BACKGROUND: Ticks, hematophagous Acari, pose a significant threat by transmitting various pathogens to their vertebrate hosts during feeding. Despite advances in tick genomics, high-quality genomes were lacking until recently, particularly in the genus Ixodes, which includes the main vectors of Lyme disease. RESULTS: Here, we present the genome sequences of four tick species, derived from a single female individual, with a particular focus on the European species Ixodes ricinus, achieving a chromosome-level assembly. Additionally, draft assemblies were generated for the three other Ixodes species, I. persulcatus, I. pacificus, and I. hexagonus. The quality of the four genomes and extensive annotation of several important gene families have allowed us to study the evolution of gene repertoires at the level of the genus Ixodes and of the tick group. We have determined gene families that have undergone major amplifications during the evolution of ticks, while an expression atlas obtained for I. ricinus reveals striking patterns of specialization both between and within gene families. Notably, several gene family amplifications are associated with a proliferation of single-exon genes-most strikingly for fatty acid elongases and sulfotransferases. CONCLUSIONS: The integration of our data with existing genomes establishes a solid framework for the study of gene evolution, improving our understanding of tick biology. In addition, our work lays the foundations for applied research and innovative control targeting these organisms.

ANSES INRAE Ecole Nationale Vétérinaire d'Alfort UMR BIPAR Laboratoire de Santé Animale 22 Rue Pierre Et Marie Curie Maisons Alfort France

Centre National de Recherche en Génomique Humaine Institut de Biologie François Jacob CEA Université Paris Saclay Evry France

Department of Medical Biology Faculty of Science University of South Bohemia in České Budějovice Branišovská 31 37005 České Budějovice Czech Republic

Department of Veterinary Microbiology Western College of Veterinary Medicine University of Saskatchewan Saskatoon Canada

Dpto de Genética Facultad de Ciencias Universidad de Granada Campus de Fuentenueva S N 18071 Granada Spain

Génomique Métabolique Genoscope Institut François Jacob CEA CNRS Univ Evry Université Paris Saclay 91057 Evry France

Genoscope Institut François Jacob CEA CNRS Univ Evry Université Paris Saclay 91057 Evry France

IGEPP INRAE Institut Agro BIPAA University of Rennes Rennes France

INRAE Université de Tours UMR1282 Infectiologie Et Santé Publique 37380 Nouzilly France

Institut d'Ecologie Et Des Sciences de L'Environnement de Paris Sorbonne Université INRAE CNRS IRD UPEC Paris France

Institute of Molecular Biology and Biotechnology Foundation for Research and Technology Hellas N Plastira 100 70013 Heraklion Crete Greece

Institute of Parasitology Biology Centre Czech Academy of Sciences Branišovská 1160 31 37005 České Budějovice Czech Republic

Lab de Bioinformática Centro de Investigación Biomédica PTS Instituto de Biotecnología Avda del Conocimiento S N 18100 Granada Spain

Oniris INRAE BIOEPAR 44300 Nantes France

Research Center for Biosafety Laboratory Animal and Pathogen Bank National Institute of Infectious Diseases Tokyo Japan

Université Côte d'Azur INRAE CNRS ISA 06903 Sophia Antipolis France

University of Rennes INRIA CNRS IRISA Rennes France

Zobrazit více v PubMed

Jongejan F, Uilenberg G. The global importance of ticks. Parasitology. 2004;129:S3-14. PubMed

Mans BJ, de Castro MH, Pienaar R, de Klerk D, Gaven P, Genu S, et al. Ancestral reconstruction of tick lineages. Ticks Tick-Borne Dis. 2016;7:509–35. PubMed

Dunlop JA. Geological history and phylogeny of Chelicerata. Arthropod Struct Dev. 2010;39:124–42. PubMed

Sharma PP, Kaluziak ST, Pérez-Porro AR, González VL, Hormiga G, Wheeler WC, et al. Phylogenomic interrogation of Arachnida reveals systemic conflicts in phylogenetic signal. Mol Biol Evol. 2014;31:2963–84. PubMed

Lozano-Fernandez J, Tanner AR, Giacomelli M, Carton R, Vinther J, Edgecombe GD, et al. Increasing species sampling in chelicerate genomic-scale datasets provides support for monophyly of Acari and Arachnida. Nat Commun. 2019;10:2295. PubMed PMC

Ballesteros JA, Santibáñez López CE, Kováč Ľ, Gavish-Regev E, Sharma PP. Ordered phylogenomic subsampling enables diagnosis of systematic errors in the placement of the enigmatic arachnid order Palpigradi. Proc R Soc B Biol Sci. 2019;286:20192426. PubMed PMC

Zhang Y-X, Chen X, Wang J-P, Zhang Z-Q, Wei H, Yu H-Y, et al. Genomic insights into mite phylogeny, fitness, development, and reproduction. BMC Genomics. 2019;20:954. PubMed PMC

Sharma PP, Ballesteros JA, Santibáñez-López CE. What is an “arachnid”? Consensus, consilience, and confirmation bias in the phylogenetics of Chelicerata. Diversity. 2021;13:568.

Guglielmone AA, Robbins RG, Apanaskevich DA, Petney TN, Estrada-Peña A, Horak IG, et al. The Argasidae, Ixodidae and Nuttalliellidae (Acari: Ixodida) of the world: a list of valid species names. Zootaxa. 2010;2528:1–28.

Mans BJ, de Klerk D, Pienaar R, Latif AA. Nuttalliella namaqua: a living fossil and closest relative to the ancestral tick lineage: implications for the evolution of blood-feeding in ticks. PLoS ONE. 2011;6: e23675. PubMed PMC

Mans BJ, de Klerk D, Pienaar R, de Castro MH, Latif AA. The mitochondrial genomes of Nuttalliella namaqua (Ixodea: Nuttalliellidae) and Argas africolumbae (Ixodae: Argasidae): estimation of divergence dates for the major tick lineages and reconstruction of ancestral blood-feeding characters. PLoS ONE. 2012;7. PubMed PMC

Mans BJ. Chemical equilibrium at the tick–host feeding interface: a critical examination of biological relevance in hematophagous behavior. Front Physiol. 2019;10. PubMed PMC

Medina JM, Jmel MA, Cuveele B, Gómez-Martín C, Aparicio-Puerta E, Mekki I, et al. Transcriptomic analysis of the tick midgut and salivary gland responses upon repeated blood-feeding on a vertebrate host. Front Cell Infect Microbiol. 2022;12. PubMed PMC

Mans BJ, Featherston J, de Castro MH, Pienaar R. Gene duplication and protein evolution in tick-host interactions. Front Cell Infect Microbiol. 2017;7. PubMed PMC

Geraci NS, Spencer Johnston J, Paul Robinson J, Wikel SK, Hill CA. Variation in genome size of argasid and ixodid ticks. Insect Biochem Mol Biol. 2007;37:399–408. PubMed

Gulia-Nuss M, Nuss AB, Meyer JM, Sonenshine DE, Roe RM, Waterhouse RM, et al. Genomic insights into the Ixodes scapularis tick vector of Lyme disease. Nat Commun. 2016;7:10507. PubMed PMC

Jia N, Wang J, Shi W, Du L, Sun Y, Zhan W, et al. Large-scale comparative analyses of tick genomes elucidate their genetic diversity and vector capacities. Cell. 2020;182:1328-1340.e13. PubMed

De S, Kingan SB, Kitsou C, Portik DM, Foor SD, Frederick JC, et al. A high-quality Ixodes scapularis genome advances tick science. Nat Genet. 2023;55:301–11. PubMed

Nuss AB, Lomas JS, Reyes JB, Garcia-Cruz O, Lei W, Sharma A, et al. The highly improved genome of Ixodes scapularis with X and Y pseudochromosomes. Life Sci Alliance. 2023;6. PubMed PMC

Charrier NP, Hermouet A, Hervet C, Agoulon A, Barker SC, Heylen D, et al. A transcriptome-based phylogenetic study of hard ticks (Ixodidae). Sci Rep. 2019;9. PubMed PMC

Keirans JE, Needham GR, Oliver Jr JR. The Ixodes ricinus complex worldwide: diagnosis of the species in the complex, hosts and distribution. In: Acarology IX: Symposia. Colombus, Ohio; 1999. p. 341–7.

Xu G, Fang QQ, Keirans JE, Durden LA. Molecular phylogenetic analyses indicate that the ixodes ricinus complex is a paraphyletic group. J Parasitol. 2003;89:452–7. PubMed

Sands AF, Apanaskevich DA, Matthee S, Horak IG, Harrison A, Karim S, et al. Effects of tectonics and large scale climatic changes on the evolutionary history of Hyalomma ticks. Mol Phylogenet Evol. 2017;114:153–65. PubMed

Oliver JH. Cytogenetics of mites and ticks. Annu Rev Entomol. 1977;22:407–29. PubMed

Ribeiro JMC, Bayona-Vásquez NJ, Budachetri K, Kumar D, Frederick JC, Tahir F, et al. A draft of the genome of the Gulf Coast tick. Amblyomma maculatum Ticks Tick-Borne Dis. 2023;14: 102090. PubMed PMC

Van Dam MH, Trautwein M, Spicer GS, Esposito L. Advancing mite phylogenomics: designing ultraconserved elements for Acari phylogeny. Mol Ecol Resour. 2019;19:465–75. PubMed

Medina JM, Abbas MN, Bensaoud C, Hackenberg M, Kotsyfakis M. Bioinformatic analysis of Ixodes ricinus long non-coding RNAs predicts their binding ability of host miRNAs. Int J Mol Sci. 2022;23:9761. PubMed PMC

Donohue KV, Khalil SMS, Ross E, Grozinger CM, Sonenshine DE, Michael RR. Neuropeptide signaling sequences identified by pyrosequencing of the American dog tick synganglion transcriptome during blood feeding and reproduction. Insect Biochem Mol Biol. 2010;40:79–90. PubMed

Waldman J, Xavier MA, Vieira LR, Logullo R, Braz GRC, Tirloni L, et al. Neuropeptides in Rhipicephalus microplus and other hard ticks. Ticks Tick-Borne Dis. 2022;13: 101910. PubMed PMC

Meyer H, Buhr A, Callaerts P, Schiemann R, Wolfner MF, Marygold SJ. Identification and bioinformatic analysis of neprilysin and neprilysin-like metalloendopeptidases in Drosophila melanogaster. MicroPublication Biol. 2021;2021. PubMed PMC

Bland ND, Pinney JW, Thomas JE, Turner AJ, Isaac RE. Bioinformatic analysis of the neprilysin (M13) family of peptidases reveals complex evolutionary and functional relationships. BMC Evol Biol. 2008;8:16. PubMed PMC

Jmel MA, Voet H, Araújo RN, Tirloni L, Sá-Nunes A, Kotsyfakis M. Tick salivary Kunitz-type inhibitors: targeting host hemostasis and immunity to mediate successful blood feeding. Int J Mol Sci. 2023;24:1556. PubMed PMC

Francischetti IMB, Valenzuela JG, Andersen JF, Mather TN, Ribeiro JMC. Ixolaris, a novel recombinant tissue factor pathway inhibitor (TFPI) from the salivary gland of the tick, Ixodes scapularis: identification of factor X and factor Xa as scaffolds for the inhibition of factor VIIa/tissue factor complex. Blood. 2002;99:3602–12. PubMed

Nazareth RA, Tomaz LS, Ortiz-Costa S, Atella GC, Ribeiro JMC, Francischetti IMB, et al. Antithrombotic properties of Ixolaris, a potent inhibitor of the extrinsic pathway of the coagulation cascade. Thromb Haemost. 2006;96:7–13. PubMed PMC

De Paula VS, Sgourakis NG, Francischetti IMB, Almeida FCL, Monteiro RQ, Valente AP. NMR structure determination of Ixolaris and factor X(a) interaction reveals a noncanonical mechanism of Kunitz inhibition. Blood. 2019;134:699–708. PubMed PMC

Dermauw W, Van Leeuwen T, Feyereisen R. Diversity and evolution of the P450 family in arthropods. Insect Biochem Mol Biol. 2020;127: 103490. PubMed

De Rouck S, İnak E, Dermauw W, Van Leeuwen T. A review of the molecular mechanisms of acaricide resistance in mites and ticks. Insect Biochem Mol Biol. 2023;159: 103981. PubMed

Claudianos C, Ranson H, Johnson RM, Biswas S, Schuler MA, Berenbaum MR, et al. A deficit of detoxification enzymes: pesticide sensitivity and environmental response in the honeybee. Insect Mol Biol. 2006;15:615–36. PubMed PMC

Grbić M, Van Leeuwen T, Clark RM, Rombauts S, Rouzé P, Grbić V, et al. The genome of Tetranychus urticae reveals herbivorous pest adaptations. Nature. 2011;479:487–92. PubMed PMC

Bajda S, Dermauw W, Greenhalgh R, Nauen R, Tirry L, Clark RM, et al. Transcriptome profiling of a spirodiclofen susceptible and resistant strain of the European red mite Panonychus ulmi using strand-specific RNA-seq. BMC Genomics. 2015;16:974. PubMed PMC

Dermauw W, Wybouw N, Rombauts S, Menten B, Vontas J, Grbić M, et al. A link between host plant adaptation and pesticide resistance in the polyphagous spider mite Tetranychus urticae. Proc Natl Acad Sci. 2013;110:E113–22. PubMed PMC

Neese PA, E. Sonenshine D, Kallapur VL, Apperson CS, Roe RM. Absence of insect juvenile hormones in the American dog tick, Dermacentor variabilis (Say) (Acari:Ixodidae), and in Ornithodoros parkeri Cooley (Acari:Argasidae). J Insect Physiol. 2000;46:477–90. PubMed

Zhu J, Khalil SM, Mitchell RD, Bissinger BW, Egekwu N, Sonenshine DE, et al. Mevalonate-farnesal biosynthesis in ticks: comparative synganglion transcriptomics and a new perspective. PLoS ONE. 2016;11: e0141084. PubMed PMC

Yang Z-M, Wu Y, Li F-F, Zhou Z-J, Yu N, Liu Z-W. Genomic identification and functional analysis of JHAMTs in the pond wolf spider. Pardosa pseudoannulata Int J Mol Sci. 2021;22:11721. PubMed PMC

Smykal V, Dolezel D. Evolution of proteins involved in the final steps of juvenile hormone synthesis. J Insect Physiol. 2023;145: 104487. PubMed PMC

Kotál J, Stergiou N, Buša M, Chlastáková A, Beránková Z, Řezáčová P, et al. The structure and function of Iristatin, a novel immunosuppressive tick salivary cystatin. Cell Mol Life Sci. 2019;76:2003–13. PubMed PMC

Huntington JA. Serpin structure, function and dysfunction. J Thromb Haemost. 2011;9:26–34. PubMed

Spence MA, Mortimer MD, Buckle AM, Minh BQ, Jackson CJ. A comprehensive phylogenetic analysis of the serpin superfamily. Mol Biol Evol. 2021;38:2915–29. PubMed PMC

Abbas MN, Chlastáková A, Jmel MA, Iliaki-Giannakoudaki E, Chmelař J, Kotsyfakis M. Serpins in tick physiology and tick-host interaction. Front Cell Infect Microbiol. 2022;12: 892770. PubMed PMC

Leboulle G, Crippa M, Decrem Y, Mejri N, Brossard M, Bollen A, et al. Characterization of a novel salivary immunosuppressive protein from Ixodes ricinus ticks *. J Biol Chem. 2002;277:10083–9. PubMed

Chmelar J, Oliveira CJ, Rezacova P, Francischetti IMB, Kovarova Z, Pejler G, et al. A tick salivary protein targets cathepsin G and chymase and inhibits host inflammation and platelet aggregation. Blood. 2011;117:736–44. PubMed PMC

Chlastáková A, Kotál J, Beránková Z, Kaščáková B, Martins LA, Langhansová H, et al. Iripin-3, a new salivary protein isolated from Ixodes ricinus ticks, displays immunomodulatory and anti-hemostatic properties in vitro. Front Immunol. 2021;12: 626200. PubMed PMC

Chlastáková A, Kaščáková B, Kotál J, Langhansová H, Kotsyfakis M, Kutá Smatanová I, et al. Iripin-1, a new anti-inflammatory tick serpin, inhibits leukocyte recruitment in vivo while altering the levels of chemokines and adhesion molecules. Front Immunol. 2023;14:1116324. PubMed PMC

Kascakova B, Kotal J, Martins LA, Berankova Z, Langhansova H, Calvo E, et al. Structural and biochemical characterization of the novel serpin Iripin-5 from Ixodes ricinus. Acta Crystallogr Sect Struct Biol. 2021;77(Pt 9):1183–96. PubMed PMC

Kascakova B, Kotal J, Havlickova P, Vopatkova V, Prudnikova T, Grinkevich P, et al. Conformational transition of the Ixodes ricinus salivary serpin Iripin-4. Acta Crystallogr Sect Struct Biol. 2023;79(Pt 5):409–19. PubMed PMC

Kotál J, Polderdijk SGI, Langhansová H, Ederová M, Martins LA, Beránková Z, et al. Ixodes ricinus salivary serpin Iripin-8 inhibits the intrinsic pathway of coagulation and complement. Int J Mol Sci. 2021;22:9480. PubMed PMC

Perner J, Sobotka R, Sima R, Konvickova J, Sojka D, Oliveira PL de, et al. Acquisition of exogenous haem is essential for tick reproduction. eLife. 2016;5:e12318. PubMed PMC

Perner J, Provazník J, Schrenková J, Urbanová V, Ribeiro JMC, Kopáček P. RNA-seq analyses of the midgut from blood- and serum-fed Ixodes ricinus ticks. Sci Rep. 2016;6:36695. PubMed PMC

Perner J, Gasser RB, Oliveira PL, Kopáček P. Haem biology in metazoan parasites – ‘the bright side of haem.’ Trends Parasitol. 2019;35:213–25. PubMed

Hajdusek O, Sojka D, Kopacek P, Buresova V, Franta Z, Sauman I, et al. Knockdown of proteins involved in iron metabolism limits tick reproduction and development. Proc Natl Acad Sci. 2009;106:1033–8. PubMed PMC

Kopáček P, Ždychová J, Yoshiga T, Weise C, Rudenko N, Law JH. Molecular cloning, expression and isolation of ferritins from two tick species—Ornithodoros moubata and Ixodes ricinus. Insect Biochem Mol Biol. 2003;33:103–13. PubMed

Oh HJ, Jung Y. High order assembly of multiple protein cages with homogeneous sizes and shapes via limited cage surface engineering. Chem Sci. 2023;14:1105–13. PubMed PMC

Perner J, Hajdusek O, Kopacek P. Independent somatic distribution of heme and iron in ticks. Curr Opin Insect Sci. 2022;51: 100916. PubMed

Xu Z, Wang Y, Sun M, Zhou Y, Cao J, Zhang H, et al. Proteomic analysis of extracellular vesicles from tick hemolymph and uptake of extracellular vesicles by salivary glands and ovary cells. Parasit Vectors. 2023;16:125. PubMed PMC

Robertson HM, Warr CG, Carlson JR. Molecular evolution of the insect chemoreceptor gene superfamily in Drosophila melanogaster. Proc Natl Acad Sci. 2003;100 suppl_2:14537–42. PubMed PMC

Rytz R, Croset V, Benton R. Ionotropic Receptors (IRs): Chemosensory ionotropic glutamate receptors in Drosophila and beyond. Insect Biochem Mol Biol. 2013;43:888–97. PubMed

Joseph RM, Carlson JR. Drosophila chemoreceptors: a molecular interface between the chemical world and the brain. Trends Genet. 2015;31:683–95. PubMed PMC

Missbach C, Dweck HK, Vogel H, Vilcinskas A, Stensmyr MC, Hansson BS, et al. Evolution of insect olfactory receptors eLife. 2014;3: e02115. PubMed PMC

Eyun S, Soh HY, Posavi M, Munro JB, Hughes DST, Murali SC, et al. Evolutionary history of chemosensory-related gene families across the Arthropoda. Mol Biol Evol. 2017;34:1838–62. PubMed PMC

Robertson HM, Wanner KW. The chemoreceptor superfamily in the honey bee, Apis mellifera: expansion of the odorant, but not gustatory, receptor family. Genome Res. 2006;16:1395–403. PubMed PMC

McBride CS. Rapid evolution of smell and taste receptor genes during host specialization in Drosophila sechellia. Proc Natl Acad Sci. 2007;104:4996–5001. PubMed PMC

McBride CS, Arguello JR. Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics. 2007;177:1395–416. PubMed PMC

Josek T, Walden KKO, Allan BF, Alleyne M, Robertson HM. A foreleg transcriptome for Ixodes scapularis ticks: candidates for chemoreceptors and binding proteins that might be expressed in the sensory Haller’s organ. Ticks Tick-Borne Dis. 2018;9:1317–27. PubMed

Kent LB, Robertson HM. Evolution of the sugar receptors in insects. BMC Evol Biol. 2009;9:41. PubMed PMC

Shim J, Lee Y, Jeong YT, Kim Y, Lee MG, Montell C, et al. The full repertoire of Drosophila gustatory receptors for detecting an aversive compound. Nat Commun. 2015;6:8867. PubMed PMC

Kumar A, Tauxe GM, Perry S, Scott CA, Dahanukar A, Ray A. Contributions of the conserved insect carbon dioxide receptor subunits to odor detection. Cell Rep. 2020;31: 107510. PubMed PMC

Meslin C, Mainet P, Montagné N, Robin S, Legeai F, Bretaudeau A, et al. Spodoptera littoralis genome mining brings insights on the dynamic of expansion of gustatory receptors in polyphagous noctuidae. G3 GenesGenomesGenetics. 2022;12:jkac131. PubMed PMC

van Schooten B, Jiggins CD, Briscoe AD, Papa R. Genome-wide analysis of ionotropic receptors provides insight into their evolution in Heliconius butterflies. BMC Genomics. 2016;17:254. PubMed PMC

Min S, Ai M, Shin SA, Suh GSB. Dedicated olfactory neurons mediating attraction behavior to ammonia and amines in Drosophila. Proc Natl Acad Sci. 2013;110:E1321–9. PubMed PMC

Hussain A, Zhang M, Üçpunar HK, Svensson T, Quillery E, Gompel N, et al. Ionotropic chemosensory receptors mediate the taste and smell of polyamines. PLOS Biol. 2016;14: e1002454. PubMed PMC

Knecht ZA, Silbering AF, Ni L, Klein M, Budelli G, Bell R, et al. Distinct combinations of variant ionotropic glutamate receptors mediate thermosensation and hygrosensation in Drosophila. eLife. 2016;5:e17879. PubMed PMC

Knecht ZA, Silbering AF, Cruz J, Yang L, Croset V, Benton R, et al. Ionotropic receptor-dependent moist and dry cells control hygrosensation in Drosophila. eLife. 2017;6:e26654. PubMed PMC

Kopácek P, Hajdusek O, Buresová V, Daffre S. Tick innate immunity. Adv Exp Med Biol. 2010;708:137–62. PubMed

Wu J, Zhou X, Chen Q, Chen Z, Zhang J, Yang L, et al. Defensins as a promising class of tick antimicrobial peptides: a scoping review. Infect Dis Poverty. 2022;11:71. PubMed PMC

Wang Y, Zhu S. The defensin gene family expansion in the tick Ixodes scapularis. Dev Comp Immunol. 2011;35:1128–34. PubMed

Després L, David J-P, Gallet C. The evolutionary ecology of insect resistance to plant chemicals. Trends Ecol Evol. 2007;22:298–307. PubMed

Oakeshott J, Claudianos C, Campbell PM, Newcomb R, Russell RJ. Biochemical genetics and genomics of insect esterases. In: Comprehensive Molecular Insect Science-Pharmacology. Gilbert, L.I., Iatrou K., Gill S.S. Amsterdam, The Netherlands: Elsevier; 2005. p. 309–81.

Rewitz KF, Rybczynski R, Warren JT, Gilbert LI. The Halloween genes code for cytochrome P450 enzymes mediating synthesis of the insect moulting hormone. Biochem Soc Trans. 2006;34:1256–60. PubMed

Beugnet F, Franc M. Insecticide and acaricide molecules and/or combinations to prevent pet infestation by ectoparasites. Trends Parasitol. 2012;28:267–79. PubMed

Nauen R, Bass C, Feyereisen R, Vontas J. The role of cytochrome P450s in insect toxicology and resistance. Annu Rev Entomol. 2022;67:105–24. PubMed

Ahn S-J, Dermauw W, Wybouw N, Heckel DG, Van Leeuwen T. Bacterial origin of a diverse family of UDP-glycosyltransferase genes in the Tetranychus urticae genome. Insect Biochem Mol Biol. 2014;50:43–57. PubMed

Perner J, Kotál J, Hatalová T, Urbanová V, Bartošová-Sojková P, Brophy PM, et al. Inducible glutathione S-transferase (GST1) from the tick Ixodes ricinus is a haem-binding protein. Insect Biochem Mol Biol. 2018;95:44–54. PubMed

Walsh AM, Kortschak RD, Gardner MG, Bertozzi T, Adelson DL. Widespread horizontal transfer of retrotransposons. Proc Natl Acad Sci. 2013;110:1012–6. PubMed PMC

Puinongpo W, Singchat W, Petpradub S, Kraichak E, Nunome M, Laopichienpong N, et al. Existence of Bov-B LINE retrotransposons in snake lineages reveals recent multiple horizontal gene transfers with copy number variation. Genes. 2020;11:1241. PubMed PMC

Mans BJ, de Klerk D, Pienaar R, de Castro MH, Latif AA. Next-generation sequencing as means to retrieve tick systematic markers, with the focus on Nuttalliella namaqua (Ixodoidea: Nuttalliellidae). Ticks Tick-Borne Dis. 2015;6:450–62. PubMed

Rosani U, Sollitto M, Fogal N, Salata C. Comparative analysis of presence-absence gene variations in five hard tick species: impact and functional considerations. Int J Parasitol. 2023. 10.1016/j.ijpara.2023.08.004. PubMed

Gao B, Wang Y, Diaby M, Zong W, Shen D, Wang S, et al. Evolution of pogo, a separate superfamily of IS630-Tc1-mariner transposons, revealing recurrent domestication events in vertebrates. Mob DNA. 2020;11:25. PubMed PMC

Wolfe KH, Shields DC. Molecular evidence for an ancient duplication of the entire yeast genome. Nature. 1997;387:708–13. PubMed

Kuzmin E, Taylor JS, Boone C. Retention of duplicated genes in evolution. Trends Genet. 2022;38:59–72. PubMed PMC

Kenny NJ, Chan KW, Nong W, Qu Z, Maeso I, Yip HY, et al. Ancestral whole-genome duplication in the marine chelicerate horseshoe crabs. Heredity. 2016;116:190–9. PubMed PMC

Aase-Remedios ME, Janssen R, Leite DJ, Sumner-Rooney L, McGregor AP. Evolution of the spider homeobox gene repertoire by tandem and whole genome duplication. Mol Biol Evol. 2023;40:msad239. PubMed PMC

Schwager EE, Sharma PP, Clarke T, Leite DJ, Wierschin T, Pechmann M, et al. The house spider genome reveals an ancient whole-genome duplication during arachnid evolution. BMC Biol. 2017;15:62. PubMed PMC

Van Zee JP, Schlueter JA, Schlueter S, Dixon P, Sierra CAB, Hill CA. Paralog analyses reveal gene duplication events and genes under positive selection in Ixodes scapularis and other ixodid ticks. BMC Genomics. 2016;17:241. PubMed PMC

Long M, Betrán E, Thornton K, Wang W. The origin of new genes: glimpses from the young and old. Nat Rev Genet. 2003;4:865–75. PubMed

Ohno S. Evolution by gene duplication. Berlin, Heidelberg: Springer; 1970.

Fablet M, Bueno M, Potrzebowski L, Kaessmann H. Evolutionary origin and functions of retrogene introns. Mol Biol Evol. 2009;26:2147–56. PubMed

Vinckenbosch N, Dupanloup I, Kaessmann H. Evolutionary fate of retroposed gene copies in the human genome. Proc Natl Acad Sci. 2006;103:3220–5. PubMed PMC

Micheli G, Camilloni G. Can introns stabilize gene duplication? Biology. 2022;11:941. PubMed PMC

Lynch M. Gene duplication and evolution. Science. 2002;297:945–7. PubMed

Lynch M, Conery JS. The evolutionary fate and consequences of duplicate genes. Science. 2000;290:1151–5. PubMed

Arcà B, Lombardo F, Struchiner CJ, Ribeiro JMC. Anopheline salivary protein genes and gene families: an evolutionary overview after the whole genome sequence of sixteen Anopheles species. BMC Genomics. 2017;18:153. PubMed PMC

Ruzzante L, Reijnders MJMF, Waterhouse RM. Of genes and genomes: mosquito evolution and diversity. Trends Parasitol. 2019;35:32–51. PubMed

Chmelař J, Kotál J, Karim S, Kopacek P, Francischetti IMB, Pedra JHF, et al. Sialomes and mialomes: a systems-biology view of tick tissues and tick–host interactions. Trends Parasitol. 2016;32:242–54. PubMed PMC

Francischetti IMB, Mans BJ, Meng Z, Gudderra N, Veenstra TD, Pham VM, et al. An insight into the sialome of the soft tick, Ornithodorus parkeri. Insect Biochem Mol Biol. 2008;38:1–21. PubMed PMC

Parola P, Raoult D. Ticks and tickborne bacterial diseases in humans: an emerging infectious threat. Clin Infect Dis. 2001;32:897–928. PubMed

Shakya M, Sharma AK, Kumar S, Upadhaya D, Nagar G, Singh K, et al. Acaricides resistance in Rhipicephalus microplus and expression profile of ABC-transporter genes in the sampled populations. Exp Parasitol. 2023;252: 108584. PubMed

Wu M, Zhang Y, Tian T, Xu D, Wu Q, Xie W, et al. Assessment of the role of an ABCC transporter TuMRP1 in the toxicity of abamectin to Tetranychus urticae. Pestic Biochem Physiol. 2023;195: 105543. PubMed

Lara FA, Pohl PC, Gandara AC, Ferreira J da S, Nascimento-Silva MC, Bechara GH, et al. ATP binding cassette transporter mediates both heme and pesticide detoxification in tick midgut cells. PLOS ONE. 2015;10:e0134779. PubMed PMC

Ali A, Khan S, Ali I, Karim S, da Silva Vaz Jr. I, Termignoni C. Probing the functional role of tick metalloproteases. Physiol Entomol. 2015;40:177–88.

Francischetti IMB, Mather TN, Ribeiro JMC. Cloning of a salivary gland metalloprotease and characterization of gelatinase and fibrin(ogen)lytic activities in the saliva of the Lyme disease tick vector Ixodes scapularis. Biochem Biophys Res Commun. 2003;305:869–75. PubMed PMC

Perner J, Helm D, Haberkant P, Hatalova T, Kropackova S, Ribeiro JM, et al. The central role of salivary metalloproteases in host acquired resistance to tick feeding. Front Cell Infect Microbiol. 2020;10. PubMed PMC

Decrem Y, Mariller M, Lahaye K, Blasioli V, Beaufays J, Zouaoui Boudjeltia K, et al. The impact of gene knock-down and vaccination against salivary metalloproteases on blood feeding and egg laying by Ixodes ricinus. Int J Parasitol. 2008;38:549–60. PubMed

Becker M, Felsberger A, Frenzel A, Shattuck WMC, Dyer M, Kügler J, et al. Application of M13 phage display for identifying immunogenic proteins from tick (Ixodes scapularis) saliva. BMC Biotechnol. 2015;15:43. PubMed PMC

Jarmey JM, Riding GA, Pearson RD, McKenna RV, Willadsen P. Carboxydipeptidase from Boophilus microplus: a “concealed” antigen with similarity to angiotensin-converting enzyme. Insect Biochem Mol Biol. 1995;25:969–74. PubMed

Suiko M, Kurogi K, Hashiguchi T, Sakakibara Y, Liu M-C. Updated perspectives on the cytosolic sulfotransferases (SULTs) and SULT-mediated sulfation. Biosci Biotechnol Biochem. 2017;81:63–72. PubMed PMC

Meyer M, Kircher M. Illumina sequencing library preparation for highly multiplexed target capture and sequencing. Cold Spring Harb Protoc. 2010;2010:pdb.prot5448. PubMed

Aury J-M, Cruaud C, Barbe V, Rogier O, Mangenot S, Samson G, et al. High quality draft sequences for prokaryotic genomes using a mix of new sequencing technologies. BMC Genomics. 2008;9:603. PubMed PMC

Alberti A, Poulain J, Engelen S, Labadie K, Romac S, Ferrera I, et al. Viral to metazoan marine plankton nucleotide sequences from the Tara Oceans expedition. Sci Data. 2017;4: 170093. PubMed PMC

Li H. Minimap2: pairwise alignment for nucleotide sequences. Bioinformatics. 2018;34:3094–100. PubMed PMC

Ranallo-Benavidez TR, Jaron KS, Schatz MC. GenomeScope 2.0 and Smudgeplot for reference-free profiling of polyploid genomes. Nat Commun. 2020;11:1432. PubMed PMC

Alonge M, Lebeigle L, Kirsche M, Jenike K, Ou S, Aganezov S, et al. Automated assembly scaffolding using RagTag elevates a new tomato system for high-throughput genome editing. Genome Biol. 2022;23:258. PubMed PMC

Flynn JM, Hubley R, Goubert C, Rosen J, Clark AG, Feschotte C, et al. RepeatModeler2 for automated genomic discovery of transposable element families. Proc Natl Acad Sci. 2020;117:9451–7. PubMed PMC

Kent WJ. BLAT—the BLAST-like alignment tool. Genome Res. 2002;12:656–64. PubMed PMC

Birney E, Clamp M, Durbin R. GeneWise and Genomewise. Genome Res. 2004;14:988–95. PubMed PMC

Rispe C, Hervet C, de la Cotte N, Daveu R, Labadie K, Noel B, et al. Transcriptome of the synganglion in the tick Ixodes ricinus and evolution of the cys-loop ligand-gated ion channel family in ticks. BMC Genomics. 2022;23:463. PubMed PMC

Mott R. EST_GENOME: a program to align spliced DNA sequences to unspliced genomic DNA. Comput Appl Biosci. 1997;13:477–8. PubMed

Dubarry M, Noel B, Rukwavu T, Farhat S, Silva CD, Seeleuthner Y, et al. Gmove a tool for eukaryotic gene predictions using various evidences. F1000Research. 2016;5.

Jones P, Binns D, Chang H-Y, Fraser M, Li W, McAnulla C, et al. InterProScan 5: genome-scale protein function classification. Bioinformatics. 2014;30:1236–40. PubMed PMC

Camacho C, Coulouris G, Avagyan V, Ma N, Papadopoulos J, Bealer K, et al. BLAST+: architecture and applications. BMC Bioinformatics. 2009;10:421. PubMed PMC

Buels R, Yao E, Diesh CM, Hayes RD, Munoz-Torres M, Helt G, et al. JBrowse: a dynamic web platform for genome visualization and analysis. Genome Biol. 2016;17:66. PubMed PMC

Holmer R, van Velzen R, Geurts R, Bisseling T, de Ridder D, Smit S. GeneNoteBook, a collaborative notebook for comparative genomics. Bioinformatics. 2019;35:4779–81. PubMed PMC

Buchfink B, Reuter K, Drost H-G. Sensitive protein alignments at tree-of-life scale using DIAMOND. Nat Methods. 2021;18:366–8. PubMed PMC

Cantalapiedra CP, Hernández-Plaza A, Letunic I, Bork P, Huerta-Cepas J. eggNOG-mapper v2: functional annotation, orthology assignments, and domain prediction at the metagenomic scale. Mol Biol Evol. 2021;38:5825–9. PubMed PMC

Götz S, García-Gómez JM, Terol J, Williams TD, Nagaraj SH, Nueda MJ, et al. High-throughput functional annotation and data mining with the Blast2GO suite. Nucleic Acids Res. 2008;36:3420–35. PubMed PMC

Dunn NA, Unni DR, Diesh C, Munoz-Torres M, Harris NL, Yao E, et al. Apollo: Democratizing genome annotation. PLOS Comput Biol. 2019;15: e1006790. PubMed PMC

Drillon G, Carbone A, Fischer G. SynChro: a fast and easy tool to reconstruct and visualize synteny blocks along eukaryotic chromosomes. PLoS ONE. 2014;9: e92621. PubMed PMC

Anand L, Rodriguez Lopez CM. ChromoMap: an R package for interactive visualization of multi-omics data and annotation of chromosomes. BMC Bioinformatics. 2022;23:33. PubMed PMC

Manni M, Berkeley MR, Seppey M, Simão FA, Zdobnov EM. BUSCO update: novel and streamlined workflows along with broader and deeper phylogenetic coverage for scoring of eukaryotic, prokaryotic, and viral genomes. Mol Biol Evol. 2021;38:4647–54. PubMed PMC

Kriventseva EV, Kuznetsov D, Tegenfeldt F, Manni M, Dias R, Simão FA, et al. OrthoDB v10: sampling the diversity of animal, plant, fungal, protist, bacterial and viral genomes for evolutionary and functional annotations of orthologs. Nucleic Acids Res. 2019;47:D807–11. PubMed PMC

Miele V, Penel S, Duret L. Ultra-fast sequence clustering from similarity networks with SiLiX. BMC Bioinformatics. 2011;12:116. PubMed PMC

Li L, Stoeckert CJ, Roos DS. OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res. 2003;13:2178–89. PubMed PMC

Emms DM, Kelly S. OrthoFinder: phylogenetic orthology inference for comparative genomics. Genome Biol. 2019;20:238. PubMed PMC

Kuraku S, Zmasek CM, Nishimura O, Katoh K. aLeaves facilitates on-demand exploration of metazoan gene family trees on MAFFT sequence alignment server with enhanced interactivity. Nucleic Acids Res. 2013;41:W22–8. PubMed PMC

Capella-Gutiérrez S, Silla-Martínez JM, Gabaldón T. trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics. 2009;25:1972–3. PubMed PMC

Lemoine F, Gascuel O. Gotree/Goalign: toolkit and Go API to facilitate the development of phylogenetic workflows. NAR Genomics Bioinforma. 2021;3:lqab075. PubMed PMC

Minh BQ, Schmidt HA, Chernomor O, Schrempf D, Woodhams MD, von Haeseler A, et al. IQ-TREE 2: new models and efficient methods for phylogenetic inference in the genomic era. Mol Biol Evol. 2020;37:1530–4. PubMed PMC

Mendes FK, Vanderpool D, Fulton B, Hahn MW. CAFE 5 models variation in evolutionary rates among gene families. Bioinformatics. 2021;36:5516–8. PubMed

Revell LJ. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol Evol. 2012;3:217–23.

Paradis E, Schliep K. ape 5.0: an environment for modern phylogenetics and evolutionary analyses in R. Bioinformatics. 2019;35:526–8. PubMed

Kanehisa M, Sato Y. KEGG Mapper for inferring cellular functions from protein sequences. Protein Sci. 2020;29:28–35. PubMed PMC

Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;30:2114–20. PubMed PMC

Charrier NP, Couton M, Voordouw MJ, Rais O, Durand-Hermouet A, Hervet C, et al. Whole body transcriptomes and new insights into the biology of the tick Ixodes ricinus. Parasit Vectors. 2018;11:364. PubMed PMC

Kim D, Paggi JM, Park C, Bennett C, Salzberg SL. Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype. Nat Biotechnol. 2019;37:907–15. PubMed PMC

Jun G, Wing MK, Abecasis GR, Kang HM. An efficient and scalable analysis framework for variant extraction and refinement from population-scale DNA sequence data. Genome Res. 2015;25:918–25. PubMed PMC

Danecek P, Bonfield JK, Liddle J, Marshall J, Ohan V, Pollard MO, et al. Twelve years of SAMtools and BCFtools. GigaScience. 2021;10:giab008. PubMed PMC

Ewels P, Magnusson M, Lundin S, Käller M. MultiQC: summarize analysis results for multiple tools and samples in a single report. Bioinformatics. 2016;32:3047–8. PubMed PMC

Liao Y, Smyth GK, Shi W. The R package Rsubread is easier, faster, cheaper and better for alignment and quantification of RNA sequencing reads. Nucleic Acids Res. 2019;47: e47. PubMed PMC

Yu G, Smith DK, Zhu H, Guan Y, Lam TT-Y. ggtree: an r package for visualization and annotation of phylogenetic trees with their covariates and other associated data. Methods Ecol Evol. 2017;8:28–36.

Wickham H. ggplot2. Cham: Springer International Publishing; 2016.

Nawrocki EP, Eddy SR. Infernal 1.1: 100-fold faster RNA homology searches. Bioinformatics. 2013;29:2933–5. PubMed PMC

Kalvari I, Nawrocki EP, Ontiveros-Palacios N, Argasinska J, Lamkiewicz K, Marz M, et al. Rfam 14: expanded coverage of metagenomic, viral and microRNA families. Nucleic Acids Res. 2021;49:D192-200. PubMed PMC

Chan PP, Lowe TM. tRNAscan-SE: searching for tRNA genes in genomic sequences. Methods Mol Biol Clifton NJ. 2019;1962:1–14. PubMed PMC

Aparicio-Puerta E, Lebrón R, Rueda A, Gómez-Martín C, Giannoukakos S, Jaspez D, et al. sRNAbench and sRNAtoolbox 2019: intuitive fast small RNA profiling and differential expression. Nucleic Acids Res. 2019;47:W530–5. PubMed PMC

Kang Y-J, Yang D-C, Kong L, Hou M, Meng Y-Q, Wei L, et al. CPC2: a fast and accurate coding potential calculator based on sequence intrinsic features. Nucleic Acids Res. 2017;45:W12–6. PubMed PMC

Pertea G, Pertea M. GFF Utilities: GffRead and GffCompare. 2020. PubMed PMC

Fu L, Niu B, Zhu Z, Wu S, Li W. CD-HIT: accelerated for clustering the next-generation sequencing data. Bioinformatics. 2012;28:3150–2. PubMed PMC

Blum M, Chang H-Y, Chuguransky S, Grego T, Kandasaamy S, Mitchell A, et al. The InterPro protein families and domains database: 20 years on. Nucleic Acids Res. 2021;49:D344–54. PubMed PMC

Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ. Basic local alignment search tool. J Mol Biol. 1990;215:403–10. PubMed

Lee E, Helt GA, Reese JT, Munoz-Torres MC, Childers CP, Buels RM, et al. Web Apollo: a web-based genomic annotation editing platform. Genome Biol. 2013;14:R93. PubMed PMC

Almagro Armenteros JJ, Tsirigos KD, Sønderby CK, Petersen TN, Winther O, Brunak S, et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol. 2019;37:420–3. PubMed

Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol. 2011;7:539. PubMed PMC

Lefort V, Desper R, Gascuel O. FastME 2.0: a comprehensive, accurate, and fast distance-based phylogeny inference program. Mol Biol Evol. 2015;32:2798–800. PubMed PMC

Ribeiro JM, Hartmann D, Bartošová-Sojková P, Debat H, Moos M, Šimek P, et al. Blood-feeding adaptations and virome assessment of the poultry red mite Dermanyssus gallinae guided by RNA-seq. Commun Biol. 2023;6:517. PubMed PMC

Waterhouse A, Bertoni M, Bienert S, Studer G, Tauriello G, Gumienny R, et al. SWISS-MODEL: homology modelling of protein structures and complexes. Nucleic Acids Res. 2018;46:W296-303. PubMed PMC

Slater GSC, Birney E. Automated generation of heuristics for biological sequence comparison. BMC Bioinformatics. 2005;6:31. PubMed PMC

Hoy MA, Waterhouse RM, Wu K, Estep AS, Ioannidis P, Palmer WJ, et al. Genome sequencing of the phytoseiid predatory mite Metaseiulus occidentalis reveals completely atomized Hox genes and superdynamic intron evolution. Genome Biol Evol. 2016;8:1762–75. PubMed PMC

Guindon S, Dufayard J-F, Lefort V, Anisimova M, Hordijk W, Gascuel O. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol. 2010;59:307–21. PubMed

Anisimova M, Gascuel O. Approximate likelihood-ratio test for branches: a fast, accurate, and powerful alternative. Syst Biol. 2006;55:539–52. PubMed

Giardine B, Riemer C, Hardison RC, Burhans R, Elnitski L, Shah P, et al. Galaxy: a platform for interactive large-scale genome analysis. Genome Res. 2005;15:1451–5. PubMed PMC

Keller O, Odronitz F, Stanke M, Kollmar M, Waack S. Scipio: Using protein sequences to determine the precise exon/intron structures of genes and their orthologs in closely related species. BMC Bioinformatics. 2008;9:278. PubMed PMC

Lefort V, Longueville J-E, Gascuel O. SMS: smart model selection in PhyML. Mol Biol Evol. 2017;34:2422–4. PubMed PMC

Anisimova M, Gil M, Dufayard J-F, Dessimoz C, Gascuel O. Survey of branch support methods demonstrates accuracy, power, and robustness of fast likelihood-based approximation schemes. Syst Biol. 2011;60:685–99. PubMed PMC

Chen C, Chen H, Zhang Y, Thomas HR, Frank MH, He Y, et al. TBtools: an integrative toolkit developed for interactive analyses of big biological data. Mol Plant. 2020;13:1194–202. PubMed

Nguyen L-T, Schmidt HA, von Haeseler A, Minh BQ. IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol. 2015;32:268–74. PubMed PMC

Kalyaanamoorthy S, Minh BQ, Wong TKF, von Haeseler A, Jermiin LS. ModelFinder: fast model selection for accurate phylogenetic estimates. Nat Methods. 2017;14:587–9. PubMed PMC

Hoang DT, Chernomor O, von Haeseler A, Minh BQ, Vinh LS. UFBoot2: improving the ultrafast bootstrap approximation. Mol Biol Evol. 2018;35:518–22. PubMed PMC

Letunic I, Bork P. Interactive Tree Of Life (iTOL) v4: recent updates and new developments. Nucleic Acids Res. 2019;47:W256–9. PubMed PMC

Ixodes persulcatus (tick) 10X Genomics reads. NCBI Project accession: PRJEB67779 [https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJEB67779] (2024)

Ixodes persulcatus (tick) genome assembly. NCBI Project accession: PRJEB67789 [https://www.ncbi.nlm.nih.gov/bioproject/PRJEB67789/] (2024)

Ixodes hexagonus (tick) 10X Genomics reads. NCBI Project accession: PRJEB67780 [https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJEB67780] (2024)

Ixodes hexagonus (tick) genome assembly. NCBI Project accession: PRJEB67790 [https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJEB67790] (2024)

Ixodes pacificus (tick) 10X Genomics reads. NCBI Project accession: PRJEB67781 https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJEB67781] (2024)

Ixodes pacificus (tick) genome assembly. NCBI Project accession: PRJEB67791 [https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJEB67791] (2024)

Ixodes ricinus (tick) 10X Genomics and Hi-C reads. NCBI Project accession: PRJEB67782 [https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJEB67782] (2024)

Ixodes ricinus (tick) genome assembly. NCBI Project accession: PRJEB67792 [https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJEB67792] (2024)