No safety in the trees: Local and species-level adaptation of an arboreal squirrel to the venom of sympatric rattlesnakes

Abby M. Pomento, Blair W. Perry, Robert D. Denton, H. Lisle Gibbs, Matthew L. Holding

Research output: Contribution to journalArticlepeer-review

10 Scopus citations

Abstract

Within some species, squirrels respond to variable selection from venomous snake predators by showing population-level variation in resistance, while between species, some rattlesnakes possess venom that is more effective at overcoming venom resistance in different species of squirrels. A functional evaluation of resistance variation to venom within and between species of squirrels and snakes can link resistance variation to its evolutionary causes across these different evolutionary scales. To do this, we compared the effectiveness of squirrel sera in inhibiting rattlesnake (Crotalus spp.) venom metalloproteinase activity between populations and between species to test for a response to local variation in selection from a single rattlesnake predator and for specialization of two resistant squirrel species to each of their distinct sympatric snake predators. We found that Timber Rattlesnake (Crotalus horridus) venom inhibition by Eastern gray squirrels (Sciurus carolinensis) is higher at a site where the rattlesnakes are present, which suggests selection may maintain venom resistance in populations separated by short distances. Next, we performed a reciprocal cross of venoms and sera from two rattlesnake and two squirrel species. This showed that squirrel resistance is lower when tested against venom from allopatric compared to sympatric rattlesnake species, demonstrating that squirrel inhibitors are specialized to sympatric venom and suggesting a tradeoff in terms of specialization to the venom of a specific species of rattlesnake predator. This pattern can be explained if inhibitors must recognize venom proteins and resistance evolution tracks venom evolution.

Original languageEnglish (US)
Pages (from-to)149-155
Number of pages7
JournalToxicon
Volume118
DOIs
StatePublished - Aug 1 2016
Externally publishedYes

Bibliographical note

Funding Information:
We thank Hardy Kern, Meghan Parsley, Mónica Saccucci, Collin Ries, Shannon Hedge, and Katie Costello for helpful discussion during project planning, and Denis Case, Rita Apanius, and Doug Wynn for assistance in the field. This research was approved by Ohio Division of Wildlife Wild Animal Permit 16-69 and Ohio State University IACUC protocol 2012A00000015-R1 . Funding was provided by Ohio State University Undergraduate Research Scholar Awards to A.M.P. and B.W.P.

Keywords

  • Coevolution
  • Functional diversity
  • Rattlesnake
  • Resistance
  • Squirrel
  • Venom

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