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.

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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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