General

• Definition of snakes:
– Anatomy
– Ecology
• Adaptations addressing 4 snake-lifeway issues:
– Moving…
– Acquiring prey…
– Swallowing prey…
– Digesting prey…
• Reproduction
• Evolution and introduction to the basic clades
• Biogeography
Next Class: the Variety of Snakes

(…and see next slide on general anatomy…)
• Snakes lack:
– External limbs (mostly)
– Sternum
– External ear openings
– Moveable eyelids
– Bony mandibular symphasis
• Organs & neural pathways associated w/ detection & analysis of chemical info are greatly advanced.
• Snakes focus the eye by moving the lens.
• Viscera are elongated:
– Kidneys and gonads are displaced, right forward.
– In advanced snakes, left lung is reduced or absent.
– Liver is large and greatly elongated.
– Skull has greatest degree of kinesis among tetrapods.

General Anatomy, advanced snake (female)

• In general, snakes live in a “chemical world.”
– Recall the general context of tongue-sensing lizards.
– Receiving information :
• Conventional-vertebrate smell and taste are reasonably acute.
• Use of tongue & vomero-nasal organ is intense; acquisition of pheromones is particularly important.
– Sending information : Snakes have special cloacal glands that provide socio-reproductive information about conspecifics.
•
In general, modern snakes are adapted to take relatively large prey & swallow it whole. Consider:
– Foraging (and moving for other reasons)…
– Capturing & killing prey…
– Swallowing prey…
– Digesting prey…
(These general feeding adaptations will be covered in more detail later.)

Basically, snake adaptations must address 4 issues:
• How do you move when you don’t have any limbs?
• How do you kill prey when you don’t have any limbs and when your mouth & teeth are fragile?
• How do you feed a big body through a relatively small hole when:
– …movement & foraging strategies (plus the anatomy that supports them) preclude eating lots of little stuff…
– …you can’t bite your big food into pieces…
– … and you have no limbs to tear your big food apart?
• How do you digest items with small surface/volume ratios– and perhaps with protective coverings?

•
Lateral undulation (most common, next slide).
• Undulatory aquatic propulsion (not illustrated; sort of an “integrated form” of lateral undulation).
• Wiggle friction (slick surfaces; energetically inefficient [sustained by glycolysis]; not illustrated).
•
Rectilinear crawling (next slide + 1; big snakes).
•
Concertina locomotion
(another slide … establishing a stable position with one segment of body while another is moved forward).
• Sidewinding (not illustrated).

Overall resultant force
• This is the most common form of serpentine locomotion.
• Muscular waves travel along alternate sides of the snake’s body and generate posterolateral forces at fixed points * on substrate. Lateral components cancel each other out, and the overall resultant force moves the snake in a forward direction.
____________________
* points d’appuis

• The Costocutaneus superior muscle pulls ventral scale forward relative to rib & vertebra. Ventral scale then anchors to substrate. The costocutaneus inferior muscle then pulls rib & vertebra (& rest of snake) forward relative to anchored ventral scale.
• Waves of such contractions pass simultaneously down the snake’s body. (This looks as if ventral skin inches forward while dorsal skin appears to move at a more or less steady rate.)

• …establish purchase with the front part of the body…
• …pull the back part of the body forward…
• …establish purchase with the back part of the body…
• …push the front part of the body forward…
• …establish purchase with the front part of the body…

• Most snakes simply grab their prey, bite it a few times to quiet its struggles, and flat swallow it down.
• This is a very efficient way of processing prey that is not dangerous.
• There is no distinct line between “just plain eating” and envenomation:
– The evolution of venom amongst squamate reptiles is a complex issue receiving increasing attention.
– Many “swallowers” have (mildly) toxic saliva & rudimentary delivery apparatus.
– See “ opistoglyphic fangs” on later slide dealing with venom-delivery systems.

• Origins of constriction:
– Probably evolved for dealing with elongate prey.
– Readily transferable to bulky, rounded prey.
• Killing mechanisms:
– Relatively small prey: cardiac arrest.
– Relatively large prey: tighten w/prey’s exhalations.
• Anatomical constraints on constrictors:
– To wind tightly, vertebrae must be short.
– This precludes rapid travel.

• Venom ingredients:
– Consist mostly of digestive-type enzymes and a spreading agent.
– The next slide gives a few more specifics.
• Venom types are correlated to a degree with Family:
– Viperidae are mostly hemotoxic.
– Elapidae are mostly neurotoxic.
– However, venom can also vary by species, population, individual, and even life-stage.
• Type of venom-delivery apparatus is more closely related to taxonomy (next slide + 3).

Venom: a few common components (+ taxa & effects)
(from Pough et al.
, 2004)
Component Taxa w/component Physiological Effects
Proteolytic enzymes
Hyaluronidase
All, especially high in most vipers
Digest tissue proteins & peptides.
All Reduces viscosity of connective tissue, increases permeability, hastens spread of other venom components.
L-amino acid oxidase
All
Basic polypeptides Elapids
Attacks many substrates; causes general tissue destruction.
Block neuromuscular transmission.
Cholinesterase High in elapids; low in vipers
Phospholipase (esp.
Phospholipase A
2
)
All
Phosphatases All
Unknown (formerly thought to block nerve-muscle connections in elapids).
Attacks cell membranes (& therefore works synergistically w/other stuff)
Attacks high-energy phosphate compounds such as ATP.

• Some “primitive” components resemble pancreatic enzymes
(and are associated with similar circulation-inhibitors).
• Viper venoms:
– “Hemotoxic” (hystolytic)
– Usually include slow-spreading digestive enzymes of high molecular weight
– Often include agents that increase or decrease clotting
• Elapid venoms:
– ( versus vipers) Fewer components, lower molecular wts.
– Neurotoxins multiple, long- and short-chain):
• Pre-synaptic: block release of acetylcholine
• Post-synaptic (more common): block combination of acetylcholine at receptor sites on muscles
•
Atractaspis :
– Many viper components plus special cardiotoxins.

Additional, ecological notes on snake venom:
– The vast majority of snakes are non-venomous in any human-practical sense of the term.
– In the technical sense, distinction between venomous & non-venomous is less clear than experts once thought.
– Inefficient-looking delivery systems (see next slide) may work quite well….
– Evolution of venom:
• Primary function: securing prey!!!!!
• Secondary functions:
– Defense– against you? (But many snakes are reluctant to use….)
– Venom & digestion. If snakes have evolved to swallow large prey whole, and if retention of undigested prey is unhealthy, then how can snakes live (for example) in high mountains (see later slide)? Also, contrast typical food & venoms of elapids versus viperids.

Four types of venom-delivery apparatus
• A: Numerous very small teeth not primarily adapted for venom delivery.
•
B : Fixed, grooved fangs toward rear of jaw
– Sometimes called opistoglyphic fangs
– Colubrids such as boomslangs
• C : Fixed, hollow fangs toward front of jaw
– Sometimes called proteroglyphic teeth
– Elapids (cobras, coral snakes, etc.)
Do not think of
•
D : Folding, hollow fangs toward front of jaw ( & see next slide ) this as a linear,
– Sometimes called solenoglyphic teeth evolutionary series!
– Viperids (rattlesnakes, vipers, etc.)
(Note: The snake world isn’t as clear-cut as this typology!)

Fang erection in vipers and pit vipers
• W/ mouth closed
(A), quadrate is rotated backwards; maxilla (black) & fang (red) lie along roof of mouth.
• W/ mouth open
(B), quadrate rotates down, pushing pterygoid
(etc.) forward, rotating maxilla & fang into upright position.
•
Blue indicates articulations.

• Squamate head glands are ripe for exaptation:
– All snakes except scolecophidians have many
(and other squamates too?)
– Modified into salt glands, multi-ducted mucous glands....
• Duvernoy’s gland
– Many “colubrids”
– More consolidated
– Mucous or serous or both
• Advanced venom glands:
– Viperids & elapids
– Connective-tissue capsule
– Dedicated compressor musculature (operates on large lumen in viperids)
– Duct connecting gland to
“hypodermic” fang

• … two problems remain:
– Opening the mouth wide enough to get the food-item in: the problem of gape …
– …and transporting the fooditem through the mouth and into the throat: the problem of swallowing .
– (Thereafter, contractions of the axial musculature can move the food-item on down the alimentary canal.)

•
Adaptations increasing the gape of snakes:
• Mandibles are not fused by bony symphasis.
• Mandibles include hinge .
• Elongated quadrates articulate w/ braincase.
• Snout is hinged to braincase.
(Note: Upper jaw elements are not shown. And don’t worry about the skin; it can stretch plenty.)

Ventral view
•
Swallowing, I:
• Notes:
– Lower jaws are not shown.
– On each diagram, left side is shown above right jaw.
– Sides work in alternation.
• Top: Left palatine & maxilla forward; right palatine & maxilla back.
• Bottom: Right palatine & maxilla forward, left palatine & maxilla back.
• Note: Palatines do most of the work (next slide), but don’t forget maxillas and lower jaws.

Side view
•
Swallowing, II:
• (Remember, sides work alternatively; only one side is shown here.)
• Palatines on one side of head are lifted
(1

2) and protracted
(2

3) to gain more forward purchase in prey (4).
• Muscles from braincase to palatines contract (4

5) to pull prey further into snake
(as shown, snake is moved forward over prey).

• Prey is often large.
• Prey items are often covered with protective chitin, feathers, scales, or hair.
• Snake digestive system is extremely powerful.
• Many snakes thermoregulate to increase digestive efficiency.
• Some prey body-parts pass through undigested.

• Big constrictors ( e.g., boas and pythons) can eat enormous meals.
• They also control their digestive systems:
– Turn off during fasts ( c.
5.5 wks); turn on after feeding.
– “On” increases metabolic rate by 1500%-4500%.
*
– Metabolic start-up burns an average of 32% of preyitem’s calories.
– “Off” reduces metabolism to 50% of snake-typical.
* Increase is about 25%-50% in mammals
• Montane vipers eat relatively big stuff & cool down at night.
• Snake metabolism would be slower than bacterial population increase, but…
• Deep injection of venom speeds digestion of prey from within!
• (Want a few million dollars? I got an idea that beats the lottery….)

• Pre-repro. behavior varies!
• About 70% of snakes lay eggs, while the other 30% bear young alive.
• Mode of reproduction follows taxonomic lines– but only approximately.
• Young typically emerge as miniature copies of adults.
• Live-bearing modalities run a continuum from merely hatching eggs inside (most common) to true viviparity.

• Paired hemipenes are carried in tail & everted (one at a time) for copulation.
• Hemipenes structure is a critical taxonomic feature. Why?

• Classification is difficult for at least two reasons:
– Fossil record is not great (fragile skulls…).
– Snakes, like frogs, have restrictive body plan; therefore convergence is a problem….
• There is a primary dichotomy between the most primitive snakes (no good common name) & others.
• There is a definite clade of modern snakes (see next slide), including>90% of all snake species (common harmless snakes, vipers, pit vipers, cobras…).
• The intermediate snakes (including boas, pythons, and others) are difficult to organize, but I have ideas.

This branch includes about 90% of living snakes; its organization is not well understood; see next slide!

perhaps the biggest mystery in modern vertebrate paleontology
• Fossils shown at left are Haasiophis terrasanctus , an aquatic snake (??) with legs from Cretaceous ( c.
95MYBP) beds near
Jerusalem.
• The rarity of cranial material for fossil snakes allows disagreement about origins to persist:
– Scenario 1: snakes are derived from small, burrowing lizards (majority position—and mine; see slide-after-next).
– Scenario 2: snakes are derived from large, aquatic lizards (old “heresy,” occasionally reconsidered).
• Any evolutionary scenario must account for body elongation, leglessness, weird eyes, & adaptations for feeding on large prey (all discussed above).

• Snakes are tongue-sensing lizards and may be considered the most successful of the many lizard experiments with leglessness.
• Snakes’ most probable ancestry lies within the anguimorph ( sensu lato ) line.
– Some experts think varonoids are closest living relatives.
– Amphisbaenians and dibamids also have their advocates.
• Snakes originated at or before the mid-Cretaceous.
• The locale of origin was Gondwanaland.
• Most (all?) modern Families of snakes probably originated in Southeast Asia.

(This is current orthodoxy; it is also “scenario 1” from 2 slides ago.)
• 1: Tongue-sensing ancestors try another experiment in leglessness and give rise to critters somewhat like the living scolecophidians. (Call these “Original Snakes.”)
• 2: The Original Snakes begin to exploit larger– but elongated– food, sometimes pursuing it above ground.
(Call these “Transition-One Snakes.”)
• 3: Surface-hunting Transition-One Snakes evolve larger gape in response to abundance of more “rounded” terrestrial prey. (Call these “Transition-Two Snakes.”)
• 4: Transition-Two Snakes give rise to varieties better adapted for surface life. (The result is early “Advanced
Snakes” such as boas and pythons.)

Living animals somehwat like “Original Snakes”
• Consider a lizard capable of efficient burrowing– and possessing the chemical-sense acuity typical of many lizards.
• This animal could follow underground pheromone trails left by ants and termites. (If the reptile’s highly developed cloacal glands could produce the right scent-passwords, it could enter ant or termite nests
& feed without danger???)
• Such an animal would be ideally suited to exploit the vastly increased abundance of colonial insects that typified the mid-Cretaceous.

“Transition-One
Snakes”
( e.g.
, Anilius scytale , top photo)
• Fossorial Original Snakes, capable of following underground scent-trails, would have opportunity to exploit prey that came in larger packages.
• Such potential prey would include earthworms, other snakes, and caecilians (lower picture).
• After heavy rains many subterranean organisms emerge to the surface.
• These would include
Transition One snakes and their prey.

“Transition-Two
Snakes”
(top: Xenopeltis unicolor , bottom: Loxocemus bicolor )
• Occasional surface-foraging by fossorial snakes would provide contact with a vast variety of prey-items having inconvenient shapes.
• Strong selective pressures would therefore exist for expanding gape.
• Two extant Families represent what I have called
Transition-Two Snakes.
• Both have rather rigid skulls, but they manage wider gape than animals like Anilius (the caecilian eater on the previous slide).

• I consider boas, pythons, & their allies to be the first advanced snakes.
• They exhibit adaptations such as broad ventral scales, flexible skulls, and immense potential gape.
• Their evolution and radiations will be considered further under
“biogeography.”

• “Non-advanced” snakes : All scolecophidians, all
Transition-1, and all Transition-2 snakes are of Gondwanian origin and remain so by distribution except for minor dispersions and raft-transport via India to Southeast Asia.
• “Advanced” Snakes
:
– Boas and pythons:
• These exhibit complex dispersions within, from, and back to Gondwanaland.
• A “Boas and Pythons” slide gives (some, but probably not enough) relevant data for addressing those mysteries.
– Colubroidea (“modern advanced snakes”):
• Southeast Asia is origin for these snakes and for their several radiations into the rest of the world. (See “Southeast Asia” slide.)
• The African colubroids are particularly interesting and probably include both an ancient clade and a more recent clade from SEA. (See “Africa” slide.)

Erycinae
1. Note that the “big boas”
(Boinae) & the pythons
(Pythoninae) occupy almost all the tropics but barely overlap.
a. Big boas occur in S. America,
Madagascar, and Pacific islands.
b. The single genus, Python , occurs almost throughout the range of the Pythoninae.
2. Note that the erycine boas
(Erycinae) are all small, often relictual, sometimes fossorial, and frequently adapted to xeric habitats.
3. Guess the biogeography!

Southeast Asia: Key to Modern-Snake Biogeography?
• SEA shares some “non-modern” snakes with Af. & S.Am.
– Scolecophidians probably came to Asia by raft transport (India).
– Transition-1 and Transition-2 snakes inhabit SEA &Neotropics; they may represent Gondwanian relict distributions.
– Python may have dispersed from Australia across SEA into Africa.
• Much later, SEA elapids colonized Australia (by islandhopping) and radiated extensively there.
• Still more recently, 3 modern “Families” expanded from
SEA to northern Asia, to Europe, and to the Americas.
– Note: temperate- & cold-Eurasian snake-faunas are similar and are depauperate. Is this because of Pleistocene glaciations?
– Obvious & fairly recent links exist between the snake faunas of the
New World and of SEA. How many radiations occurred?
– Dispersals into Africa are considered on the next slide.

(biogeography:)
African mysteries
• Two major African patterns:
– Africa’s non-modern snake lineages show affiliation w/snakes of other regions (SEA, SAm, & Australia).
This is explainable by Gondwanaland radiations.
– But the most modern African snakes appear closely related only to each other.
• I hypothesize 2 time-separate invasions (probably of SEA origins) of colubroid founder stocks into Africa. The invaders underwent rapid evolution and speciation, diverging phenotypically from non-African ancestors.
• Molecular biologists still have not teased out the relationships– in part because geographical intermediates have been lost due to climatic change (Sahara Desert).