Parallel Arms Races between Garter Snakes and Newts Involving Tetrodotoxin as the Phenotypic Interface of Coevolution

Abstract

Parallel "arms races" involving the same or similar phenotypic interfaces allow inference about selective forces driving coevolution, as well as the importance of phylogenetic and phenotypic constraints in coevolution. Here, we report the existence of apparent parallel arms races between species pairs of garter snakes and their toxic newt prey that indicate independent evolutionary origins of a key phenotype in the interface. In at least one area of sympatry, the aquatic garter snake, Thamnophis couchii, has evolved elevated resistance to the neurotoxin tetrodotoxin (TTX), present in the newt Taricha torosa. Previous studies have shown that a distantly related garter snake, Thamnophis sirtalis, has coevolved with another newt species that possesses TTX, Taricha granulosa. Patterns of within population variation and phenotypic tradeoffs between TTX resistance and sprint speed suggest that the mechanism of resistance is similar in both species of snake, yet phylogenetic evidence indicates the independent origins of elevated resistance to TTX.

The evolutionary origins of beneficial alleles during the repeated adaptation of garter snakes to deadly prey

“…To provide a phylogenetic perspective on the evolution of elevated TTX resistance, we also collected resistance data from 228 specimens from 7 other garter snakes species representing the major Thamnophis clades (33) and from 34 snakes from 4 outgroup taxa representing pertinent New World natricine lineages (54) (Table S1). Some TTX resistance data came from our previous work (24,37).…”

“…By paralyzing nerves and excitable muscle cells, TTX causes immobilization, respiratory failure, and often death (18,21). Despite the fact that TTX is one of the most potent neurotoxins known (22), garter snakes from a number of populations are able to prey on toxic Taricha (23)(24)(25). In fact, the levels of TTX resistance in garter snakes and concentrations of TTX in newts often covary over much of western North America, suggesting the two are engaged in a coevolutionary ''arms race'' characterized by adaptation and counteradaptation (17,23,26).…”

“…Multiple species of garter snakes are known to engage in ecological interactions with toxic newts in western North America: Thamnophis sirtalis from coastal California (23), Thamnophis couchii from the southern Sierra Nevada mountain range of California (24), and Thamnophis atratus from coastal California (25) (Fig. 1).…”

Four Central Points About Coevolution

“…The traits of the conifers and the crossbills show just the kinds of geographic differences you would expect to find in regions with squirrels as compared with regions without squirrels (Edelaar and Benkman 2006;Siepelski and Benkman 2007;Parchman and Benkman 2008;Benkman and Parchman 2009;Benkman 2010). Toxic newts and the garter snakes that eat them differ geographically in western North America in the level of chemical defenses in the newts and the ability of the snakes to detoxify those chemical defenses (Brodie et al 2002;Brodie et al 2005;Hanifin et al 2008). Wild parsnips and parsnip webworms, introduced to North America from Europe only within the past few hundred years, have coevolved into a geographic mosaic in the mix of chemical defenses deployed by the plants against these insects and the detoxification enzymes in the insects that counteract these defense chemicals (Berenbaum and Zangerl 1998;Zangerl and Berenbaum 2003).…”

Constraint shapes convergence in tetrodotoxin-resistant sodium channels of snakes

“…S1) and are exceptional as the only known vertebrate predators of tetrodotoxic organisms (17). In western North America, populations of Pacific newts (Taricha) harbor extreme levels of TTX (18) but are preyed on by multiple garter snake species (Thamnophis): Thamnophis sirtalis preys on Taricha granulosa (17,19); Thamnophis couchii preys on Taricha torosa (20) and Taricha sierrae (21); and Thamnophis atratus consumes Taricha granulosa (22). In Central and South America, the only known predator of highly poisonous Atelopus toads (23,24) is the Neotropical ground snake, Liophis epinephelus (25,26).…”