10 1016@j Geobios 2020 09 005
10 1016@j Geobios 2020 09 005
10 1016@j Geobios 2020 09 005
Original article
Jason J. Head
PII: S0016-6995(20)30097-8
DOI: https://doi.org/10.1016/j.geobios.2020.09.005
Reference: GEOBIO 935
Please cite this article as: J.J. Head, A South American snake lineage from the Eocene Greenhouse of North
America and a reappraisal of the fossil record of “anilioid” snakes, Geobios (2020), doi: https://doi.org/10.1016/
j.geobios.2020.09.005
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A South American snake lineage from the Eocene Greenhouse of
North America and a reappraisal of the fossil record of “anilioid”
snakes
Jason J. Head *
Corresponding editor: Thierry Smith.
Abstract
“Anilioidea” is a likely paraphyletic assemblage of pipe snakes that includes extant
Aniliidae from equatorial South America, Uropeltoidea from South and Southeast
Asia, and a fossil record that consists primarily of isolated precloacal vertebrae
ranging from the earliest Late Cretaceous and includes geographic distributions in
North America, South America, Europe, and Africa. Articulated precloacal vertebrae
from the middle Eocene Bridger Formation of Wyoming, attributed to Borealoilysia
nov. gen., represent an unambiguous North American aniliid record and prompts a
reconsideration of described pipe snakes and their resultant biogeographic histories.
On the basis of vertebral apomorphies, the vast majority of reported fossils cannot be
assigned to “Anilioidea”. Instead, most records represent stem taxa and
macrostomatans erroneously assigned to anilioids on the basis of generalized
features associated with fossoriality. A revised fossil record demonstrates that the
only extralimital distributions of fossil “anilioids” consist of the North American aniliid
record, and there is no unambiguous fossil record of Old World taxa. The occurrence
of aniliids in the mid-high latitudes of the late early Eocene of North America is
consistent with histories of northward shifts in equatorial ecosystems during the early
Paleogene Greenhouse.
Keywords:
Serpentes
Aniliidae
Pipe snake
Systematics
Eocene
North America
1. Introduction
Snakes are a highly diverse, successful vertebrate clade occupying nearly all
non-polar terrestrial, as well as tropical marine, habitats. As such, they are
extensively studied with respect to phylogenetics, evolutionary tempo and mode,
evolutionary development, evolutionary ecology, and origins (Cohn and Tickle, 1999;
Pyron and Burbrink, 2012; Head and Polly, 2015; Hsiang et al., 2015; Leal and Cohn,
2016; Streicher and Wiens, 2016; Myers et al., 2019). Fossils play a central role in
providing temporal, paleoenvironmental, and biogeographic data for such studies
(e.g., Burbrink et al., 2020), which requires rigorous, testable phylogenetic
hypotheses for the identity of fossil taxa in order for them to provide accurate
information (Parham et al., 2012).
The vast majority of the snake fossil record consists of isolated or associated
precloacal vertebrae, and descriptions and interpretations of the record have
historically been inconsistent in justification for, and meaning of, taxonomic
assignments based on vertebral morphology. As a result, the described fossil record
of snakes consists of taxonomic histories that are a conflation of phylogenetically
justified assignments and generalized “form taxon” assignments that are not explicitly
phylogenetic (Head, 2015). This inconsistency has resulted in inflated temporal and
geographic distributions for extant snake clades, which becomes positively
misleading for neontological studies (Noonan and Chippindale, 2006).
The fossil record of pipe snakes represents a prominent example of the
problems with taxonomic identification. Extant pipe snakes include monotypic
Neotropical Anilius scytale and Southern Asian Cylindrophis and Anomochilus
species. They are fossorial and occasionally semi-aquatic taxa that inhabit wet
lowland forests and specialize in preying primarily on elongate vertebrates and
invertebrates (Greene, 1983; Himstedt et al., 2003). Traditional morphological
phylogenetic hypotheses place pipe snakes with uropeltids (shield-tailed snakes) in a
monophyletic clade historically named Aniliidae and subsequently Anilioidea (Bellairs
and Underwood, 1951; Hecht, 1959; McDowell, 1975), which is either sister-taxon to
booid snakes in the clade Henophidia or sister-taxon to Macrostomata, the clade that
includes booids and caenophidians (Rieppel, 1988; Kluge, 1991; Tchernov et al.,
2000; Lee and Scanlon, 2002; Wilson et al., 2010; but see Cundall et al., 1993;
Gauthier et al., 2012). Conversely, molecular phylogenetic analyses find strong
support for paraphyly of Anilioidea with respect to the majority of snakes: Anilius is
consistently recovered as the sister taxon to New World tropidophiid dwarf boas,
whereas Cylindrophis, Anomochilus, and uropeltids either form a poorly resolved
clade with more derived taxa or form the monophyletic Uropeltoidea as sister-taxon
to the clade composed of pythonids, Loxocemus, and Xenopeltis (Gower et al., 2005;
Vidal et al., 2007, Vidal and Hedges, 2009; Vidal et al., 2009; Wiens et al., 2012;
Pyron et al., 2013a, 2013b; Reynolds et al., 2014, Figueroa et al., 2016). Combined
molecular-morphological analyses either recover the generalized molecular topology
with Anilius+Tropidophiidae as sister taxon to all other alethinophidians and
Cylindrophis+Uropeltidae as henophidians (Harrington and Reeder, 2017) or recover
either the morphological or molecular topology, depending on constraint methods
(Hsiang et al., 2015).
The fossil record has the potential to inform on these radically different
hypotheses in terms of timing and geographic distribution. Rochebrune (1880) first
identified a fossil aniliid, “Scytalophis” lafonti from the Eocene of Quercy (see
Hoffstetter, 1955 for reidentification of the taxon as booid), but Hecht (1959) was the
first study to explicitly list vertebral characters considered unique to aniliids in
assigning fossils. Fossil aniliid/“anilioid” taxa have been subsequently described from
the early Late Cretaceous through Pliocene on all continents except for Australia
(e.g., Auffenberg, 1963; Rage, 1974; Holman, 1976; Szyndlar, 1994; Rage, 1998;
Gardner and Cifelli, 1999; Rage and Werner, 1999). Most assignments have used
character combinations similar to Hecht (1959), but many of these characters are
generalized fossorial ecomorphologies present in other snakes and non-snake
squamates (Hoffstetter and Gasc, 1969). Although a few anilioid fossil taxa have
been reidentified as boid (Rage, 1984), reliance on coarse, generalized characters in
assignment persists (e.g., Syromyatnikova et al., 2019), and there has been no
previous attempt to examine which, if any, vertebral characters are diagnostic for
pipe snakes and their relatives.
Here I describe an aniliid snake lineage from the middle Eocene Bridger Fm.,
Green River Basin, Wyoming, based on description of new material, reassessment of
previously described specimens, and re-examination of diagnostic vertebral
morphology within a molecular phylogenetic topology. I then discuss the implications
of the revised record for inferring evolutionary histories of pipe snakes. Because the
molecular phylogenetic topologies I use to infer both vertebral character histories and
the relationships of fossil material support paraphyly of the traditional concept of
Anilioidea with respect to other alethinophidians, I follow the taxonomy of Vidal et al.
(2009) in restricting Aniliidae to Anilius scytale and its fossil relatives and identifying
the clade of Old World taxa as Uropeltoidea. Subsequent discussion of “Anilioidea”
refers explicitly to the traditional, inclusive monophyletic hypothesis.
4. Systematic paleontology
Serpentes Linnaeaus, 1758 sensu Head et al., 2020
Alethinophidia Nopcsa, 1923
Aniliidae Fitzinger, 1826
Genus Borealoilysia nov. gen.
Derivation of the name: “Boreal” (Gr. “boreas”), meaning north, and “Ilysia”, a junior
synonym of Anilius, meaning “Northern Ilysia”, referring to the occurrence of an aniliid
in North America.
Type species: Borealoilysia carinata nov. comb.
Other included species: Borealoilysia gunnelli nov. gen., nov. sp.
Diagnosis (modified in part from Hecht, 1959): Aniliid snake possessing the
following characters: neural spine consisting of low lamina with concave dorsal
margin anteriorly connecting to a short, flat-topped, subtriangular process at the
posterodorsal edge the neural arch; posterior edge of neural spine bifid; accessory
ridges present lateral to the neural spine, terminating posteriorly at the edge of the
neural arch, resulting in a roughly tricarinate posterior edge of the arch in dorsal view;
posteromedian margin of neural arch thick and straight at posterior margins of neural
spine and accessory ridges, posteromedian notch absent; centrum anteriorly wide;
and anterior margin of zygosphene broadly concave.
5. Discussion
5.1. Taxonomic validity of Borealoilysia nov. gen. and vertebral morphological
diagnosis of Aniliidae and Uropeltoidea
The type species of Borealoilysia nov. gen., B. carinata nov. comb., was
originally assigned to Coniophis (Hecht, 1959) but, as discussed below, that genus is
a taxonomic wastebasket of fossorial ecomorphs whose monophyly has long been
considered dubious, and to whom taxonomic referrals have been for convenience
(e.g., Rage et al., 2004; Head and Holroyd, 2008; Smith, 2013; Albino and Brizuela,
2014). The type specimen of Borealoilysia carinata nov. comb., an incomplete
precloacal vertebra, does not share any unique characters with Coniophis
precedens, the type species of the genus, but does possess unique apomorphies of
the posterior neural arch. The species is therefore retained and used to anchor the
new generic designation. Referral of Borealoilysia nov. gen. to Aniliidae requires a
review of vertebral apomorphies of Aniliidae and Uropeltoidea based on
reassessment of previous studies and specimen examination.
Hecht (1959) provided the first explicit vertebral character list for his Aniliidae,
consisting of Anilius, Cylindrophis, and Anomochilus: “(1) the lack of a well-
developed neural spine; (2) the presence of an upward-flaring zygosphene; (3) the
lack of a posterior notch in the neural arch; (4) the lack of a well-developed haemal
carina; and (5) the outline of the vertebrae, square and not broader than long.” Rage
(1984) (reiterated in Holman, 2000, and Ikeda, 2007), diagnosed his superfamily
Anilioidea in part on vertebral characters: “vertebrae depressed; zygapophysial
facets slanting; mid and posterior trunk vertebrae without hypapophyses; paracotylar
foramina absent”, and included within it the family Aniliidae, diagnosed in part on:
“vertebrae rather depressed; neural arch flattened; neural spine poorly developed;
caudal vertebrae without hemapophyses.” Hsiou et al. (2010) included a list of
characters shared by Anilius and Cylindrophis: “a clearly depressed neural arch;
prominent and strongly inclined zygapophyses; short prezygapophyseal process; a
shallow median notch in the posterior border of the neural arch; and a centrum not
markedly widened anteriorly.” A precise angle of greater than 20° for the
prezygapophyses was considered a shared character of Anilius, Cylindrophis, and
fossil taxa referred to Anilioidea sensu lato (Hsiou et al., 2010). Hsiou et al. (2010)
additionally listed a uniform centrum width and small prezygapophyses, as
characters shared by Anilius, Cylindrophis, and the fossil taxon Colombophis.
The coarse degree of morphological specificity provided in these diagnoses
encompasses characters present in a wider sample of taxa than those grouped into
Aniliidae, Uropeltoidea, or “Anilioidea”. For example, reduction of the neural spine
and depression of the neural arch are characters associated with fossoriality among
scolecophidians and macrostomatans (e.g., Hoffstetter and Gasc, 1969; Rage, 1984;
Lawing et al., 2012), and the absence of characters such as a haemal keel,
hypapophyses on mid-trunk vertebrae, hemapophyses, and paracotylar foramina, as
well as a possession of a reduced or absent posteromedian notch, uniform centrum
width, and small prezyagpophyseal accessory processes are plesiomorphies for
crown Serpentes (e.g., Hoffstetter, 1959; Lee and Scanlon, 2002; Wilson et al.,
2010). Additionally, these diagnoses either implicitly assume monophyly of Anilius
with Old World uropeltoids or treat “Anilioidea” as a form taxon (Hsiou et al., 2010;
see also Smith, 2013 for discussion). No study has examined vertebral morphology
of Aniliidae or Uropeltoidea (sensu Vidal et al., 2007) for diagnostic characters under
a hypothesis of “anilioid” paraphyly.
Examination of Anilius, Cylindrophis, and uropeltid species, as well as
representative scolecophidians and fossorial macrostomatans, provides revision of
these characters in order to determine the interrelationships of Borealoilysia nov.
gen. and the published fossil record of anilioids sensu lato. The following list
examines the most common characters used to identify “anilioids”:
High-angled prezygapophyses (Fig. 3): High-angled zygapophyses with
angles exceeding 30° occur in taxa across Squamata (e.g., Hoffstetter and
Gasc, 1969: fig. 42), and measuring variation of prezygapophyseal angle within
the mid to posterior precloacal vertebral column in representative crown snakes
does not support a high angle as a diagnostic feature shared by Anilius and
uropeltoids to the exclusion of other taxa (Fig. 3). Uropeltoidea does possess
higher average angles than other taxa (>24°, represented by Cylindrophis and
Uropeltis); however, the approximate 20° angle in Anilius is lower than in at
least some typhlopid taxa (Fig. 3(D)) and is approached by boid taxa including
Charina and Eryx species (Fig. 3(H, I)). Intracolumnar variation within sampled
taxa is approximately 5-7°, which additionally limits the ability to identify or
distinguish taxa based on a limited sample size. Anilius and uropeltoids do
share a dorsal extension of the prezygapophyses; however, there is variation in
this character as well. In uropeltoids, the prezygapophyses will reach or extend
dorsally to the level of, or beyond, the zygosphenial roof due to the high angle
of the processes, whereas they generally extend just ventral to the roof in
Anilius due to the lateral elongation of lower-angled processes (compare Fig.
3(A-C));
Neural spine (Fig. 4): The neural spine in squamates generally consists of a
thin lamina that extends along the anteroposterior midline of the neural arch
and is continuous with a more thickened posterior process that arises from the
posteromedian edge of the arch. In Anilius (Fig. 4(A.1, A.2)), the lamina is
reduced with a concave to straight anterodorsal margin that joins with the short
posterior process. There is anterior-posterior intracolumnar variation in spine
height, and the spine is more distinct in anterior precloacal vertebrae, becoming
progressively reduced posteriorly. Among uropeltoids, Cylindrophis completely
lacks any anterior lamina (Fig. 4(C.1, C.2)), and only a small ridge is present at
the midpoint of the neural arch in some uropeltids (Fig. 4(D.1, D.2));
Depression of the neural arch (Figs. 3, 4): In Anilius and uropeltoids, the
neural arch is low with an approximately straight posterodorsal margin that
diverges ventrolaterally from the midline of the element at a low angle between
ca. 10° and 20° in mid-posterior precloacal vertebrae. This differs from the
condition in most alethinophidian and examined scolecophidian snakes, in
which the neural arch is high and ventrolaterally curved or bi-angled (Fig. 4(B.1,
B.2)) where it roofs a comparatively elevated zygantrum, and the straight-line
angle of the arch, measured from the lateral edge of the postzygapophysis to
the base of the neural spine or midline of the element, is generally between 20°
and 30°;
Posteromedian notch of the neural arch (Fig. 4): In most squamates, the
posterior margin of the neural arch is transversely straight. In alethinophidians,
the posterior margin of the neural arch is deeply medially emarginated forming
an acutely-angled notch that exposes the dorsal surface of the condyle and
posterior central body in disarticulated specimens. In Anilius and uropeltoids,
the posterior edge of the arch ranges from nearly straight in the most anterior,
and sometimes posterior vertebrae to shallowly emarginated in most elements.
The emarginated edges are broadly convex and well-developed consistently in
Anilius (Fig. 4(A.1)) and variably in uropeltid species (e.g., Uropeltis
madurensis). The notch is most weakly developed in Cylindrophis, where it is
nearly absent in some specimens, and most uropeltid species among examined
alethinophidians (Fig. 4(C.1, D.1));
Development of the haemal keel (Fig. 4): A keel is present in Anilius and
variably present in uropeltoids. In Anilius, the keel is a narrow ridge with a wider
spatulate posterior extent in the anterior region of the precloacal vertebral
column and becomes slightly wider and medially constricted in mid and
posterior precloacal vertebrae (Fig. 4(A.3)) as the ventral surface becomes
progressively more excavated by subcentral paralymphatic fossae. In
Cylindrophis species, the pattern of anterior-posterior variation is similar to
Anilius, but the keel is wider and more poorly developed (Fig. 4(C.3)). In
uropeltids, development of the keel ranges from a similar extent as in Anilius to
practically absent (Fig. 4(D.3)), being only weakly defined by paralymphatic
fossae.
To test the systematic utility of these characters, I discretized different states
based on specimen observation (see above, Material and methods), and optimized
character states onto a tree topology that represents the consensus of molecular
studies (e.g., Pyron et al., 2013a, 2013b; Reynolds et al., 2014) (Fig. 5). I included
Borealoilysia nov. gen., based on character states of both B. carinata nov. comb. and
B. gunnelli nov. gen., nov. sp., and included Cylindrophis and uropeltid species to
represent Uropeltoidea because specimens of Anomochilus were not available for
study. I used parsimony ancestral state reconstruction in Mesquite 3.61 (Maddison
and Maddison, 2019) to infer potentially diagnostic characters for Aniliidae and
Uropeltoidea. The following is the list of character codings I used in analysis based
on the aforementioned character observations. The taxon-character matrix is
provided in Table 1:
1. Prezygapophyseal angle: > 25° = 0; 20°-25° = 1; <20° = 2;
2. Prezygapophyses extend to level of top of neural canal: present = 0;
absent = 1;
3. Neural spine lamina: present = 0; reduced = 1; absent = 2;
4. Angle of neural arch in posterior view: 20°-30° = 0; 10°-20° = 1;
5. Posteromedian neural arch: absent or shallowly concave = 0; present, weakly
defined = 1; strongly defined with acute edges = 2;
6. Haemal keel: absent = 0; broad, poorly defined = 1; narrow = 2.
Under the molecular phylogenetic hypothesis of pipe snake paraphyly,
traditional characters are homoplasies associated with fossorial habits between
Anilius and uropeltoids, as additionally indicated by the variable occurrence of
several of these characters in scolecophidians. Conversely, optimization of refined
character states reduces the amount of inferred homoplasy and provides
differentiating diagnoses based on vertebral morphology. Of the six characters
examined, only elevation of prezygapophyses to the level of the top of the neural
canal and a depressed neural arch optimize as homoplastic between Aniliidae and
Uropeltoidea (Fig. 5).
Aniliidae, based on Anilius, is diagnosable on the combination of: elongate
prezygapophyses elevated to just shorter than zygosphene, and angled at an
average of 20°-25°; neural spine with short anterior lamina running much of neural
arch length; and depressed neural arch. A narrow, medially emarginated haemal keel
on mid and posterior precloacal vertebrae additionally distinguishes Anilius from
uropeltoids but is present in the greater diversity of alethinophidians. Uropeltoidea is
diagnosable on the combination of: high-angled prezygapophyses (an average of
>24°); neural spine lamina absent or greatly reduced, spine restricted to posterior
edge of neural arch resulting in a saddle-shaped dorsal margin of the neural arch in
lateral view; depressed neural arch; and shallow concave posteromedian notch.
Within Uropeltoidea, examined uropeltid species all possess relatively narrow
zygosphenes with strongly concave dorsal margins, to the exclusion of Cylindrophis.
Borealoilysia nov. gen. shares the orientation and elevation of the
prezygapophyses, presence of a reduced neural spine lamina, and a depressed
neural arch with Anilius (Fig. 5), and B. carinata nov. comb. additionally shares a
narrow haemal keel. The neural spine lamina is more prominent in the type
specimens of B. carinata nov. comb. and Coniophis platycarinatus (see below)
(Hecht, 1959: pls. 52, 53) than in B. gunnelli nov. gen., nov. sp., though this may
represent taphonomic abrasion on DMNH EVP 57990A. The posteromedian notch of
the neural arch is more weakly developed in Borealoilysia nov. gen. and is more
superficially similar to the condition in uropeltoids. However, the posteromedian
margin of arch is uniquely thick and expanded in Borealoilysia nov. gen., suggesting
that the notch is apomorphically shallow relative to other taxa. Placement of
Borealoilysia nov. gen. as sister taxon to Anilius requires one less character
transformation than as sister to uropeltoid taxa, and the shared diagnostic characters
with Anilius provides justification for assigning Borealoilysia nov. gen. to Aniliidae.
6. Conclusions
The fossil record of “anilioid” snakes is not nearly as diverse as previously
described based on revision of systematically informative vertebral morphology. The
North American Paleogene record of Borealoilysia nov. gen. represents the only
continental-scale extralimital distribution of the clade and is a component of the larger
pattern of Northward expansion of equatorial faunas during the Paleogene
Greenhouse. There is no unambiguous record of Old World Uropeltoidea, despite a
wide geographic distribution, ecological specialization, and relative species richness
among extant taxa. Studies that use the fossil record to inform on evolutionary
histories, such as calibrating evolutionary rates and estimating biogeographic mode,
of extant snake taxa should rely only on fossil records that have been critically
evaluated (e.g., Parham et al., 2012).
Acknowledgements
Research was funded by a Natural Environmental Research Council Award
(NE/S000739/1) to JJH. For access to specimens, I thank R. Stucky, J. Sertich, and
T. Lyson (DMNS), M.T. Carrano (NMNH), D. Gower and P. Campbell (NHM-UK),
C.J. Bell (TMM), and N. Jones, M. Lowe, and R. Stebbings (UMZC). I thank J.
Maisano (UTCT) for C-T scanning, postprocessing, and image construction of
DMNH EVP 57990A and K. Smithson (CBC) for C-T scanning of extant specimens. I
thank J.I. Bloch and T. Smith for discussion and T. Smith for the invitation to
contribute. I thank A. Folie, K. Smith, and an anonymous reviewer for comments that
greatly improved the manuscript. Most of all, I thank Gregg Gunnell for his
mentorship and support through our many years of friendship.
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Table and Figure captions
Table 2. Described fossil record of aniliid and “anilioid” snakes and their systematic
reassessments based on this study.
Figure 1. Map of Wyoming showing location of Greater Green River Basin (dark
grey). Fossil localities: 1, “Hyposodus Hill”; 2, DMNH loc. 727 “Gatortown”.
Figure 2. Borealoilysia gunnelli nov. gen., nov. sp. Articulated precloacal vertebrae in
anteroventral (A), dorsal (B), left lateral (C), ventral (D), and posterior (E) views.
Anatomical abbreviations: ar, accessory ridges; hk, haemal keel; nspl, neural spine
lamina; pcvlp, paracotylar ventrolateral processes; prz, prezygapophyses; psp,
posterior spine process; tpm, thickened posterior margin of the neural arch. Scale
bar: 5 mm.
Taxon 1 2 3 4 5 6
Squamate outgroup 0 0 0 0 0 0
Scolecophidia 1&2 1 2 0 0 0
Anilius scytale 1 0 1 1 1 2
Borealoilysia 1 0 1 1 0 1&2
Tropidophiidae 2 1 0 0 2 2
Boidae 2 1 0 0 2 2
Pythonidae 2 1 0 0 2 2
Cylindrophis 0 0 2 1 0&1 1
Uropeltidae 0 0 1&2 1 0&1 0&1&2
Bolyeridae 2 1 0 0 2 2
Caenophidia 2 1 0 0 2 2