Geographic Variation in Venom Allelic Composition and Diets of the Widespread Predatory Marine Gastropod Conus ebraeus

Abstract

BackgroundMembers of the predatory gastropod genus Conus use a venom comprised of a cocktail of peptide neurotoxins, termed conotoxins or conopeptides, to paralyze prey and conotoxin gene family members diversify via strong positive selection. Because Conus venoms are used primarily to subdue prey, the evolution of venoms is likely affected by predator-prey interactions.Methodology/Principal FindingsTo identify the selective forces that drive the differentiation of venoms within species of Conus, we examined the distribution of alleles of a polymorphic O-superfamily conotoxin locus of Conus ebraeus at Okinawa, Guam and Hawaii. Previous analyses of mitochondrial cytochrome oxidase I gene sequences suggest that populations of C. ebraeus, a worm-eating Conus, are not structured genetically in the western and central Pacific. Nonetheless, because the sample size from Guam was relatively low, we obtained additional data from this location and reexamined patterns of genetic variation at the mitochondrial gene at Okinawa, Guam and Hawaii. We also utilized a DNA-based approach to identify prey items of individuals of C. ebraeus from Guam and compared this information to published data on diets at Okinawa and Hawaii. Our results show that conotoxin allelic frequencies differ significantly among all three locations, with strongest differentiation at Hawaii. We also confirm previous inferences that C. ebraeus exhibits no genetic differentiation between Okinawa, Guam and Hawaii at the mitochondrial locus. Finally, DNA-based analyses show that eunicid polychaetes comprise the majority of the prey items of C. ebraeus at Guam; while this results compares well with observed diet of this species at Okinawa, C. ebraeus preys predominantly on nereid polychaetes at Hawaii.Conclusions/SignificanceThese results imply that strong selection pressures affect conotoxin allelic frequencies. Based on the dietary information, the selection may derive from geographic variation in dietary specialization and local coevolutionary arms races between Conus and their prey.

Intraspecific variations in the venom peptidome of the ant Odontomachus haematodus (Formicidae: Ponerinae) from French Guiana

“…Such inter-colonial variations have previously been reported for Dinoponera quadriceps (Ponerinae) collected from different areas in Brazil (Cologna et al 2013). Among animal venoms, intraspecific variations related to geography are a common phenomenon and have been reported in snakes (Shashidharamurthy et al 2002), cone snails (Duda et al 2009), scorpions (Omran and McVean 2000), spiders (Escoubas et al 1998) and both social ) and parasitoid wasps (Poirié et al 2014). In snakes, intraspecific variations have been shown to exhibit a differential venom effectiveness towards different prey (Casewell et al 2013).…”

“…In snakes, intraspecific variations have been shown to exhibit a differential venom effectiveness towards different prey (Casewell et al 2013). This may be the result of allelic variations in the genes coding the peptides as shown for Conus ebraeus venom (Duda et al 2009), increasing the venom peptidic diversity in this species. This intraspecific diversity is essential for natural selection and ant venom diversification.…”

Effects of geographical heterogeneity in species interactions on the evolution of venom genes

“…We identified prey species from faecal samples of C. ebraeus individuals with a DNA-based approach that was described previously by Duda et al [26]. In brief, we extracted DNA from faeces and amplified a region of the mitochondrial 16S rRNA gene with primers that should preferentially amplify annelid but not gastropod 16S rRNA gene.…”

“…Based on the analyses of sequences of a region of the mitochondrial cytochrome oxidase I (COI) gene, this species exhibits little if any genetic population structure throughout tropical Pacific regions of the Indo-West Pacific [24,25]. Nonetheless, populations exhibit significant difference in allelic frequencies at a conotoxin gene E1, a pattern that may have resulted from selection on venom composition owing to difference in prey utilization among populations [26].…”

Conotoxins and Other Conopeptides

“…They represent a large natural library of compounds that are specific for receptor subtypes, and are commonly used in neurophysiological studies to understand the role of receptor subtypes in nervous system functions or diseases (Dutton and Craik, 2001;Lewis, 2009;Olivera and Cruz, 2001). Fundamental biological studies have also been carried out to understand how cone snail venoms mature (Dobson et al, 2012;Safavi-Hemami et al, 2011a), how the environment influences conopeptide expression (Duda and Lee, 2009;Duda and Palumbi, 2004;Duda et al, 2009a), and the genetic events at the origin of conopeptide diversity (Biggs et al, 2010;Chang and Duda, 2012;Duda and Palumbi, 2000;Puillandre et al, 2012). Conopeptides also have outstanding potential as drugs or drug leads as they are the result of millions of years of natural optimization of both specificity and potency; combining both properties is a major challenge faced in drug design programs (Teichert and Olivera, 2010).…”