Lack of signal for the impact of venom gene diversity on speciation rates in cone snails

Abstract

25Understanding why some groups of organisms are more diverse than others is a central goal in 26 macroevolution. Evolvability, or lineages' intrinsic capacity for evolutionary change, is thought 27 to influence disparities in species diversity across taxa. Over macroevolutionary time scales, 28 clades that exhibit high evolvability are expected to have higher speciation rates. Cone snails 29 (family: Conidae, >900 spp.) provide a unique opportunity to test this prediction because their 30 venom genes can be used to characterize differences in evolvability between clades. Cone snails 31 are carnivorous, use prey-specific venom (conotoxins) to capture prey, and the genes that encode 32 venom are known and diversify through gene duplication. Theory predicts that higher gene 33 diversity confers a greater potential to generate novel phenotypes for specialization and 34 adaptation. Therefore, if conotoxin gene diversity gives rise to varying levels of evolvability, 35 conotoxin gene diversity should be coupled with macroevolutionary speciation rates. We applied 36 exon capture techniques to recover phylogenetic markers and conotoxin loci across 314 species, 37 the largest venom discovery effort in a single study. We paired a reconstructed timetree using 12 38 fossil calibrations with species-specific estimates of conotoxin gene diversity and used trait-39 dependent diversification methods to test the impact of evolvability on diversification patterns.40 Surprisingly, did not detect any signal for the relationship between conotoxin gene diversity and 41 speciation rates, suggesting that venom evolution may not be the rate-limiting factor controlling 42 diversification dynamics in Conidae. Comparative analyses showed some signal for the impact 43 of diet and larval dispersal strategy on diversification patterns, though whether or not we 44 detected a signal depended on the dataset and the method. If our results remain true with 45 increased sampling in future studies, they suggest that the rapid evolution of Conidae venom 46 may cause other factors to become more critical to diversification, such as ecological opportunity 47 or traits that promote isolation among lineages. 48 49 93 natural way to characterize differences in evolvability between clades. 94 We employ a sequence capture technique previously used in cone snails (Phuong & 95 Mahardika 2017) to recover phylogenetic markers and conotoxin genes from 314 described 96 species. We use the phylogenetic markers to reconstruct a time-calibrated phylogeny and 97 perform trait-dependent diversification analyses to test the impact of evolvability on 98 diversification patterns. We predict that clades with a greater number of conotoxin gene copies 99 should have higher speciation rates. In addition, we test other traits that may have an impact on 100 diversification patterns, including diet and larval dispersal strategy. 101 102 Methods 103 104Bait design 105 We used a targeted sequencing approach to recover markers for phylogenetic inference and 106 ob...