Evolution and Taxonomy of Snakes

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CHAPTER
2
2.1 INTRODUCTION
This chapter arrives at an interesting and exciting time in the study of
snake systematics. The last part of the 20th century and the early part
of the 21st century might ultimately be highlighted as the intersection
between traditional classifications of snakes based on morphology and
those based on molecular data. Classification of organisms has typically
and traditionally relied on morphological traits to guide the process, either
by phylogenetic methods that attempt to be concordant with evolutionary
history or by more arbitrary methods that apply the use of authoritative
interpretation of morphology by experts in the field. Given the real
possibility of evolutionary convergence among morphological characters in
organisms, such as in snakes and other limbless squamates (see Wiens et al.
2006), it seems that having a credible understanding of relationships among
extant serpents will be through the use of molecular systematics. Another
advantage is that molecular systematics can provide thousands to millions
of characters as well produce species tree relationships using independently
evolving gene estimates free from linkage or convergence. However, there
have been important studies using rigorous phylogenetic methods on a
large suite of morphological characters scored from extant and extinct
snakes (something molecular methods cannot address) that reveal the
utility of these characters to address phylogeny (Lee and Scanlon 2002; Lee
et al. 2007). Therefore, we are not saying that traditional classifications based
on morphology are entirely incorrect; in fact many of them still hold up
well. However, several studies are revealing that certain traditional groups
Evolution and Taxonomy of
Snakes
Frank T. Burbrink
1
and Brian I. Crother
2
1
Biology Department, 6S-143, 2800 Victory Blvd., College of Staten Island/CUNY, Staten Island,
New York 10314 USA
2
Department of Biology, College of Science and Technology, Southeastern Louisiana University,
Hammond, LA 70402 USA

20 Reproductive Biology and Phylogeny of Snakes
simply cannot be credible given the agreement among independently
evolving genes (e.g., the traditional macrostomata, Anilioidea, Colubridae
are all likely paraphyletic). Moreover, molecular methods will be more
useful at examining relationships at the levels of species, genera, and
families. Arriving at a strong consensus with robust trees among studies
using unlinked genetic markers has already helped illuminate evolutionary
relationships among snake species. These molecular studies inform
taxonomy by naming groups that are concordant (i.e., monophyletic) with
the evolutionary history of the taxon. These phylogenies ultimately help
comparative biologists attain a better understanding of the independent
origins of various morphological characteristics, ecologies and behavior.
While we extol the virtues of the current state of molecular systematics
and realize how the field will aid the “scholarly snake community” to better
comprehend the origins and relationships of snakes, we also realize that our
understanding based on a handful of markers is likely to change as snake
phylogeneticists lumber into the world of phylogenomics and coalescent
based species tree estimation (Edwards 2009). Currently, the only species
tree estimation paper that also uses the largest number of genes to date
(25 independent loci) has been applied using single representatives of only
21 major snake groups/families (Pyron and Burbrink, unpublished data;
but see Wiens et al. 2008). In contrast, the densest sampling of snakes for
a single phylogenetic project is only 232 species out of ~3,150 described
taxa, and using only a single gene (Eckstut et al. 2009). Given the decreasing
costs for next generation DNA sequencing, it is conceivable that snake
systematists will produce phylogenetic trees using thousands of single
copy, unlinked genes sampled across the genome for hundreds of species,
while properly inferring the species tree given the uncertainty in the
gene tree. This again may rapidly change our notions of snake taxonomy
and evolutionary relationships. On the other hand, it may show that the
information given in number of substitutions and sorting of lineages may
never be adequate to resolve some situations. That is, some relationships
may simply not be knowable.
This chapter provides a brief overview of the relationships, defining
characteristics, and geographic area and dates of origin of all major extant
snake groups. Several radical taxonomic changes have been proposed for
certain groups in the last decade, leaving little strong consensus about the
taxonomy of a given group. For example, several researchers have proposed
major changes to the group Colubroidea, yet no single taxonomic scheme has
taken hold. We therefore discuss the most conservative aspects of modern
snake taxonomy based on published research. This chapter is not meant to
be the lexicon of snake taxonomy but rather a fairly detailed introduction
to snake systematics primarily based on results from modern studies.
2.1.1 What are Snakes?
We know that snakes are squamates and deeply embedded in the lizard
phylogeny. In fact, snakes are simply a very specialized group of extremely

Evolution and Taxonomy of Snakes 21
diverse limbless lizards. As such, snakes are members of the second most
speciose group of living reptile (see Reptile Database: http://www.reptile-
database.org/). The evolution of limblessness is quite common in lizards
and, including snakes, has evolved independently at least 25 times (Wiens
et al. 2006). However, no limbless lizard clade is as successful as snakes,
with ~3,150 species occurring in nearly every habitat on every continent
except Antarctica. Snakes form a monophyletic group and the best available
phylogenetic evidence using molecular data, free from morphological
convergence due to reduction in character states, suggest that snakes are not
related to other limbless lizards like amphisbaenids or dibamids, but rather
group with iguanians, lacertiforms and anguimorphs (Townsend et al. 2004;
Eckstut et al. 2009; see Douglas et al. 2006 for a contrasting molecular view).
The exact placement of snakes within the lizards has yet to be determined,
but using multiple independently evolving loci, both Townsend et al. (2004)
and Vidal and Hedges (2005) demonstrated a close relationship between
snakes and anguimorphs, which has also been suggested by other authors
(e.g., McDowell and Bogert 1954; Jamieson 1995; Lee 1998; Reynoso 1998;
Lee and Caldwell 2000; Eckstut et al. 2009). Several studies that include
morphological data have claimed a closer relationship between varanids
or mosasaurs and snakes (Lee 1997, 1998, 2000; Caldwell 1999; Lee and
Caldwell 2000; Lee and Scanlon 2001; Scanlon and Lee 2002; Caldwell
and DalSasso 2004) or a group consisting of amphisbaenids, dibamids and
snakes. The most recent large scale morphological study, which included
fossils, suggested snakes are most closely related to scincoids, the sister
to a clade of trogonophids, amphisbaenids, and rhineurids (Conrad 2008).
The relationships suggested by these morphological studies have been
soundly rejected by those using multiple independently evolving genetic
markers, suggesting that convergent evolution or poor character scoring
was responsible for these hypothesized relationships.
The early evolutionary history of snakes inferred from the fossil
record portrays a fascinating story about the independent evolution of
limb reduction in serpents. The earliest identified snake, Najash rionegrina,
found in Upper Cretaceous deposits in Argentina, was a small terrestrial
or burrowing serpent with sacral vertebrae, pelvic elements and hindlimbs
(Apesteguia and Zaher 2006). This study conflicts with some theories that
suggest snakes (along with their adaptive limb reduction) originated in
aquatic habitats, as this earliest snake fossil provides solid evidence for a
burrowing/terrestrial origin of snakes. Other Cretaceous fossils, Pachyrhachis
problematicus, Haasiophis terrasanctus, and Eupodophis descouensi are all
shallow marine species from Northern Gondwana, found along the Tethyan
Coast. These three taxa have hindlimb bones but lack differentiated sacral
vertebrae for anchoring pelvic elements (Caldwell and Lee 1997; Tchernov
et al. 2000; Rage and Escuillié 2000). Moreover, Apesteguia and Zaher (2006)
using phylogenetic analyses of morphological data demonstrated that
these three fossil taxa do not represent the earliest snakes but are rather
nested within the radiation of macrostomatan snakes (see our discussion

22 Reproductive Biology and Phylogeny of Snakes
on Alethinophidia for an alternate view of macrostomatan monophyly).
Along with some extant groups (e.g., scolecophidians, boids, pythonids
and aniliids), these fossils show that complete limb loss has occurred
independently throughout the early evolution of snakes.
All extant snakes share a series of characters including absence of the
pectoral girdle and forelimbs. However, remnants of the pelvic girdle are
found in various groups including scolecophidians, pythonids, boids, and
aniliids. Cloacal spurs appear in boids, pythonids and aniliids (McDowell
1987; Cundall et al. 1993). The elongated features of snakes are due to an
increase in vertebrae ranging from 120 to 500. Like lizards, all snakes are
covered in scutes, with ventral scales extending from the throat to the
tail tip, and genitalia are either a single or bilobed organ referred to as
a hemipenis. Characters (or character states) unique to snakes include: a
supraoccipital that is excluded from the border of the foramen magnum by
the exoccipitals, down growths of the parietal bones enclose the ophthalmic
branch of the trigeminal nerve which enters the orbit through the optic
foramen, the size of the left arterial arch is greater than the right (the reverse
is found in most tetrapods), flexible ligamentous connection between
dentaries, and a lack of ciliary muscles in the eyes. Many other characters
(e.g., characters responsible for increasing gape) appear only as derived
conditions in certain groups of snakes (Underwood 1967; McDowell 1987;
Pough et al. 2004; Vitt and Caldwell 2009).
Although the classification of extant snakes began with Linnaeus in
1758 and received various rearrangements by herpetological luminaries
like Duméril (1853), Cope (1894, 1895), Boulenger (1896) and Hoffstetter
(1946, 1962), most modern treatments of taxonomy can be traced to
Underwood (1967). Since then, numerous studies and lists have been
produced attempting to classify snakes. Many of these studies chart the
rise of modern computational and molecular systematics (immunological
or DNA hybridization). However, our basic treatment of major snake
taxonomy in this chapter will primarily be discussed in the context of
molecular DNA sequence, character based systematics, while occasionally
referring to concordant morphological data.
Among extant snakes, the basal divisions occur between the
scolecophidians and the alethinophidians (Rage 1984; Cundall et al. 1993;
Dessauer et al. 1987; Vidal and Hedges 2002; White et al. 2005; Burbrink and
Pyron 2008; Wiens et al. 2008; Eckstut et al. 2009), although other classification
schemes have been presented (Vidal et al. 2009). Outside of the purview of
most neontologists are the large number of extinct families and genera of
snakes known because of the dedicated work of a few paleoherpetologists.
Many of these taxa cannot be confidently placed within the phylogeny
of extant serpents because of the absence of various characters or
convergence in states, not to mention the obvious complete lack of DNA
data. We underscore the importance of these fossils in understanding the
area and dates of origins of snakes, as well as morphological changes
through time. We also realize that the correct placement of many of these

Evolution and Taxonomy of Snakes 23
taxa may actually help better understand relationships among extant
families. Several of these families, including Palaeopheidae, Dinilysiidae,
Nigerophiidae, Lapparentopheidae, Simoliopheidae, Pachyophiidae,
Russellopheidae, and several unincorporated genera, Eupodophis, Goniophis,
likely represent extinct alethinophidians, but the exact position remains
contentious (Lydekker 1888; Nopcsa 1923; Romer 1956; Hoffstetter 1961;
Rage 1975;1984; McDowell 1987; Holman and Case 1988; Carroll 1988;
Holman et al. 1991; Averianov 1997; Caldwell and Lee 1997; Khajuria and
Prasad 1998; Nessov et al. 1998; Zaher 1998; Lee et al. 1999; Rage and
Werner 1999; Zaher and Rieppel 1999; Caldwell 2000; Lee and Scanlon 2002;
Sepkoski 2002; Zaher and Rieppel 2002; Caldwell and Albino 2003; Rieppel
and Head 2004; Head et al. 2005; Parmley and DeVore 2005; Scanlon 2006;
Head et al. 2009). A recent study by Apesteguia and Zaher (2006) places
Najash as the sister taxon to all serpents, Dinilysiidae (Dinilysia) as the
sister group to all Alethinophidia (including Aniliidae) and Pachyophiidae
(represented by Haasiophis, Pachyrhachis, and Eupodophis) unresolved
within a group containing colubroids, pythonids, boids, loxocemids and
xenopeltids (Zaher 1998; Zaher and Rieppel 2002). Furthermore, these
authors placed the giant extinct snake, Wonambi, as sister to the Boidae.
This genus along with Yurlunggur, are placed within Madtsoiiidae by
Scanlon and Lee (2000) and Scanlon (2006). In contrast to Apesteguia
and Zaher (2006), Caldwell (2000), Lee and Scanlon (2002) suggest that
Madtsoiiidae, Pachyrhachis, Haasiophis and Dinilysia fall outside the most
common ancestor of Scolecophidia and Alethinophidia, are all subtended
by the basal nodes in the tree of serpents, and undermine the concept of
Macrostomata. We leave the subject of fossil snakes to now focus on the
major groups and families within extant snakes.
2.2 SCOLECOPHIDIA
The blind snakes are easily recognized as generally small uniformly
scaled snakes, that superficially resemble worms more than they do
their sister group, alethinophidian snakes. All scolecophidians retain
pelvic elements but display no external limb vestiges. A large number of
morphological synapomorphies for this group have been discussed by
several authors (McDowell 1987; Rieppel 1988; Cundall et al. 1993; Holman
2000; Lee and Scanlon 2002; Vitt and Caldwell 2009). Three families,
Anomalepididae, Leptotyphlopidae, and Typhlopidae traditionally
represent the scolecophidians. Morphological support for a most recent
common ancestor for these three families is large and includes multiple
premaxillary foramina, a fenesta for the duct of the Jacobson’s organ that
opens posteroventrally as well as 27 other characters (Lee and Scanlon
2002). Unfortunately, it is not clear how many of these traits are simply
associated with burrowing or simply represent independently evolved
states. Therefore, a real possibility is that morphology is overstating
support for a monophyletic Scolocophidia. Contrary to the idea that

24 Reproductive Biology and Phylogeny of Snakes
morphology supports monophyly, Cundall and Irish (2008) state “The
jaw elements of scolecophidians provide a strong argument in favor of
paraphyly.” For more information concerning either advanced or primitive
morphological characters that separate Scolecophidia from Alethinophidia,
see McDowell (1967, 1974, 1987), Cundall et al. (1993) and Lee and
Scanlon (2002). Recent molecular studies are conflicting with regard to a
monophyletic Scolecophidia. Macey and Verma (1997), Vidal and Hedges
(2002), Lee et al. (2007), suggested they were monophyletic, but Heise et
al. (1995), Forstner et al. (1995), Eckstut et al. (2009), Vidal et al. (2009) and
Wiens et al. (2008) all inferred the Scolecophidia to not be monophyletic.
Pyron and Burbrink (unpublished data) using species tree methods
from 25 loci revealed a sister relationship between Typhlopidae and the
remainder of all snakes, with Leptotyphlopidae appearing sister to the
group containing Anomalepididae and the Alethinophidia (Fig. 2.1). The
combined morphological and molecular analysis of snake relationships in
White et al. (2005) also inferred a paraphyletic Scolecophidia but Lee et al.
(2007) indicated that Scolecophidia are monophyletic. Bowing to historical
inertia and for ease of discussion, we treat Scolecophidia as monophyletic
here, but realize there is considerable uncertainty about this assumption.
The most species rich group of scolecophidians, Typhlopidae, are
represented by nine genera and 232 taxa (Reptile Database) and mostly
occur in the tropical regions of the world, although two species are
found in North America and one in Europe (McDiarmid et al. 1999). This
group has a toothless dentary as well as 12 other states listed in Lee and
Scanlon (2002).
Leptotyphlopidae are found in the tropics and subtropics of Africa
and the Americas as well as southwest Asia and are composed of
116 species. They are represented by two genera, although in a rare
study on the phylogenetics of any scolecophidian groups using
molecular data, Adalsteinsson et al. (2009) divided leptotyphlopids
into 12 genera. Leptotyphlopidae may be the sister family to the other
scolecophidian groups and is distinguished from them by having 11 unique
character states, including a toothless maxilla (McDowell 1987; Lee and
Scanlon 2002).
The most range restricted group, Anomalepididae, is found in southern
Central America and South America. Represented by only 17 species and
four genera (Reptile Database; McDowell et al. 1999), anomalepidids can be
diagnosed by 18 diagnostic character states, including a toothed a maxilla
and dentary as well as absence of all pelvic vestiges (see McDowell 1967;
McDowell 1987; Lee and Scanlon 2002; Pough et al. 2004).
Although the oldest scolecophidian fossils are from the Paleocene (Folie
2006), molecular divergence dating has suggested that the group originated
in the early Cretaceous or late Jurassic (Burbrink and Pyron 2008; Vidal et al.
2009), a time frame deduced by White et al. (2005) based on minimal fossil
ages and constrained by phylogeny. Given that the first appearance of a
fossil probably underestimates the actual date of origin for the group, it is

Evolution and Taxonomy of Snakes 25
likely that molecular dating might provide a more realistic estimate of the
origin of any group of organisms. The downside to estimating molecular
dates of origin is that all of the inferences discussed here assume some
very realistic and large quantity of error around the mean date. Yet, it is
encouraging that the molecular dates and the deduced dates are similar.
However, please consult the original articles where estimated of dates of
divergence are concerned.
All scolecophidians are oviviparous (although delayed egg deposition
is known from Typhlops squamosus). The often-introduced typhlopid
Ramphotyphlops braminus is parthenogenic. Most scolecophidians are fossorial
(although some exceptions are known) and consume termites, ants or the
eggs and larvae of these prey (Webb et al. 2000; Vitt and Caldwell 2009).
2.3 ALETHINOPHIDIA
The remainder of extant snakes belongs to Alethinophidia, and for the
most part, these are the serpents with which people are most familiar.
They are generally differentiated from the scolecophidians by possessing
a well developed squamosal bone that articulates with the quadrate and
brain case (absent in Uropeltidae) and lacking or having a small coronoid
bone and vertebrae possessing a neural spine (lacking in Uropeltidae).
McDowell (1987) provides a detailed review of the anatomy of this group.
Fossil records for alethinophidians date to the mid-Cretaceous (Rage and
Werner 1999), although the origin of this group has been suggested to have
occurred in the late Jurassic or early Cretaceous (White et al. 2005). Recent
studies using relaxed molecular clocks also indicate they diverged from
a common ancestor with scolecophidians around that time (Burbrink and
Pyron 2008; Vidal et al. 2009).
Based on various morphological studies and combined morphological
and molecular phylogenetic analyses (Rieppel 1988; Lee and Scanlon
2002; Lee et al. 2007), alethinophidians typically have been divided into
Anilioidea (Aniliidae, Cylindrophiidae, Uropeltidae and Anomochilidae)
and Macrostomata (Pythonidae, Boidea, Colubroidea and Acrochordidae).
However, several molecular and morphological studies have demonstrated
this to be in error and conditions that increase gape in macrostomatan
genera have either evolved numerous times or have been lost several
times, resulting in paraphyletic classifications (Cadle et al. 1990; Slowinski
and Lawson 2002; Wilcox et al. 2002; Lawson et al. 2004; Gower et al. 2005;
Wiens et al. 2008; Eckstut et al. 2009; Vidal et al. 2009).
Molecular phylogenetic studies have shown support for an initial
division in Alethinophidia occurring in the later half of the Cretaceous,
which sometimes join the Aniliidae and two genera of the Tropidopheidae
(Tropidophis and Trachyboa; the other two genera Ungaliophis and Exiliboa are
related to the Boidea; Wilcox et al. 2002; Vidal and Hedges 2002; Lawson et
al. 2004; Burbrink and Pyron 2008; Wiens et al. 2008; Eckstut et al. 2009; Vidal
et al. 2009). The remainder of alethinophidians, the second division, includes

26 Reproductive Biology and Phylogeny of Snakes
Pythonidae (with the closely related Loxocemidae and Xenopeltidae) and
Boidae, which also encompass Ungaliopheidae (Exiliboa and Ungaliophis),
erycine boids and Calabaria (Vidal and Hedges 2002; Burbrink and Pyron
2008; Wiens et al. 2008; Eckstut et al. 2009; Vidal et al. 2009). Also, within this
second division are the massively diverse caenophidians (Acrochordidae
and Colubroidea) as well as Bolyeriidae, Xenophidiidae, Uropeltidae,
Cylindrophiidae and Anomochilidae. Pyron and Burbrink (unpublished
data) demonstrated, using species tree methods, that the initial division
within Alethinophidia divided caenophidians and the remainder of
alethinophidians including Aniliidae and Tropidopheidae. This later group
was commonly referred to as Henophidia (Fig. 2.1).
In two recent molecular studies using numerous mtDNA and nDNA
genes, Bolyeriidae and Uropeltidae (including Cylindrophiidae) are
sometimes considered to be removed from the clade containing pythonids,
loxocemids, xenopeltids and boids (Vidal et al. 2009) or of uncertain position
within this second division of alethinophidians, but with a possible sister
relationship between the boids and bolyeriids (Wiens et al. 2008). Pyron
and Burbrink (unpublished data) showed a clade containing pythonids,
loxocemids and xenopeltids as the sister group to a clade containing Boidea
(and Calabariidae), Bolyeriidae and Uropeltidae (Fig. 2.1). By examination
of morphological characters, the extremely rare Xenophidiidae, found only
in peninsular Malaysia and Borneo, has been proposed to be closely related
to various groups including colubroids, aniliids, tropidopheids or boids
(Günther and Manthey 1995; Wallach and Günther 1998). After obtaining
a rare, but decayed tissue sample, Lawson et al. 2004, demonstrated from
only a single gene that xenophidiids are closely related to bolyeriids,
which in turn may be related to pythonids or boids. Finally, the remaining
group, Anomochilidae, may not actually deserve family ranking. In a study
using 12S and 16S DNA sequences, Anomochilus, representing the family
Anomochilidae, was found to be closely related to Cylindrophiidae, which
rendered the genus Cylindrophis paraphyletic (Gower et al. 2005).
2.3.1 Aniliidae
The South American pipesnakes are a monotypic family composed of
a single species, Anilius scytale (McDiarmid et al. 1999). This species is
found throughout tropical northern South America (Greene 1997). The
oviviparous species superficially resembles bi-colored coral snakes, lacks
a distinctly differentiated head and neck region, and a single scale covers
each eye. Additionally, femurs are present as cloacal spurs and remnants
of pelvic elements are found in the musculature of the trunk (McDowell
1987). A large number of morphological characters (~28) appear to diagnose
this monotypic family (Underwood 1967; McDowell 1987; Lee and Scanlon
2002; Pough et al., 2004; Vitt and Caldwell 2009). The species is usually
smaller than one meter and occurs in tropical forest litter and near water.
They are viviparous and generally give birth from 4 to 18 young in either

Evolution and Taxonomy of Snakes 27
Fig. 2.1 Phylogenetic relationships among snake families and higher level groups using
species tree methods (Pyron and Burbrink, unpublished data). Posterior probability support
is greater than 95% for all nodes unless indicated otherwise. While Scolecophidia is
designated on this tree it was not found to be monophyletic. Taxa illustrated and photo
credits from top to bottom: Leptotyphlops brasiliensis (Jalapão National Park, Tocantis, Brazil,
by Donald Shepard); Python reticulatus (Danum Valley, Sabah, Borneo, by Frank Burbrink);
Boa constrictor (Tortuguero, Costa Rica, by Frank Burbrink); Anilius scytale (Cristalino River
near Alta Floresta, Mato Grosso, Brazil, by David Shepard); Oxybelis fulgidus (Tortuguero,
Costa Rica, by Frank Burbrink); Agkistrodon piscivorus (Florida, USA, by Frank Burbrink);
Aplopeltura boa (Danum Valley, Sabah, Borneo, by Frank Burbrink).
Color image of this figure appears in the color plate section at the end of the book.

28 Reproductive Biology and Phylogeny of Snakes
the wet or dry season (Martins and Oliveira 1999; Cisneros-Heredia 2005;
Maschio et al. 2007). Molecular divergence dating indicates that this family
likely originated at the K/T boundary (Burbrink and Pyron 2008).
2.3.2 Tropidopheidae
Once considered to have been composed of four genera, Tropidopheidae,
now only includes Tropidopheinae and contains only two genera,
Tropidophis and Trachyboa, totaling 23 species (Zaher 1994; Wilcox et al. 2002;
Lawson et al. 2004; Gower et al. 2005; Eckstut et al. 2009; Reptile Database).
These moderate to small snakes are found in the West Indies, Central
America and South America. During the late Cretaceous or early Tertiary
they diverged from a recent common ancestor with the New World aniliids
(Schwartz and Henderson 1991; Tolson and Henderson 1993; Wallach and
Günther 1998; Burbrink and Pyron 2008; Vitt and Caldwell 2009). Unlike
aniliids, these terrestrial/arboreal snakes share the macrostomatan skull
condition and have edentulous premaxillaries. Tropidopheids still retain
some pelvic elements. Morphological characters discerning tropidopheines
and ungaliopheines (now in Boidae), including parallelization of hyoid
horns, are described in Zaher (1994). Tropidopheids primarily feed on
lizards and other small vertebrates, are viviparous and are recorded to
have two to 12 young (Henderson and Powell 2009). Relationships among
~50% of the species were examined in Wilcox et al. (2002).
2.3.3 Uropeltidae
This family, which should also include Cylindrophiidae and the single
species of Anomochilidae (Gower 2005), represents a radiation of southern
and southeastern Asian non-macrostomatan alethinophidians. Occasionally,
the family is considered to be a superfamily composed of Uropeltidae,
Cylindrophiidae and Anomochilidae (Reptile Database). However, given
that Cylindrophis is rendered paraphyletic by Anomochilus, the most
conservative approach to the classification of this group would be to
abandon all separate families except Uropeltidae. If we assume Uropeltidae
includes all three families, then it is composed of 10 genera and 62 species.
The monophyly of the family for at least three genera (Cylindrophis,
Rhinophis, and Uropeltis) was found in Eckstut et al. (2009), which supports
an early molecular evolution study on this group (Cadle et al. 1990). These
unusual secretive snakes are distributed in southern India and southeastern
Asia. The diet appears to vary in this eclectic group, from earthworms in
the uropeltines to larger elongate prey like eels and snakes in Cylindrophis
(Murphy et al. 1999). The closely related Anomochilus and Cylindrophis still
retain pelvic elements with cloacal spurs, whereas all other genera (in the
restricted family Uropeltidae) have no limb elements. The stem uropeltids
originated in the late Cretaceous or early Tertiary (Burbrink and Pyron
2008; Vidal et al. 2009). All members of Uropeltidae appear to be fossorial
with the uropeltines possessing biochemical specializations that allow

Evolution and Taxonomy of Snakes 29
continuous muscle activity for borrowing (Gans et al. 1978), and prefer to
forage at night on the surface or in loose soil. This habitat preference is
suggested for Anomochilus, although given the rarity of this species (known
from less than one dozen specimens) their lifestyle has yet to be confirmed.
All species of uropeltids are viviparous, except Anomochilus.
2.3.4 Bolyeriidae
The Mascarene boas found only on Mauritius Island and surrounding
islets, contain only two genera and two species, Bolyeria multocarinata and
Casarea dussumieri (McDiarmid et al. 1999). A key defining feature in these
snakes is their intramaxillary joint. Unique for this enigmatic group, the
maxillary is divided into an anterior and posterior section, presumably as
an adaptation for feeding on skinks (Bullock 1986; Cundall and Irish 1986;
1989; Wallach and Günther 1998). The stem members of this group probably
diverged in the late Cretaceous (Vidal et al. 2009). Presumably Bolyeria
became extinct in the 20th century (Bullock 1986). Casarea is apparently
oviviparous and reproduction in Bolyeria is unknown (Cundall and Irish
1989; Vitt and Caldwell 2009).
2.3.5 Xenophidiidae
The family Xenophidiidae is known from only two species, Xenophidion
acanthognathus and Xenophidion schaeferi, found in Sabah, Borneo and
Peninsular Malaysia, respectively (Günther and Manthey 1995; Wallach
and Günther 1998). Prior to molecular analyses, it had been suggested
this family was related to aniliids, tropidopheids, boids, or colubroids.
Modern molecular phylogenetic analyses demonstrated that it might be
the sister group to Bolyeriidae, or was at least likely to be part of a clade
containing bolyeriids, uropeltids, loxocemids, xenopeltids and pythonids
(Lawson et al. 2004). Dates of origin for this group are unknown, but given
their placement among alethinophidians and particularly close relationship
with bolyeriids, it is likely that they originated in the later Cretaceous or
early Tertiary. Spinejaw snakes are known to live in rainforest habitats
and the single female specimen found in Borneo contained large shelled
eggs. Presumably the large tooth on the anterior portion of the mandible
is used to secure struggling prey, perhaps small vertebrates (Cundall and
Irish 1986, 1989; Vitt and Caldwell 2009).
2.3.6 Loxocemidae
The Mexican Burrowing Python (Loxocemus bicolor), the only living member
of the family, is found from Costa Rica to southeastern Mexico (McDiarmid
et al. 1999; Reptile Database). Their taxonomic position has been discussed
by various authors using morphological data (Haas 1955; Underwood
1967), but based on a review of recent literature on molecular systematics,
it is quite clear L. bicolor is the sister species to all Old World pythons
(Fig. 2.1; Slowinski and Lawson 2002; Wilcox et al. 2002; Lawson et al.

30 Reproductive Biology and Phylogeny of Snakes
2004; White et al. 2005; Burbrink and Pyron 2008; Wiens et al. 2008; Eckstut
et al. 2009; Vidal et al. 2009). However, using combined molecular and
morphological data, Lee et al. (2007) demonstrated that Loxocemus was sister
to Xenopeltis, and this clade was sister to pythonids. Also demonstrating
that they are the sister group to pythonids, Burbrink and Pyron (2008)
estimated these two groups shared a common ancestor in the Eocene. Like
pythonids, Loxocemus has remnant femurs represented as cloacal spurs as
well as vestigial pelvic elements (Wilson and Meyer 1985; Savage 2002).
Loxocemus can attain lengths greater than one meter, though usually they
are smaller. They live in tropical and subtropical forests and appear to
be fossorial or at least secretive and terrestrial. This species is nocturnal
and feeds on small mammals or lizards. Loxocemus is oviparous and lays
clutches of four large eggs (Odinchenko and Latyshev 1996; Greene 1997;
Savage 2002).
2.3.7 Xenopeltidae
Sunbeam snakes are known from two species, Xenopeltis unicolor and
X. hainanensis, known from southern and southeastern China (McDiarmid
et al. 1999). This family is the sister group to a clade containing pythonids
and loxocemids (Slowinski and Lawson 2002; Wilcox et al. 2002; Burbrink
and Pyron 2008; Wiens et al. 2008; Eckstut et al. 2009; Vidal et al. 2009) and
likely diverged from a common ancestor with pythonids and loxocemids in
the early Eocene. These snakes have distinctly iridescent scales but lack any
pelvic or limb elements. Xenopeltis unicolor often occur in rainforests, human
modified habitats (e.g., rice fields) and coastal areas. Adults are generally
smaller than 1.5 meters and burrow in mud and forage for lizards, snakes
and frogs either in the daytime or nighttime. They are oviparous and lay
clutches generally smaller than 17 eggs (Cox 1991).
2.3.8 Pythonidae
This family includes nine genera (Aspidites, Antaresia, Apodora, Bothrochilus,
Broghammerus, Leiopython, Liasis, Morelia, and Python) and 38 species
found in the Old World, mostly tropical regions (Schleip and O’Shea in
review; Reptile Database). Pythonids are generally large snakes with teeth
on their premaxillaries (except Aspidites; Frazetta 1975) and a low (or
lack of) supraoccipital crest (Underwood 1967; Kluge 1991). They have
vestigial limb elements (cloacal spurs) and remnants of pelvic elements.
Additionally they have no tracheal lung but possess a large left lung.
Pythons are oviparous and females usually coil around egg clutches. True
brooding is associated with Python molurus in order to maintain incubating
temperatures by increasing body temperatures (Van Mierop and Barnard
1976, 1978). A combined mtDNA and morphological study on python
phylogenetics has demonstrated a basal split that subtends one lineage of
Afro-Asian pythons (P. regius, P. brongersmai, P. sebae and P. molurus) and

Evolution and Taxonomy of Snakes 31
another which includes the sister species P. reticulatus and P. timorensis
and the remainder of the Indo-Australian species, indicating the genus
Python is paraphyletic (Rawlings et al. 2008). Divergence dates suggest
that the stem group likely originated in the early to mid-Tertiary (Noonan
and Chippindale 2006; Burbrink and Pyron 2008; Rawlings et al. 2008).
Additionally, Rawlings et al. (2008) demonstrated a four-fold decrease in
diversification 45 Ma, with the last speciation events taking place prior to
the Pliocene.
2.3.9 Boidae
This family is divided into Boinae and Erycinae. Boinae are composed
of 28 species, with two genera occurring in Madagascar (Acrantophis and
Sanzinia), one in southeastern Asia (Candoia) and six in the New World
tropics (Boa, Corallus, Epicrates, Eunectes, Exiliboa, and Ungaliophis). Erycinae
are composed of 14 species, with one genus in North America (Charina) and
four genera found in Africa, the Middle East and Europe (Calabaria, Charina,
Eryx and Gonglyophis) (McDiarmid et al. 1999; Reptile Database). In contrast
to Kluge (1991) molecular studies have all shown that the New World
and Madagascar Boinae each form monophyletic groups (Burbrink 2005;
Noonan and Chippindale 2006). Burbrink (2005) demonstrated that the
New World boines (Boa, Corallus, Epicrates and Eunectes) are monophyletic,
while Noonan and Chippindale (2006) demonstrated that Calabaria is the
sister species to a clade containing Acrantophis and Sanzinia, which is in turn
sister to a group containing three major geographic radiations; Neotropical
(Corallus, Epicrates, Eunectes and Boa) sister to a Pacific/African/Indian
group (Eryx and Candoia) and a North/Central American group (Exiliboa,
Lichanura and Charina). Eckstut et al. (2009) found Calabaria as the sister to
the rest of the boids and both Ungaliophis and Exiliboa were nested within
the boid clade, as suggested by Zaher (1994), contra Wilcox et al. (2002).
Stem members of what we include as Boidea most likely originated
in the late Cretaceous (White et al. 2005; Noonan and Chippendale 2006;
Burbrink and Pyron 2008; Vidal et al. 2009). Interestingly, Noonan and
Chippindale (2006) demonstrated that all diversification events, even
among sister species, within boidae occurred prior to the Neogene. Head
et al. (2009) discovered one of the earliest boid fossils. Titanoboa cerrejonesis
was found in deposits 58-60 Ma in the Cerrajon Basin in Colombia, and
is expected to have attained the massive size of 13 meters (Head et al.
2009).
Boids have edentulous premaxillaries, a coronoid bone, a strongly
developed supraoccipital crest, and like pythons have remnant pelvic
elements and femurs represented as cloacal spurs. All boids are viviparous
and exhibit a large range of litter size (Vitt and Caldwell 2009).

32 Reproductive Biology and Phylogeny of Snakes
2.4 CAENOPHIDIA
2.4.1 Acrochordidae
This family is composed of a single genus, Acrochordus, with three species,
A. arafurae, A. granulatus, and A. javanicus. The filesnakes snakes occur in
southern and southeastern Asia as well as Australia. Nearly all modern
molecular studies (Lawson et al. 2005; Wiens et al. 2008; Eckstut et al. 2009;
Vidal et al. 2009; except Kelly et al. 2003 who inferred the acrochordids as
sister to the Xenodermatidae) have demonstrated that this group represents
the sister taxon to the massive superfamily Colubroidea. The placement
of Acrochordidae as sister to Colubroidea is supported by a large suite of
morphological characters as well (Rieppel 1988, Cundall et al. 1993, Scanlon
and Lee 2000; Lee and Scanlon 2002). Fossils of putative acrochordids are
known from the early Miocene (Head et al. 2007) and molecular dates
suggest this group originated in the late Cretaceous or early Tertiary
(Burbrink and Pyron 2008). This highly aquatic snake is covered with baggy
skin in small nonoverlapping, granular scales. No limb or pelvic elements
are present (Vitt and Caldwell 2009). These large snakes (ranging from
1.0–2.7 m) are usually found in marine or brackish water and primarily feed
on fish (Shine 1986). All species of Acrochordus are viviparous and generally
give birth from 4 to 40 young in the water. It is thought they reproduce
less frequently than other snakes (Shine 1986) and there is evidence that
occasionally some females of A. arafurae exhibit parthenogenesis (Dubach
et al. 1997).
2.4.2 Colubroidea
This largest clade of snakes represents 85% of all serpent species and is
composed of ~2670 taxa (Reptile Database). This superfamily occurs on
every continent (excluding Antarctica) and likely are the most commonly
encountered snakes (particularly in North America). It contains all
dangerously venomous and medically important snakes and many families
have taxa that occupy a wide variety of niches, including arboreal, terrestrial,
fossorial, temperate, tropical desert and oceanic habitats (Pough et al. 2004).
Among a series of characters not possessed by Colubroidea, McDowell
(1987) suggested that they are a morphologically distinct superfamily all
possessing distinctive rib ends and unique cranioquadrate muscles (Haas
1973; Rieppel 1980). Lee and Scanlon (2002) diagnose this group with only
eight morphological characters, including a lack of vomerine flaps, poorly
developed or a complete lack of a coronoid process, and intercostal arteries
that arise from the dorsal aorta at intervals which span multiple body
segments (Wallach and Günther 1998; Pough et al. 2004).
A detailed treatment on the taxonomic history of this group is beyond
the scope of this chapter. However, we note that a large number of
molecular studies that have changed the taxonomy of this group have seen
print in the new millennium (Slowinski and Keogh 2000; Kelly et al. 2003;

Evolution and Taxonomy of Snakes 33
Lawson et al. 2005; Vidal et al. 2007; Pinou et al. 2004; Nagy et al., 2003;
Vidal et al. 2007; Eckstut et al. 2009; Kelly et al. 2009; Zaher et al. 2009). Some
of these have made radical changes to the taxonomy of this group relative
to Dowling and Duellman (1978) and Zaher (1999). We take a conservative
approach to the taxonomy of colubroid snakes in this chapter and primarily
use the classification presented in Lawson et al. (2005), which minimizes
the number of name changes, such as the retention of Colubroidea as the
name for the sister clade to the Acrochordidae [as opposed to, for example,
Colubroides (Zaher et al. 2009)]. We attempt to strike a balance between
long-used taxonomic schemes and molecular phylogenetic estimates.
Therefore, given recent evidence presented in Vidal et al. (2007), Eckstut
et al. (2009), Kelly et al. (2009), Zaher et al. 2009 and Pyron et al. (in press),
we have made a few modifications from Lawson et al. (2005; see Colubridae
and Lamprophiidae).
Gone are the days where Colubroidea was nicely divided into four
families: Colubridae, Viperidae, Atractaspididae and Elapidae (e.g., Pough
et al. 2004). All molecular studies have shown that this classification is
paraphyletic and in keeping with a Linnaean based hierarchy, this means that
other subfamilies have been elevated to familial level. Based on congruence
among the multiple studies mentioned previously, we recognize the
following seven families and subfamilies (in parentheses): Xenodermatidae,
Homalopsidae, Pareatidea, Colubridea (Calamariinae, Colubrinae,
Natricinae, Pseudoxenodontinae, and Dipsadinae), Elapidae (Elapinae
and Hydrophiinae), Lamprophiidae (Atractaspidinae, Lamprophiinae,
Psammophiinae and Pseudoxyrhophiinae), and Viperidae (Azemiopinae,
Crotalinae, and Viperinae). This classification limits the proliferation of
unnecessary familial ranks but we fully realize that these taxonomic
proposals are subject to future testing, like any good scientific hypothesis.
We use the traditional definition of Colubroidea in this chapter.
Colubroidea, which is sister to Acrochordidae, includes the families
Colubridae, Elapidae, Homalopsidae, Lamprophiidae, Pareatidae, Viperidae,
and Xenodermatidae and takes historical precedence (Romer 1956)
over other definitions. It is still widely used by systematists, ecologists,
conservationists and ethologists (e.g., Dowling and Duellman 1978;
Greene 1997; Zaher 1999; Lawson et al. 2005; Wiens et al. 2008; Vitt and
Caldwell 2009). This view is in contrast to Vidal et al. (2007) and Zaher
et al. (2009), who redefine Colubroidea to include only Colubridae (sensu
Lawson et al. 2005). Concomitantly, these authors elevated the subfamilies
of Colubridae to the family level (i.e., Calamariidae, Colubridae,
Pseudoxenodontidae, Natricidae, and Dipsadidae [or Xenodontidae]),
which required that Colubridae be ranked as a superfamily (Colubroidea).
Moreover, along with Pinou et al. (2004) they named the node Elapoidea to
include Elapidae and Lamprophiidae. Realistically, there is no phylogenetic
justification for recognizing these traditional colubrid subfamilies as distinct
families, changing the long-standing definition of Colubroidea, or naming
Elapoidea to be ranked alongside their newer definition of Colubroidea.

34 Reproductive Biology and Phylogeny of Snakes
Therefore, we retain the traditional meaning of Colubroidea, and maintain
the subfamilies within Colubridae in the remainder of this chapter.
Colubroidea may have diverged from their sister group, Acrochordidae
during the early Tertiary. White et al. (2005) suggested a late Cretaceous
divergence of the Colubroidea. Interestingly, Burbrink and Pyron (2008)
showed that an origin of the Colubroidea prior to the K/T boundary at
65 MA is likely when accounting for skewed estimates of divergence
dates. This suggests that colubroids survived the cataclysm that effectively
ended 76% of life on Earth (Pope et al. 1998). There is little doubt that
the diversification of families, subfamilies within Colubroidea occurred
throughout the Tertiary (Rage 1987; Holman 2000; Burbrink and Pyron
2008; Vidal and Hedges 2009)
2.4.3 Colubridae
This family once contained about 63% of all snake species (Pough et al.
2004) but now may contain as few as just over 100 genera (Zaher et al.
2009). The former Colubridae is at the heart of most higher-level taxonomic
changes within snakes. Of the four original colubroid snake families
(e.g., Viperidae, Elapidae, Atractaspididae and Colubridae), it was clear
from various molecular phylogenetic studies that Atractaspididae and
Elapidae shared a most recent common ancestor with certain colubrid
groups (Psammophiinae, Pseudoxyrhophiinae, Lamprophiinae [formerly
Boodontinae and Pseudoxyrhophiinae]). Additionally, other colubrid
subfamilies (e.g., Pareatinae, Xenodermatinae, and Homalopsinae) fell
well outside the traditional Colubridae, which required familial ranking
for these groups (e.g., Cadle 1994; Vidal and Hedges 2002; Kelly et al.
2003; Nagy et al. 2003; Lawson et al. 2005; Vidal et al. 2007; Eckstut et al.
2009; Zaher et al. 2009; Pyron et al. in press). Many authors have proposed
various taxonomic schemes that have yet to be completely accepted (e.g.,
Kelly et al. 2003; Lawson et al. 2005; Vidal et al. 2007; Zaher et al. 2009)
but which at least show similar groupings (albeit with different names).
The challenge here is to provide a classification that bridges all the recent
phylogenies. As noted above, we take a more conservative approach than
recent classifications (e.g., Zaher et al. 2009), but nonetheless we believe
it reflects the congruent features of the recent phylogenies. Therefore, the
original Colubridae should be divided into Pareatidae, Homalopsidae,
Xenodermatidae, and Lamprophiidae (containing Lamprophiinae,
Atractaspidinae, Psammophiinae, and Pseudoxyrhophiinae). We discuss
the remainder of Colubridae in this section.
There is clear congruence among phylogenies for the contents of
the clades within what we call the Colubridae: Pseudoxenodontinae,
Calamariinae, Dipsadinae (formerly Xenodontinae in Lawson et al., 2005),
Natricinae, and Colubrinae (Kelly et al. 2003; Lawson et al. 2005; Vidal
et al. 2007; Eckstut et al. 2009; Kelly et al. 2009; Zaher et al. 2009). However,
the relationships among these groups remain uncertain, with the exception
of Calamariinae and Colubrinae. Even this latter relationship is unclear

Evolution and Taxonomy of Snakes 35
because in some cases Calamariinae render Colubrinae paraphyletic. Even
though the content of the Colubridae is reduced, it still is global in scope
and exhibits great diversity.
Given these recent taxonomic changes, diagnosing Colubridae using
morphological characters has yet to be widely discussed. Zaher et al.
(2009) diagnose Colubridae (their Colubroidea) exclusively with hemipenal
characters and noted that one of these characters, calyces on the hemipenal
lobes, has been lost in the natricines.
Natricinae (approximately 33 genera and 207 species) are found on
every habitable continent (and Indoaustralian islands) except for South
America. They occupy aquatic, mostly freshwater but some brackish and
coastal waters, semi-fossorial, and terrestrial habitats. They exhibit a wide
diet diversity, including fish and amphibians and some show unusual
specialization on prey like slugs, earthworms, and crawfish (a crustacean).
Reproductive modes include viviparity (all North American species are
viviparous) and oviparity and, interestingly, one taxon, Tropidonophis mairii
represents one of the only confirmed cases of multi-clutching by a single
female during the reproductive season (Brown and Shine 2002). A molecular
phylogeny of the entire subfamily using a majority of recognized genera
awaits publication, but de Queiroz et al. (2002) have examined relationships
among and within some New World genera, particularly Thamnophis.
Calamariinae is a group of seven genera and 82 species that are
distributed in southeastern Asia and the Indonesian-Malaysian islands.
Based on their head morphology and other characters as well as field
observations it is thought that these snakes are probably fossorial. They
are all oviparous (Greene 1997). A molecular phylogeny of these genera
has yet to be published and very few specimens are ever included within
any molecular phylogeny of Colubroidea.
The smallest clade of colubrids is the Pseudoxenodontinae, composed
of two genera (Plagiopholis and Pseudoxenodon) and 10 species. The species
range through southeastern Asia, including one in India, and occupy islands
in Indonesia and Malaysia. This subfamily was erected by McDowell (1987).
Based on the hemipenes, McDowell (1987) suggested a close relationship
with natricines, xenodontines or colubrines, which turned out to be fairly
prescient given the subsequent reorganization of Colubridae. Little is known
about the natural history of this group, but apparently some of them occur
in montane forests and eat frogs and at least one species, Pseudoxenodon
macrops, is known to be oviparous (Zhao et al. 1998).
Dipsadinae (=Dipsadidae in Zaher et al. 2009) contains 88 genera and
is the most speciose group in all of Colubroidea with almost 700 species.
The group is often referred to as Xenodontinae (Bonaparte 1845), however,
the name Dipsadinae (Bonaparte 1838) has priority by seven years. The
distribution has been considered strictly New World until three recent
papers all indicated that the Asian Thermophis is nested within Dipsadinae
(Guo et al. 2009; He et al. 2009; Huang et al. 2009). Traditionally Dipsadinae
has been diagnosed using hemipenal characters and currently this remains

36 Reproductive Biology and Phylogeny of Snakes
the case (Zaher et al. 2009). Interestingly, Xenodontinae of Zaher et al.
(2009) is not diagnosable by any characters, which appears to us to be a
good reason to recognize the larger, diagnosable subfamily, Dipsadinae.
Furthermore, there are diagnosable subclades within the Dipsadinae (sensu
lato), as hinted by early immunological studies (Cadle 1984a,b,c) and
discussed in Zaher et al. (2009), but we wait for these diagnoses. Little
is known about the natural history of this group, but apparently some
of them occur in montane forests and eat frogs and at least one species,
Pseudoxenodon macrops, is known to be oviparous (Zhao et al. 1998). Such
a speciose group, as expected, shows extreme diversity in body form,
habitat preferences, and diets, but if one wished to stereotype these snakes
morphologically then they could be considered as mostly rear fanged
tropical and mild temperate reptile and amphibian feeders (with obvious
exceptions like the goo-eaters). The group also contains individuals that
might be considered dangerously venomous (e.g., Conophis lineatus).
This group is predominantly oviparous with some viviparous members.
Recent studies have attempted to use molecular phylogenetic methods
to infer relationships among some tribes and genera (Crother 1999; Vidal
et al. 2000; Mulcahy 2007; Zaher et al. 2009).
The nominate subfamily Colubrinae is composed of approximately 100
genera and some 650 species. With respect to distribution, the colubrines
are global, found on all continents (excluding Antarctica) and in all habitats
from the tropics to the deserts and high mountains and high latitudes.
There are fossorial, arboreal, aquatic, terrestrial, and even flying (gliding)
forms (Chrysopelea). Although some genera are dangerously venomous
(Dispholidus and Thelotornis), most species of Colubrinae are not considered
harmful. This massive group exhibits an extreme breadth in diet from
generalist to peculiar specializations like feeding on tarantulas, scorpions
and centipedes. Like dipsadines, colubrines are almost exclusively
oviparous with a few notable viviparous taxa (e.g., Oocatochus rufodostatus,
Ji et al. 1997). There have been few attempts at inferring the phylogeny
on this massive group, although a few smaller studies exist that have
attempted to examine phylogenetic relationships and dates divergence for
various subcomponents including Old World and New World ratsnakes/
kingsnakes (e.g., Elaphe, Coelognathus, Gonyosoma, Rhinechis, Pantherophis,
Pituophis, and Lampropeltis, Utiger et al. 2002; 2005; Burbrink and Lawson
2007; Pyron and Burbrink 2009), and Old World and New World racers
and whipsnakes (e.g., Coluber, Masticophis, Hemorrhois, Hierophis, and
Eirenis; Nagy et al. 2004). From Burbrink and Lawson (2007) it is likely that
colubrines originated in the Eocene of the Old World.
2.4.4 Xenodermatidae
Composed of six genera and 18 species, this group of colubroids is confined
to southern and southeastern Asia and appears to be the sister clade to the
rest of the colubroids (Fig. 2.1; Kelly et al. 2003; Vidal et al. 2007; Eckstut et
al. 2009; Zaher et al. 2009). This obviously required the removal of the group

Evolution and Taxonomy of Snakes 37
as a subfamily of Colubridae. Other studies (e.g., Lawson et al. 2005; Kelly
et al. 2009) that used Oxyrhabdium (instead of Xenodermus and Stoliczkia
like the former studies) found it nested deep in the colubroid clade. Zaher
et al. (2009) suggested that Oxyrhabdium is probably not a member of the
Xenodermatidae. Interestingly, Oxyrhabdium was only recently added to
the family (along with Xylophis) by McDowell (1987) because of the shared
maxilla–palatine connection among Xenodermatidae, which he even mused
as “perhaps merely primitive.”
These strange-scaled snakes are unusual in that the scales are almost
entirely fused to the skin and have, in some places, large interscalar areas
of exposed skin. This contrasts the typical condition where the scales are
usually fixed to the underlying skin at one point and the rest of the scale
is free and also typical is that the scales are imbricating (although there are
other snakes without imbricating scales). These snakes are poorly known
but considered to feed primarily on frogs and possibly fish. Xenodermus is
known to be oviparous (Greene 1997).
2.4.5 Pareatidae
Composed of three genera and 14 species, this group is distributed in
southeastern Asia. These snakes are the Old World slug eaters, with
probable convergence in jaw and skull characters with New World slug
eaters in the family Dipsadinae (e.g., Dipsas), such as possessing a reduced
preorbital portion of the maxilla and elongate narrow teeth (Cundall and
Irish 2008). Molecular phylogenies have inferred the pareatids to be the
sister to all the colubroids, exclusive of xenodermatids (Lawson et al. 2005;
Vidal et al. 2007; Eckstut et al. 2009; Zaher et al. 2009). Like Zaher et al.
(2009), we do not see the need to erect the name Pareatoidea as a monotypic
superfamily as proposed by Vidal et al. (2007).
Pareatids are widespread in the tropical and subtropical regions of
southeastern Asia and occupy terrestrial and arboreal habitats. They are
almost exclusively gastropod feeders except for Aplopeltura, which eats
lizards. For the gastropod feeders at least, it is thought they do not exhibit
ontogenetic changes in diet (Hoso 2007). They are oviparous (Greene 1997)
and in one species, Iwasaki’s Snail Eater (Pareas iwasakii), clutch sizes have
ranged from six to 11 (Hoso 2007).
2.4.6 Viperidae
We recognize three subfamilies (following Liem et al. 1971), Crotalinae,
Viperinae, and Azemiopinae, in this globally (except Australia and
Antarctica) distributed group of highly specialized venomous snakes. The
most distinctive synapomorphy for Viperidae is the solenoglyph condition,
characterized by reduced maxilla each possessing a single modified tooth,
which is a hollow hinged fang that is retractable to sit against the roof of
the mouth (McDowell 1987). Composed of 28 genera and 81 species, the
crotalines are the most diverse group of viperids and found throughout the

38 Reproductive Biology and Phylogeny of Snakes
New World, and through Asia into southeastern Europe. Viperinae, known
from 13 genera and 81 species, are distributed in Africa, Europe, and Asia.
The single species of the enigmatic Azemiopinae is restricted to montane
regions of Myanmar, Vietnam, and China.
Azemiopinae is monotypic (Azemiops), and in some recent molecular
phylogenies is inferred to be the sister taxon of a crotaline–viperine clade
(Kelly et al. 2003 ML tree; Eckstut et al. 2009). Castoe and Parkinson (2006)
and Zaher et al. (2009) indicated that the Azemiopinae is nested within the
Viperidae and is the sister clade to the Crotalinae. The preferred tree in Kelly
et al. (2003) illustrates that Azemiops renders the Viperinae paraphyletic.
On the other hand, Wüster et al. (2008) demonstrated that Azemiops was
sister to Crotalinae. Currently, there seems to be little consensus about the
placement of Azemiops.
As one would expect of globally distributed viperids of nearly 300 species,
these snakes occupy diverse habitats and exhibit a wide variety of ecologies.
They are found in deserts, tropical forests, and freshwater aquatic systems.
They are terrestrial, fossorial, and arboreal. Perhaps if there is something
shared by all members it is diet: they all appear to feed on vertebrates and
mostly sit and wait predators (but see Causus). Crotalines have a pair of
specialized heat sensing pits between the nares and eyes that allow them to
see prey items based on heat signatures. Viperids exhibit several interesting
reproductive strategies. Most crotalines are viviparous but several taxa
are oviparous and among viperines both oviparity and ovoviviparity are
exhibited. Apparently, even parthenogenesis occurs in viperids (Alemeida-
Santos and Salomão 2002). While the general perception of vipers is that of
cold-blooded killers, parental care is surprisingly broadly distributed among
oviparous and viviparous viperine and crotaline taxa (Greene et al. 2002).
The crown group of Viperidae likely originated in the early Tertiary
(Wüster et al. 2008) and apparently viviparity was a key innovation that
coincided with global cooling in the Cenozoic and resulted in rapid
adaptive radiation in this group (Lynch 2009). For more information
about the biology of these organisms, see several comprehensive texts on
the biology of viperids (Campbell and Brodie 1992; Schuett et al. 2002;
Campbell and Lamar 2004).
2.4.7 Homalopsidae
Eleven genera and 35 species are currently considered homalopsids
(Lawson et al. 2005; Zaher et al. 2009) and they are distributed in southern
and southeastern Asia and Australasia (Murphy 2007). The majority
of these taxa are grooved rear-fanged aquatic specialists and the key
morphological synapomorphies that diagnose this clade are associated
with aquatic specialization, such as the dorsal position of the nares and
eyes on the head, specialized structures for breathing underwater, and the
ability to close the nostrils (Santos-Costa and Hofstadler-Deiques 2002).
One taxon, Brachyorrhos, is not aquatic, not rear fanged, has lateral eyes,
and anterior nares (Murphy 2007). Based on hemipenes, vertebrae and

Evolution and Taxonomy of Snakes 39
skull characters, McDowell (1987) included it in the group and Zaher
et al. (2009) followed this suggestion. Lawson et al. (2005) treated Brachyorrhos
as incertae sedis. Additionally, Anoplohydrus (known from a single specimen
collected in Sumatra but lost during the bombing of Dresden in WWII)
is supposedly a homalopsid but no phylogenetic study has confirmed its
placement (Murphy 2007). Several recent molecular studies are congruent
in their inference of the homalopsids as the sister to the remainder of the
Colubroidea, exclusive of the xenodermatids, pareatids, and viperids (Kelly
et al. 2003, Lawson et al. 2005; Eckstut et al. 2009; Zaher et al. 2009, Pyron
and Burbrink, unpublished data).
These snakes (except Brachyorrhos) inhabit all manner of aquatic
environments including freshwater ponds, streams, freshwater wetlands,
and agricultural systems (e.g., flooded rice paddies) as well as coastal
marine systems like tidal flats, mangrove forests, and estuaries (Gyi 1970;
Heatewole 1999). In all of these diverse aquatic habitats homalopsids
are mostly associated with mud substrates (Murphy 2007). They feed on
amphibians, fish and crustaceans. One of the most interesting observations
about the latter food item is that the Crab-eating water snake (Fordonia
leucobalia) actually dismember the crustaceans as they eat, the only
snakes known to do so (Jayne et al. 2002). All members are thought to be
viviparous and multiple paternities have been documented for two species
(Voris et al. 2008). A recent study on the phylogenetic history of this group
using sequences from a majority of taxa demonstrated that the crown
group originated ~22 Ma. Moreover, this phylogeny produced the telling
signals that suggested this group diversified in an early explosive burst of
speciation (Alfaro et al. 2008).
2.4.8 Lamprophiidae
Containing primarily an African radiation of snakes, this group may be
sister to Elapidae (Vidal et al. 2007; Pyron et al. in press). Some studies
suggest it might be paraphyletic with regard to elapids (Lawson et al.
2005; Kelly et al. 2009). Although we use Lamprophiidae to cover the
subfamilies Atractaspidinae, Psammophiinae, Pseudoxyrhophiinae, and
Lamprophiinae, others have considered these subfamilies (and more)
included within Elapidae (Lawson et al. 2005) or joined with Elapidae in the
superfamily Elapoidea (Pinou et al. 2004 [in part]; Vidal et al. 2007; Kelly et
al. 2009; Zaher et al. 2009). All of these taxonomic suggestions have yet to
be bolstered with a phylogeny inferred using large number of independent
loci. Dates and area of origin for Lamprophiidae are hampered by a lack
of fossils from Africa. Although the composition and relationships are not
identical to a monophyletic Lamprophiidae, it might be inferred from Kelly
et al. (2009) the family likely originated in late Eocene in Africa.
One of the most distinct subfamilies, Atractaspidinae, contains a dozen
genera and 70 species that occupy sub-Saharan Africa. The stem group
likely originated in Africa in the late Eocene/Early Oligocene (Kelly et
al. 2009). Frequently, Aparallactus is excluded from this subfamily. For

40 Reproductive Biology and Phylogeny of Snakes
example, Kelly et al. (2003) and Vidal et al. (2007) did not find those two
genera in the same clade (possibly because of sample size issues). However,
given evidence in Eckstut et al. (2009), Kelly et al. (2009) and Pyron et
al. (in press), we recognize an Atractaspidinae that includes Aparallactus.
Diagnostic morphological characters that define this subfamily have yet to
be found. Hemipenal characters examined in Zaher et al. (2009) are variable
throughout the groups and the dentition that once marked the subfamily
as unique is now confined to a subset of the taxa. Remarkably, this clade
contains opistoglyphous, aglyphous, proteroglyphous and solenoglyphous
forms! Perhaps, as Zaher et al. (2009) stated, the current contents of
this clade exist for “…convenience and historical legacy.” However, at
minimum, several studies are congruent in showing the proteroglyphous
Homoroselaps, the solenoglyphous Atractaspis, and the opistoglyphous/
aglyphous Aparallactus to share a most recent common ancestor (Kelly
et al. 2003; Lawson et al. 2005; Vidal et al. 2008; Eckstut et al. 2009; Kelly et al.
2009; Zaher et al. 2009). Diet varies among this group from small mammals
like shrews and naked mole rats (Atractaspis) to elongate vertebrates such
as amphisbaenians, and also centipedes. All members are thought to be
oviparous (Pough et al. 2004).
Lamprophiinae contains 20 genera and 81 species that are distributed
through Africa and is much more restricted than the concept in Zaher et al.
(2009) and more similar to the contents of Kelly et al. (2009) and Lawson
et al. (2005; although Lawson et al. 2005 referred to the group as Boodontinae).
Vidal et al. (2008), Pyron et al. (in press) found the lamprophiines to be the
sister clade to the pseudoxyrhophiines. To understand the exact generic
content of these two groups will require a more thorough sampling of taxa
and genes. McDowell (1987) recognized a polyphyletic Boodontinae (sensu
Dowling et al. 1983) and the molecular data have supported this contention.
Essentially, the old Boodontinae has been found to be composed of two
groups the lamprophiines, pseudoxyrhophiines and some psammophiines.
Obvious diagnostic morphological characters are absent, but Zaher et al.
(2009) considers the arrangement of spines in transverse rows that form
flounce-structures on the hemipenal body indicative of most of the clade.
Presumably, snakes in this group are oviparous (e.g., Lamprophis, Ford
2001; Lycophidion, Greer 1968; Pseudoboodon, Spawls 1997). Kelly et al.
(2009) demonstrated that the stem of this group likely originated in the
late Eocene in Africa.
Pseudoxyrhophiinae, as noted above, contains the other portion of the
old Boodontinae (sensu Dowling et al. 1983) and comprises about 20 genera
and 80 species (Lawson et al. 2005; Zaher et al. 2009; Reptile Database).
Vidal et al. (2008) and Eckstut et al. (2009) included 16 genera of this group
in their studies and found them to form a monophyletic group. Lawson
et al. (2005), Kelly et al. (2009) and Zaher et al. (2009) all considered this
group to contain mostly genera from Madagascar plus some mainland
taxa (Amplorhinus, Ditypophis, and Duberria). Morphologically, these taxa
are diagnosed with the presence of only spinules on the hemipenal lobes

Evolution and Taxonomy of Snakes 41
(Zaher 1999), which is apparently also shared with homalopsids. The
Madagascar radiation is extremely diverse and may have been colonized
more than once. The main radiation of the crown group in Madagascar and
Socotra occurred in the late Eocene (Nagy et al. 2003; Kelly et al. 2009). They
feed on vertebrates may be arboreal, fossorial, terrestrial and troglodytic.
Most taxa are oviparous but viviparity is known in some species (Pough
et al. 2004).
Psammophiinae, another primarily African group of snakes (although
they reach into southern Europe and western Asia) is composed of six
genera and 46 species. The delimitation and monophyly of this subfamily
is without dispute (Kelly et al. 2008) and the clade is easily diagnosed by a
number of morphological characters such as extremely reduced hemipenes
and differentiated maxillary and mandibular dentition (Zaher et al. 2009).
What remains in dispute are their placement within Lamprophiidae. Kelly
et al. (2003) and Zaher et al. (2009) inferred that the psammophiines were
the sister to the rest of the lamprophiids and elapids. Lawson et al. (2005)
found psammophiines to share a more recent common ancestor with
pseudoxyrhophiines. Vidal et al. (2007) inferred psammophiines as sister to
a clade composed of lamprophiines-atractaspidines and later (Vidal et al.
2008) inferred they were the sister clade to all the elapids minus the elapines.
Eckstut et al. (2009) recovered a psammophiine-Prosymna clade and Kelly
et al. (2009) found the psammophiines related to a pseudoxyrhophiine-
Prosymna clade. Stem origins for this group likely occurred in Africa near
the late Eocene (Kelly et al. 2009).
This clade of snakes most resemble New World racers or whipsnakes
in that they are slender, often big eyed, diurnal serpents that hunt lizards
and small mammals (Shine et al. 2006). The diet may change ontogenetically
with larger individuals taking more mammals. The largest species of the
group, Malpolon monspessulanus, has a notoriously catholic diet, apparently
eating anything it can subdue and swallow, such as lizards, rabbits, snakes,
birds, and even tortoises (Shine et al. 2006). They are apparently oviparous
(Shine et al. 2006).
Finally, within Lamprophiidae, Kelly et al. (2009) recognized two more
groups, Prosymninae and the Pseudaspidinae. The former is monotypic
for the genus Prosymna, which based on the studies discussed here, is
clearly a member of the Lamprophiidae (sensu lato) but where it belongs
exactly is unclear. In Lawson et al. (2005) Prosymna could be placed as
sister to a number of groups depending on the analysis. The placement
of this genus was incongruent in several other studies (Lawson et al.
2005; Vidal et al. 2008; Eckstut et al. 2009; Kelly et al. 2009). Pyron et al.
(in press) demonstrated that they might be sister to Atractaspidinae. Kelly
et al. (2009) included only two genera in their Pseudaspididae and these
were inferred to be monophyletic in all the studies that included them
(Lawson et al. 2005; Eckstut et al. 2009; Kelly et al. 2009). Pyron et al. (in
press) demonstrated that the basal Lamprophiidae node subtends the two
genera of Pseudaspididae.

42 Reproductive Biology and Phylogeny of Snakes
2.4.9 Elapidae
One of the important revelations of modern molecular phylogenetics
of snakes was the discovery that the fixed front fanged snakes of the
Elapidae (sensu stricto) rendered the Colubridae (sensu lato) paraphyletic
(Kelly et al. 2003; Lawson et al. 2005) and that several groups of colubrids
(lamprophiids, including Atractaspidinae) were more closely related to
these proteroglyph snakes than to other snakes without the fixed, front
fang condition (Lawson et al. 2005). Subsequent to this discovery, as noted
above under Colubridae, a number of classification schemes have been
put forward to organize this new found set of relationships. Some have
considered the families Lamprophiidae and Elapidae combined in the
superfamily Elapoidea, which is sister to a redefined Colubroidea (see
above; Pinou et al. 2004 [in part]; Vidal et al. 2007; Kelly et al. 2009 and
Zaher et al. 2009). Because we prefer to retain the broader and more widely
used definition of Colubroidea in this chapter (Romer 1956), we are forced
to refrain from using Elapoidea.
All elapids have the proteroglyph condition—a fixed, erect fang on
each maxillary. The group likely contains two subfamilies, Elapinae and
Hydrophiinae (Lawson et al. 2005; Castoe et al. 2007). Establishing the
monophyly of these subfamilies, particularly Elapinae has been somewhat
troublesome. Although Elapinae has been recognized in some studies
(Lawson et al. 2005; Castoe et al. 2007), others have not (Zaher et al.
2009; Kelly et al. 2009). Several studies have demonstrated support for
a monophyletic Hydrophiinae (Keogh 1998; Keogh et al., 1998; Scanlon
and Lee 2004; Lawson et al. 2005; Castoe et al. 2007; Sanders et al., 2008).
Occasionally, a third subfamily, Laticaudinae is recognized but often is
included within Hydrophiinae. Kelly et al. (2009) demonstrated that stem
elapids likely originated in Asia during the Eocene.
Elapinae is composed of 19 genera and 162 species found throughout
the New World, Africa, Asia and Eurasia. Castoe et al. (2007) divided
Elapinae into two tribes, Calliophiinae containing mostly New World
and Old World coralsnakes (i.e., Micrurus, Micruroides, Sinomicrurus, and
Calliophis) and Hemibungarini containing Asian and African cobras, kraits
and relatives (e.g., Naja, Bungarus, Dendroaspsis, etc.). While dates of origin
for this subfamily are not yet known, divergence date estimates have been
produced for some groups. For instance, the diversification of spitting
cobras in Africa took place during the Mid-Miocene (Wüster et al. 2007)
and the origin of Calliophiinae occurred in the late Oligocene (Kelly et al.
2009). Excluding mambas (Dendroaspis) and tree cobras (Pseudohaje), most
elapines are terrestrial. Many elapids display aposematic coloring and
generally feed on vertebrates. Most species are oviparous and clutch size
seems to be correlated with body size. The viviparous Hemachatus is an
exception (Vitt and Caldwell 2009).
The Australo-Melanasian Hydrophiinae is composed of 46 genera and
188 species (Reptile Database) and is generally found in Australasia, the
Pacific and Indian Oceans. Diversification within this morphologically

Evolution and Taxonomy of Snakes 43
very variable group of elapids occurred very recently, within the last 10
Ma, relative to other colubroid groups (Sanders and Lee 2008; Sanders et
al. 2008).
Terrestrial hydrophiines generally feed on vertebrates and may be either
oviparous or viviparous. True seasnakes, referred to as Hydrophiini (Lee
et al. 2007; Sanders and Lee 2008; Sanders et al. 2008) are much more
adapted for oceanic life. These adaptations include laterally compressed
bodies, paddle-shaped tails and a lack of enlarged ventral scales. All sea
snakes are viviparous. In contrast, Laticauda (sometimes placed in the
subfamily Laticaudinae) lays eggs on land. The sea snake Pelamis platurus
has one of the largest ranges of any snake, occurring in the Persian Gulf,
throughout the Indian Ocean, through the Pacific Ocean in Asia and
Australia to Baja California, Central America and South America.
2.5 CONCLUSION
We have attempted to produce a concise introduction to the current state
of the taxonomy, systematics, and origins of extant snakes in one compact
chapter. Comprehensive chapters like this one are both good and bad.
The good first: they identify the most relevant literature and uptodate
knowledge on a subject. The bad: they are likely to become woefully out
of date and incorrect as new literature on the subject is produced. For
snake taxonomy, the bad aspect may not be entirely dismal; like any good
science, systematics is likely to change as new evidence is presented and
old taxonomic hypotheses are challenged. Unfortunately, many researchers
in other fields require that taxonomies remain stable. Imposed stability
without regard to new discoveries, however, forces systematics to become
religion and not testable science (Crother 2009). Therefore, fluidity in
taxonomy should be expected as new data are generated and tested. While
many groups discussed will remain taxonomically stable, as they have for
decades, we still look forward to the changes in snake systematics as the
field enters into the world of phylogenomics.
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