Abstract
Venoms are primarily believed to evolve under strong diversifying selection resulting from persistent coevolution between predator and prey. Recent research has challenged this hypothesis, proposing that venoms from younger venomous lineages (e.g., snakes and cone snails) are governed predominantly by diversifying selection, while venoms from older venomous lineages (e.g., centipedes, scorpions, and spiders) are under stronger purifying selection. However, most research in older lineages has tested selection at more diverse phylogenetic scales. Although these tests are important for evaluating broad macroevolutionary trends underlying venom evolution, they are less equipped to detect species-level evolutionary trends, which likely have large impacts on venom variation seen at more diverse phylogenetic scales. To test for selection among closely related species from an older venomous lineage, we generated high-throughput venom-gland transcriptomes and venom proteomes for four populations of Giant Desert Hairy Scorpions (Hadrurus), including three Hadrurus arizonensis populations and one Hadrurus spadix population. We detected significant episodic and pervasive diversifying selection across a highly abundant toxin family that likely has a major role in venom function (\(\alpha \)KTxs), providing a contrast to the stronger purifying selection identified from other studies on scorpion venoms. Conversely, we detected weak episodic diversifying and/or stronger purifying selection in four toxin families (non-disulfide bridged peptides, phospholipase A2s, scorpine-like antimicrobial peptides, and serine proteases), most of which were less abundant and likely have ancillary functional roles. Finally, although we detected several major toxin families at disproportionate transcriptomic and/or proteomic abundances, we did not identify significant sex-based variation in Hadrurus venoms.
Similar content being viewed by others
Data Availability
Raw sequencing reads for H. arizonensis individuals were submitted to the National Center for Biotechnology Information’s (NCBI) Sequence Read Archive (SRA) under BioProject PRJNA340270 and BioSample accessions SAMN35672238 (C0337), SAMN35672239 (C0340), SAMN35672240 (C0343), SAMN35672241 (C0344), SAMN35672242 (C1032), and SAMN35672243 (C1034) and SRA accessions SRR24872967 (C0337), SRR24872966 (C0340), SRR24872964 (C0343), SRR24872965 (C0344), SRR24872963 (C1032), and SRR24872962 (C10340). The assembled consensus transcriptomes for each H. arizonensis population were submitted to the NCBI Transcriptome Shotgun Assembly (TSA) database at DDBJ/EMBL/GenBank using the accession GKMY00000000, with GKMY01000000 representing both the version used in this mansuscript and the first version. Raw sequencing reads for H. spadix were downloaded from the NCBI SRA under BioProject PRJNA340270, which was previously submitted by Rokyta and Ward (2017) using the BioSample accessions SAMN05711363 (C0195) and SAMN05711364 (C0196) and SRA accessions SRR4069277 (C0195) and SRR4069278 (C0196). Similar to our H. arizonensis samples, we submitted our H. spadix assembled transcriptome to the NCBI TSA database using the accession number GKMZ00000000, with GKMZ01000000 representing the first version and version used in this manuscript. Venom LC-MS/MS data, including raw mass spectrometry reads and the consensus proteome files were deposited in the ProteomeXchange Consortium with the PRIDE partner repository (Vizcaíno et al. 2016) using the following dataset identifiers: PXD042968 and 10.6019/PXD042968. Cytochrome c oxidase subunit 1 and venom gene coding sequence alignments for toxin families used in the selection analyses can be found in Supplemental Data 1. All other data corresponding to this project is available within the manuscript and/or supplemental data files.
References
Abdel-Rahman MA, Omran MAA, Abdel-Nabi IM, Ueda H, McVean A (2009) Intraspecific variation in the Egyptian scorpion Scorpio maurus palmatus venom collected from different biotopes. Toxicon 53:349–359
Aird SD, Aggarwal S, Villar-Briones A, Tin MMY, Terada K, Mikheyev AS (2015) Snake venoms are integrated systems, but abundant venom proteins evolve more rapidly. BMC Genomics 16:1–20
Aitchison J (1986) The statistical analysis of compositional data. Chapman and Hall, London
Almaaytah A, Albalas Q (2014) Scorpion venom peptides with no disulfide bridges. Peptides 51:35–45
Almeida F, Pimenta A, De Figueiredo S, Santoro M, Martin-Eauclaire M, Diniz C, De Lima M (2002) Enzymes with gelatinolytic activity can be found in Tityus bahiensis and Tityus serrulatus venoms. Toxicon 40:1041–1045
Andrews S, et al. (2010) FastQC: a quality control tool for high throughput sequence data
Anisimova M, Bielawski JP, Yang Z (2001) Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol 18:1585–1592
Barboni E, Kemeny D, Campos S, Vernon C (1987) The purification of acid phosphatase from honey bee venom (Apis mellifica). Toxicon 25:1097–1103
Binford GJ, Gillespie RG, Maddison WP (2016) Sexual dimorphism in venom chemistry in Tetragnatha spiders is not easily explained by adult niche differences. Toxicon 114:45–52
Brazón J, Guerrero B, D’Suze G, Sevcik C, Arocha-Piñango CL (2014) Fibrin (ogen) olytic enzymes in scorpion (Tityus discrepans) venom. Comput Biochem Physiol B 168:62–69
Brewer MS, Cole TJ (2023) Killer knots: molecular evolution of inhibitor cystine knot toxins in wandering spiders (Araneae: Ctenidae). Toxins 15:112
Carcamo-Noriega EN, Possani LD, Ortiz E (2019) Venom content and toxicity regeneration after venom gland depletion by electrostimulation in the scorpion Centruroides limpidus. Toxicon 157:87–92
Casewell NR, Wüster W, Vonk FJ, Harrison RA, Fry BG (2013) Complex cocktails: the evolutionary novelty of venoms. Trends Ecol Evol 28:219–229
Cid-Uribe JI, Santibáñez-López CE, Meneses EP, Batista CV, Jiménez-Vargas JM, Ortiz E, Possani LD (2018) The diversity of venom components of the scorpion species Paravaejovis schwenkmeyeri (Scorpiones: Vaejovidae) revealed by transcriptome and proteome analyses. Toxicon 151:47–62
Cid-Uribe JI, Veytia-Bucheli JI, Romero-Gutierrez T, Ortiz E, Possani LD (2020) Scorpion venomics: a 2019 overview. Expert Rev Proteom 17:67–83
Dashevsky D, Fry BG (2018) Ancient diversification of three-finger toxins in Micrurus coral snakes. J Mol Evol 86:58–67
Daugherty MD, Malik HS (2012) Rules of engagement: molecular insights from host-virus arms races. Annu Rev Genet 46:677–700
De Sousa L, Borges A, Vásquez-Suárez A, den Camp HJO, Chadee-Burgos RI, Romero-Bellorín M, Espinoza J, De Sousa-Insana L, Pino-García O (2010) Differences in venom toxicity and antigenicity between females and males Tityus nororientalis (Buthidae) scorpions. J Venom Res 1:61
Delgado-Prudencio G, Cid-Uribe JI, Morales JA, Possani LD, Ortiz E, Romero-Gutiérrez T (2022) The enzymatic core of scorpion venoms. Toxins 14:248
Delgado-Prudencio G, Possani LD, Becerril B, Ortiz E (2019) The dual \(\alpha \)-amidation system in scorpion venom glands. Toxins 11:425
Díaz-García A, Yglesias-Rivera A, Ruiz-Fuentes JL, Ochoa-Cardentey R, Viltres JRT, Rodríguez-Sánchez H, Peña TG (2019) Effect of frequency of Rhopalurus junceus scorpion venom collection on protein content and biological activity. Trends Med 19:1–5
Drabeck DH, Rucavado A, Hingst-Zaher E, Dean A, Jansa SA (2022) Ancestrally reconstructed von willebrand factor reveals evidence for trench warfare coevolution between opossums and pit vipers. Mol Biol Evol 39:msac140
Duckert P, Brunak S, Blom N (2004) Prediction of proprotein convertase cleavage sites. Protein Eng Des Sel 17:107–112
Dutertre S, Jin AH, Vetter I, Hamilton B, Sunagar K, Lavergne V, Dutertre V, Fry BG, Antunes A, Venter DJ et al (2014) Evolution of separate predation-and defence-evoked venoms in carnivorous cone snails. Nat Commun 5:3521
Duzzi B, Silva CCF, Kodama RT, Cajado-Carvalho D, Squaiella-Baptistão CC, Portaro FCV (2021) New insights into the hypotensins from Tityus serrulatus venom: pro-inflammatory and vasopeptidases modulation activities. Toxins 13:846
Egozcue JJ, Pawlowsky-Glahn V, Mateu-Figueras G, Barceló-Vidal C (2003) Isometric logratio transformations for compositional data analysis. Math Geol 35:279–300
Fatima L, Fatah C (2014) Pathophysiological and pharmacological effects of snake venom components: molecular targets. J Clin Toxicol 4:2161–0495
Furtado M, Travaglia-Cardoso SR, Rocha MMTd (2006) Sexual dimorphism in venom of Bothrops jararaca (Serpentes: Viperidae). Toxicon 48:401–410
Gao B, Peigneur S, Dalziel J, Tytgat J, Zhu S (2011) Molecular divergence of two orthologous scorpion toxins affecting potassium channels. Comput Biochem Physiol A 159:313–321
Gao B, Tian C, Zhu S (2007) Inducible antibacterial response of scorpion venom gland. Peptides 28:2299–2305
Garnier, Simon, Ross, Noam, Rudis, Robert, Camargo, Pedro A, Sciaini, Marco, Scherer, Cédric (2021) viridis - Colorblind-Friendly Color Maps for R. https://sjmgarnier.github.io/viridis/. R package version 0.6.2
Gibbs HL, Rossiter W (2008) Rapid evolution by positive selection and gene gain and loss: PLA2 venom genes in closely related Sistrurus rattlesnakes with divergent diets. J Mol Evol 66:151–166
Grabherr MG, Haas BJ, Yassour M, Levin JZ, Thompson DA, Amit I, Adiconis X, Fan L, Raychowdhury R, Zeng Q, Chen Z, Mauceli E, Hacohen N, Gnirke A, Rhind N, di Palma F, Birren BW, Nusbaum C, Lindblad-Toh K, Friedman N, Regev A (2011) Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29:644–652
Graham MR, Jaeger JR, Prendini L, Riddle BR (2013) Phylogeography of the Arizona hairy scorpion (Hadrurus arizonensis) supports a model of biotic assembly in the Mojave Desert and adds a new Pleistocene refugium. J Biogeogr 40:1298–1312
Guo C, Liu S, Yao Y, Zhang Q, Sun MZ (2012) Past decade study of snake venom l-amino acid oxidase. Toxicon 60:302–311
Harrison PL, Abdel-Rahman MA, Miller K, Strong PN (2014) Antimicrobial peptides from scorpion venoms. Toxicon 88:115–137
Herzig V, Khalife AA, Chong Y, Isbister GK, Currie BJ, Churchill TB, Horner S, Escoubas P, Nicholson GM, Hodgson WC (2008) Intersexual variations in northern (Missulena pruinosa) and eastern (M. bradleyi) mouse spider venom. Toxicon 51:1167–1177
Holding ML, Margres MJ, Mason AJ, Parkinson CL, Rokyta DR (2018) Evaluating the performance of de novo assembly methods for venom-gland transcriptomics. Toxins 10:249
Inceoglu B, Lango J, Jing J, Chen L, Doymaz F, Pessah IN, Hammock BD (2003) One scorpion, two venoms: prevenom of Parabuthus transvaalicus acts as an alternative type of venom with distinct mechanism of action. Proc Natl Acad Sci USA 100:922–927
Jansa SA, Voss RS (2011) Adaptive evolution of the venom-targeted vWF protein in opossums that eat pitvipers. PLoS ONE 6:e20997
Kearse M, Moir R, Wilson A, Stones-havas S, Sturrock S, Buxton S, Cooper A (2012) Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28:1647–1649
Khan I, Maldonado E, Silva L, Almeida D, Johnson WE, O’Brien SJ, Zhang G, Jarvis ED, Gilbert MTP, Antunes A (2019) The vertebrate TLR supergene family evolved dynamically by gene gain/loss and positive selection revealing a host-pathogen arms race in birds. Diversity 11:131
Kosakovsky Pond SL, Frost SD (2005) Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol Biol Evol 22:1208–1222
Krayem N, Gargouri Y (2020) Scorpion venom phospholipases A2: a minireview. Toxicon 184:48–54
Krueger F (2015) Trim Galore. A wrapper tool around Cutadapt and FastQC to consistently apply quality and adapter trimming to FastQ files, with some extra functionality for MspI-digested RRBS-type (Reduced Representation Buisulfite-Seq) libraries. https://github.com/FelixKrueger/TrimGalore
Langmead B, Salzberg SL (2012) Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359
Letunic I, Bork P (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49:W293–W296
Li B, Dewey CN (2011) RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12:1–16
Li H (2013) Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM. arXiv preprint arXiv:1303.3997
Li W, Godzik A (2006) Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformatics 22:1658–1659
Luna-Ramírez K, Quintero-Hernandez V, Juárez-González VR, Possani LD (2015) Whole transcriptome of the venom gland from Urodacus yaschenkoi scorpion. PLoS ONE 10:e0127883
Lynch VJ (2007) Inventing an arsenal: adaptive evolution and neofunctionalization of snake venom phospholipase A\(_2\) genes. BMC Evol Biol 7:2
Menezes MC, Furtado MF, Travaglia-Cardoso SR, Camargo ACM, Serrano SMT (2006) Sex-based individual variation of snake venom proteome among eighteen Bothrops jararaca siblings. Toxicon 47:304–312
Miller DW, Jones AD, Goldston JS, Rowe MP, Rowe AH (2016) Sex differences in defensive behavior and venom of the striped bark scorpion Centruroides vitattus (Scorpiones: Buthidae). Integr Comput Biol 56:1022–1031
Minh BQ, Nguyen MAT, Von Haeseler A (2013) Ultrafast approximation for phylogenetic bootstrap. Mol Biol Evol 30:1188–1195
Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, Von Haeseler A, Lanfear R (2020) IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol 37:1530–1534
Murrell B, Moola S, Mabona A, Weighill T, Sheward D, Kosakovsky Pond SL, Scheffler K (2013) FUBAR: a fast, unconstrained Bayesian approximation for inferring selection. Mol Biol Evol 30:1196–1205
Murrell B, Weaver S, Smith MD, Wertheim JO, Murrell S, Aylward A, Eren K, Pollner T, Martin DP, Smith DM et al (2015) Gene-wide identification of episodic selection. Mol Biol Evol 32:1365–1371
Murrell B, Wertheim JO, Moola S, Weighill T, Scheffler K, Kosakovsky Pond SL (2012) Detecting individual sites subject to episodic diversifying selection. PLoS Genet 8:e1002764
Nguyen LT, Schmidt HA, Von Haeseler A, Minh BQ (2015) IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32:268–274
Nisani Z, Boskovic DS, Dunbar SG, Kelln W, Hayes WK (2012) Investigating the chemical profile of regenerated scorpion (Parabuthus transvaalicus) venom in relation to metabolic cost and toxicity. Toxicon 60:315–323
Nystrom GS, Ellsworth SA, Rokyta DR (2023) The remarkably enzyme-rich venom of the Big Bend scorpion (Diplocentrus whitei). Toxicon P. 107080
Nystrom GS, Fry LG, Ellsworth SA, Rokyta DR (2022) Contrasting patterns of venom regeneration in a centipede (Scolopendra viridis) and a scorpion (Centruroides hentzi). Toxicon 210:132–140
Nystrom GS, Ward MJ, Ellsworth SA, Rokyta DR (2019) Sex-based venom variation in the eastern bark centipede (Hemiscolopendra marginata). Toxicon 169:45–58
Oksanen J, Blanchet F, Kindt R, Legendre P, Minchin P, O’Hara R, Simpson G, Solymos P, Stevens M, Wagner H (2013) Vegan: community ecology package. R package ver. 2.0–10
Olguín-Pérez L, Francke OF, Carbajal-Saucedo A (2021) Evidence of piercing and sexual differences in venom composition in a sexual stinging scorpion (Scorpiones: Euscorpiidae). J Arachnol 49:98–107
Oliveira AL, Viegas MF, da Silva SL, Soares AM, Ramos MJ, Fernandes PA (2022) The chemistry of snake venom and its medicinal potential. Nat Rev Chem 6:451–469
Oliveira-Mendes BBRd, Miranda SEM, Sales-Medina DF, Magalhaes BdF, Kalapothakis Y, Souza RPd, Cardoso VN, de Barros ALB, Guerra-Duarte C, Kalapothakis E et al (2019) Inhibition of Tityus serrulatus venom hyaluronidase affects venom biodistribution. PLOS Negl Trop Dis 13:e0007048
Petersen TN, Brunak S, von Heijne G, Nielsen H (2011) SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8:785–786
Pimenta AMC, Almeida FDM, de Lima ME, Martin-Eauclaire MF, Bougis PE (2003) Individual variability in Tityus serrulatus (Scorpiones, Buthidae) venom elicited by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. Rapid Commun Mass Spectrom 17:413–418
Polis G, Sissom W (1990) Life history. The biology of scorpions, pp 161–223
Quintero-Hernández V, Jiménez-Vargas J, Gurrola G, Valdivia H, Possani L (2013) Scorpion venom components that affect ion-channels function. Toxicon 76:328–342
Quintero-Hernández V, Ramírez-Carreto S, Romero-Gutiérrez MT, Valdez-Velázquez LL, Becerril B, Possani LD, Ortiz E (2015) Transcriptome analysis of scorpion species belonging to the Vaejovis genus. PLoS ONE 10:e0117188
R Core Team (2021) R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria. https://www.R-project.org/
Rech GE, Vargas WA, Sukno SA, Thon MR (2012) Identification of positive selection in disease response genes within members of the Poaceae. Plant Signal Behav 7:1667–1675
Rice P, Longden I, Bleasby A (2000) EMBOSS: the European molecular biology open software suite
Rokyta DR, Lemmon AR, Margres MJ, Aronow K (2012) The venom-gland transcriptome of the eastern diamondback rattlesnake (Crotalus adamanteus). BMC Genom 13:312
Rokyta DR, Ward MJ (2017) Venom-gland transcriptomics and venom proteomics of the blackback scorpion (Hadrurus spadix) reveal detectability challenges and an unexplored realm of animal toxin diversity. Toxicon 128:23–37
Romero-Gutiérrez MT, Santibáñez-López CE, Jiménez-Vargas JM, Batista CVF, Ortiz E, Possani LD (2018) Transcriptomic and proteomic analyses reveal the diversity of venom components from the Vaejovid scorpion Serradigitus gertschi. Toxins 10:359
Romero-Gutierrez T, Peguero-Sanchez E, Cevallos MA, Batista CV, Ortiz E, Possani LD (2017) A deeper examination of Thorellius atrox scorpion venom components with omic technologies. Toxins 9:399
Santibáñez-López CE, Cid-Uribe JI, Zamudio FZ, Batista CV, Ortiz E, Possani LD (2017) Venom gland transcriptomic and venom proteomic analyses of the scorpion Megacormus gertschi Díaz-Najera, 1966 (Scorpiones: Euscorpiidae: Megacorminae). Toxicon 133:95–109
Santibáñez-López CE, Graham MR, Sharma PP, Ortiz E, Possani LD (2019) Hadrurid scorpion toxins: evolutionary conservation and selective pressures. Toxins 11:637
Santibáñez-López CE, Ojanguren-Affilastro AA, Graham MR, Sharma PP (2023 In Press) Congruence between ultraconserved element-based matrices and phylotranscriptomic datasets in the scorpion tree of life. Cladistics. https://www.sciencedirect.com/science/article/pii/B0123708796002647
Santibáñez-López CE, Ojanguren-Affilastro AA, Sharma PP (2020) Another one bites the dust: taxonomic sampling of a key genus in phylogenomic datasets reveals more non-monophyletic groups in traditional scorpion classification. Invertebr Syst 34:133–143
Schwartz EF, Diego-Garcia E, de la Vega RCR, Possani LD (2007) Transcriptome analysis of the venom gland of the Mexican scorpion Hadrurus gertschi (Arachnida: Scorpiones). BMC Genom 8:119
Seppey M, Manni M, Zdobnov EM (2019) Busco: assessing genome assembly and annotation completeness, pp. 227–245. In: Gene prediction. Springer, New York
Shaikh NY, Sunagar K (2023) The deep-rooted origin of disulfide-rich spider venom toxins. Elife 12:e83761
Sievers F, Higgins DG (2018) Clustal Omega for making accurate alignments of many protein sequences. Protein Sci 27:135–145
Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, Lopez R, McWilliam H, Remmert M, Söding J et al (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539
Smith MD, Wertheim JO, Weaver S, Murrell B, Scheffler K, Kosakovsky Pond SL (2015) Less is more: an adaptive branch-site random effects model for efficient detection of episodic diversifying selection. Mol Biol Evol 32:1342–1353
Soleglad M, Fet V (2003) High-level systematics and phylogeny of the extant scorpions (Scorpiones: Orthosterni). Euscorpius 11, ii+ 1–175
Soleglad ME, Fet V (2010) Further observations on scorpion genera Hadrurus and Hoffmannihadrurus (Scorpiones, Caraboctonidae). ZooKeys P. 1
Soleglad ME, Fet V, Lowe G (2011) Contributions to scorpion systematics. IV. Observations on the Hadrurus “spadix’’ subgroup with a description of a new species (Scorpiones: Caraboctonidae). Euscorpius 2011:1–36
Spielman SJ, Weaver S, Shank SD, Magalis BR, Li M, Kosakovsky Pond SL (2019) Evolution of viral genomes: Interplay between selection, recombination, and other forces. In: Evolutionary genomics: statistical and computational methods, pp. 427–468
Stahnke HL (1945) Scorpions of the genus Hadrurus Thorell. American Museum Novitates 1298
Sunagar K, Johnson WE, O’Brien SJ, Vasconcelos V, Antunes A (2012) Evolution of crisps associated with toxicoferan-reptilian venom and mammalian reproduction. Mol Biol Evol 29:1807–1822
Sunagar K, Moran Y (2015) The rise and fall of an evolutionary innovation: contrasting strategies of venom evolution in ancient and young animals. PLoS Genet 11:e1005596
Sunagar K, Undheim EA, Scheib H, Gren EC, Cochran C, Person CE, Koludarov I, Kelln W, Hayes WK, King GF, Antunes A, Fry BG (2014) Intraspecific venom variation in the medically significant Southern Pacific Rattlesnake (Crotalus oreganus helleri): biodiscovery, clinical and evolutionary implications. J Proteom 99:68–83
Sunagar K, Undheim EAB, Chan AHC, Koludarov I, Muñoz-Gómez SA, Antunes A, Fry BG (2013) Evolution stings: the origin and diversification of scorpion toxin peptide scaffolds. Toxins 5:2456–2487
Tallarovic SK, Melville JM, Brownell PH (2000) Courtship and mating in the giant hairy desert scorpion, Hadrurus arizonensis (Scorpionida, Iuridae). J Insect Behav 13:827–838
Tange O et al (2011) Gnu parallel-the command-line power tool. USENIX Mag 36:42–47
Torres-Larios A, Gurrola GB, Zamudio FZ, Possani LD (2000) Hadrurin, a new antimicrobial peptide from the venom of the scorpion Hadrurus aztecus. Eur J Biochem 267:5023–5031
Trentini MM, das Neves RC, Santos BdPO, DaSilva RA, Souza AC, Mortari MR, Schwartz EF, Kipnis A, Junqueira-Kipnis AP, (2017) Non-disulfide-bridge peptide 5.5 from the scorpion Hadrurus gertschi inhibits the growth of Mycobacterium abscessus subsp. massiliense. Front Microbiol 8:273
Vizcaíno JA, Csordas A, Del-Toro N, Dianes JA, Griss J, Lavidas I, Mayer G, Perez-Riverol Y, Reisinger F, Ternent T et al (2016) 2016 update of the PRIDE database and its related tools. Nucleic Acids Res 44:D447–D456
Waddington J, Rudkin DM, Dunlop JA (2015) A new mid-Silurian aquatic scorpion-one step closer to land? Biol Lett 11:20140815
Ward MJ, Ellsworth SA, Hogan MP, Nystrom GS, Martinez P, Budhdeo A, Zelaya R, Perez A, Powell B, He H et al (2018) Female-biased population divergence in the venom of the Hentz striped scorpion (Centruroides hentzi). Toxicon 152:137–149
Ward MJ, Ellsworth SA, Rokyta DR (2018) Venom-gland transcriptomics and venom proteomics of the Hentz striped scorpion (Centruroides hentzi; Buthidae) reveal high toxin diversity in a harmless member of a lethal family. Toxicon 142:14–29
Weinberger H, Moran Y, Gordon D, Turkov M, Kahn R, Gurevitz M (2010) Positions under positive selection-key for selectivity and potency of scorpion \(\alpha \)-toxins. Mol Biol Evol 27:1025–1034
Wickham H (2016) ggplot2: Elegant Graphics for Data Analysis. Springer, New York. https://ggplot2.tidyverse.org
Zancolli G, Casewell NR (2020) Venom systems as models for studying the origin and regulation of evolutionary novelties. Mol Biol Evol 37:2777–2790
Zeng XC, Corzo G, Hahin R (2005) Scorpion venom peptides without disulfide bridges. IUBMB Life 57:13–21
Zhang J, Kobert K, Flouri T, Stamatakis A (2014) PEAR: a fast and accurate Illumina Paired-End reAd mergeR. Bioinformatics 30:614–620
Zhang L, Shi W, Zeng XC, Ge F, Yang M, Nie Y, Bao A, Wu S, Guoji E (2015) Unique diversity of the venom peptides from the scorpion Androctonus bicolor revealed by transcriptomic and proteomic analysis. J Proteom 128:231–250
Zhou L, Feng T, Xu S, Gao F, Lam TT, Wang Q, Wu T, Huang H, Zhan L, Li L et al (2022) ggmsa: a visual exploration tool for multiple sequence alignment and associated data. Brief Bioinform
Zhu S, Bosmans F, Tytgat J (2004) Adaptive evolution of scorpion sodium channel toxins. J Mol Evol 58:145–153
Zhu S, Peigneur S, Gao B, Luo L, Jin D, Zhao Y, Tytgat J (2011) Molecular diversity and functional evolution of scorpion potassium channel toxins. Mol Cell Proteom 10:S1–S11
Župunski V, Kordiš D, Gubenšek F (2003) Adaptive evolution in the snake venom kunitz/BPTI protein family. FEBS Lett. 547:131–136
Acknowledgements
We thank Carl Whittington from the Florida State University (FSU) Department of Biological Science for assistance with proteomics. Finally, we thank Rakesh Singh and Cynthia Vied from the FSU College of Medicine’s Translational Science Laboratory for their assistance with proteomics and transcriptomics, respectively.
Funding
We recognize the National Science Foundation for funding this work (NSF DEB 1145978 and NSF DEB 1638902).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflicts of Interest
The authors declare no conflict of interest.
Additional information
Communicated by Angela Roles.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.
About this article
Cite this article
Nystrom, G.S., Ellsworth, S.A., Ward, M.J. et al. Varying Modes of Selection Among Toxin Families in the Venoms of the Giant Desert Hairy Scorpions (Hadrurus). J Mol Evol 91, 935–962 (2023). https://doi.org/10.1007/s00239-023-10148-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00239-023-10148-7