Research Article |
Corresponding author: David Marjanović ( david.marjanovic@gmx.at ) Academic editor: Florian Witzmann
© 2024 David Marjanović, Hillary C. Maddin, Jennifer C. Olori, Michel Laurin.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Marjanović D, Maddin HC, Olori JC, Laurin M (2024) The new problem of Chinlestegophis and the origin of caecilians (Amphibia, Gymnophionomorpha) is highly sensitive to old problems of sampling and character construction. Fossil Record 27(1): 55-94. https://doi.org/10.3897/fr.27.e109555
|
The description of the small Late Triassic temnospondyl Chinlestegophis ushered in a potentially radically new understanding of the origins of the extant amphibian clades. Together with the fragmentary Rileymillerus, Chinlestegophis was argued to link extant caecilians to Permo-Triassic stereospondyl temnospondyls rather than to frogs and salamanders (and through them to amphibamiform temnospondyls or to brachystelechid and lysorophian “lepospondyls”). We critically review the comparative description of Chinlestegophis and phylogenetic analyses of previous studies. Most of the features previously interpreted to be shared by caecilians, Chinlestegophis and/or other stereospondyls have different distributions than scored in the analysis. We also find no evidence for an incipient tentacular sulcus in Chinlestegophis, and note that its vertebrae, unreduced ribs and dermal shoulder girdle are unlike those of any extant amphibians (nor their likely sister group, Albanerpetidae). Furthermore, the original matrices contain misscores accreted over more than a decade that likewise influence the results. Some features are coded as multiple redundant characters: the double toothrow of Chinlestegophis, other stereospondyls, and caecilians is represented as seven characters. Analysis of the unmodified matrix yields much less resolution than originally reported, and tree topology is altered by a small change to the taxon sample (the addition of Albanerpetidae), limited revisions of irreproducible scores, and ordering the most obviously clinal characters; any one of these changes removes Chinlestegophis from Lissamphibia, and confirms it as a stereospondyl.
Amphibia, Chinlestegophis, Funcusvermis, Gymnophiona, Gymnophionomorpha, Lissamphibia, majority-rule consensus, phylogenetics, phylogeny
Caecilians have a scanty fossil record (
To this controversy,
Although we agree that Chinlestegophis presents an interesting mix of characters, we wish to respond to claims
Recent works have investigated selected aspects of the work of
Our usage of the clade names Gymnophiona, Amphibia and Lissamphibia follows
We use “caecilians” for crown-group caecilians (Gymnophiona:
We use “coding” for the process of choosing and defining the characters and their states, and “scoring” for filling in the matrix. Observed morphology is “miscoded” if, for example, it is represented as two redundant characters in the character sample, but “misscored” if the scores (numbers, state symbols) in the matrix are not what they should be according to the existing state definitions.
AMNH FARB Collection of Fossil Amphibians, Reptiles and Birds at the American Museum of Natural History (New York).
app. appendix (of cited works).
CI consistency index.
MPT most parsimonious tree.
MRC majority-rule consensus.
OTU operational taxonomic unit (a line in a data matrix).
RC rescaled consistency index.
RI retention index.
supp. inf. supplementary information (of cited works).
Strict consensus of the four MPTs obtained by Marjanović & Laurin (2009: electronic supplementary material 2) from their modified version of the matrix of
The published matrix (
It is, of course, common practice to modify and expand existing data sets, and underlying errors are frequently perpetuated into later generations of matrices when first-hand reassessment of specimens is infeasible, detailed comparison to the literature is deemed too time-consuming, or the full history of characters becomes obscured over time, leading to different meanings of the same character for different taxa that were added or revised at different times (
The merging of existing matrices can also generate additional problems related to redundant characters and states. As an example, multiple characters related to the lower jaw in the published matrix of
Robust analyses also may be thwarted by constraints related to the original taxon sampling of the underlying matrices; in other words, matrices compiled by other authors were (implicitly or explicitly) constructed with the intent to apply them to specific problems, and thus any clade may be densely or sparsely sampled depending on the question that was originally addressed, rather than on questions of later interest. Inserting new taxa may be difficult if additional variation is not easily accommodated without major character revisions, and this may limit which taxa can be speedily added. The matrix of
The more narrowly focused published matrix of
In short,
The published matrix further lacks representation of Albanerpetidae (a member or the sister group of Lissamphibia), despite their presence in the unpublished matrix.
The original parsimony analysis of the published matrix yielded 882 shortest trees (
Investigating that problem specifically,
Of the other islands, one (figured by
Another island (
In other words, parsimony analysis of the published matrix of
With the result of the parsimony analysis of the published matrix wholly inconclusive, an argument can still be made that the topology shown in fig. S7B of
The supposed problem of common branch lengths for all characters in previous simulations, pointed out by
Even more importantly, as paleontological matrices generally do (contrary to the implication by King [2020]), the matrix of
We also would like to draw attention to figure 1 of
Further, by default, parsimony is somewhat less vulnerable than parametric methods to the long-known problem of heterotachy (
As noted above,
Analysis | Our figure | Base matrix of |
Modifications from |
Ordering of clinal characters | inf. char. | Length of MPTs | Topology |
---|---|---|---|---|---|---|---|
– | 1 | – | n/a | yes | 212 | 1264 | Marjanović & Laurin (2009: supplementary figure), matrix modified from |
a1 | 2 | unpublished: SM 1 | None | no | 292 | 1450 | as in |
a2 | 3 | unpublished: SM 1 | constraint de facto for LH | no | 292 | 1454 | LH; Lissamphibia contains Gerobatrachus, positions of Chinlestegophis + Rileymillerus as in a1 |
b | – | published: SM 3 | None | no | 322 | 1514 | five islands: Lissamphibia, when present, in Amphibamiformes or Stereospondyli; Chinlestegophis in Gymnophionomorpha and/or Stereospondyli; figures in Serra Silva & Wilkinson (2021: fig. 2–4), simplified figures in Marjanović & Laurin (2019: fig. 30I–K), only one island figured by |
bootstrap of b | 4 | published: SM 3 | None | no | 322 | n/a | Diphyly of modern amphibians: Karauridae + Batrachia next to Gerobatrachus (43%), caecilians next to Chinlestegophis (52%) in Stereospondyli |
c | 5 | published: SM 3 | addition of Albanerpetidae from |
no | 329 | 1565 | as in |
d1 | 6 | published: SM 4 | None | yes | 324 | 1554 | Lissamphibia next to Chinlestegophis + Rileymillerus in Stereospondyli |
bootstrap of d1 | 7 | published: SM 4 | None | yes | 324 | n/a | Lissamphibia (46%) next to Chinlestegophis + Rileymillerus (29%); Chinlestegophis as gymnophionomorph not compatible with bootstrap tree (44%) |
d2 | 8 | published: SM 4 | Albanerpetidae | yes | 329 | 1605 | Lissamphibia in Amphibamiformes (closer to Apateon than to Doleserpeton or Gerobatrachus), Chinlestegophis and Rileymillerus in Stereospondyli |
bootstrap of d2 | 9 | published: SM 4 | Albanerpetidae | yes | 329 | n/a | Lissamphibia (52%) next to Chinlestegophis + Rileymillerus (27%); Chinlestegophis as gymnophionomorph not compatible with bootstrap tree (40%) |
e1 | 10–12 | published: SM 5 | corrections of characters and scores | no | 319 | 1514 | seven islands: Lissamphibia either next to Gerobatrachus in Amphibamiformes or next to Chinlestegophis + Rileymillerus in Stereospondyli |
e2 | 13, 14 | published: SM 6 | corrections of characters and scores | yes | 321 | 1558 | Lissamphibia next to Chinlestegophis + Rileymillerus in Stereospondyli |
e3 | 15 | published: SM 5 | corrections; Albanerpetidae | no | 326 | 1564 | (Albanerpetidae (Karauridae, Lissamphibia)) in Amphibamiformes, Chinlestegophis + Rileymillerus in Stereospondyli |
e4 | 16, 17 | published: SM 6 | corrections; Albanerpetidae | yes | 326 | 1601 | three islands; Lissamphibia always in Amphibamiformes (closer to Apateon than Doleserpeton or Gerobatrachus), Chinlestegophis + Rileymillerus in Stereospondyli |
bootstrap of e4 | 18 | published: SM 6 | corrections; Albanerpetidae | yes | 326 | n/a | Lissamphibia (77%) in Amphibamiformes (Dissorophoidea: 35%), Chinlestegophis + Rileymillerus in Stereospondyli (34%); Chinlestegophis + Rileymillerus as gymnophionomorphs (15%) or next to Lissamphibia (29%), let alone Lissamphibia in Stereospondyli (10%), not compatible with bootstrap tree |
As described below, for some of our analyses of the published matrix, we added Albanerpetidae from
We reanalyzed the originally unpublished matrix (associated with figure S6 of
In both analyses, all characters were unordered, and no changes were made to the matrix. The search parameters were as follows: 10,000 random addition sequence replicates (far more than proved necessary) were performed holding one tree at each step, followed by branch swapping using TBR (tree bisection and reconnection) with a reconnection limit of 8 and a limit of 50 million rearrangements per replicate (which was never hit); steepest descent was not in effect; unlimited automatic increases on the Maxtrees setting; branches collapsed if maximum branch length was 0.
We reanalyzed (analysis b) an unrevised version of the published matrix of
We also present a bootstrap analysis of this matrix (200 bootstrap replicates, each with 500 addition sequence replicates limited to 10 million rearrangements) to enable a better understanding of its support for various hypotheses. Most bootstrap values returned by
Instead of publishing matrix files,
In the analyses of both matrices performed by
In the process of ordering all such clines in the unmodified published matrix, we discovered (like
For characters 3, 26 and 201, the implementation of state 2 as published in part D seems complete even though it is likewise missing from part C in all three cases. Conversely, character 292 has three states in part C, of which state 1 does not occur in the matrix. Characters 301 and 318 have three states in part C as well, of which the matrix lacks state 2.
We performed two parsimony and two bootstrap analyses—without (d1) and with (d2) Albanerpetidae as in analyses b and c—ordering the following clinal characters of the published matrix: 67, 75, 110, 143, 145, 158, 163, 170, 182, 187, 191, 201, 205, 209, 213, 214, 221, 226, 229, 242, 243, 262, 264, 266, 269, 271, 273, 279, 298, 300, 302, 304, 327, 328, and 334 (35 ordered out of 345 total characters; 10.1%). We first reordered the states of characters 205, 221, 327 and 328 to allow linear ordering because the original order did not follow the cline: states 0 and 1 of characters 205 and 221 had to be exchanged, as well as states 1 and 2 of characters 327 and 328. The resulting data matrix (and PAUP block) is available as Suppl. material
The search settings were as above. 200 bootstrap replicates were performed, each using 500 random addition sequences. Instead of presenting the bootstrap values on consensus trees, we present the bootstrap trees (including the clades with greater frequencies than their alternatives) with their bootstrap values.
The resulting modified matrix is presented in Suppl. materials
The diagnosis of Chinlestegophis states on p. E5389: “A shared feature with stereospondyls and caecilians is opisthotics fused to exoccipitals.” As pointed out by
“Shared features with brachyopoids and caecilians” were proposed to (p. E5389) “include lacrimal fused to maxilla”. This hypothesis is difficult to evaluate. The maxillopalatine of Funcusvermis does not contain the nasolacrimal duct, so there is no evidence that it contains the lacrimal bone (
The sentence quoted above continues: “and two small posterior processes (‘horns’) on the occipital exposure of the tabular, just posterior to the otic notch (as in chigutisaurids).” Part B of the supplementary text of
On the same page, “[s]hared features with Rileymillerus and caecilians include the following: orbits small and laterally directed.” Orbit size, not coded in the published matrix, should be quantified before it can be evaluated, but is expected to be convergent among animals that live in darkness. Indeed, the orbits of Funcusvermis appear to have been considerably larger than those of other caecilians, Chinlestegophis or Rileymillerus (
“Shared features with caecilians include double tooth row on mandible” is stated in the next sentence of
Character 146 reads: “Symphyseal teeth. No accessory teeth posterior to symphyseal tusks (0), or a transverse row of such teeth (1).” State 1 is found in some stereospondyl taxa. Despite the absence of symphysial tusks, state 1 also was scored for Chinlestegophis, Eocaecilia and the two extant caecilians (
Characters 147 and 148 describe presence/absence of teeth on specific coronoids and are thus redundant with character 272, which describes presence/absence of coronoid teeth in general (
147. Dentition lingual to distal half of labial toothrow. Present (0), or absent (1).
148. Dentition lingual to mesial half of labial toothrow. Present (0), or absent (1).
Character 322, “Splenial teeth. Present (0), absent (1)”, was scored 0 exclusively for Ichthyophis, Epicrionops and the dvinosaurian temnospondyl Trimerorhachis insignis Cope, 1878. The scores for the former two refer to the fact that the lingual toothrow of caecilians has historically been thought to be borne on the splenial (references in
It is worth mentioning that all three caecilians were correctly scored as lacking splenials in the published matrix of
Character 344 also appears to target the presence of a lingual row of dentition on the mandible as seen in gymnophionans and taxa like Chinlestegophis. The character is defined as: “Dentary marginal dentition. Single row (0), multiple rows (1).” The three caecilian OTUs and Chinlestegophis, and no other OTUs, were scored as having multiple rows (1); however, Chinlestegophis has only one dentary toothrow as described and illustrated by
Additionally, character 273 is: “Coronoid teeth. Larger than marginal (0), equal to marginal (1), smaller than marginal (2).” State 1 was scored exclusively for the three caecilians, Chinlestegophis and the stereospondyl Benthosuchus. We rescored Chinlestegophis as possessing state 2 because
The next feature listed as shared between Chinlestegophis and caecilians is “quadrate completely anterior to ear”, possibly meaning the otic capsules. If so, this character state—which is not coded in the matrix—is standard among brachystelechid and lysorophian lepospondyls (
Next is “broad, parallel-sided parasphenoid cultriform process >20% skull width”. Three characters in the published matrix (112, 114, 343) attempt to capture variation in parasphenoid shape, particularly that of the cultriform process, but “broad” and “parallel-sided” have different distributions. Although the cultriform process of Chinlestegophis is even broader than that of Eocaecilia, this condition is more or less universal among lissamphibians (references in
Character 112 is presented in the character list as having two states: “Cultriform process (width). Base not wider than rest, clearly set off from basal plate (0), or merging continuously into plate (1)” (
Character 114 is: “Cultriform process (outline). Of similar width throughout (0), or posteriorly expanding abruptly to about twice the width (1).” State 1 was scored only for the two extant caecilian OTUs and for the temnospondyls Rileymillerus, Eryops and Onchiodon. We are not sure if the conditions of those taxa should be considered primarily homologous: the two eryopids have a bulbous expansion near the base of the cultriform process, followed caudally by a constriction and then the basal plate along with its contacts to the pterygoids (
“[O]ccipital condyles extend far beyond posterior edge of skull roof” is the next character state proposed to be shared by Chinlestegophis and caecilians (
The last character state proposed to be shared by Chinlestegophis and caecilians (
The pterygoquadrate may be coded as state 2 of character 318: “Quadrate-maxilla separated by. [sic] Pterygoid (0), small pterygoid and pterygoid process of quadrate (1), by pterygoid process of quadrate only (pterygoid absent) (2).” In agreement with the discussion above, state 2 does not occur in the matrix, which lacks teresomatans.
The implication later in the same paragraph (
In their Discussion section,
See Table
Our unconstrained analysis (a1; Fig.
Strict consensus of the 12 MPTs obtained from our analysis a1 (see Table
The MPTs form two islands that differ in their resolution of Lissamphibia: (1) Gerobatrachus as the sister-group of Lissamphibia, within which “frogs” + Triadobatrachus is the sister-group of a clade formed by “salamanders” + Karaurus on one side and Albanerpetidae + Eocaecilia and crown caecilians on the other; (2) crown caecilians + Eocaecilia as the sister-group of the other lissamphibians, within which Gerobatrachus is the sister-group of a clade formed by “frogs” + Triadobatrachus on one side and Albanerpetidae + (“salamanders” + Karaurus) on the other. Note that only (2) is compatible with phylogenies of extant amphibians based on molecular data (
Constraining Eocaecilia to be closer to the lepospondyl Carrolla (analysis a2; Fig.
Strict consensus of the 48 MPTs obtained from the unpublished matrix used by
The differences in fit to the matrix between the unconstrained and the constrained trees are not significant (Kishino/Hasegawa test: p = 0.6284; Templeton test: p = 0.6276; winning-sites test: p = 0.7160).
Reanalysis of the published matrix (analysis b) yielded identical results to those of
The bootstrap tree of analysis b (Fig.
Bootstrap tree obtained from the published matrix used by
Inspection of the list of bipartitions in the output of PAUP* (Suppl. material
The matrix of
Strict consensus of the 45 MPTs obtained from the published matrix of
The addition of Albanerpetidae renders seven characters parsimony-informative, so that 329 of the total of 345 now have this status.
Ordering of clinal characters (analysis d1) in the otherwise unmodified published matrix of
The bootstrap tree of analysis d1 (Fig.
When the clinal characters are ordered and Albanerpetidae is added (analysis d2), 329 characters are parsimony-informative, and the published matrix yields a single island of 30 MPTs (1605 steps, CI excluding uninformative characters = 0.2453, RI = 0.6830, RC = 0.1711). The strict consensus (Fig.
Bootstrapping analysis d2 (Fig.
The list of bipartitions not compatible with the bootstrap tree (Suppl. material
The matrix including the changes we propose was run both with all characters unordered, as they were in
Strict consensus of each of two further islands of MPTs from analysis e1. For space reasons, one of the two resolutions of Trematosauria is mirrored and presented without species names. For the other MPTs, see Figs
Strict consensus of each of the remaining four islands of MPTs from analysis e1. Except for Lissamphibia, the part depicted here is identical in all four islands; Lissamphibia is resolved either as shown or as in Fig.
The second analysis, using ordered characters (e2), resulted in three islands of 99 MPTs in total (1558 steps; CI excluding parsimony-uninformative characters = 0.2489, RI = 0.6870, RC = 0.1759). 321 characters were parsimony-informative. The well-resolved strict consensus is shown in Figs
The third and fourth analyses differ from the first and second by the addition of Albanerpetidae (from
In the ordered analysis e4, 81 MPTs are recovered (1609 steps, CI without uninformative characters = 0.2434, RI = 0.6817, RC = 0.1695). They all group the Rileymillerus + Chinlestegophis clade with Brachyopoidea as in analysis e3, while Lissamphibia is nested among the amphibamiform dissorophoids, closer to Apateon than to Gerobatrachus or Doleserpeton. PAUP* groups the MPTs into three islands depending on how they resolve amphibamiform phylogeny: one island (Fig.
Strict consensus of all (to the left and above the stippled line) or some (to the right and below the stippled line) of the 81 MPTs recovered in analysis e4 (published matrix of
Bootstrapping analysis e4 reveals (Fig.
Groupings not compatible with the bootstrap tree (Suppl. material
Our work corroborates some of the results of the analyses performed by
First, we stress that the unpublished matrix (our analysis a1, see Table
All of our remaining analyses focused on the published matrix of
However, adding Albanerpetidae to the matrix (analysis c; Fig.
The effect of ordering characters within the original published matrix (i.e., without Albanerpetidae and without corrections other than renumbering the states of some ordered characters) (analysis d1; Fig.
A modest revision of the published matrix, without Albanerpetidae, replicated the basic results of analyses c and d1 as equally parsimonious when all characters were unordered (analysis e1; Figs
In all four cases, ordering increased the resolution of the results. We interpret this as an example of ordering bringing out phylogenetic signal in data, congruent with results from simulations and some empirical examples; note that ordering does not automatically increase the net resolution (
Strikingly, none of the trees from analyses c, d or e (most parsimonious or bootstrap) support affinities between Chinlestegophis and caecilians to the exclusion of other lissamphibians. The bootstrap analysis of the original matrix under original conditions (analysis b; Fig.
The published matrix of
As further support for a close relationship between Chinlestegophis and caecilians,
We note several other features, not discussed by
What little is known and described of the postcranial skeleton of Chinlestegophis (
Interpretations of functional biology and evolutionary trends rely on our perspective of phylogenetic relationships. In the original description of Chinlestegophis, once a consensus tree was selected and reported, a number of the characteristics used in the matrices and discussed above were used to infer a stepwise evolution of traits toward the specialized fossorial and head-first burrowing lifestyle of caecilians. Those features include fusion of the lacrimal + maxilla and exoccipital + opisthotic (interpreted as stages in the consolidation of the skull), repositioning of the jaw suspension, small and laterally oriented eyes, etc. However, as we demonstrate above, most of those features have a wider distribution across Paleozoic tetrapods or present confounding problems of homoplasy across many disparate clades, extinct and extant.
In particular, we regard as unfortunate the aforementioned removal of all lepospondyls from the unpublished matrix to create the published matrix after the initial recovery of Chinlestegophis as a temnospondyl by
Considering that alternative hypotheses of relationships are equally supported by the published matrix, even without broader taxonomic sampling to include lepospondyls, the proposed stepwise evolution of caecilian features falls apart. Rather than traits linking Chinlestegophis and caecilians, those same characteristics appear to represent homoplasy, as shown in trees that place Chinlestegophis close to but outside Lissamphibia (our analyses a, d, e2 and some MPTs of b and e1 plus the bootstrap of b) or far away (our analyses c, e3, e4 and some MPTs of b and e1).
The grooves for the lateral-line organ identified by
The discussion above takes at face value both the coding and scoring of the two matrices, and their character and taxon samples, apart from our limited modifications in analyses c, d2 and e; but these issues deserve comments. We have not scrutinized the matrices in full (see
Published in one of the most prestigious journals, the description of Chinlestegophis (
Concerning phylogenetics, we reiterate that the majority-rule consensus is not a useful representation of the result of a parsimony analysis, and that not all issues with Bayesian analysis of matrices with missing data have been solved; but most importantly, matrix quality remains paramount in phylogenetic analysis. This concerns typographic errors, misinterpretations of published literature, redundant characters (in the dataset we revised, the double toothrow in the lower jaw of caecilians was coded as seven characters that an analysis could only treat as independent), characters that represent two or more independently varying features, and inconsistencies in scoring. As previously pointed out (e.g.
Jason Pardo and Adam Huttenlocker kindly sent us both matrices, and J. Pardo and Ben Kligman discussed certain characters with us. The reviewers Marvalee Wake and Christian Sidor led us to improve the clarity of our writing. D. M.’s understanding of current issues in phylogenetics benefited from a course taught by Tiago Simões and Oksana Vernygora and organized by Transmitting Science.
Mesquite NEXUS file of
Data type: nex
Explanation note: We have added a PAUP block that repeats our unconstrained and constrained analyses (a1, a2) if the file is executed in PAUP*, and a TREES block that contains one tree resulting from each analysis; before conducting the analyses, the PAUP block performs the statistical tests comparing the trees in the TREES block. Otherwise the file remains as provided by J. Pardo and A. Huttenlocker.
Frequencies of bipartitions in our (unrooted) bootstrap analyses
Data type: pdf
Explanation note: Tables
Mesquite NEXUS file of
Data type: nex
Explanation note: No scores are changed, all characters are unordered. We have also added a PAUP block and deleted the CHARSTATELABELS block because Mesquite could not deal with it correctly. If the file is executed in PAUP*, it repeats our analysis b (without Albanerpetidae), bootstraps it, and repeats analysis c (with Albanerpetidae).
Mesquite NEXUS file of
Data type: nex
Explanation note: For characters 205, 221, 327 and 328, the states had to be reordered to allow for linear ordering as described in the text. If executed in PAUP*, the file repeats our analysis d1 (without Albanerpetidae), bootstraps it, repeats analysis d2 (with Albanerpetidae) and bootstraps it as well.
Mesquite NEXUS file of
Data type: nex
Explanation note: If executed in PAUP*, the file repeats our analyses e1 (without Albanerpetidae) and e3 (with Albanerpetidae).
Mesquite NEXUS file of
Data type: nex
Explanation note: If executed in PAUP*, the file performs our analyses e2 (without Albanerpetidae) and e4 (with Albanerpetidae) and then bootstraps e4.