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Toxin expression in snake venom evolves rapidly with constant shifts in evolutionary rates

DOI: 10.1098/rspb.2020.0613

Agneesh Barua(1*), Alexander S. Mikheyev(1,2)

  1. Ecology and Evolution Unit, Okinawa Institute of Science and Technology Graduate University, 1919-1 Tancha, Onna-son, Kunigami-gun, Okinawa-ken, Japan 904-0495
  2. Evolutionary genomics group, Australian National University

Agneesh Barua: https://orcid.org/0000-0002-8347-2171

*Corresponding Author: agneesh.barua@oist.jp

Key words: Gene expression evolution, complex traits, early burst, key innovation, snake venom.

Key innovations provide ecological opportunity by enabling access to new resources, colonization of new environments, and are associated with adaptive radiation. The most well known pattern associated with adaptive radiation is an early burst of phenotypic diversification. Venoms evolve rapidly, facilitate prey capture, and are widely believed to be key innovations leading to adaptive radiation. However, few studies have estimated their evolutionary rate dynamics. Here, we test for patterns of adaptive evolution in venom gene expression data from 52 venomous snake species. By identifying shifts in tempo and mode of evolution along with models of phenotypic evolution, we show that snake venom exhibits the macroevolutionary dynamics expected of key innovations. Namely, all toxin families undergo shifts in their rates of evolution, likely in response to changes in adaptive optima. Furthermore, we show that rapid-pulsed evolution modeled as a Lévy process better fits snake venom evolution than conventional early burst or Ornstein–Uhlenbeck models. While our results support the idea of snake venom being a key innovation, the innovation of venom chemistry lacks clear mechanisms that would lead to reproductive isolation and thus adaptive radiation. Therefore, the extent to which venom directly influences the diversification process is still a matter of contention.

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