A Late Devonian coelacanth reconfigures actinistian phylogeny, disparity, and evolutionary dynamics

Domain: earth_science
Published: 2024-09-12
Editorial outcome: minor_revision

Abstract
The living coelacanth Latimeria (Sarcopterygii: Actinistia) is an iconic, so-called ‘living fossil’ within one of the most apparently morphologically conservative vertebrate groups. We describe a new, 3-D preserved coelacanth from the Late Devonian Gogo Formation in Western Australia. We assemble a comprehensive analysis of the group to assess the phylogeny, evolutionary rates, and morphological disparity of all coelacanths. We reveal a major shift in morphological disparity between Devonian and post-Devonian coelacanths. The newly described fossil fish fills a critical transitional stage in coelacanth disparity and evolution. Since the mid-Cretaceous, discrete character changes (representing major morphological innovations) have essentially ceased, while meristic and continuous characters have continued to evolve within coelacanths. Considering a range of putative environmental drivers, tectonic activity best explains variation in the rates of coelacanth evolution.

Introduction
Coelacanths are evolutionarily unique, lobe-finned fishes that first appeared in the fossil record in the Lower Devonian Period (late Lochkovian, ~419–411 million years ago)1, with over 175 fossil taxa described throughout the Palaeozoic and Mesozoic eras. Since the discovery of Latimeria chalumnae by Western scientists in 1938, the phylogenetic relationships among coelacanths have been investigated in more than 20 studies (see Supplementary Text for full list). In most analyses, a good congruence exists between the phylogeny and the stratigraphic record. Coelacanths are considered to be morphologically conservative in terms of body plan2–7 and they achieved a peak of diversity during the Triassic6,8–11. Meanwhile, rates of morphological evolution have been examined stratophenetically12 and phylogenetically3,9,13, indicating that there was an early burst of evolution during the Devonian followed by a precipitous decrease and then a steady, low rate of morphological evolution. However, no driver has ever been proposed to explain these distinctive evolutionary dynamics of coelacanths, nor has their status as ‘living fossils’ been quantitatively evaluated.

Devonian coelacanth material is rare, representing only a small component of the ~175 fossil coelacanth species—there are only 20 known taxa, about half of which are too incomplete to describe formally. Their earliest fossils (Early Devonian) are known from mostly isolated bones from the late Lochkovian and Pragian of China1,14 and the mid–late Pragian of Australia15. Most Devonian coelacanths are rare and fragmentary, except for the middle Frasnian Miguashaia bureaui from eastern Canada16,17, and the late Famennian Serenichthys kowiensis18 based on juvenile specimens from South Africa. Until now, Diplocercides kayseri19 from Gerolstein in Germany is the only Devonian coelacanth known from three dimensions (3-D) and revealing part of the neurocranium, but it has since been destroyed by serial grinding. The material presented here, comprising two specimens (Fig. 1), represents the first-known coelacanth from the Late Devonian Gogo Formation of Australia20–25. Exceptional 3-D preservation of our specimens facilitates rare insight into the neurocranial, branchial, and palaeoneurological conditions of the group. These data also allow us to re-evaluate the phylogeny and phenotypic evolution of all coelacanths in detail, using an expanded character matrix, as well as the first geometric morphometric study of the group to our knowledge, and an analysis of putative drivers of evolutionary rates. Along with this description, such an expansive time series of detailed evolutionary patterns for a single taxon extending right up to the present offers an opportunity to determine the global processes steering evolution more generally.

Results
Systematic palaeontology
Osteichthyes Huxley 1880
Sarcopterygii Romer 1955
Actinistia Cope 1871
Ngamugawiwirngarri gen. et sp. nov.

Etymology. Generic name meaning “ancient fish” in Gooniyandi/Guniyandi, language of the First Nations people from Country around Fitzroy Crossing in the Kimberley region of Western Australia. Specific name is given in honour of respected Gooniyandi elder and ancestor Wirngarri, who lived in the Emanuel Range. Generic and specific names were both provided to Prof. John Long in September 2023, who has a longstanding and ongoing relationship with the community, with permissions to use the language granted by elder Rosemary Nuggett, on behalf of the Gooniyandi people of the Mimbi community.

Holotype. The holotype (WAM09.6.148; Figs. 1, 2) is a small but mostly complete skull (measuring just over 2 cm in length) with all dermal skull bones, an intact neurocranium, gill-arch skeleton, and pectoral girdle preserved in close articulation. The anterior section of the body is also present comprising many scales and vertebral arch elements, but the pectoral fin and its endoskeleton are missing.

Referred material. The paratype (NMVP231504; Figs. 1, 2) contains associated elements comprising two cleithra, the ventral portion of the basisphenoid and parasphenoid, and several isolated scales.

Locality and horizon. Canning Basin, in northern Western Australia, circa 100 km southeast of Fitzroy Crossing; Gogo Formation, early Frasnian, Late Devonian (~384–382 Ma). The holotype was found between Stromatoporoid Camp and Longs Well, the paratype was found in Paddys Valley (see map of Gogo fossil localities in figure 1 within ref. 23).

Diagnosis. Ngamugawiwirngarri gen. et sp. nov. is distinguished from all other coelacanths by the following apomorphies: jugal canal with prominent branches; large sensory pore openings between supraorbitals and parietals; teeth on parasymphysial tooth plate, but not on the dentary; prearticular and/or coronoid teeth rounded; cleithra and extracleithra with broad triangular anteroventral overlap for clavicle bearing a large ventral foramen; and scales with long ornamental ridges extending beyond the posterior margin of the base (Figs. 1, 2, Supplementary Fig. 1).

This published work and the nomenclatural acts it contains have been registered in ZooBank, the proposed online registration system for the International Code of Zoological Nomenclature (ICZN). The ZooBank LSIDs (Life Science Identifiers) can be resolved and the associated information viewed through any standard web browser by appending the LSID to the prefix “http://zoobank.org/”. The LSIDs for this publication are: B2B4AA94-E9A5-4D05-9724-CBE5B54760EA; 567A96D6-654A-4201-BFDB-0D81BBBF6226.

Description
The holotype (WAM09.6.148) was fossilised in an inter-reef palaeoenvironment with the dorsal surface of the skull roof in contact with the substrate, so that during decay the lower jaws and some cheek elements disarticulated, resting anterior to the skull, while the snout has collapsed inwards. The main block (part A) contains the complete skull including neurocranium, left mandible, cheek, pectoral girdle, and branchial elements, while the counterpart (block B) includes the parasphenoid and right-side mandibular ramus, operculum, entopterygoid, as well as a complete set of branchial arches. The specimen lacks the posterior portion of the body.

The well-preserved skull roof is ornamented with enamel-capped tubercles. The well-developed dorsal lamina of the premaxilla is pierced by a single large opening for the anterior tube of the rostral organ, which is diagnostic for coelacanths. There are paired parietals and postparietals partially fused in their anterior half, preparietals, and no pineal opening (Figs. 1, 2). The parietals and postparietals are approximately equidimensional in length each about 10 mm long (parietal length ÷ postparietal length = 0.8252; mean = 0.7824, n = 47 coelacanth species). The parietal/postparietal ratio varies greatly among Devonian coelacanths: ranging from 0.38 for Diplocercides kayseri26, 0.51 for Serenichthys kowiensis18, to 0.70 for Miguashaia bureaui17. The preorbital, orbital, and postorbital regions of the ethmoidal shield (parietonasal shield) make up 48%, 34%, and 18% of the total length of the shield, respectively, consistent with the proportions of “anatomically modern coelacanths” sensu Zhu et al.14 with elongate preorbital and orbital regions. There are six or seven supraorbitals preserved as in D. kayseri26; the posteriormost supraorbital corresponds most likely to a fusion of two or three elements. The supraorbital sensory canal passes through the sutures between the supraorbitals and the parietals, with 7–8 large pores opening through the skull roof highlighting its lyre-shaped course (Fig. 1). Narrow tabulars are fused to the postparietals.

Similar to other Devonian coelacanths (e.g., Gavinia, Miguashaia, Diplocercides), the cheek region of Ngamugawi is long compared to post-Devonian coelacanths. The postorbital, squamosal, preopercular, and lachrymojugal bones are arranged as in D. kayseri9,27 and Serenichthys18 in having the squamosal and preoperculum set atop one another, the postorbital farther anteriorly, and an elbow-shaped lachrymojugal expanded ventrally and bearing large, medial sensory pores as in D. kayseri. The sub-oval postorbital has a short orbital margin and bears six infraorbital sensory canal pores. Unlike the condition in Serenichthys, Gavinia, and post-Devonian coelacanths, whereby the postorbital anterior margin is long and curved to fit behind the orbit, in Ngamugawi the orbital margin is short as in D. heiligenstockiensis27 and M. bureaui17. The squamosal is sub-triangular and bears a vertical cheek pit line posteroventrally, and pores for the jugal and preopercular sensory canals. The preoperculum is trapezoidal, with four or five large pores of the preopercular canal, and abuts the squamosal ventrally, yet is separated from the lachrymojugal. The operculum bears a distinctive, strong ridge running anteroposteriorly through the bone, with a series of associated foramina likely to be the “epibranchial line” of Northcutt28 as in M. bureaui17.

The lower jaw of Ngamugawi is distinctive, with a long dentary (40% of the mandible length), a long splenial, a unique arrangement of coronoids, and lacking a dentary sensory pore (Fig. 2K–N). The dentary is unusually long compared to most other coelacanths (35% of the mandible length), but similar to the proportion of the dentary observed in the most primitive coelacanth Styloichthys (50%) as well as some Carboniferous taxa (e.g., Rhabdoderma elegans 40%; Caridosuctor populosum 43%; Allenypterus montanus 42%). Unique among coelacanths, Ngamugawi has a large, denticulated (not ‘toothed’, nor bearing ‘pointed teeth’) bone sutured medially to the dentary, which we interpret as a parasymphysial bone (Fig. 1G). Enlarged parasymphysials are also found in onychodontids and porolepiforms, so we propose that the specific position and elongation of this bone is a sarcopterygian synapomophy. There are three equidimensional coronoids, and an additional, enlarged principal coronoid. The angular bears an oral pit-line in its anterior half and some large sensory pores along its ventral margin. The prearticular bone lacks elongate ridges in its ventral portion. The glenoid fossa has a single posterodorsally facing facet, and the Meckelian bone bears an articulation point for the symplectic posteriorly. The left lateral gular is long and flat, only slightly shorter than the mandible as in most coelacanths. It has a small pit-line located posterior to the centre of the bone as in D. heiligenstockensis29 and Chagrinia enodis30.

The braincase of Ngamugawi is exceptionally well-preserved in 3-D (Figs. 1B, D, 2A–D, H–J), and is the best-preserved braincase known for a Palaeozoic coelacanth. Much of the braincase is well-ossified, preserving most of the ethmosphenoid and otico-occipital, with the unossified areas of the braincase where cartilage prevailed precisely matching the same regions of cartilage formation in Latimeria31. The braincase, cranial endocast, and palate bears many similarities to that of D. kayseri32. The interorbital cartilage is ossified. The processus connectens extends to the level of the antotic process and does not meet the parasphenoid. The antotic processes are large and teardrop-shaped, whereas the basipterygoid processes are smaller and knob-like. The occipital area appears to have been less-ossified than more anterior portions and might have been cartilaginous as in Latimeria33. The posterolateral wall of the otico-occipital bears a distinct, short otic process not seen in any other coelacanth, nor sarcopterygian. Two endolymphatic ducts face dorsally, opening through the endoskeletal cranial roof (Fig. 2E). The parasphenoid forms an elongate ‘spatulate’ outline as in Diplocercides17,34, with a gently rounded anterior margin and covered in a denticle field that ends abruptly posterior to the internal carotid foramen (Supplementary Fig. 2E–H). The parasphenoid is medially concave with an open buccohypophyseal canal. The entopterygoids are sub-triangular with a broad posterior flange as in other coelacanths. They are smooth laterally but ridged across most of their palatal surface.

The nasal capsules are shallow and rounded, situated in line with the cranial cavity as in many sarcopterygians (contra Latimeria). The general proportions of the rostral organ can be reconstructed from the position of the pore openings and by comparison with that of Latimeria33 (Fig. 2E–G). The olfactory tracts seemingly travelled through the large common anterior section of the endocranial cavity, rather than via separate olfactory tracts as in dipnomorphs and tetrapodomorphs. Canals for the optic nerves (n. II), oculomotor nerves (n. III), and trochlear nerves (n. IV) all exit the cranial cavity laterally. Those of the trochlear nerves travel just over a millimetre anterolaterally before meeting the superficial ophthalmic canals. The hypophysial fossa is short compared to that of juvenile and adult Latimeria specimens33. It extends anteroventrally as in that taxon but lacks an obvious posterior lobe as in Diplocercides kayseri32. There is no evidence of pineal or parapineal recesses. The endocast is narrow in the ethmosphenoid region but broadens from the level of the intracranial joint to reach its maximum width anterior to the labyrinths (Fig. 2E–G). Posterior to this, a large canal for the facial nerve (n. VII) exits the braincase laterally before splitting into three branches, and a canal for the auditory nerve (n. VIII) leads into the labyrinths.

The inner-ear region and the posterior portion of the endocast are more poorly ossified and were likely cartilaginous as in Latimeria33. Two long, open endolymphatic ducts are situated at the posterior of the skull roof. Anterior and posterior semicircular canals are preserved on the right-hand side of the specimen, and portions of the external semicircular canal and the sacculus are preserved on the left (Fig. 2E–G). The labyrinth region shows a large ampulla on the anterior semicircular canal, but the condition for the other two is unknown. The sacculus appears to have been large and deep as in Diplocercides, with the sinus superior not projecting above the cranial cavity dorsally.

Ngamugawi contains the best-preserved visceral skeleton of any Palaeozoic coelacanth (Supplementary Fig. 1G, H). While most of the visceral skeleton is preserved as a thin, ossified perichondral layer, we note an ossified hyomandibular is absent; we consider this due to it being cartilaginous as in Latimeria. The anterior end of the urohyal forms a single point, but the posterior bifurcation of the urohyal is pronounced as in most coelacanths. The single basibranchial has parallel lateral margins, and the ceratohyal is long and narrow. Five ceratobranchials are strongly curved and expanded proximally, while the epibranchials are triradiate, rod-like elements similar to those of Latimeria chalumnae.

Within the pectoral girdle, the cleithrum, extracleithrum, and clavicle form a prominent postbranchial lamina (Fig. 1E, G; Supplementary Fig. 1I). The cleithra are rounded dorsally, bear a ridged ornament, have a distinct anterior grove for the articulation of the operculum, and are partially fused with the broad extracleithrum (a synapomorphy of coelacanths). There is a broad, triangular anteroventral overlap between the extracleithrum and the clavicle. A large foramen lies on the visceral surface on the smooth overlap area for the clavicle lateral surface. The triangular clavicle is short as in Miguashaia. The sigmoid anocleithrum bears no ornament and has an anteriorly-pointed tip with an articular facet.

The scales are either teardrop-shaped, similar to Lualabaea or Caridosuctor35, or ovate, with a longitudinal, ridged enamel ornament. The spiny apices of the thicker ridges protrude from the posterior margin of the scales (Supplementary Fig. 1D); this feature seems to be unique to Ngamugawi among coelacanths. Lateral line scales have large pore openings. There are no bumps on the inner surface of the scales as for Miguashaia17,35.

Although the two specimens are small, they likely represent adults based on the presence of many fusions between bones, the degree of ossification of the branchial elements, and the degree of development of the scales.

Phylogenetic and Evolutionary Analyses
First, we evaluated the phylogenetic position of Ngamugawiwirngarri gen. et sp. nov. via Bayesian inference and maximum parsimony using an exhaustive and greatly expanded data matrix of 87 species (82 coelacanths and 5 onychodontiform outgroups) coded for 322 total characters (268 discrete, 14 meristic, and 40 continuous—see Supplementary Text for detailed description of all characters and analyses and Supplementary Fig. 3 for the position of the 88 landmarks for the 40 continuous characters). These matrices combine characters from 16 previous analyses including Forey’s9 classic matrix (some original characters have been deleted, split, or redefined; Forey’s matrix has been used in 20 analyses so far), in addition to 85 new characters. Autapomorphies (unique characters of terminal taxa) have been scored and coded. We double-checked all characters for each taxon, validating or invalidating previous coding. Both Bayesian inference (Fig. 3) and maximum parsimony (Supplementary Fig. 6) recover broadly congruent topologies: Ngamugawi is recovered as sister taxon to Gavinia, crownward of Miguashaia spp. and Holopterygius, and basal to Diplocercides and Serenichthys. Styloichthys is sister taxon to all other coelacanths.

Bayesian tip-dating revealed a striking uncoupling between rates of evolution of discrete, meristic, and continuous character types. The uncorrelated log-normal clock (which allowed all branches to have separate rates: Fig. 4) and the epoch clock (which constrained rates to be the same within time slices: Supplementary Fig. 6) retrieved similar patterns. We found that coelacanths experienced a rapid burst of morphological evolution with the highest rates occurring early in their history during the Devonian Period, but these rates then slowed substantially (with rare exceptions). Discrete characters, which often reflect evolutionary innovations, virtually stopped evolving after the Cretaceous (Fig. 4D); the substitution tree reveals Latimeria has undergone no more anagenesis than Cretaceous relatives, i.e. for discrete characters, it has indeed been frozen in evolutionary time. In contrast, meristic and continuous characters, which often reflect changes in proportions, have continued to evolve at typical Mesozoic rates (Fig. 4E-F). There are other instances of uncoupled rates of evolution for different character types: Holopterygius and Allenypterus exhibit fast rates for continuous and meristic changes, but unremarkable rates for discrete characters. These are explicable, e.g., Holopterygius and Allenypterus are unusually shaped coelacanths, but have retained most typical coelacanth traits.

Next, we constructed a resampled boosted regression tree analysis to identify the relative contribution of five putative palaeoenvironmental drivers to rates of coelacanth evolution: namely, subduction flux; continental flooded area (incorporating percentage of shallow sea); sea surface temperature; atmospheric CO2; and dissolved O2, (see Supplementary Information 3a) (Fig. 5). We used a combined rate of evolution, considering the discrete, meristic, and continuous characters, for each species (i.e., the rate associated exclusively to the species on the leading phylogenetic branch). The resampled final trees had high coefficients of variation (a measure of goodness of fit) ranging from 48% to 91%. Of the putative environmental drivers considered, the influence of subduction flux (a proxy of tectonic activity) was the most strongly associated environmental measure to the rate of evolution (median relative influence = 36%; range = 13–60%)—thus, indicating that coelacanth species evolved more rapidly during periods of higher global tectonic activity (Fig. 5B), suggesting that the creation of new habitats favoured rapid morphological evolution. The percentage of continental flooded area (Fig. 5C) had the next-highest explanatory power, albeit considerably lower than subduction flux (median relative influence = 24%; range = 2–46%). There was little support for a relationship between the remaining environmental drivers (atmospheric CO2, sea surface temperature, dissolved O2) and the rate of coelacanth evolution (Fig. 5).

Lastly, we evaluated disparity of coelacanth morphology using two approaches: (i) principal coordinates analysis (PCoA) applied to the discrete phylogenetic matrix (with missing data for each coelacanth species reconstructed using parsimony), and (ii) principal component analysis (PCA) of the 2-D geometric morphometrics to analyse shape of the body, lower jaw, and cheek (Fig. 6; Supplementary Fig. 7). Variation in body shape and lower jaw are conservative2,3,9, while the cheek region is more variable among species (or disparate)3,9,36.

For the principal coordinates analysis of discrete characters, we recovered a profound shift in overall disparity between Devonian and all post-Devonian coelacanths, but the highest disparity (discrete) during the Devonian and Triassic (Fig. 6A; Supplementary Fig. 8A). Again, Latimeria appears to have moved little outside the morphospace of its closest Mesozoic relatives, despite having an additional 66 million years to evolve, consistent with the stasis for discrete characters found in the tip-dated phylogenetic analyses.

For the principal component analysis of overall body shape (Fig. 6B; Supplementary Fig. 8B), the Devonian Miguashaia bureaui, the Carboniferous Allenypterus montanus, and the Triassic Foreyia maxkuhni are three outliers highly modified in body shape compared to the generalised coelacanth body type, accounting for approximately 35% of the total variation. A second source of body-shape variation considers the discrepancies associated with the heterocercal and triphycercal caudal fins (Supplementary Fig. 9A). A major shift of disparity occurred between Devonian and post-Devonian species. Latimeria is positioned away from its closest Mesozoic relatives, again consistent with the lack of stasis found for continuous (shape) characters in the tip-dated phylogenetic analyses. The disparity in the cheek region offers a distinct pattern of temporal evolutionary disparity. Two temporal shifts characterized the cheek disparity (Fig. 6C; Supplementary Fig. 8C): one post-Devonian (narrowing of the cheek, Supplementary Fig. 9B) and the second between the Triassic and Jurassic (deepening of the cheek, Supplementary Fig. 9B). The disparity of the cheek region is greater than that of body shape and lower jaw, while the disparity of the lower jaw is slightly greater than that of the body shape and shows a relatively constant temporal overlap (Fig. 6D, Supplementary Fig. 10).

Methods
Material
Both specimens were collected during the 2008 Museum Victoria Gogo Expedition led by JAL and funded by the Australian Research Council. Landowners and leaseholders gave permission to do field work, and no additional permits were required under the Lands Administration Act. The specimens are registered in the collections of the Western Australian Museum as WAM 09.6.148 (holotype) and Museum Victoria as NMV P231504 (paratype). David Pickering and John A. Long (MV) extracted the specimens from their limestone matrix using repeated 10% acetic acid baths, with newly exposed bones strengthened with Paraloid/Mowital B30 in ethanol. JAL dusted specimens with a sublimate of ammonium chloride prior to photography and drew illustrations using a camera lucida.

Computed tomography
We were granted permission to CT scan the material by Rosemary Nuggett, on behalf of the Gooniyandi people of the Mimbi community, and Mikael Siversson of the Western Australian Museum. We imaged part and counterpart (parts A & B) of the holotype WAM 09.6.148 at the Australian National University (ANU) X-ray Micro-CT Laboratory. Later, we (re)imaged the holotype (part A) and the paratype MVP 231504 at the Adelaide Microscopy CT Facility (University of Adelaide) on a Skyscan 1076 X-ray microtomography scanner using the following parameters: holotype, 74 kV; 135 μA; 0.5 mm aluminium (Al) filter; 360° rotation at 0.4° increments; frame averaging = 2; 2.4 second acquisition time; and paratype, 100 kV; 70 μA; 1.0 mm aluminium (Al) filter; 360° rotation at 0.4° increments; 3 frames/rotation; 4.1 second acquisition time. The resultant pixel size for the initial holotype scan was 150 μm, the paratype was 9 μm, and the holotype (part a) rescan was 17 μm. We reconstructed the resultant 16-bit depth TIFF images using the Skyscan NRecon software (Bruker microCT, Belgium), after which we completed 3-D segmentation and rendering using Mimics v.19.0 (biomedical.materialise.com/mimics; Materialise, Leuven, Belgium). Skull reconstruction was done in 3-matic (Materialise, Leuven, Belgium), and animations assembled using Adobe Premier Pro. Scan data and all resulting 3-D models (STLs) and animations are available via MorphoSource (www.morphosource.org/projects/000485769?locale=en), as well as the Github repository github.com/cjabradshaw/CoelacanthEvolution/.

Phylogenetic analyses
To assess the phylogeny, we compiled three phylogenetic matrices for 82 coelacanth species and five onychodontiform outgroups containing 268 discrete, 14 meristic, and 40 continuous characters (see Supplementary Information for detailed description of all characters). Detailed description of the characters, states, scores and sources is provided in the supplementary information. We applied Bayesian (BEAST2) and maximum parsimony analyses (TNT) to create a newly proposed phylogeny. The discrete matrix is available on MorphoBank (Project 3471), the meristic and continuous characters are available at https://doi.org/10.5281/zenodo.8054092.

Bayesian tip-dated analyses. We were performed Bayesian tip-dated analyses using BEAST 1.10.539 (BEAST2 currently cannot accommodate continuous traits with missing data). The data were explicitly gathered to satisfy the assumptions of tip dating, namely sampling all variable traits, including autapomorphies (see Supplementary Information). The most appropriate available tree prior was the birth-death serial-sampling model (BDSS40); the alternative SABD tree prior is only available in BEAST241. The optimal evolutionary histories that explain the discrete, meristic and continuous traits, as well as stratigraphic dates, were inferred using Markov-chain Monte Carlo (MCMC) approaches, as implemented in BEAST. The executable XML files, with annotations describing model, prior, MCMC run and logging settings, and R scripts, are available in Github https://github.com/cjabradshaw/CoelacanthEvolution. Four runs of all analyses were conducted, with run lengths and burnin confirmed as adequate for convergence using Tracer42; the post-burnin samples of all 4 runs were then combined and summarised using post-processing BEAST modules LogCombiner and TreeAnnotator43 as well as R scripts available in scripts/evolrate using libraries disparity44, phytools45, phylotate46 and geoscale47.

Tip calibrations were employed using the full stratigraphic range (including uncertainty) for each species; taxa from the same deposit were constrained to co-vary in age by putting a tight (exponential) prior on their age variance (cf48). The maximum root age was unconstrained, but there was an exponential prior putting 95% of probability distribution between the oldest sampled fossil (412.15 Ma) and the oldest unequivocal sarcopterygians (418 Ma). Trees were rooted with five onychodontiform outgroup taxa.

Discrete morphological characters were analyzed using the Mkv-model which corrects for non-sampling of constant characters49. Multistate characters that formed clear morphoclines (characters 1, 2, 6, 8, 10, 15-16, 23, 26, 36, 53, 60, 74, 76, 97, 100, 110, 112, 135, 137, 208, 218, 224, 227, 240, and 258) were treated as ordered; others were treated as unordered. Among-character rate variation was modelled using the gamma parameter50. A state-partitioned model was employed, with substitution rates scaled by state number to correct for state (= base) frequencies (see King et al.51).

Meristic characters were analyzed using a high-state ordered Mk-model. Essentially, meristic characters were treated as ordered multistate characters with very large numbers of states, the possible states being the minimum observed value, the maximum observed value, and all intervening whole numbers. Changes between any two states were constrained to pass through all intervening values (states). The large number of states for some characters required the use of unorthodox state labels, which are detailed in the Supplementary Information.

Continuous characters were log-transformed (to base 10) to reduce heteroscedasticity where relevant (highly right-skewed). The transformed data were then analysed using Brownian motion models implemented in BEAST52, with the average evolutionary rate (i.e., variance) for each continuous character estimated separately.

Rate variation across the tree was modelled using two different clock models; in the main analyses, rate variation was estimated separately for the discrete, meristic and continuous characters to test for concordance in patterns.

Uncorrelated lognormal (UCLN) relaxed clock. This clock model assumes rates vary independently across branches, with the values approximating a lognormal distribution with variance estimated from the data53. To achieve convergence, these analyses had to be performed using MC3 methods (4 chains, delta 0.08). The dated tree from this clock model is shown in Fig. 3, along with the estimated rates of discrete, meristic and continuous characters across time (in Fig. 4 and Supplementary Fig. 5).

For testing correlates of evolutionary rates, where it was desirable to have a single rate value for all 3 types of traits, the UCLN relaxed clock analysis was repeated with discrete, meristic and continuous data modelled under a single (i.e., linked) clock.

Epoch clock. This clock model assumes rates vary independently across time slices, but rates in all branches within each time slice are the same54. Branches spanning multiple time slices are allocated multiple rates (i.e., the segment of branch within time slice a is allocated the rate for time slice a, etc.). Seven epochs were employed: Devonian (and earlier), Carboniferous, Permian, Triassic, Jurassic, Cretaceous, and Tertiary. The rates of evolution for discrete, meristic, and continuous characters across the seven epochs is shown in Supplementary Fig. 5.

Parsimony analyses. Parsimony analyses used TNT55 included the discrete, meristic and continuous characters (scaled to the same weight as binary characters), without group and ordering assumptions as above. In order to remove negative log values (unreadable by TNT), all continuous characters had +2 added; the magnitude of the addition makes no difference under parsimony. Searches involved 1000 TBR replicates holding 100000 trees at each step. The strict consensus tree was calculated for all taxa, and with the three most unstable taxa pruned56 (Supplementary Fig. 6). Clade support was calculated using 200 bootstrap replicates. The executable TNT files are in Github at https://doi.org/10.5281/zenodo.8054092.

Boosted regression trees
We also built boosted-regression trees to test the relationship between rate of coelacanth evolution and five putative environmental drivers, namely subduction flux57, continental flooded area (combined with percentage of shallow seas)58,59, sea surface temperature57, dissolved O260 atmospheric CO261 (see Supplementary Information for data collection for these parameters) to account for potential nonlinearity in the relationships. We hypothesised that the rate of evolution would increase within relatively higher concentrations of dissolved O2 given its suggested role in the evolution of animal life during the Phanerozoic62 (but see Schachat63,64). We further hypothesised that variation in atmospheric CO2 might have influence coelacanth evolution given its role in modifying climate65 and the flow of trophic energy through ecological networks66. We predicted that relatively higher sea surface temperatures would indicate higher rates of coelacanth evolution given the positive influence of temperature on poikilotherm metabolism67. Finally, we predicted that increasing subduction flux57, a measure of relative tectonic activity, would facilitate episodes of biogeographic differentiation and influence patterns of speciation65,68 through the exploitation of novel niches, and that a higher percentage of shallow seas globally would provide more opportunity for evolution since most coelacanth species have been discovered mainly in marine and estuarine palaeoenvironments9,69,70.

We also accounted for potential phylogenetic non-independence and temporal autocorrelation by resampling the dataset 1000 times using the following procedure: (i) we constructed a temporal vector of ages by Gaussian-resampling the mean and standard deviation of the intervals between fossil appearance periods (based on the first and last appearances) using one-third of the calculated standard deviation and removing the negative intervals; (ii) for each resampled temporal sequence, we determined which species appeared within the sequence points (again, based on first and last appearances), (iii) for each of the species within the resampled sequence, we resampled a random uniform value for each putative environmental driver between its maximum and minimum, and (iv) we transformed, centred, and scaled the extracted environmental values using the scale function in R. For each of these 1000 resampled datasets, we ran a boosted regression tree emulator to predict the rate of coelacanth evolution (scaled, centred, log-transformed itself to produce a Gaussian-liked distribution) from the scaled environmental variables using a learning rate = 0.0003, tolerance = 0.00005, error family = Gaussian, bag fraction = 0.75, tree complexity = 2, and maximum number of trees = 1,000,000 in the function gbm.step from the dismo R library71. For each of the 1000 iterations, we retained the coefficient of variation as a measure of goodness of fit, the relative influence of each environmental variable, and the predicted relationship between scaled rate of evolution and each scaled environmental variable, from which we estimated 95% confidence limits using the quantile function in R. However, we also applied a kappa (κ) limitation to the resampled selections to limit the influence of outliers72, where we retained only the resampled mean ranks within κσ of the overall average mean (κ = 2). We then recalculated the average and standard deviation of the mean rank, with the process repeated five times. All data and R code necessary to run this procedure are available at Github https://doi.org/10.5281/zenodo.8054092.

Disparity analyses
We evaluated coelacanth morphological disparity using two approaches. (i) We used a matrix of discrete characters (268 characters for 82 coelacanth species excluding outgroups) to explore morphological disparity based on Gower’s coefficient73. We plotted the morphospaces for taxa in seven time-bins: Devonian, Carboniferous, Permian, Triassic, Jurassic, Cretaceous, and extant. The first two axes of the principal coordinates analysis explained 42.01% and 11.30% of the variation, respectively (Fig. 6A). (ii) We did 2-D geometric morphometric analyses of body shape, lower jaw, and cheek region for taxa that included the relevant information. We digitized 2-D landmarks with tpsDig2 v.2.3274 on reconstructions of coelacanths previously verified and corrected when needed. We did three separate analyses to optimize both the number of landmarks and species in each analysis. We digitized 14 2-D landmarks on 35 species to describe the lateral body outline and relative positions of the fins, 17 2-D landmarks on 34 species to capture the shape of the cheek, and seven 2-D landmarks on 38 species to describe the shape of the lower jaw (see Supplementary Information Table 2.1 for a detailed description of the landmarks). We rotated, scaled, and translated landmark coordinates with a Procrustes superimposition using the function gpagen in the R package geomorph v.4.0.175. We constructed morphospaces based on the two first axes of the principal component analyses. (iii) We calculated Procrustes variance for each time-bin using the function morphol.disparity in the package geomorph. All data and R code necessary to repeat disparity analyses are available at Github https://doi.org/10.5281/zenodo.8054092.

Peer review rounds
[{"round": 1, "reviewer_comments": {"reviewer_1": "This is a very important contribution to the understanding of the evolutionary pattern of coelacanths, on the basis of an exceptionally comprehensive dataset of coelacanths, which will form a new start for the follow-up dataset construction to resolve the relationships and interrelationships of coelacanths. The extensive analyses of this dataset using various methods provide some new insights into the coelacanth evolution relating to the environmental changes, although some links are weak or rather tentative. The new fossil also provides valuable anatomical data to the early coelacanths, eventually impacting on the character evolution of early coelacanths, the evolution of neurocranial features in particular. As such, I recommend it to be published in NC after revisions.\nIn overall, the manuscript is well written. However, some figures should be greatly improved to meet the standards of the journal. Text-figures 1 and 2 are fine, but the rest should be well edited. For instance, the taxon name (genus and species) in Figure 3 should be in italics (not just copied from the analysis). The silhouettes in Figure 5 should have some interpretations, which species, to which dot.\nThe connection between the two topics (new taxon, evolutionary dynamics) is not clearly demonstrated. In the present form, this connection is not tight. I can download the TNT file from Github, but the zip file seems broken (better avoid uploading the zip file). Thus I cannot run the file independently. It will be interesting to compare the phylogenetic results with and without the new taxon. Also are there any influences from the continuous characters? All these analyses will potentially help to understand the contribution of the new taxon to evolutionary dynamics.\nThe anatomical description well stands, but the identification of the so-called ‘parasymphysial’ deserves re-consideration. The denticulated band more looks like a part of the dentary. The groove on the surface of the mandible should be carefully examined on all the available mandible specimens (more photos?). Even if this so-called ‘parasymphysial’ is true, ‘the specific position and elongation’ should be an autapomorphy of this taxon, not “a sarcopterygian synapomophy”.\nTiny points:\nl.47: Is it necessary to say, “by western science”? How to define ‘western science’?\nl.60-61: If you regard Styloichthys as a basal coelacanth, the described specimens are not the isolated bones.\nl.124: data sources or details (in SI?).\nl.179: oticcoccipital (typo error)\nl.220: branchial lamina or postbranchial lamina?", "reviewer_2": "I can only congratulate the authors on a well-written article and conclusions that make a significant contribution to the knowledge of the evolution of coelacanths. A formal note to be considered for include is related to the list of all taxa mentioned and discussed in the supplementary information. There is missed a mention of the occurrence of well-preserved and equally well-dated Diplocercides fossils from the Upper Devonian of the Holy Cross Mountains described in the paper:\nSZREK, P. 2007. coelacanths (Actinistia, Sarcopterygii) from the Famennian (Upper Devonian) of Kadzielnia Chain, Holy Cross Mountains, Poland. Acta Geologica Polonica, 57, 403-413.\nWhile these are not remains that would force a significant change in the overall account of the reviewed paper, they would make this one article cover all the remains of representatives of this group described so far in the palaeogeographical area, which is transitional between the East European platform (Latvia) and Germany, where Stensio (1937) described the genus DIplocercides for the first time.\nFor the rest of the manuscript and supplementary information I have no comments. It is a valuable work and, in my opinion, will find interest among a large group of vertebrate palaeontologists.\nRegards,\nPiotr Szrek", "reviewer_3": "Clement et al. produce a very interesting manuscript describing a new species from Gogo and generally attempting to track rates of evolution across the clade. It is obvious a lot of effort went into this, including the formulation of 85 new characters, construction of a morphospace, and testing relationships between environmental variables. The descriptions and tree seem solid. However, some of the choices of methods and variables are a bit odd, which affects whether the results of the rate and environmental analyses support the main assertions of the authors. It also seems like some of the analyses are unrelated or extraneous.\nFirst, it is not clear whether subduction flux/tectonic actually approximates the production of new habitat area as originally described by Marcilly et al. During the Devonian, as Pangaea was formed, this would have been mostly creation in the deep sea (which the sampled coelacanths did not inhabit) as Pangaea came together and destroyed shallow water environments and increased cosmopolitanism (see work by Alycia Stigall). It seems like a better parameter for testing the hypothesis is Marcilly et al.’s “Flooded land area”, which represents the shallow sea habitats available. This can also be separated out by region/latitude (since they do it for exposed land in their Fig. 3). This might be the same as shallow seas, but with a more exact calculation than using paleomaps. Another option would be to calculate separate environments. In any case, my guess is that there would be a negative correlation between new habitat and coelacanth diversity during the formation of Pangaea.\n2. Figure 4 is hard to interpret in light of the description of the method in text and the caption. How was the relative influence of each parameter inferred?\n3. If I understand correctly, the values for environmental variables were assigned to taxa based based on a random draw from the range of potential values at that time. This introduces a lot of noise. Wouldn’t it be better to try to get values for more specific variables like sea surface temperature, latitude, habitat, etc from the exact sites where these species originated, rather than depending on global variables with high uncertainty?\n4. While it is interesting that modern coelacanths do not show additional changes in discrete characters versus meristic characters, is this not an outcome of character selection focused on Devonian forms and small sample size? Is there anything which might distinguish modern coelacanths from their Mesozoic relatives, which might have been included as an 86th new character? I do not doubt modern/late Mesozoic coelacanths show less disparity than Devonian forms, but is seems like the rate estimations are unnecessary to assert this. There is one species on a long branch, belonging to the same clade as Mesozoic forms.\n5. Why were rates of evolution in morphospace (based on scores) not calculated?\n6. Why were continuous and meristic characters used to construct the tree rather than be used to estimate rates of diversification? I would like to see a estimate of change in these characters from a tree only constructed from discrete characters, given there is some change in modern coelacanths.\nOverall, this paper has a lot of good pieces, but it not clear how they come together, or if the main results are supported by the relevant analyses. I do believe it is worth fixing however."}, "author_response": "Reviewer #1 (Remarks to the Author):\nThis is a very important contribution to the understanding of the evolutionary pattern of coelacanths, on the basis of an exceptionally comprehensive dataset of coelacanths, which will form a new start for the follow-up dataset construction to resolve the relationships and interrelationships of coelacanths. The extensive analyses of this dataset using various methods provide some new insights into the coelacanth evolution relating to the environmental changes, although some links are weak or rather tentative. The new fossil also provides valuable anatomical data to the early coelacanths, eventually impacting on the character evolution of early coelacanths, the evolution of neurocranial features in particular. As such, I recommend it to be published in NC after revisions.\n* In overall, the manuscript is well written. However, some figures should be greatly improved to meet the standards of the journal. Text-figures 1 and 2 are fine, but the rest should be well edited. For instance, the taxon name (genus and species) in Figure 3 should be in italics (not just copied from the analysis). The silhouettes in Figure 5 should have some interpretations, which species, to which dot.\nAUTHOR RESPONSE: we wholeheartedly agree. Several of the figures were indeed not publication quality, but this was due to their inclusion within text only for the review process. We have now updated and/or expanded several figures, and provided high resolution and high-quality versions of all figures. Regarding the specific requests, we have added lines in Figure 5 to the relevant silhouettes. Additionally, we added Supplementary Figures 4 and 10 with the identification of all the silhouettes (complete body shape, cheek region and lower jaw). In addition, the original reference from which the silhouettes were made are provided in the respective figure captions.\n* The connection between the two topics (new taxon, evolutionary dynamics) is not clearly demonstrated. In the present form, this connection is not tight. I can download the TNT file from Github, but the zip file seems broken (better avoid uploading the zip file). Thus I cannot run the file independently.\nAUTHOR RESPONSE: Firstly, it is not only the description of a new taxon that prompted us to investigate evolutionary dynamics necessarily, but rather the macroevolutionary study of all described coelacanths. The description of the best-preserved 3D Devonian coelacanth prompted us to re-examine the whole coelacanth group in firstly aiming to place the new taxon phylogenetically, and secondly examine rates of evolution of e.g. Devonian vs post-Devonian forms. Taxonomic structure underpins the documentation of rates of lineage origination and is therefore central to understanding the dynamics of diversification at a macroevolutionary scale.\nSecondly, the GitHub files have since been updated.\n* It will be interesting to compare the phylogenetic results with and without the new taxon. Also are there any influences from the continuous characters? All these analyses will potentially help to understand the contribution of the new taxon to evolutionary dynamics.\nAUTHOR RESPONSE: Text added to SI: “To test the effects of Namugawi on tree topology, we repeated both the Bayesian and parsimony searches with Namugawi excluded. In both cases, the similar topological changes were observed. With the inclusion of Namugawi, both this taxon and Gavinia group as sister taxa, positioned crownward of basal coelacanths (Styloichthys, Miguashaia, Holopterygius). However, when Namugawi is excluded, Gavinia falls more basally, at the same grade as Miguashaia and Holopterygius. The parsimony results are shown in Fig S3; the Bayesian results were similar. The difference in the position of Gavinia in the tree topology with and without Namugawi is in part related to the percentage of missing data: Gavinia has 69%, whereas Namugawi has 21% of missing data. For those characters coded for both species, there are 9 characters that differ in the condition. The main differences that bring Gavinia closer to Miguashaia are the characters related to the condition of the caudal fin and more specifically the interlocking segmentation of the lepidotrichial segments. Most postcranial characters are unknown in Namugawi.\n* The anatomical description well stands, but the identification of the so-called ‘parasymphysial’ deserves re-consideration. The denticulated band more looks like a part of the dentary. The groove on the surface of the mandible should be carefully examined on all the available mandible specimens (more photos?). Even if this so-called ‘parasymphysial’ is true, ‘the specific position and elongation’ should be an autapomorphy of this taxon, not “a sarcopterygian synapomophy”.\nAUTHOR RESPONSE: Because the specimen is perfectly preserved in 3-D and we have imaged it with a micro-CT scanner, we can see this feature clearly and without ambiguity. We show this clearly in the illustrations (Fig. 2 K,L,M) that there is a separate toothed element sitting on top of the dentary (which is toothless), and this can be examined closely by the reader by accessing the CT segmentations online via Morphosource. We have included an additional photograph and CT cross section in SI Fig J, K, to show this condition more clearly.\nIncidentally, this feature is also corroborated on Diplocercides kayseri where we have examined the Holotype specimens studied by Erik Stensiö based on new casts obtained from the Natural History Museum in Berlin (still on loan to us). This means the small bone is topographically in the same position as the parasymphysial bone in all other sarcopterygians. It differs only in being slightly larger. We stand by our identification, as this is the most parsimonious explanation for the toothed bone on top of the dentary (is that it is a parasymphysial plate).\n* Tiny points:\nl.47: Is it necessary to say, “by western science”? How to define ‘western science’?\nAUTHOR RESPONSE: We have amended this to “western scientists” in the updated manuscript. We are using this language so as not to erase local and indigenous knowledge of this animal prior to it’s “discovery” in 1938.\nl.60-61: If you regard Styloichthys as a basal coelacanth, the described specimens are not the isolated bones.\nAUTHOR RESPONSE: We added the word “mostly” here so to avoid the ambiguity about the completeness of Styloichthys specimens.\nl.124: data sources or details (in SI?).\nAUTHOR RESPONSE: We have now added in the relevant citations here.\nl.179: oticcoccipital (typo error)\nAUTHOR RESPONSE: Corrected to “otico-occipital”.\nl.220: branchial lamina or postbranchial lamina?\nAUTHOR RESPONSE: Corrected to “postbranchial lamina”\n\nReviewer #2 (Remarks to the Author):\nI can only congratulate the authors on a well-written article and conclusions that make a significant contribution to the knowledge of the evolution of coelacanths.\nA formal note to be considered for include is related to the list of all taxa mentioned and discussed in the supplementary information. There is missed a mention of the occurrence of well-preserved and equally well-dated Diplocercides fossils from the Upper Devonian of the Holy Cross Mountains described in the paper:\nSZREK, P. 2007. coelacanths (Actinistia, Sarcopterygii) from the Famennian (Upper Devonian) of Kadzielnia Chain, Holy Cross Mountains, Poland. Acta Geologica Polonica, 57, 403-413.\nWhile these are not remains that would force a significant change in the overall account of the reviewed paper, they would make this one article cover all the remains of representatives of this group described so far in the palaeogeographical area, which is transitional between the East European platform (Latvia) and Germany, where Stensio (1937) described the genus DIplocercides for the first time.\nFor the rest of the manuscript and supplementary information I have no comments. It is a valuable work and, in my opinion, will find interest among a large group of vertebrate palaeontologists.\nRegards,\nPiotr Szrek\nAUTHOR RESPONSE: The coelacanth from Holy Cross Mountain is highly incomplete, but we are able to comment about the anterior part of the lower jaw. We have included this important reference in the section concerning the morphology of Diplocercides kayseri in our Supplementary Information. We also cited Szrek (2007) with regard to the condition of the dentition associated with the dentary (character 116).\n\nReviewer #3 (Remarks to the Author):\nClement et al. produce a very interesting manuscript describing a new species from Gogo and generally attempting to track rates of evolution across the clade. It is obvious a lot of effort went into this, including the formulation of 85 new characters, construction of a morphospace, and testing relationships between environmental variables. The descriptions and tree seem solid. However, some of the choices of methods and variables are a bit odd, which affects whether the results of the rate and environmental analyses support the main assertions of the authors. It also seems like some of the analyses are unrelated or extraneous.\n1. First, it is not clear whether subduction flux/tectonic actually approximates the production of new habitat area as originally described by Marcilly et al. During the Devonian, as Pangaea was formed, this would have been mostly creation in the deep sea (which the sampled coelacanths did not inhabit) as Pangaea came together and destroyed shallow water environments and increased cosmopolitanism (see work by Alycia Stigall). It seems like a better parameter for testing the hypothesis is Marcilly et al.’s “Flooded land area”, which represents the shallow sea habitats available. This can also be separated out by region/latitude (since they do it for exposed land in their Fig. 3). This might be the same as shallow seas, but with a more exact calculation than using paleomaps. Another option would be to calculate separate environments. In any case, my guess is that there would be a negative correlation between new habitat and coelacanth diversity during the formation of Pangaea.\nAUTHOR RESPONSE: We have now included the Marcilly et al. (2022) ‘continental flooded area’ variable into the boosted regression tree analysis, combined with area of shallow seas. The addition has not changed our conclusion, only the relative contribution of said variables.\n2. Figure 4 is hard to interpret in light of the description of the method in text and the caption. How was the relative influence of each parameter inferred?\nAUTHOR RESPONSE: We have now added the following text to the Methods describing the boosted regression trees:\n“To assess the relative effect of each putative environmental driver on the rate of coelacanth evolution, we calculated the boosted-regression tree metrics of relative influence (Prowse et al. 2016). Relative influence I is the contribution of the individual drivers xj on the variation of the function F (̂ x). The latter is the function that maps the explanatory variables x to the response variable y. For a collection of M decision (regression) trees {T_m }_1^M, the squared influence I ^̂ 2 is:\nI ^̂ 2=1/M ∑_(m=1)^M▒〖I _̂ j^2 (T_m ) 〗,\nwhere I _̂ j^2 (T)=∑_(t=1)^(J-1)▒〖i _̂ t^2 (v_t=j) 〗, which is the sum over the nonterminal nodes t of the J-terminal node tree T, vt = the splitting variable associated with node t, and i ̂_t^2 = the corresponding empirical improvement in squared error resulting from the split (Friedman 2001 ). These squared influences sum to 100 over all x explanatory parameters, analogous to the percentage of variation in the response variable y explained by each parameter.”\n3. If I understand correctly, the values for environmental variables were assigned to taxa based on a random draw from the range of potential values at that time. This introduces a lot of noise. Wouldn’t it be better to try to get values for more specific variables like sea surface temperature, latitude, habitat, etc from the exact sites where these species originated, rather than depending on global variables with high uncertainty?\nAUTHOR RESPONSE: This is an interesting idea, but we are attempting to explain global drivers of evolution among all taxa, so assuming that localised conditions per specimen represented the global conditions experienced by all individuals of that species across its entire global range at any given time potentially biases the results taphonomically. Even if we had local-scale measurements of the environmental variables (most are not available at the site scale), we would risk biasing our outcomes to the best-sampled species.\n4. While it is interesting that modern coelacanths do not show additional changes in discrete characters versus meristic characters, is this not an outcome of character selection focused on Devonian forms and small sample size? Is there anything which might distinguish modern coelacanths from their Mesozoic relatives, which might have been included as an 86th new character? I do not doubt modern/late Mesozoic coelacanths show less disparity than Devonian forms, but is seems like the rate estimations are unnecessary to assert this. There is one species on a long branch, belonging to the same clade as Mesozoic forms.\nAUTHOR RESPONSE: Our character selection explicitly tried to sample all variable discrete characters, including autapomorphies, and was not focused on only characters that varied in Devonian forms. As an example, we include characters such as 256 and 265, where the derived states are exclusively found in post-Devonian forms, and characters such as 48, 185, 220 and 249(1), where the derived states are restricted to single terminal taxa. We are confident the relative lack of change (in discrete characters) between modern and Cretaceous coelacanths is a genuine pattern rather than an artefact of character selection.\n5. Why were rates of evolution in morphospace (based on scores) not calculated?\nAUTHOR RESPONSE: We made an a priori decision to keep the phylogenetic and disparity analyses as independent data sets and independent sources of evidence. However, in order to respond to Reviewer 3, we have done the analysis of evolutionary rates using the morphospace data. We used “compare.evol.rates” in the package geomorph (version 3.0.4) performed in R to evaluate the rates per geological period for the three morphological systems. We used the main topology of the Bayesian analysis (saved as NERWICK format).\nPlease find below the data as well as a graphic of the evolutionary rates through time for the postcrania, cheek region and lower jaw.\nPostcranial Cheek Jaw\nDevonian 0,00000996 0,0000404 0,0000322\nCarboniferous 0,0000335 0,00005 0,0000512\nPermian 0,00000809 0,0000514 0,0000157\nTriassic 0,0000194 0,0000303 0,0000396\nJurassic 0,00000607 0,0000181 0,0000307\nCretaceous 0,00000395 0,0000206 0,000022\nExtant 0,0000109 0,00000587 0,0000932\nResults of this analysis show similar trends as we presented in the evaluation of the morphological disparity using the sums of variances provided in Supplementary Figure 10. Thus, we still maintain our original idea to not include this analysis in our paper.\n6. Why were continuous and meristic characters used to construct the tree rather than be used to estimate rates of diversification? I would like to see a estimate of change in these characters from a tree only constructed from discrete characters, given there is some change in modern coelacanths. Overall, this paper has a lot of good pieces, but it not clear how they come together, or if the main results are supported by the relevant analyses. I do believe it is worth fixing however.\nAUTHOR RESPONSE: The topology from discrete only is very poorly resolved due to high levels of missing data and low character number, especially for parsimony, so this hasn’t produced a strong result in the past. Nevertheless, the vast majority of characters are in fact discrete characters (268 discrete versus 14 meristic and 40 continuous).\nIn any case, due to the large amount of missing data generated by our high taxon coverage (i.e. inclusion of incomplete taxa), it was impossible to get a well-resolved tree from discrete data alone.\nFurthermore, it has been demonstrated that continuous characters can improve phylogenetic reconstruction (e.g. Parins-Fukucji 2018, Syst Biol 67: 328-339), so we prefer an analysis based on all sources of data. We should emphasise that there are many more discrete characters than continuous and meristic characters, so the main tree topology is most heavily influenced by discrete characters and indeed is highly consistent with earlier analyses that used only discrete characters."}, {"round": 2, "reviewer_comments": {"reviewer_1": "The authors well answered my comments and made the revisions accordingly. As such, I look forward to seeing its publication with a wealth of data for the follow-up research on the coelacanth evolution.", "reviewer_3": "I am pleased with the explanations and additional analyses provided by the authors. While I still think it would be worth looking at the rates of meristic character and continuous character change on a tree constructed only from discrete characters (since they were the majority of characters used), I accept that this would be at the expense of tree resolution. Therefore, I believe this manuscript is now suitable for publication without additional analyses."}, "author_response": ""}]

Decision letter