Introduction
The early–middle Permian transition was a crucial period in the evolution of
early synapsids. During the Cisuralian, terrestrial faunas were dominated by
a paraphyletic grade of six synapsid families known as pelycosaurs. However,
at the start of the Guadalupian these declined in diversity, possibly due to
a mass extinction event (Sahney and Benton, 2008; Brocklehurst et al.,
2013), and the Therapsida (the clade containing mammals) became more diverse
and abundant. This transition coincides with a shift in the location of
greatest sampling from the palaeoequatorial localities of North America and
western Europe to the palaeo-temperate localities of South Africa and Russia.
There is only a brief period of temporal overlap between the Russian and
North American localities in the latest Kungurian and Roadian (Benton,
2012).
Two of the six pelycosaur families are known to have survived into the
middle Permian and dispersed into the palaeo-temperate latitudes. Species of
Varanopidae are known from both Russia and South Africa (Dilkes and Reisz,
1996; Reisz et al., 1998; Modesto et al., 2011; Reisz and Modesto, 2007;
Botha-Brink and Modesto, 2009), as late as the Pristerognathus
Assemblage Zone (latest Capitanian) of the Karoo Supergroup (Modesto et al.,
2011). Thus, Varanopidae represents not only the geologically longest living pelycosaur family
but also the geographically most widespread. The second such
family is Caseidae. Although this family was most diverse in the San Angelo
and Chickasha formations of North America (Olson, 1962, 1965, 1968;
Brocklehurst et al., 2013), a substantial species richness of caseids was
recently also reported from Europe (Berman et al., 2004; Reisz et al., 2011;
Romano and Nicosia, 2015; Spindler et al., 2015), and the Russian species
Ennatosaurus tecton appears to have been quite abundant in the
Mezen Faunal Complex (Efremov, 1956).
A possible second Russian caseid has been tentatively put forward:
Phreatophasma aenigmaticum, from the middle Permian Golyusherma
Group. First described as a therapsid from the family Phreatosuchidae
(Efremov, 1954), it was reassigned to Caseidae by Olson (1962), although the
lack of material made this assignment extremely uncertain.
Phreatophasma is represented by only a single femur and has not
received substantial attention since Olson's monograph on the family
Caseidae (Olson, 1968). A brief note by Golubev (2000) cast doubt on its
caseid affinities and suggested it might be a seymouriamorph, although no
discussion of specific morphological characters was supplied.
Now, however, our knowledge of the postcranial morphology of early synapsids
has substantially increased (Benson, 2012), as has our knowledge of the
evolution and phylogeny of caseids (Reisz, 2005; Maddin et al., 2008; Reisz
and Fröbisch, 2014; Spindler et al., 2015; Romano and Nicosia, 2015;
Brocklehurst et al., 2016a). Thus, following a re-examination and
phylogenetic analysis of the specimen, we are able to confirm the assignment
of Phreatophasma to Caseidae.
Discussion
Caseid affinities of Phreatophasma
Phreatophasma aenigmaticum has been assigned at various points in
history to three different clades. In the original description, Efremov
(1954) assigned it to the family Phreatosuchidae along with two other
Russian genera: Phreatosuchus and Phreatosaurus.
Phreatosuchidae are usually inferred to be therapsid synapsids, possibly of
dinocephalian affinity (Olson, 1962; King, 1988; Ivakhnenko, 1991). However,
Efremov (1954) acknowledged that Phreatophasma showed some
similarities with edaphosaurid and caseid pelycosaurs. Olson (1962)
suggested that Phreatophasma should be assigned to Caseidae, based
on the dorsal inflection of the proximal end of the femur (giving, as he
described it, a “sphinx-like” profile in anterior view), a deep
intertrochanteric fossa, and the widely spaced distal condyles. Olson (1962)
did add a note of caution to this assignment, acknowledging the scant
material. In later summaries of pelycosaurian-grade synapsids and their
evolution (e.g. Olson, 1968; Reisz, 1986; Brocklehurst et al., 2013), this
assignment was repeated with the same advice of caution.
A third suggestion for Phreatophasma's affinity was made by Golubev
(2000) in his summary of the faunal assemblages of the Permian terrestrial
vertebrates in Russia. In this monograph, he assigned Phreatophasma
to Leptorophinae, a subfamily of seymouriamorph amphibians. This
assignment was justified in a brief footnote, noting that
Phreatophasma closely resembled the femur of the seymouriamorph
Kotlassia. The leptorophines, closely related to
Kotlassia, are common in the copper mines where
Phreatophasma was found. Unfortunately, Golubev (2000) did not
actually state any of the characteristics that he felt united
Phreatophasma with seymouriamorphs. Moreover, the femora of the two
leptorophine taxa from Golyusherma (Biarmica and
Leptoropha) are unknown, making a direct comparison impossible.
While Kotlassia's femur does share with Phreatophasma the
broad proximal end flexed dorsally, in other respects there seem to be great
differences. In general proportions, the taxa show few similarities;
Kotlassia has a long, slender femoral shaft; the distal condyles
are narrowly spaced; and the intertrochanteric fossa, though
antero-posteriorly broad, is shallow (Bystrow, 1944). It is true that there
is considerable variation in femoral proportions in seymouriamorphs;
Seymouria itself had an extremely robust femur with a short shaft,
that of Utegenia was short and dorso-ventrally flattened, and the
Russian leptorophines include forms with longer shafts and deeper
intertrochanteric fossae (Kuhn, 1972; Klembara and Ruta, 2004). However,
there are other reasons to reject a seymouriamorph affinity for
Phreatophasma. The proximal and distal ends of its femur are
heavily ossified, contrasting strongly with those of seymouriamorphs. The
prominent separation of the bulbous distal condyles also conflicts strongly
with seymouriamorphs, whose condyles are pressed close to each other as well
as being more antero-posteriorly slender. Moreover, although the
heavily weathered ventral surface of Phreatophasma does make
comparison difficult, there is no evidence of the large and prominent
adductor ridge that extends far distally, often onto the posterior condyle, in Kotlassia and the Russian seymouriamorphs.
A therapsid affinity is also rejected. The intertrochanteric fossae of
therapsid femora are greatly reduced compared to pelycosaurs, while the
distal condyles are low and indistinctly separated (Sidor and Hopson,
1998). These characters are seen in Phreatosuchus and
Phreatosaurus (Fig. 2) but are absent in Phreatophasma.
Instead, Phreatophasma is deemed to be a caseid, as judged by Olson
(1962). Although the sphinx-like profile is not as strong a support of
caseid affinity as was thought (it is also observed in edaphosaurids and
several amphibian clades, including seymouriamorphs), the other
characteristics cited above do support such an assignment. Also indicating a
caseid affinity are the short, robust femoral shaft and the lack of a
longitudinal ridge enclosing the posterior margin of the intertrochanteric
fossa.
Two femoral specimens assigned to the therapsid clade
Phreatosuchidae. (a) PIN 954/75, holotype of Phreatosaurus bazhovi;
(b) PIN 1954/76, holotype of Phreatosuchus qualeni. Abbreviations
as in Fig. 1.
If Phreatophasma is indeed a caseid, it is necessary to compare it
to the only other Russian caseid known: Ennatosaurus tecton
(Efremov, 1956) from the younger Mezen faunal complex. It is obvious that
these taxa are not synonymous, and it appears unlikely that they are closely
related beyond both being caseids. Although the Ennatosaurus femur
studied represents a juvenile individual (PIN 1580/107) and
Phreatophasma appears to be more advanced in its ontogeny due to
the extensive ossification of the distal condyles, the femur of the juvenile
Ennatosaurus is substantially larger. The rugose mound on the
dorsal surface of the femur is considerably more prominent in
Ennatosaurus than Phreatophasma, and the dorsal inflection
of the proximal end is more pronounced in the former. Phreatophasma
appears to be more plesiomorphic than Ennatosaurus, as its anterior
condyle is not compressed and the posterior condyle does not extend
considerably further distally than the anterior. A basal position within
caseids might also be supported by the small size; caseids appear to have
shown a trend towards increased body size during their evolution (Reisz and
Fröbisch, 2014).
Phylogenetic analysis
In order to test the relationships of Phreatophasma, the specimen
was incorporated into two phylogenetic analyses: the first was a global analysis
of pelycosaurian-grade synapsids in order to confirm the caseid affinity,
and the second was an analysis devoted to caseids, containing a wider sampling
of caseid taxa. For the first of these analyses, Phreatophasma was
added to the matrix of Brocklehurst et al. (2016b). This matrix is an
expanded version of that of Benson (2012), who incorporated a larger number
of postcranial characters than had previously been considered. At present,
this matrix represents the most comprehensive examination of pelycosaur
relationships, both in terms of character and taxon sampling. The matrix was
analysed in TNT version 1.5 (Goloboff et al., 2008), using the new
technology-driven search at level 100. The minimum length was searched
100 times using the drift, fusion, and sectorial search algorithms. Each most
parsimonious tree found using this search was then used as the starting tree
in a branch and bound search. Node support was calculated using the relative
fit difference (Goloboff and Farris, 2002).
The analysis identified 1920 most parsimonious trees of a length of 785 and
retention index of 0.74, with very little resolution within caseids. After
removing the wildcard taxon Caseopsis agilis, 361 trees remained,
with considerably better resolution in this family. Phreatophasma
was found to occupy a basal position within Caseidae (Fig. 3), in a
polytomy with Datheosaurus, Oromycter, and the clade
containing Casea broilii and all caseids more derived. Although a
caseid affinity for Phreatophasma is well supported, its precise
position within Caseidae is not as well supported, which is unsurprising given the
completeness of the specimen. Its position in a clade containing all caseids
except for Callibrachion and Eocasea is based on the lack of
the ridge enclosing the posterior margin of the intertrochanteric fossa. Its
more basal position than Casea broilii is indicated by the femoral
condyles having very similar distal extents and by the lack of compression
of the anterior condyle. It should be noted, however, that the latter
character appears to be somewhat plastic, being reversed (uncompressed) in
more derived taxa such as Casea nicholsi, Caseopsis, and
Ruthenosaurus.
Relationships of caseids found by adding Phreatophasma to
the matrix of Brocklehurst et al. (2016b) after removing the wildcard taxon
Caseopsis. Relationships within Eupelycosauria are identical to
those found by Brocklehurst et al. (2016b).
Phreatophasma was also added to the matrix of Romano and Nicosia
(2015), who analysed caseid relationships using a mixture of discrete
characters and what they termed morphometric characters (ratios of linear
measurements treated as continuous characters). Also added to this matrix
was Vaughnictis smithae (formerly Mycterosaurus smithae),
recently redescribed as an eothyridid caseasaur (Brocklehurst et al.,
2016b), in order to add some postcranial data from this family. Two separate
analyses were carried out using this dataset. First the morphometric
characters were analysed unaltered as continuous characters in TNT. Each
morphometric character was scaled from 0 to 65 (the minimum and maximum values
allowed in TNT), and the discrete characters were weighted at 65 to allow
for the reduced possible number of character changes. The matrix was
analysed in TNT using the same settings described above.
The second analysis using the Romano and Nicosia matrix followed the
suggestion of Brocklehurst et al. (2016a). The ratios were first transformed
using the log-ratio method (Aitchison, 1986) and were then subjected to a
principal component analysis in order to reduce issues of redundancy and
character non-independence. The principal component scores were treated as
continuous characters (hereafter these characters are referred to as PC
characters). The log-ratio transformations were carried out in R version
3.03 (R core team, 2013) using functions from the packages robCompositions
(Templ et al., 2011), and the principal component analysis was carried out in
Past 3.11 (Hammer et al., 2001) using the iterative imputation method to
treat missing values. The PC characters were scaled in the manner described
by Brocklehurst et al. (2016a) so that each contained values between 0 and
65, and the relative variances of the PC characters were equal to the relative
variances of the principal coordinates.
Both analyses using the Romano and Nicosia (2015) dataset
supported the global pelycosaur analysis in finding Phreatophasma
in a basal position within caseids (Fig. 4). Again, in both analyses, support
for a monophyletic Caseidae containing Phreatophasma is high, but
support for its precise position is low. Each found three most parsimonious
trees, the first of length 42 883.237 and the second of 1434.131, and in the
strict consensus Phreatophasma resides in a polytomy with
Oromycter, “Casea” halselli, and the clade containing all
other caseids. The positions of “Casea” halselli as a basal caseid
is novel, although it should be noted that this is an extremely incomplete
taxon and its position in the phylogeny has been highly unstable in previous
analyses (Romano and Nicosia, 2015; Brocklehurst et al., 2016a).
Unfortunately the limited overlap between the preserved elements of
Phreatophasma, Oromycter, and “Casea” halselli
limits the possible resolution at the base of Caseidae.
Relationships of caseids found by adding Phreatophasma to
the matrix of Romano and Nicosia (2015). (a) Continuous characters
represent morphometric characters of Romano and Nicosia (2015).
(b) Continuous characters represent PC characters of Brocklehurst et al. (2016a).
In addition to the discrete characters described above, the morphometric
characters add further information. The characters supporting a basal
position of Phreatophasma include a lower value for the ratio of the
anterior condyle width and total femur length than more derived caseids, i.e.
Phreatophasma either has a longer femur or a narrower anterior
condyle. This is supported by the phylogenetic analysis using PC characters;
Phreatophasma has a lower value of PC character 12 than more
derived caseids. This PC character is heavily loaded towards, among other things,
ratios indicating a relatively longer femur in Phreatophasma but
with wider proximal and distal heads and shaft.
Evolution of Caseidae
The phylogenetic analyses including Phreatophasma have some
important implications for caseid evolution and biogeography. The basal
position of Phreatophasma, far from that of Ennatosaurus,
indicates that there were at least two dispersal events between the
palaeoequatorial and palaeo-temperate latitudes in this family (Fig. 5).
This, combined with the fact that the European taxa are widely dispersed
through the tree rather than forming a closely related grouping, implies
relatively free dispersal between the different environments. Although
Phreatophasma is of Roadian age, its position in the phylogeny
implies a ghost lineage extending at least as far back as the early
Artinskian, and possibly even earlier depending on its precise position
(Fig. 5). The position of Ennatosaurus also implies a ghost lineage
extending back into the early Permian, although not as far. It is
unfortunate that we have no knowledge of the Russian terrestrial vertebrate
faunas prior to the Kungurian, meaning that the precise timing of the caseid
invasions and their abundance prior to the diversification of therapsids is
unknown.
Distribution of caseids through time and space. Tip labels
represent geographic location. Abbreviations: WEU – western Europe; RUS –
Russia; USA – the United States of America.
The phylogenetic analyses also imply the survival of a broader range of taxa
into the middle Permian than previously thought. Earlier examinations
indicated that the taxa that crossed the Kungurian–Roadian boundary were all
large, derived herbivores (Benton, 2012; Brocklehurst et al., 2013).
However, Phreatophasma demonstrates that small basal caseids were
also able to survive into the middle Permian. The taxa most closely related
to Phreatophasma, such as Datheosaurus and
Oromycter, seem to have represented medium-sized omnivores or
carnivores (Reisz, 2005; Reisz and Fröbisch, 2014; Spindler et al., 2015)
rather than high-fibre herbivores. The confirmation of
Phreatophasma's caseid affinity implies that middle Permian caseids
were not only more speciose than other pelycosaur clades (Brocklehurst et
al., 2013) but were also more morphologically diverse.