The Ecology and Evolution of Venomous Snakes

The evolution and ecology of venomous snakes is a topic which was not well
understood until recently. Researchers are still trying to understand the evolution of
snakes due to the difficulty in obtaining data in the field.
Venomous snakes have evolved and diversified into front and rear fanged snakes
and the factors that led to their evolution. This paper will examine the factors that
influenced their evolution and how they differ from constrictors.

Evolution of Rear Fanged Snakes and Evolution of Fanged Snakes

The evolution of front and rear fanged snakes is not well understood due to the
difficulty of collecting data in the field with venomous snakes. However, there are
pieces of the puzzle that can help understand the evolution and ecology of
venomous snakes. The work done by Westeen has shown the method of prey
capture (venom, constriction, both or neither) and diet specialisation have factored
heavily on the evolution of fanged snakes alongside dental traits, for example the
size of the maxilla, type of fang/teeth (grooved, hollow, tubular, and standard teeth),
and number of maxilla teeth (Westeen, 2020). The maxilla is the upper jawbone in
snakes. Different families of snakes have evolved their fangs in different ways and
the phenological relationship is shown (figure 1).
Figure 1: Showing family of snakes. The maxillary phenotype and the tooth
phenotype. (Westeen, 2020)

Snake families like vipers and Elapidae (cobras, sea snakes) shortened their maxilla
bone and elongated their fangs and leading to them having a single phenotype for
the maxilla. Similarly, with colubrids but to a lesser extent than vipers and Elapidae
(Westeen, 2020). However, there is evidence of ne/nv colubriformis snakes losing
their fangs entirely. The common origin of snake fangs and grooving of snake teeth
may explain why ne/nv colubriformis have lost their fangs in some groups (Westeen,
2020). Likely due to dietary shifts and adoption of non-venomous hunting methods
for colubriformis snakes (Westeen, 2020). Another hypothesis for the evolution of
venomous snakes is that constrictors failed to adapt to certain environmental
pressures, for example the loss of forested areas and the expansion of more open
habitats.
Rapid locomotion and passive locomotion are two types of animal movement that
differ in their energy requirements and environmental interactions.
Rapid locomotion is the form of movement that requires extensive muscular effort
and energy expenditure and allows animals to pursue prey and escape predators.
Passive locomotion is a passive form of movement and does not require as much
muscular effort or energy expenditure. It results in considerably slower motion, for
example in constrictors and relies on the environment to provide transportation. In
the case of snakes, passive locomotion is often used as a secondary mode of
movement.
One possible scenario for the evolution of venom delivery systems in snakes is that
rapid locomotion and active prey pursuit required adaptations in feeding and
locomotion mechanisms. With the increase of colubrid diversity, some colubrids
evolved front fangs and venom glands derived from the Duvernoy gland, which
allowed them to separate feeding and locomotion functions. This led to the
emergence of front-fanged snake families such as vipers and elapids.

Even though the Duvernoy gland is lost in some members of the colubrid family,
hypertrophied in others, or integrated into the venom delivery systems of others
(Savitzky, 1980). The independent evolution of posterior and anterior fangs is
supported from the results found by Freek is that anterior and posterior fanged snake
morphology had developed independently from each other. (Freek, 2008)

Evolution of Proteins in Snake Venom

Snake venom is an abundant source of functionally diverse protein multigene

families, though only a relatively small number of these protein families have been
studied, for example serine proteases, PLA2 inhibitors etc. These families evolved by
gene duplication and diversification of positive selection (Zupunski, 2003). Many
serine proteases are found in snake venom of the Viperidae and Elapidae families.
Which is part of the bovine pancreatic trypsin inhibitor family (BPTI). These Kunitz
/BPTI inhibitors are characterised by a fold of about 60 amino acids and 3 disulfide
bridges. These Kunitz/BPTI can be split into two different groups being the
non-neurotoxin Kunitz/BPTI inhibitors and the neurotoxin Kunitz inhibitor have lost
their ability to inhibit Kunitz/BPTI and now block K+ and Ca2+ channel pathways
(Zupunski, 2003). Kunitz/BPTI homologs can be put into two families: Kunitz
inhibitors and anti- coagulant proteins where the latter has secondary structures
similar to BPTI but differs in the folds of certain loops and in orientation. Kunitz
inhibitors inhibit serine proteinase through a conversed anti-proteinase site
(Zupunski, 2003). This is completely different for the Kunitz/BPTI inhibitors in snakes
where the neurotoxic important regions are adjacent to the dendrotoxin c terminals,
and the non-neurotoxic parts are conserved in the core and at the n terminal, not at
the anti-proteinase site. This shows they have retained the same fold but have
developed and expanded the functions (Zupunski, 2003).
The venom for Vipera ammodytes contains several Kunitz/BPTI inhibitors that target
Trypsin and chymotrypsin. These inhibitors have shown 80% sequence identity with
each other, and their chains consist of 61 and 65 amino acids and with 3 conserved
disulfide bridges. They are similar to the Kunitz/BPTI inhibitors that are found in
snake venoms, with 50% sequence similarity.
Ti and Chi inhibitors were sequenced from Vipera ammodytes venom glands
(Zupunski, 2003). This was compared to other multigene families from snake
venom. More evidence was found that snake venom contains multigene families that
had diversified from positive selection (Arid, 2015). This could give an advantage to
venomous snakes when hunting diverse prey species through the adaptive evolution
of venomous proteins (Arid, 2015).
Further evidence of the adaptive evolution of venomous proteins is rapid evolution
under positive selection, similar to Kunitz/BPTI inhibitor protein families. These
proteins are abundant and the fact that snakes energetically invest in venomous
proteins, gives them an advantage in survival allowing for the abundance of certain
proteins and the natural selection of snake venom proteins. Therefore, natural
selection favours the expansion and variation of snake venom proteins (Arid, 2015).

Diversification of feeding evolution in snakes:

During Cenozoic period, after the end-Cretaceous extinction event, was a time for
the rapid diversification of snakes into the different families of snakes seen today into
4000 known species (Grundler, 2021). There was a dietary shift in early snakes from
invertebrates, mostly insect eating, to vertebrates, which led to increased digestive
system volume as a result of morphological changes in response to fossorial
changes (Grunder, 2021).
Modifications to the skull morphology of snakes evolved to accommodate large prey,
resulting in diverse and elaborate feeding strategies.
This diversification was especially rapid in the Eocene epoch, following the
end-Cretaceous extinction event that eliminated many top predators.
When trophic diversification was extremely rapid after the end-cretaceous extinction
event. The rapid diversification of snake feeding strategies was due to deduced
ecological competition for top predator and allowed for snakes to fill in that top
predator role which was left empty after the cretaceous extinction event (Grundler,
2021), example (Titanoboa cerrejonensis).
The findings from Grundler’s work showed that the idea of generalists evolved into
specialists is rejected due to ancestral snakes having slightly specialised diets and
that specialists were no less versatile than generalists in evolution (Grundler, 2021).
For example 13/15 prey items of the egg eating snake Rhachidelus brazili those prey
items were bird eggs but 5 of its closest relatives 139 prey items none were recorded
as being bird eggs and were mostly snakes, mammals, and lizards and at least one
species of Galapagos snake has started to forage for fish which is not known in any
close relatives or other populations and helps lend to the claim of behaviour can
change the niche of a species (Grundler, 2021). The Eocene had shown the rapid
diversification of snakes and mammals, predominantly rodents had most snakes that
came from a common ancestor at this time that had eaten those diversifying rodents
(Grundler, 2021). This was particularly true with the colubrid family of snakes based
on the reconstructed diet of the ancestor snake which is extremely diverse in their
feeding strategies (Grundler, 2021).
The diversity of colubrid feeding strategies is shown in the colonisation of tropic and
Nearctic regions where colubrid subfamilies like Natricinae, Dipsadinae, and
Colubrinae. This remains consistent with the idea of new biogeographic
opportunities opens up new niches for snake evolution (Grundler, 2021).
One of the unresolved issues in the evolution of feeding mechanisms in snakes is
the identity of the intermediate step. Some researchers have suggested that the
mosasaur family was the ancestor of snakes, based on the flexible lower jaw, the
phylogenetic relationship, and the similar tooth structure of mosasaurs and snakes
(Lee, 1999). Another hypothesis suggests that early burrowing lizards were the
common ancestors of snakes. These lizards had hard skulls for digging through soil,
and later evolved reduced skull size, body elongation, and large prey consumption
(Shine, 2008).
The multiple conflicting points on the origin of feeding mechanisms has still not been
resolved completely and is still being pieced together on the common ancestor of
snakes. There is some common ground held, wherein snakes shifted their feeding
strategies and that has affected their diversification significantly.

Ecological and Evolutionary Effects of Venomous Snake Body Sizes

Bermann’s and Rapoport’s rules were used to follow the ecological and evolutionary
effects of venomous snake body sizes. Bergmann’s rule suggests that body size
increases with latitude (Reed, 2003). Rapoport's rule suggests that animals at
smaller latitudes have smaller latitudinal ranges than those at higher latitudes (Reed,
2003).
There is very little evidence of either of these rules being present in new world
snakes of the Elapidae and Viperidae families.
The region between 10°N and 20°N, which includes Central America and southern
Mexico, has a high diversity of snakes (Reed, 2003). This region has a complex
biogeographic history, with multiple episodes of fragmentation and isolation that
facilitated allosteric speciation.
Thus, biogeographic histories could have a more important role in species richness,
even though they could be limited in range longitude (Reed, 2003). This imposes a
caveat to the presumption that species with large geographic ranges are more likely
to speciate. Snakes tend to be right skewing in geographic ranges meaning they
tend to have smaller geographic ranges. Elapidae display a skew towards smaller
ranges while Viperae have no particular skew and had broad amount of ranges
(Reed, 2003). For example, the neotropical rattlesnake has a geographic range of
about 7.5 x 107km2 (Reed, 2003).
However, instead of a single species, that range contains several distinct species
that have been classified into their own taxon based on phylogenetic trees. This
could indicate other species with similar broad geographic ranges could face similar
taxonomic revisions. The positive correlation between body size and geographic
range. The upper limits of geographic range is constrained by the continental area,
while lower limits may be set by minimum viable population and other factors.
Various mechanisms may help explain the relationship between body size and range
size by Brown in 1995 that larger animals needed larger geographic ranges due to
higher energy maintenance and needed to maintain a stable population. Also, that
smaller animals did not follow this rule due to not needing as many resources.
However, the brown hypothesis used endotherms exclusively. Endotherms being
warm blooded animals and ectotherms being cold blooded (Reed, 2003). Contrary to
Brown's hypothesis some of the largest reptiles have high population densities due
to significantly lower energy requirements (Reed, 2003), for example some crocodile
species (saltwater crocodiles, Nile crocodiles etc). Body size seems to be a poor
indicator of dispersal ability of a species due to the largest Elapidae and Viperae all
being in tropical geographic ranges. Larger snakes have broad ranges where smaller
snakes have smaller ranges. A possible explanation is that smaller snakes have
narrower ranges because they are ecologically specialised for specific habitats
(Reed, 2003). Smaller species need less energy for their energy expenditure for
survival and reproduction in comparison to larger snakes and can adapt to cooler
climates (Reed, 2003). The evidence of Bergmann’s and Rapoport’s rules not being
applicable to snakes is further evidenced by there being no distinct pattern for body
size variance. Different snake groups, their evolution and environmental gradients
play a role in the variance in body size of different snake families (Carina, 2009).
Conclusion:
The evolution and ecology of venomous snakes still doesn't have a defined origin.
However, the application of Bergmann's rule in identifying the relationship between
body size and geographic range made inroads into understanding the ecology of
snakes. However, the evidence provided in this paper allows for the conclusion to
be made that we are closer to understanding that there is strong correlation between
these factors, but the influence of biogeographical and environmental gradients is
not yet fully explored and cannot be denied (Reed, 2003; Carina, 2009).

To further advance the field, researchers should explore these factors in more depth
and detail. Clarifying the identity and origin of the common ancestor of snakes could
shed light on the evolutionary pathways and adaptations of snakes, whether they
arose from aquatic origins or burrowing lizards (Lee, 1999; Grundler, 2021; Shine,
2009).
Citations:
- TERRIBLE, LEVI CARINA, et al. “Ecological and Evolutionary Components of Body
Size: Geographic Variation of Venomous Snakes at the Global Scale.” Biological
Journal of the Linnean Society, vol. 98, no. 1, 2009, pp. 94–109,
https://doi.org/10.1111/j.1095-8312.2009.01262.x.
- Westeen, Erin P., et al. “What Makes a Fang? Phylogenetic and Ecological Controls
on Tooth Evolution in Rear-Fanged Snakes.” BMC Ecology and Evolution, vol. 20,
no. 1, 2020, pp. 1–80, https://doi.org/10.1186/s12862-020-01645-0.
- Savitzky, Alan H. “The Role of Venom Delivery Strategies in Snake Evolution.”
Evolution, vol. 34, no. 6, 1980, pp. 1194–204,
https://doi.org/10.1111/j.1558-5646.1980.tb04065.x.
- Aird, Steven D., et al. “Snake Venoms Are Integrated Systems, but Abundant
Venom Proteins Evolve More Rapidly.” BMC Genomics, vol. 16, no. 1, 2015,
pp. 647–647, https://doi.org/10.1186/s12864-015-1832-6
- SHINE, RICHARD, and MICHAEL WALL. “Interactions between Locomotion,
Feeding, and Bodily Elongation during the Evolution of Snakes.” Biological
Journal of the Linnean Society, vol. 95, no. 2, 2008, pp. 293–304,
https://doi.org/10.1111/j.1095-8312.2008.01046.x.
- Lee, Michael S. Y., et al. “The Origin of Snake Feeding.” Nature (London), vol.
400, no. 6745, 1999, pp. 655–59, https://doi.org/10.1038/23236.
- Reed, Robert N. “Interspecific Patterns of Species Richness, Geographic
Range Size, and Body Size among New World Venomous Snakes.”
Ecography (Copenhagen), vol. 26, no. 1, 2003, pp. 107–17,
https://doi.org/10.1034/j.1600-0587.2003.03388.x.
- Zupunski, Vera, et al. “Adaptive Evolution in the Snake Venom Kunitz/BPTI
Protein Family.” FEBS Letters, vol. 547, no. 1, 2003, pp. 131–36,
https://doi.org/10.1016/S0014-5793(03)00693-8.
- Grundler, Michael C., and Daniel L. Rabosky. “Rapid Increase in Snake
Dietary Diversity and Complexity Following the End-Cretaceous Mass
Extinction.” PLoS Biology, vol. 19, no. 10, 2021, pp. e3001414–e3001414,
https://doi.org/10.1371/journal.pbio.3001414.
- Richardson, Michael K., et al. “Evolutionary Origin and Development of Snake
Fangs.” Nature (London), vol. 454, no. 7204, 2008, pp. 630–33,
https://doi.org/10.1038/nature07178.