Lack of Signal for the Impact of Conotoxin Gene Diversity on Speciation Rates in Cone Snails

Abstract

Understanding why some groups of organisms are more diverse than others is a central goal in macroevolution. Evolvability, or the intrinsic capacity of lineages for evolutionary change, is thought to influence disparities in species diversity across taxa. Over macroevolutionary time scales, clades that exhibit high evolvability are expected to have higher speciation rates. Cone snails (family: Conidae, $>$900 spp.) provide a unique opportunity to test this prediction because their toxin genes can be used to characterize differences in evolvability between clades. Cone snails are carnivorous, use prey-specific venom (conotoxins) to capture prey, and the genes that encode venom are known and diversify through gene duplication. Theory predicts that higher gene diversity confers a greater potential to generate novel phenotypes for specialization and adaptation. Therefore, if conotoxin gene diversity gives rise to varying levels of evolvability, conotoxin gene diversity should be coupled with macroevolutionary speciation rates. We applied exon capture techniques to recover phylogenetic markers and conotoxin loci across 314 species, the largest venom discovery effort in a single study. We paired a reconstructed timetree using 12 fossil calibrations with species-specific estimates of conotoxin gene diversity and used trait-dependent diversification methods to test the impact of evolvability on diversification patterns. Surprisingly, we did not detect any signal for the relationship between conotoxin gene diversity and speciation rates, suggesting that venom evolution may not be the rate-limiting factor controlling diversification dynamics in Conidae. Comparative analyses showed some signal for the impact of diet and larval dispersal strategy on diversification patterns, though detection of a signal depended on the dataset and the method. If our results remain true with increased taxonomic sampling in future studies, they suggest that the rapid evolution of conid venom may cause other factors to become more critical to diversification, such as ecological opportunity or traits that promote isolation among lineages.

Conotoxin Diversity in the Venom Gland Transcriptome of the Magician’s Cone, Pionoconus magus

“…Therefore, one of the main challenges in cone venomics is cataloguing the exact composition of the conotoxin toolkit of each of the species [7,8,9,12]. This is important for evolutionary studies, as comparing species venom repertoires within a phylogenetic framework provides insights on how their diversity was generated, their adaptation to different diet specializations, and their relative influence in the extraordinary species diversification of the group [8,13,14,15,16]. Moreover, the enormous conotoxin diversity available in nature is considered a potentially valuable source of novel drugs to advance in neuroscience research [17,18,19], as well as to treat human neuropathology disorders and clinical complications [20,21].…”

Venom Diversity and Evolution in the Most Divergent Cone Snail Genus Profundiconus

“…Among taxa that have developed a venomous function, the globally distributed gastropod superfamily Conoidea is a highly diversified group of carnivorous species including the family Conidae J. Fleming, 1822 [4,5]. Based on the latest published molecular phylogeny of the Conidae [6] six genera, comprising ~850 species, can be recognized: Profundiconus Kuroda, 1956, Californiconus J. K. Tucker & Tenorio, 2009, Lilliconus G. Raybaudi Massilia, 1994, Pygmaeconus Puillandre & Tenorio, 2017, Conasprella Thiele, 1929, and Conus Linnaeus, 1758. The Conidae venom arsenal, combined with sophisticated envenomation strategies, has allowed these slow-moving snail species to prey on worms, other molluscs, and fish [7].…”

A phylogeny-aware approach reveals unexpected venom components in divergent lineages of cone snails

“…Eight genera (herein referred to as divergent Conidae ) are currently included in the family Conidae, in addition to Conus [12]. Among them, recent phylogenetic studies on the family [13,14] demonstrate that the genera Conasprella , Californiconus , Pygmaeconus and Lilliconus form a separate lineage, sister to Conus , whereas Profundiconus is found to be the earliest diverging lineage of the family (figure 1 a ). Current knowledge of venom composition among these taxa is highly skewed [15].…”

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Figure 1( a ) Phylogenetic tree of the family Conidae (after Phuong et al . [14]). ( b ) Venn diagram showing numbers of SSCs shared by divergent Conidae genera.

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