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
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
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
M1 - 20182735
ER -