Is Hybridization a Source of Adaptive Venom Variation in Rattlesnakes? A Test, Using a Crotalus scutulatus × viridis Hybrid Zone in Southwestern New Mexico.
Venomous snakes often display extensive variation in venom composition both between and within species. However, the mechanisms underlying the distribution of different toxins and venom types among populations and taxa remain insufficiently known. Rattlesnakes (Crotalus, Sistrurus) display extreme inter- and intraspecific variation in venom composition, centered particularly on the presence or absence of presynaptically neurotoxic phospholipases A₂ such as Mojave toxin (MTX). Interspecific hybridization has been invoked as a mechanism to explain the distribution of these toxins across rattlesnakes, with the implicit assumption that they are adaptively advantageous. Here, we test the potential of adaptive hybridization as a mechanism for venom evolution by assessing the distribution of genes encoding the acidic and basic subunits of Mojave toxin across a hybrid zone between MTX-positive Crotalus scutulatus and MTX-negative C. viridis in southwestern New Mexico, USA. Analyses of morphology, mitochondrial and single copy-nuclear genes document extensive admixture within a narrow hybrid zone. The genes encoding the two MTX subunits are strictly linked, and found in most hybrids and backcrossed individuals, but not in C. viridis away from the hybrid zone. Presence of the genes is invariably associated with presence of the corresponding toxin in the venom. We conclude that introgression of highly lethal neurotoxins through hybridization is not necessarily favored by natural selection in rattlesnakes, and that even extensive hybridization may not lead to introgression of these genes into another species.
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. giulia.zancolli@gmail.com.
Giulia
G
Zancolli
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. bsu057@bangor.ac.uk.
Timothy G
TG
Baker
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. axel.barlow.ab@gmail.com.|Evolutionary and Adaptive Genomics Group, Institute for Biochemistry and Biology, University of Potsdam, Karl-Liebknecht-Str. 24-25, Haus 29, 14476 Potsdam (Golm), Germany. axel.barlow.ab@gmail.com.
Axel
A
Barlow
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. bsu069@bangor.ac.uk.
Rebecca K
RK
Bradley
Venomics and Structural Proteomics Laboratory, Instituto de Biomedicina de Valencia, Consejo Superior de Investigaciones Cient&#237;ficas (CSIC), Jaume Roig 11, 46010 Valencia, Spain. jcalvete@ibv.csic.es.
Juan J
JJ
Calvete
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. kimc@live.co.uk.
Kimberley C
KC
Carter
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. bsue65@bangor.ac.uk.
Kaylah
K
de Jager
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. bsu052@bangor.ac.uk.
John Benjamin
JB
Owens
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. jennyp@live.co.uk.
Jenny Forrester
JF
Price
Venomics and Structural Proteomics Laboratory, Instituto de Biomedicina de Valencia, Consejo Superior de Investigaciones Cient&#237;ficas (CSIC), Jaume Roig 11, 46010 Valencia, Spain. libia.sanz@ibv.csic.es.
Libia
L
Sanz
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. amy.scholes.higham@gmail.com.
Amy
A
Scholes-Higham
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. bsu049@bangor.ac.uk.
Liam
L
Shier
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. woodlc08@hotmail.com.
Liam
L
Wood
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. c.wuster@me.com.
Catharine E
CE
Wüster
Molecular Ecology and Fisheries Genetics Lab, School of Biological Sciences, Bangor University, Bangor LL57 2UW, UK. w.wuster@bangor.ac.uk.|Chiricahua Desert Museum, P.O. Box 376, Rodeo, NM 88056, USA. w.wuster@bangor.ac.uk.
Wolfgang
W
Wüster
D000818:Animals; D003435:Crotalid Venoms / Q000737:chemistry* / Q000235:genetics; D017839:Crotalus / Q000145:classification / Q000235:genetics*; D004272:DNA, Mitochondrial / Q000235:genetics; D019143:Evolution, Molecular; D006824:Hybridization, Genetic; D009245:NADH Dehydrogenase / Q000235:genetics; D009498:Neurotoxins / Q000737:chemistry* / Q000235:genetics; D009516:New Mexico; D025341:Principal Component Analysis; D019655:Quantitative Trait, Heritable
D003435:Crotalid Venoms; D004272:DNA, Mitochondrial; C018107:Mojave toxin; D009498:Neurotoxins; D009245:NADH Dehydrogenase
Crotalus; Mojave toxin; adaptation; evolution; hybridization; introgression; molecular evolution; venom