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. 2009 Jul 7;276(1666):2443-9.
doi: 10.1098/rspb.2009.0048. Epub 2009 Apr 1.

Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution

Affiliations

Coevolution of diet and prey-specific venom activity supports the role of selection in snake venom evolution

Axel Barlow et al. Proc Biol Sci. .

Abstract

The processes that drive the evolution of snake venom variability, particularly the role of diet, have been a topic of intense recent research interest. Here, we test whether extensive variation in venom composition in the medically important viper genus Echis is associated with shifts in diet. Examination of stomach and hindgut contents revealed extreme variation between the major clades of Echis in the proportion of arthropod prey consumed. The toxicity (median lethal dose, LD(50)) of representative Echis venoms to a natural scorpion prey species was found to be strongly associated with the degree of arthropod feeding. Mapping the results onto a novel Echis phylogeny generated from nuclear and mitochondrial sequence data revealed two independent instances of coevolution of venom toxicity and diet. Unlike venom LD(50), the speed with which venoms incapacitated and killed scorpions was not associated with the degree of arthropod feeding. The prey-specific venom toxicity of arthropod-feeding Echis may thus be adaptive primarily by reducing venom expenditure. Overall, our results provide strong evidence that variation in snake venom composition results from adaptive evolution driven by natural selection for different diets, and underscores the need for a multi-faceted, integrative approach to the study of the causes of venom evolution.

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Figures

Figure 1
Figure 1
Bayesian phylogeny of the major Echis species groups, inferred using a single representative taxon from each. Bayesian posterior probabilities are shown by relevant nodes. Columns to the right indicate the proportion of arthropod prey consumed (diet) and venom toxicity to scorpions (venom):++, high; +, moderate; −, low; nt, not tested. Instances of dietary shifts in prey type accompanied by coevolution of venom activity are indicated by vertical bars along branches.
Figure 2
Figure 2
Venom protein profiles; venom from B. arietans (Ba), C. cerastes (Cc), E. c. sochureki (Ecs), E. ocellatus (Eo), E. p. leakeyi (Epl) and E. coloratus (Ec) were fractionated using 15% reduced SDS–PAGE.
Figure 3
Figure 3
Scorpion LD50 for Echis and B. arietans venoms. Species abbreviations are consistent with figure 2. Error bars show 95% confidence intervals. Pairwise statistical comparisons are shown by asterisks (*=p<0.05; ***=p<0.001; n.s., not significant) and superscripts (a: Z=0.0, p=1.0; b: Z=3.48, p<0.001; c: Z=2.47, p=0.014; d: Z=2.02, p=0.043). The pie charts above show the proportion of arthropods (black portions) and vertebrates (grey portions) consumed by each Echis species group.
Figure 4
Figure 4
Mean time to scorpion incapacitation (white bars) and death (grey bars) following a biologically realistic venom dose. Species abbreviations are consistent with figure 2. Error bars show standard error.

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