Response: Commentary: A Reassessment of the Taxonomic Position of Mesosaurs, and a Surprising Phylogeny of Early Amniotes

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GENERAL COMMENTARY
published: 03 December 2018
doi: 10.3389/feart.2018.00220
Frontiers in Earth Science | www.frontiersin.org 1December 2018 | Volume 6 | Article 220
Edited by:
Corwin Sullivan,
University of Alberta, Canada
Reviewed by:
Tiago Simoes,
University of Alberta, Canada
*Correspondence:
Michel Laurin
michel.laurin@mnhn.fr
Specialty section:
This article was submitted to
Paleontology,
a section of the journal
Frontiers in Earth Science
Received: 26 September 2018
Accepted: 14 November 2018
Published: 03 December 2018
Citation:
Laurin M and Piñeiro G (2018)
Response: Commentary: A
Reassessment of the Taxonomic
Position of Mesosaurs, and a
Surprising Phylogeny of Early
Amniotes. Front. Earth Sci. 6:220.
doi: 10.3389/feart.2018.00220
Response: Commentary: A
Reassessment of the Taxonomic
Position of Mesosaurs, and a
Surprising Phylogeny of Early
Amniotes
Michel Laurin 1
*and Graciela Piñeiro 2
1CR2P (UMR 7207), CNRS/MNHN Sorbonne Université, “Centre de Recherches sur la Paléobiodiversité et les
Paléoenvironnements”, Muséum National d’Histoire Naturelle, Paris, France, 2Departamento de Paleontología, Facultad de
Ciencias, Montevideo, Uruguay
Keywords: Mesosauridae, Parareptilia, Synapsida, Sauropsida, Amniota, Paleozoic, temporal fenestration
A Commentary on
Commentary: A Reassessment of the Taxonomic Position of Mesosaurs, and a Surprising
Phylogeny of Early Amniotes
by MacDougall, M. J., Modesto, S. P., Brocklehurst, N., Verrière, A., Reisz, R. R., and Fröbisch, J.
(2018). Front. Earth Sci. 6:99. doi: 10.3389/feart.2018.00099
INTRODUCTION
Mesosaurs, known from the Early Permian of southern Africa, Brazil, and Uruguay, are the oldest
known amniotes with a primarily, though probably not strictly, aquatic lifestyle (Nuñez Demarco
et al., 2018). Despite having attracted the attention of several prominent scientists, such as Wegener
(1966), who used them to support his theory of continental drift, and the great anatomist and
paleontologist von Huene (1941), who first suggested the presence of a lower temporal fenestra
in Mesosaurus, several controversies still surround mesosaurs. One concerns the presence of the
lower temporal fenestra in mesosaurs, which we accept (Piñeiro et al., 2012a; Laurin and Piñeiro,
2017, p. 4), contrary to Modesto (1999, 2006) and MacDougall et al. (2018); the other concerns
the systematic position of mesosaurs, which have been argued, in the last decades, to be either
the basalmost sauropsids (Laurin and Reisz, 1995; Laurin and Piñeiro, 2017), or the basalmost
parareptiles (Gauthier et al., 1988; Modesto, 1999; MacDougall et al., 2018). Note that we adopt
a branch-based definition of Parareptilia as Laurin and Reisz (1995) did, but use Procolophon
trigoniceps as an internal specifier rather than turtles, because of the controversy surrounding the
affinities about turtle origins.
In their recent response to our recent paper on the taxonomic position of mesosaurs,
MacDougall et al. (2018) make a number of problematic claims, which we wish to discuss. These
claims are that we used an outdated matrix and ignored over two decades of parareptile research,
that our taxon selection was insufficient and that along with variability in temporal fenestration
in parareptiles, all these choices explain the different taxonomic position of mesosaurs that we
obtained (as the basalmost sauropsids rather than the basalmost parareptiles). Below, we respond to
these claims by providing additional background data and by performing various analyses of their
matrix and ours that show, through taxon and character deletion among other approaches, that
neither the omission of some taxa, nor variability in temporal fenestration explains the differences

Laurin and Piñeiro Response: Commentary: A Taxonomic Position of Mesosaurs
in topologies between our study and theirs. We also highlight
problems with their analyses and discuss why reusing phenotypic
data matrices produced by other systematists is difficult.
MATERIALS AND METHODS
The reanalyses below use a version of our data matrix (Laurin and
Piñeiro, 2017) in which we deleted characters linked to temporal
fenestration, to assess the impact of this complex of characters
on the resulting topology. We also reanalyze the data matrix of
MacDougall et al. (2018), in three versions: unmodified, modified
by ordering characters that form morphoclines, and modified
further by removing the parareptile taxa not found in our matrix
(Laurin and Piñeiro, 2017). We have not studied the scores of
the cells of the data matrix of MacDougall et al. (2018) because
this would be very time-consuming and would largely duplicate
a more ambitious project focusing on early amniote phylogeny
and the origin of turtles (mesosaurs are in the matrix, though
the project does not focus particularly on their affinities) initiated
by one of us (ML) in January 2018 in collaboration with Ingmar
Werneburg, Gabriel Ferreira, and Márton Rabi.
All phylogenetic analyses were carried out with PAUP∗
(Swofford, 2003) version 4.0a, build 163 for Macintosh (the latest
version available as of July 28, 2018), using the branch and bound
algorithm for our own data matrix, using the heuristic search
with 50 random addition sequence replicates, holding 3 trees
at each step, and using the tree-bisection-reconnection (TBR)
algorithm for the various versions of the matrix by MacDougall
et al. (2018) because that matrix had too many taxa for the branch
and bound algorithm to conclude tree search in a reasonable
amount of time. The branch and bound algorithm guarantees
discovery of all possible most parsimonious trees. No heuristic
algorithm provides a similar guarantee, but we verified for each
of our analyses that all most parsimonious islands of trees had
been recovered at least three times (most were recovered far more
frequently and all were found at least 4 times), allowing us to be
reasonably certain that we had all the most parsimonious trees.
We also repeated one of these analyses (on the original version
of the matrix of MacDougall et al., 2018) using 1,000 addition
sequence replicates, to ensure that our settings (in particular, use
of 50 addition replicates) were appropriate; we found exactly the
same set of trees, which validated our choice. The results of these
analyses allow us to test the main claims made by MacDougall
et al. (2018).
Information associated with the analyses carried out in this
paper (modified list of characters, in which we document
which characters were ordered, and how the states had to be
reordered to reflect the underlying continuous characters, and
modified Mesquite Nexus file, which incorporates these ordering
modifications) is available on the journal web site.
RESULTS
Taxon Selection in Recent Studies on
Mesosaur Affinities
MacDougall et al. (2018) claim that we engage in “use of an
outdated phylogenetic matrix” and that we “patently ignore over
two decades of parareptilian research.” These two closely related
claims are factually wrong. The second point (that we ignore
two decades of parareptilian research) is refuted by a simple
examination of the bibliography of our paper. We did not claim
to have cited all recent papers on parareptiles (given that our
paper was not a review of recent studies on parareptiles), but
we cited several papers published in the 1998–2018 period that
discuss parareptile extensively (Reisz and Scott, 2002; Cisneros
et al., 2004; Müller and Tsuji, 2007; Modesto et al., 2009; Lyson
et al., 2010, 2013; Tsuji et al., 2010, 2012; Lee, 2013; Bever
et al., 2015). Note that this list does not include papers about
mesosaurs, which our results suggest are not parareptiles. The
first point (that the matrix is obsolete) is equally factually
wrong as shown by the fact that we extensively updated the
original matrix (Laurin and Reisz, 1995) using both the literature
and direct observations of specimens, especially mesosaurs, and
explained this clearly (Laurin and Piñeiro, 2017, p. 4). For
instance, Owenetta, which we added to the matrix (it was not
in the matrix of Laurin and Reisz, 1995), was scored using the
detailed description of Reisz and Scott (2002). We also added
one of the basalmost, best-known parareptiles (Acleistorhinus),
to better test previous suggestions that mesosaurs are basal
parareptiles, and made other changes to the taxon set (see below).
Given all these changes, we do not consider that we used an
outdated phylogenetic matrix.
MacDougall et al. (2018) object to the use of suprageneric
taxa as terminals because they claim that the resulting higher
rate of polymorphism can weaken support values. We think
that the interpretation of support values is more complex than
MacDougall et al. (2018) suggest because these values tend to
reflect character congruence and the number of characters (or the
ratio between number of characters and number of OTUs). For
many taxa, various mutually incompatible phylogenies with good
support values have been published, which shows that such values
should not be equated with reliability (Marjanovi´
c and Laurin,
2018). The famous case of “The guinea-pig is not a rodent”
(D’Erchia et al., 1996) illustrates this point. Furthermore, while
the increased polymorphism in OTUs corresponding to large
clades is unavoidable and simply reflects reality, the relationship
between that elevated rate of polymorphism and support values
in a matrix is far more complex than suggested by MacDougall
et al. (2018). This is illustrated by the fact that the taxa (typically
ranked as genera) that they introduced to replace the OTU
Synapsida yield a tree that suggests that this taxon, as currently
delimited, is paraphyletic! Of course, a monophyletic Synapsida
could still be recognized in accordance with the definition of
this clade that has been proposed under the PhyloCode (using
Cynognathus crateronotus as the sole internal specifier, and
three extant sauropsids as external specifiers), but in their most
parsimonious trees (and under both of their analyses) varanopids
and the presumed ophiacodontid Archaeothyris would move
out of Synapsida and become basal sauropsids (if we assume
Cynognathus to be closer to edaphosaurids than to other taxa
included in the tree). Thus, the support value for Synapsida
in their tree (not provided) is presumably very low (bootstrap
values) to negative (Bremer or decay index), depending on which
index is used to assess it. Nevertheless, we moved to some degree
in the direction of selecting smaller terminal taxa by breaking
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Laurin and Piñeiro Response: Commentary: A Taxonomic Position of Mesosaurs
up the Testudines OTU present in Laurin and Reisz (1995) into
Odontochelys, Proganochelys and Chelonii, the last of which could
be broken up further in subsequent studies.
We recognize that using lower-level taxa is beneficial. The
small OTUs that replace Synapsida in MacDougall et al.’s
(2018) matrix yielded a new hypothesis about the position
of varanopids (outside Synapsida), and this is an interesting
result. As epitomized in “A hitchhiker’s guide to the galaxy”
(Adams, 2017), it is more important to have a good question
than a precise answer, and in phylogenetics, it is perhaps more
important to get interesting results that raise new questions
(about the monophyly of Synapsida and Diapsida as currently
delimited, for instance) than to obtain high support values
which, in some cases, may simply reflect the fact that only a
trivial question was asked (about affinities between a small set
of closely related taxa, for instance). Note further that there
is no special justification for using nominal genera as OTUs
given the subjective nature of Linnaean categories; all taxonomic
ranks, even species, are artificial constructs, ontologically empty
designations (Ereshefsky, 2002). In addition, all taxa represent
phylogenetic hypotheses, so the most rigorous approach would
be to do a specimen-level analysis, though this would result in
much more missing data than working on taxa, which would in
turn raise new problems (e.g., Simmons, 2012a,b).
Phylogeny and Evolution of
Permo-Carboniferous Amniotes
The finding by MacDougall et al. (2018) that Synapsida, as
defined under the draft PhyloCode (Laurin and Reisz, in press)
may exclude varanopids and the ophiacodontid Archaeothyris
(other ophiacodontids were not included), which appear at
the base of Sauropsida in their trees, raises two important
points that MacDougall et al. (2018) did not discuss. First, it
now seems likely that the phylogeny of Permo-Carboniferous
amniotes is much less robust than previously thought, given
that our analysis also found unorthodox results (parareptiles
nested within diapsids). This is also highlighted by the fact that
protorothyridids (represented by Paleothyris and Protorothyris)
are paraphyletic in their consensus trees.
Second, their topology, if correct, implies that the lower
temporal fenestra is an amniote synapomorphy, a possibility
that we suggested earlier (Piñeiro et al., 2012a) on the basis
of the presence of a fenestra in mesosaurs. MacDougall et al.
(2018) clearly viewed this part of their tree as preliminary
and problematic, but it is a result that should be investigated
further, as they pointed out, and it adds some support to
the hypothesis that the lower temporal fenestra is an amniote
synapomorphy. They also discussed fenestration extensively and
suggested that its great variability in amniotes both decreased its
taxonomic value, a point that we already made (Piñeiro et al.,
2012a), and raised doubts about our results. This last point
is misleading because our matrix includes only two characters
directly linked to temporal fenestration (characters 30 and 31).
MacDougall et al. (2018), in their first analysis, emphasized
temporal fenestration much more than we did by adding four
new characters linked to temporal fenestration (their characters
171–174), even though the older version of their matrix already
had three other characters also linked with temporal fenestration
(their characters 44–46), in addition to their characters 42 and 43,
which are the same as our characters 30 and 31. This may have
resulted in undue weight being given to temporal fenestration in
analyses including all these characters. They removed all these
characters linked with temporal fenestration in their second
analysis to assess the impact of fenestration on their results; this
impact is apparently negligible, which does not support their
claim.
MacDougall et al. (2018) criticized us for accepting our
own anatomical interpretations (rather than theirs) about the
temporal fenestra of mesosaurs: “the authors adhere to the
interpretation of Piñeiro et al. (2012a) that Mesosaurus possessed
a lower lateral temporal fenestra, a condition that actually may
be absent or ontogenetically variable within the taxon.” This is
a strange comment given that science is based on observation
rather than authority, and that we have had access to far more
specimens than they to support our interpretations. Should
scientists prefer others’ opinions over their own observations?
This would run counter to the most basic scientific principles.
We have seen no good evidence for absence of the fenestra in any
mesosaur so far, even though many specimens are not sufficiently
well-preserved to yield decisive evidence on this point.
They also claim that “specimens with supposed temporal
fenestration, such as that presented in Piñeiro et al. (2012a), are
extremely poorly preserved.” This is misleading. Our specimens
preserve bone (Figures 1C–E), whereas the specimens studied by
Modesto lacked bone (Modesto, 2006, p. 347): “All specimens
of Mesosaurus tenuidens examined here are preserved as natural
molds in black shale. These were cast in latex rubber and drawn
from photographs or by use of a camera lucida.” Thus, we believe
that at least some of our specimens are better-preserved than
those described by Modesto, which is not surprising given that
the Mangrullo Formation, from which most of our specimens
originate, is a recognized Konservat-Lagerstätte (Piñeiro et al.,
2012b). No author of MacDougall et al. (2018) saw more than
a small proportion of the specimens that we have studied, so
they are not in a good position to discuss preservation of the
specimens that support our interpretation. In any case, quality
of preservation can be assessed through several criteria, such
as whether or not bone is present (although some external
molds beautifully reconstruct the original anatomy of the bones),
the degree of flattening of the skeleton, and whether or not
elements are broken and disarticulated. According to three of
these four criteria (presence of bone, articulation, and whether
or not bones are broken), our specimens are better than those
studied by Modesto (2006) because in the latter, the temporal
region is disarticulated, bone is absent (only impressions remain),
and several elements appear to be incompletely preserved, with
broken edges, as shown by the high variability of the shape of
the squamosal in the specimens illustrated by Modesto (2006).
Also, disarticulation of the specimens studied by Modesto is
such that in one case the basisphenoid is visible in dorsal view
(Modesto, 2006, Figure 3) and in another the epipterygoid is
visible in lateral view (Modesto, 2006, Figure 6). In the latter
specimen, it is obvious that the jugal is bifurcated posteriorly and
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Laurin and Piñeiro Response: Commentary: A Taxonomic Position of Mesosaurs
FIGURE 1 | Mesosaur lateral temporal fenestra. (A) FC-DPV 1462, right jugal, probably of a newborn individual showing the typical triradiate structure normally
associated with a temporal fenestra. (B) FC-DPV 1083, right jugal of a juvenile individual showing the same typical triradiate structure. (C) FC-DPV 2534B, partial skull
of an adult Mesosaurus tenuidens showing a well-preserved temporal region. Some of the bones that delimit the lateral temporal fenestra (jugal and quadratojugal) are
partly disarticulated. However, the jugal displays the typical triradiate structure commonly associated with the presence of a temporal fenestra. (D) Schematic drawing
of the FC-DPV 2534B left postorbital region as it was preserved, showing the jugal and quadratojugal partially disarticulated. (E) Schematic reconstruction of the
possible natural anatomical configuration of the FC-DPV 2534B left postorbital region. The jugal-postorbital contact and the position of the quadratojugal relative to
the jugal are approximate given that the skull bones were compressed by sediment deposition, disrupting their original three dimensional arrangement. However, the
proposed configuration is the most plausible one given the morphology observed in other specimens, and the general anatomy of the bones in question. Scale: (A,B)
5 mm; (C) 10mm.
defined the anteroventral corner of the lower temporal fenestra,
though Modesto (2006, p. 352) interpreted this region differently.
Modesto (2006) argued that the squamosal has a complementary
shape and overlapped the posterior edge of the jugal, but given
the extreme variability in the preserved portion of the squamosals
illustrated by Modesto (2006), this interpretation seems to rest on
tenuous evidence. Regarding the other preservational criterion
(flattening), quality is equivalent between the specimens from
Uruguay and those from Brazil and South Africa studied by
Modesto (2006; 2018). One last point to consider is that the
Mangrullo formation of Uruguay has yielded isolated elements,
including those that border the temporal fenestra (Figures 1A,B),
and these support our interpretation.
Aside from issues of preservation of the specimens from
Uruguay compared with those of Brazil and South Africa,
it is clear that some specimens from Brazil display a well-
preserved temporal region featuring a lower temporal fenestra
(Laurin and Piñeiro, 2017,Figure 1). Moreover, we are not the
first to interpret the temporal region of Mesosaurus tenuidens
specimens from the Iratí formation (Brazil) as displaying a
lower temporal fenestra; our great predecessor von Huene (1941)
illustrated, described, reconstructed, and discussed the systematic
significance of that fenestra.
MacDougall et al. (2018) claim that “Laurin and Piñeiro
made no effort to reexamine the Mesosaurus specimens that
had been previously described by Modesto (2006; 2018).” This
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Laurin and Piñeiro Response: Commentary: A Taxonomic Position of Mesosaurs
is again misleading at best; one of us (GP) examined many
specimens from the collection studied by Modesto (though
not the specimens that he illustrated) which were available as
casts in Frankfurt, and has studied good photos of specimens
from the American Museum of Natural History. Modesto has
not studied the Brazilian collections containing thousands of
mesosaur specimens; he apparently examined materials housed
in South African museums and institutions, and the best
specimens from the Iratí Formation in European and North
American collections. Thus, one of us (GP) has examined far
more mesosaur specimens (79 are mentioned in our papers; see
Supplementary Data Sheet 1) than Modesto (we counted only
36 specimens mentioned in his thesis and his various papers); see
Supplementary Data Sheet 1 for the source of these numbers.
More importantly, why has Modesto (2006) studied only one
(GPIT [Institut und Museum für Geologie und Paläontologie
der Universität Tübingen] 1757-1) of the many specimens (33
are illustrated) studied by von Huene (1941), which collectively
led this great paleontologist and anatomist to conclude that
mesosaurs had a lower temporal fenestra? The specimen (GPIT
1757-1) studied by Modesto (2006) is exposed in dorsal view
and is not very informative about the temporal region. Thus, we
believe that on this front, our study rests on better grounds than
that of MacDougall et al. (2018).
Nevertheless, we take this opportunity to assess the impact of
temporal fenestration on our analysis by analyzing our matrix
again without the two temporal fenestration characters that
we originally included (our characters 30 and 31). The search,
carried out in PAUP∗4.0a (build 163) for Macintosh (the latest
version available as of July 28, 2018) using the branch and
bound algorithm, yielded two most parsimonious tree of 328
steps (consistency index of 0.497; homoplasy index of 0.503;
retention index of 0.6626), whose strict consensus is identical
with the tree that we published (Laurin and Piñeiro, 2017, Figure
5). Thus, as with MacDougall et al.’s (2018) matrix, exclusion of
the temporal fenestration characters does not change the results
in any significant way. This refutes the claim by MacDougall
et al. (2018, p. 5) that the variability of the temporal fenestration
explains the topology that we obtained.
We also reanalyzed the matrix by MacDougall et al. (2018),
using the version posted on the journal’s web site, initially
without any modifications. We used a heuristic search with 50
random addition sequence replicates, holding 3 trees at each
step, and using the tree-bisection-reconnection (TBR) algorithm.
Surprisingly, we found not 9 optimal trees of 669 steps as
reported by MacDougall et al. (2018), but 225 of the same length
(669 steps). The strict consensus (Figure 2A; illustrated here to
facilitate comparisons with our other results presented below)
is identical to theirs (MacDougall et al., 2018, Figure 1A), so
the mismatch in the number of most parsimonious trees might
possibly attributed to subtle settings in PAUP∗such as whether or
not zero-length branches are automatically collapsed, but we note
that their tree was rooted improperly as it implied an “anamniote”
clade including Seymouria and diadectomorphs that excluded
amniotes, whereas there is a fairly widespread consensus that
diadectomorphs are more closely related to amniotes than to
seymouriamorphs (e.g., Laurin and Reisz, 1995; Ruta and Coates,
2007; Marjanovi´
c and Laurin, 2018). The rooting option of any
phylogenetic tree is a hypothesis, not a result.
MacDougall et al. (2018) did not order any characters.
However, simulations have shown that for characters that
form morphoclines (including all characters that represent
discretization of an inherently continuous variable, such as
size or ratios between measurements), ordering states leads to
better results, in terms of both power to recover true clades
and avoidance of erroneous clades (Rineau et al., 2015, 2018).
Thus, we have ordered the following multi-state characters (their
numbering): 6, 47, 48, 52, 69, 89, 105, 129, 132, 147, 150,
165, 167, 168, 178. In some cases, we had to reorder states
because the order in which they were listed made no sense if
the character were to be ordered linearly, which is the simplest
approach and also the one that best reflects the underlying
quantitative (continuous) character. For instance, character 6,
“Pineal foramen position: in the middle of the body of the
parietal (0); displaced posteriorly (1); displaced anteriorly (2)”
was reordered by inverting states 0 and 1. Characters 47, 89,
147, and 178 were likewise reordered. Character 147, pertaining
to humeral morphology, requires an explanation. MacDougall
et al. (2018:Supplementary Data Sheet 1) indicate that this
is “Modified from (Laurin and Reisz, 1995) #104.” The only
modification that we see is the deletion of the ratio that served
to make the state definitions more objective. In Laurin and
Reisz (1995), we had indicated that the states depended on the
ratio between distal humeral head width and humeral length,
using 35 and 65% as thresholds. With this information, it is
clear that the states should be ordered. In the list of characters
(see Supplementary Data Sheet 2), we have tracked the changes
made to state numbering to facilitate comparisons between our
settings and those used by MacDougall et al. (2018). We also
provide the revised data matrix (Supplementary Data Sheet 3)
with the states reordered and ordering (or lack thereof) of
multi-state characters specified, to facilitate its use by other
scientists.
Analysis of the matrix with some characters ordered
(as mentioned above), conducted with the same settings as
previously, yielded 1,560 trees requiring 679 steps each and
with a consistency index of 0.2975, a homoplasy index of
0.7025, and a retention index of 0.6446. Their strict consensus
(Figure 2B), unsurprisingly, is less resolved than the tree
reported by MacDougall et al. (2018, Figure 1A). Notably,
polytomies occur near the base of Parareptilia, in the clade
that includes all parareptiles except for Milleretta, and at the
base of Lanthanosuchoidea. Yet another polytomy is formed by
Nyctiphruretidae, Procolophonoidea, and a clade that includes
Pareiasauria and nycteroleterids. Furthermore, Nycteroleteridae
may be paraphyletic as its component taxa form a polytomy that
also includes Pareiasauria. This last polytomy was also obtained
by MacDougall et al. (2018, Figure 1B) when they excluded the
characters linked with temporal fenestration, so the monophyly
of Nycteroleteridae might be worth reassessing. It might be
tempting to view the lower resolution of our tree as a refutation
of our ordering scheme, but it is more likely that the clades
found by MacDougall et al. (2018, Figure 1A) are erroneous
because simulations have shown that not ordering intrinsically
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Laurin and Piñeiro Response: Commentary: A Taxonomic Position of Mesosaurs
FIGURE 2 | Early amniote phylogeny as assessed through various reanalyses of a slightly modified version of the matrix of MacDougall et al. (2018).(A) Strict
consensus obtained by reanalyzing the data matrix without any modifications. This is basically identical with the tree obtained by MacDougall et al. (2018, Figure 1A),
but it is reproduced here to facilitate comparisons among the results obtained in our various analyses. (B) Strict consensus obtained by reanalyzing the data matrix
after ordering characters 6, 47, 48, 52, 69, 89, 105, 129, 132, 147, 150, 165, 167, 168, 178. Note that in some cases, the order of the states had to be altered to
reflect the nature of the morphocline. (C) Majority-rule consensus tree (nodal values represent frequencies in the source trees) from the same analysis. (D) Strict
consensus tree from analysis of the same matrix, except that taxa not represented in Laurin and Piñeiro (2017) were removed before analyzing the data. This refutes
the claim that the topology obtained by Laurin and Piñeiro (2017) results from exclusion of several parareptile taxa (in red on parts A–C) that were considered by
MacDougall et al. (2018), because exclusion of these taxa from the matrix of MacDougall et al. (2018) does not change the topology.
ordered characters yields a greater proportion of erroneous clades
(Rineau et al., 2015, 2018).
The majority-rule consensus of the 1,560 trees obtained
with some states ordered (Figure 2C) reveals some interesting
information not provided by MacDougall et al. (2018). Namely,
varanopids may be more closely related to other sauropsids than
to Archaeothyris. This result is admittedly very poorly supported
(occurring in only 20% of the most parsimonious trees), but is
also found (with the same frequency) when no states are ordered
(not shown here, but available in Supplementary Data Sheet 3).
MacDougall et al. (2018 p. 5) claimed that the omission of
several parareptile taxa in our matrix explained our topology
(which placed mesosaurs outside Parareptilia). To test this
hypothesis, we deleted from their matrix the parareptiles that
they included but that were excluded from our matrix, although
we did not remove low-ranking taxa belonging to higher-ranking
taxa that we included. Thus, the OTUs belonging to Pareiasauria
included in MacDougall et al. (2018) were retained, but we
excluded Australothyris, Microleter, Nyctiphruretus, Barasaurus,
Bashkyroleter mesensis, Bashkyroleter bashkyricus, Nycteroleter,
Emeroleter, Ripaeosaurus, Lanthanosuchus, Feeserpeton,
Colobomycter pholeter, Colobomycter vaughni, Delorhynchus
cifellii, Abyssomedon, Eudibamus, Belebey, Erpetonyx, and
Bolosaurus. The search, conducted with the same settings
as above, yielded 18 trees of 465 steps, with a consistency
index of 0.4151, a homoplasy index of 0.5849, and a retention
index of 0.6397. Their strict consensus resembles closely the
tree published by MacDougall et al. (2018, Figure 1A), with
Mesosaurus as the basalmost parareptile, and varanopids and
the presumed ophiacodontid Archaeothyris appearing at the
base of Sauropsida (Figure 2D). We also repeated this analysis
with the characters linked to temporal fenestration excluded,
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Laurin and Piñeiro Response: Commentary: A Taxonomic Position of Mesosaurs
as in MacDougall et al.’s (2018) second analysis. The results
(not shown, but available in Supplementary Data Sheet 4)
show a very similar topology, with Mesosaurus at the base of
Parareptilia, varanopids, and Archaeothyris forming a polytomy
at the base of Sauropsida, etc. This, along with the fact that
exclusion of the temporal fenestration characters from our
own matrix does not change the resulting topology, directly
refutes the conclusion by MacDougall et al. (2018, p. 5) that
“we illustrate that the lack of taxa in their matrix combined
with the variability of temporal fenestration in Reptilia are likely
contributing to the tree topology that they obtained in their
phylogenetic analysis...”. Obviously, the differences (including in
the position of mesosaurs) in the topologies supported by our
matrix and theirs must rather be attributed to discrepancies in
character scoring and selection.
DISCUSSION
The differences in character treatment mentioned above
(including the decision to order or not order the states, the
numbering of the states, and most importantly, the way in which
the states are delimited) partly explain why we did not wish
to build our matrix on the basis of more recent versions of
the Laurin and Reisz (1995) matrix, which were produced in
Reisz’s lab after one of us (ML) left that lab, or other matrices
with much more tenuous links with that matrix (e.g., Schoch
and Sues, 2018). In addition to the minor problems discussed
above, our experience has convinced us that it is very difficult for
one systematist to expand another systematist’s matrix because a
certain amount of subjective judgment is involved in character
scoring, and each systematist has his or her own perception
of a given character state. The only way to ensure coherent
application of character state definitions is for a single systematist
to score a given character for all taxa included in a matrix.
Thus, to adequately reuse another systematist’s matrix, it is
unfortunately necessary to more or less redo all the scoring,
after having checked, as we did, which characters should be
ordered and how the ordering should be conducted. Several of
these problems were among those recently discussed, along with
potential solutions, by Simões et al. (2017). And of course, is it
desirable to have studied specimens directly, as illustrations only
provide limited information, even though recent 3D imaging
developments have led to improvements on that front (e.g.,
Tissier et al., 2017).
MacDougall et al. (2018) argue that recent works have
attempted to solve these various problems by improving on
previous state definitions, but our own examination of recently-
published data matrices leads us to believe that we are
unfortunately still very far from that ideal situation. In fact,
some of the changes introduced by MacDougall et al. (2018),
such as their removal of the ratio and threshold values used to
give their character 147 (humeral morphology) a quantitative
basis by Laurin and Reisz (1995), make character scoring less
replicable, so their work certainly does not back up their claim
that substantial progress has been made on this front (at least,
in the last two decades). Updating other systematists’ matrices is
extremely time-consuming if done carefully, as illustrated by the
reanalysis of the matrix by Ruta and Coates (2007) initiated by
one of us (ML) and first tackled in the doctoral thesis of Germain
(2008), continued in another doctoral thesis (Marjanovi´
c, 2010),
and recently published as a pre-print, in three successive versions
in 2015, 2016, and 2018. This work has been under review since
2015 and will be published soon (Marjanovi´
c and Laurin, 2018).
Even though this is an extreme case with respect to the time
investment it required, it does not represent the most thorough
rescoring of a matrix that we have performed. Rather, our work
on a much smaller data matrix of 23 taxa and 42 characters, in
which it was feasible to re-examine the scoring of all cells, resulted
in changes in the scores assigned to 35% of the cells of the matrix,
spread over all taxa and all but two characters (Marjanovi´
c
and Laurin, 2008). These examples well illustrate the point that
reusing other people’s data matrices is not a trivial exercise,
at least if it is to be done correctly, contrary to MacDougall
et al.’s (2018) claim. By starting from one of our own matrices,
we minimized this problem, although we did not eliminate it
completely. According to McShea (2000, p. 330), “It has been
said that most scientists would rather use another scientist’s
toothbrush than his terminology.” We feel the same about other
authors’ phenotypic data matrices (and the stakes in this case
are much higher), unless time is taken to study thoroughly each
character and its distribution to ensure that whoever reworks a
matrix has the same understanding about each character state as
the original author. To sum up, our method did not “patently
ignore over two decades of parareptilian research,” and the
resulting matrix is not outdated; it results from a deliberate
choice to obtain a reasonably reliable matrix with an appropriate
taxonomic sample for a reasonable time investment. It is a
compromise, and as such, we recognize that it is imperfect
and that it can be improved; we only disagree about how this
should be done. Our preferred path is to work with a matrix
that we know well and expand it ourselves, rather than rely
on a patchwork containing additions by several scientists who
may not have understood their predecessors’ concept of each
character.
We showed, through the new analyses presented above,
that taxon selection and temporal fenestration variability do
not appear to explain different topologies obtained by our
group and MacDougall et al. (2018). Strangely, MacDougall
et al. (2018) had all the data required to check these claims
themselves but did not perform the necessary analyses before
publishing their conclusions. At least one other reasonably
recent phylogenetic analysis recovered mesosaurs in a fairly
basal (though unresolved) position among amniotes, outside
Parareptilia (Hill, 2005).
MacDougall et al. (2018) also failed to recognize that
differences between our taxon selection and theirs reflect
different strategies and goals. Rather than trying to sample
densely parareptiles, we included three turtle OTUs
(Odontochelys, Proganochelys, and Chelonii) because turtles
may be parareptiles (Laurin and Reisz, 1995) and because the
presence of this extant taxon in the matrix could have altered
the most parsimonious topology, given their strongly divergent
morphology (compared to parareptiles and diapsids). Thus,
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Laurin and Piñeiro Response: Commentary: A Taxonomic Position of Mesosaurs
including turtles may be a more important way of minimizing
phylogenetic artifacts than adding more parareptile taxa that
strongly resemble those already present in our matrix, though
the taxon deletion tests that we carried out (Laurin and Piñeiro,
2017) neither confirm nor refute this possibility. The origin
of turtles remains one of the great controversies of vertebrate
phylogeny (e.g., Lyson et al., 2010, 2013; Lee, 2013), and it
is potentially relevant to many zoologists. Our matrix, which
we will continue to develop by adding taxa and characters
(through the project involving I. Werneburg, G. Ferreira, and
M. Rabi evoked above), is a step toward resolving this problem.
MacDougall et al. (2018) built their matrix for a more limited
goal (not looking beyond Permo-Triassic taxa), and both
approaches are valid and complementary. Of course, it is possible
to include both many additional parareptile taxa and turtles, but
the more taxa are added, the more characters need to be included
to resolve their relationships. Given that research time is limited,
the more cells a matrix includes, the less time goes into scoring
each of them. In this respect, we agree with Simões et al. (2017)
that too much attention has been given to data quantity, to the
detriment of data quality, in many recent phylogenetic analyses
of morphological data. Thus, there is an optimal number of
taxa and characters for phenotypic matrices; more is not always
better.
The fact that six authors collaborated to publish a short paper
(MacDougall et al., 2018) in response to our own paper (which
has only two co-authors) might be interpreted as an indication
that the response paper carries the strength of consensus among
a significant proportion of the (very small) community of experts
on Permo-Carboniferous amniotes. However, multiple factors
may have contributed to this, including the fact that these
authors had collaborated in previous works, that one of them
supervised the thesis of another, etc. Regardless of these possible
explanations for the number of authors, we note that majority
opinion has never been a safe indicator of scientific accuracy.
This is illustrated by the pamphlet “100 Authors against Einstein”
(in which case the reason for the high number of authors was
clear, contrary to the present situation), which attempted to
refute Einstein’s theory of relativity. Einstein reportedly replied
(Hawking, 1993, p. 98) “If I were wrong, then one [author] would
have been enough!”
AUTHOR CONTRIBUTIONS
ML planned this research, carried it out and wrote most of the
draft. GP wrote part of the text, drafted Figure 1, and provided
comments to improve other parts of the text.
ACKNOWLEDGMENTS
We thank Mark MacDougall for sending the draft of the
paper and the supplements before their publication (but after
definitive acceptance of their paper), at our request. The draft was
improved by comments from David Marjanovi´
c, the handling
editor Corwin Sullivan, and two other reviewers. This work
was financed by a recurring grant from the French Ministry of
Research and the CNRS to the CR2P (for ML) and by a grant
from ANII (GP).
SUPPLEMENTARY MATERIAL
The Supplementary Material for this article can be found
online at: https://www.frontiersin.org/articles/10.3389/feart.
2018.00220/full#supplementary-material
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Conflict of Interest Statement: The authors declare that the research was
conducted in the absence of any commercial or financial relationships that could
be construed as a potential conflict of interest.
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