TY - JOUR
T1 - When one phenotype is not enough
T2 - 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
AU - Herrmann, Hans-Werner
AU - Holycross, Andrew T.
AU - Lannutti, Dominic I.
AU - Mulley, John
AU - Sanz, Libia
AU - Travis, Zachary D.
AU - Whorley, Joshua R.
AU - Wüster, Catharine E.
AU - Wüster, Wolfgang
N1 - Publisher Copyright:
© 2019 The Author(s) Published by the Royal Society.
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 - population structure
KW - diet
KW - phenotypic variation
KW - structural polymorphism
KW - adaptive trait
KW - venom
KW - Crotalid Venoms/genetics
KW - Genotype
KW - California
KW - Crotalus/genetics
KW - Gene-Environment Interaction
KW - Biological Evolution
KW - Phenotype
KW - Animals
KW - Diet
KW - Environment
KW - Arizona
KW - Population Dynamics
UR - http://www.scopus.com/inward/record.url?scp=85062827141&partnerID=8YFLogxK
U2 - 10.1098/rspb.2018.2735
DO - 10.1098/rspb.2018.2735
M3 - Article
C2 - 30862287
SN - 0962-8452
VL - 286
JO - Proceedings of the Royal Society B: Biological Sciences
JF - Proceedings of the Royal Society B: Biological Sciences
IS - 1898
M1 - 20182735
ER -