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

Type Article
Date 2019-09
Language English
Author(s) Phuong Mark A.1, Alfaro Michael E.1, Mahardika Gusti N.2, Marwoto Ristiyanti M.3, Prabowo Romanus EdyORCID4, von Rintelen Thomas5, Vogt Philipp W. H.5, Hendricks Jonathan R.6, Puillandre Nicolas7
Affiliation(s) 1 : Univ Calif Los Angeles, Dept Ecol & Evolutionary Biol, 612 Charles E Young Dr, Los Angeles, CA 90095 USA.
2 : Udayana Univ Bali, Fac Vet Med, Anim Biomed & Mol Biol Lab, Jl Sesetan Markisa 6, Denpasar 80225, Bali, Indonesia.
3 : LIPI, Museum Zool Bogoriense, Res Ctr Biol, Zool Div, Km 46, Bogor 16911, West Java, Indonesia.
4 : Univ Jenderal Soedirman, Fac Biol, Aquat Biol Lab, Jalan Dr Suparno 63 Grendeng, Purwokerto 53122, Indonesia.
5 : Leibniz Inst Evolut & Biodivers Sci, Museum Nat Kunde, Invalidenstr 43, D-10115 Berlin, Germany.
6 : Paleontol Res Inst, Ithaca, NY 14850 USA.
7 : Sorbonne Univ, EPHE, Museum Natl Hist Nat, Inst Systemat Evolut Biodiversite ISYEB,CNRS, 1259 Trumansburg Rd,57 Rue Cuvier,CP 26, F-75005 Paris, France.
Source Systematic Biology (1063-5157) (Oxford Univ Press), 2019-09 , Vol. 68 , N. 5 , P. 781-796
DOI 10.1093/sysbio/syz016
WOS© Times Cited 12
Keyword(s) Macroevolution, phylogenetics, venom evolution
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.
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Phuong Mark A., Alfaro Michael E., Mahardika Gusti N., Marwoto Ristiyanti M., Prabowo Romanus Edy, von Rintelen Thomas, Vogt Philipp W. H., Hendricks Jonathan R., Puillandre Nicolas (2019). Lack of Signal for the Impact of Conotoxin Gene Diversity on Speciation Rates in Cone Snails. Systematic Biology, 68(5), 781-796. Publisher's official version : https://doi.org/10.1093/sysbio/syz016 , Open Access version : https://archimer.ifremer.fr/doc/00760/87177/