Scholar
58. 1. Schultze HP

    (2010) A dipterid dipnoan from the Middle Devonian of Michigan, U.S.A

    Journal of Vertebrate Paleontology 2:155–162.

    https://doi.org/10.1080/02724634.1982.10011926

    • Google Scholar
59. 1. Sedgwick A
    2. Murchison RI

    (1828) On the structure and relations of the deposits contained between the primary rocks and the oolitic series in the north of Scotland

    Transactions of the Geological Society, London 2:125–160.

    https://doi.org/10.1144/transgslb.3.1.125

    • Google Scholar
60. 1. Sharp EL
    2. Clack JA

    (2013) A review of the Carboniferous lungfish genus Ctenodus Agassiz, 1838 from the United Kingdom, with new data from an articulated specimen of Ctenodus interruptus Barkas, 1869

    Earth and Environmental Science Transactions of the Royal Society of Edinburgh 104:169–204.

    https://doi.org/10.1017/S1755691013000479

    • Google Scholar
61. 1. Song CQ
    2. Chang MM

    (1991)

    Early Vertebrates and Related Problems of Evolutionary Biology

    Discovery of Chirodipterus (Dipnoi) from lower Upper Devonian of Hunan, south China, Early Vertebrates and Related Problems of Evolutionary Biology, Beijing, Science Press.

    • Google Scholar
62. 1. Spoor F
    2. Bajpai S
    3. Hussain ST
    4. Kumar K
    5. Thewissen JGM

    (2002) Vestibular evidence for the evolution of aquatic behaviour in early cetaceans

    Nature 417:163–166.

    https://doi.org/10.1038/417163a

    • PubMed
    • Google Scholar
63. 1. Spoor F
    2. Garland TJ
    3. Krovitz G
    4. Ryan TM
    5. Silcox MT
    6. Walker A

    (2007) The primate semicircular canal system and locomotion

    PNAS 104:10808–10812.

    https://doi.org/10.1073/pnas.0704250104

    • PubMed
    • Google Scholar
64. 1. Stacklies W
    2. Redestig H
    3. Scholz M
    4. Walther D
    5. Selbig J

    (2007) pcaMethods--a bioconductor package providing PCA methods for incomplete data

    Bioinformatics (Oxford, England) 23:1164–1167.

    https://doi.org/10.1093/bioinformatics/btm069

    • PubMed
    • Google Scholar
65. 1. Stensiö EA

    (1927) The Downtonian and Devonian vertebrates of Spitzbergen

    Skrifter Om Svalbard Og Nordishavet 12:1–31.

    https://doi.org/10.3402/polar.v14i1.6649

    • Google Scholar
66. Book

    1. Stensiö E

    (1963)

    The Brain and the Cranial Nerves in Fossil, Lower Craniate Vertebrates

    Skrifter utgitt av Det 1005 Norske Videnskaps-Akademi.

    • Google Scholar
67. Book

    1. Striedter GF
    2. Northcutt RG

    (2020) Brains Through Time

    New York: Oxford University Press.

    https://doi.org/10.1093/oso/9780195125689.001.0001

    • Google Scholar
68. 1. Walsh SA
    2. Knoll MA

    (2011) Directions in palaeoneurology

    Palaeontology 86:263–279.

    https://doi.org/10.1111/J.1475-4983.2011.01085.x

    • Google Scholar
69. 1. Wang S
    2. Drapala V
    3. Barwick RE
    4. Campbell KSW

    (1993) The dipnoan species, Sorbitorhynchus deleaskitus, from the Lower Devonian of Guangxi, China

    Philosophical Transactions of the Royal Society of London (Biol) 340:1–24.

    https://doi.org/10.1098/rstb.1993.0045

    • Google Scholar
70. 1. Yopak KE
    2. Lisney TJ
    3. Darlington RB
    4. Collin SP
    5. Montgomery JC
    6. Finlay BL

    (2010) A conserved pattern of brain scaling from sharks to primates

    PNAS 107:12946–12951.

    https://doi.org/10.1073/pnas.1002195107

    • PubMed
    • Google Scholar
71. 1. Yopak KE
    2. Lisney TJ
    3. Collin SP

    (2015) Not all sharks are “swimming noses”: variation in olfactory bulb size in cartilaginous fishes

    Brain Structure & Function 220:1127–1143.

    https://doi.org/10.1007/s00429-014-0705-0

    • PubMed
    • Google Scholar
72. 1. Yopak KE
    2. McMeans BC
    3. Mull CG
    4. Feindel KW
    5. Kovacs KM
    6. Lydersen C
    7. Fisk AT
    8. Collin SP

    (2019) Comparative Brain Morphology of the Greenland and Pacific Sleeper Sharks and its Functional Implications

    Scientific Reports 9:1–15.

    https://doi.org/10.1038/s41598-019-46225-5

    • PubMed
    • Google Scholar
73. 1. Zhu YA
    2. Giles S
    3. Young GC
    4. Hu YZ
    5. Bazzi M
    6. Ahlberg PE
    7. Zhu M
    8. Lu J

    (2021) Endocast and Bony Labyrinth of a Devonian “Placoderm” Challenges Stem Gnathostome Phylogeny

    Current Biology 31:1112–1118.

    https://doi.org/10.1016/j.cub.2020.12.046

    • PubMed
    • Google Scholar

Author details

1. Alice M Clement

   College of Science and Engineering, Flinders University, Adelaide, Australia

   Contribution

   Conceptualization, Data curation, Formal analysis, Funding acquisition, Investigation, Methodology, Visualization, Writing - original draft, Writing - review and editing

   For correspondence

   alice.clement@flinders.edu.au

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-0380-7347

2. Tom J Challands

   School of Geosciences, University of Edinburgh, Edinburgh, United Kingdom

   Contribution

   Conceptualization, Data curation, Investigation, Methodology, Visualization, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

3. Richard Cloutier

   Département de Biologie, Chimie et Géographie, Université du Québec à Rimouski, Rimouski, Canada

   Contribution

   Formal analysis, Methodology, Software, Writing - original draft, Writing - review and editing

   Competing interests

   No competing interests declared

4. Laurent Houle

   Département de Biologie, Chimie et Géographie, Université du Québec à Rimouski, Rimouski, Canada

   Contribution

   Formal analysis, Visualization

   Competing interests

   No competing interests declared

5. Per E Ahlberg

   Subdepartment of Evolution and Development, Department of Organismal Biology, Uppsala University, Uppsala, Sweden

   Contribution

   Conceptualization, Funding acquisition, Software, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9054-2900

6. Shaun P Collin

   School of Life Sciences, La Trobe University, Melbourne, Australia

   Contribution

   Funding acquisition, Writing - review and editing

   Competing interests

   No competing interests declared

7. John A Long

   College of Science and Engineering, Flinders University, Adelaide, Australia

   Contribution

   Funding acquisition, Software, Writing - review and editing

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-8012-0114

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