TY - JOUR

T1 - When one phenotype is not enough: divergent evolutionary trajectories govern venom variation in a widespread rattlesnake species

AU - Zancolli, Giulia

AU - Calvete, Juan J.

AU - Cardwell, Michael D.

AU - Greene, Harry W.

AU - Hayes, William K.

AU - Hegarty, Matthew J.

AU - Herrmann, Hans-Werner

AU - Holycross, Andrew T.

AU - Lannutti, Dominic I.

AU - Mulley, John F.

AU - Sanz, Libia

AU - Travis, Zachary D.

AU - Whorley, Joshua R.

AU - Wuster, Catharine E.

AU - Wuster, Wolfgang

PY - 2019/3/13

Y1 - 2019/3/13

N2 - Understanding the origin and maintenance of phenotypic variation, particularly across a continuous spatial distribution, represents a key challenge in evolutionary biology. For this, animal venoms represent ideal study systems: they are complex, variable, yet easily quantifiable molecular phenotypes with a clear function. Rattlesnakes display tremendous variation in their venom composition, mostly through strongly dichotomous venom strategies, which may even coexist within a single species. Here, through dense, widespread population-level sampling of the Mojave rattlesnake, Crotalus scutulatus, we show that genomic structural variation at multiple loci underlies extreme geographical variation in venom composition, which is maintained despite extensive gene flow. Unexpectedly, neither diet composition nor neutral population structure explain venom variation. Instead, venom divergence is strongly correlated with environmental conditions. Individual toxin genes correlate with distinct environmental factors, suggesting that different selective pressures can act on individual loci independently of their co-expression patterns or genomic proximity. Our results challenge common assumptions about diet composition as the key selective driver of snake venom evolution and emphasize how the interplay between genomic architecture and local-scale spatial heterogeneity in selective pressures may facilitate the retention of adaptive functional polymorphisms across a continuous space.

AB - Understanding the origin and maintenance of phenotypic variation, particularly across a continuous spatial distribution, represents a key challenge in evolutionary biology. For this, animal venoms represent ideal study systems: they are complex, variable, yet easily quantifiable molecular phenotypes with a clear function. Rattlesnakes display tremendous variation in their venom composition, mostly through strongly dichotomous venom strategies, which may even coexist within a single species. Here, through dense, widespread population-level sampling of the Mojave rattlesnake, Crotalus scutulatus, we show that genomic structural variation at multiple loci underlies extreme geographical variation in venom composition, which is maintained despite extensive gene flow. Unexpectedly, neither diet composition nor neutral population structure explain venom variation. Instead, venom divergence is strongly correlated with environmental conditions. Individual toxin genes correlate with distinct environmental factors, suggesting that different selective pressures can act on individual loci independently of their co-expression patterns or genomic proximity. Our results challenge common assumptions about diet composition as the key selective driver of snake venom evolution and emphasize how the interplay between genomic architecture and local-scale spatial heterogeneity in selective pressures may facilitate the retention of adaptive functional polymorphisms across a continuous space.

KW - Animals

KW - Arizona

KW - Biological Evolution

KW - California

KW - Crotalid Venoms/genetics

KW - Crotalus/genetics

KW - Diet

KW - Environment

KW - Gene-Environment Interaction

KW - Genotype

KW - Phenotype

KW - Population Dynamics

UR - https://doi.org/10.5061/dryad.1473s5c

U2 - 10.1098/rspb.2018.2735

DO - 10.1098/rspb.2018.2735

M3 - Article

C2 - 30862287

VL - 286

SP - 20182735

JO - Proceedings of the Royal Society B: Biological Sciences

JF - Proceedings of the Royal Society B: Biological Sciences

SN - 0962-8452

IS - 1898

ER -