Abstract
Current sequencing technology allows for the relatively affordable generation of highly contiguous genomes. Technological advances have made it possible for researchers to investigate the consequences of diverse sorts of genomic variants, such as gene gain and loss. With the extraordinary number of high-quality genomes now available, we take stock of how these genomic variants impact phenotypic evolution. We take care to point out that the identification of genomic variants of interest is only the first step in understanding their impact. Painstaking lab or fieldwork is still required to establish causal relationships between genomic variants and phenotypic evolution. We focus mostly on arthropod research, as this phylum has an impressive degree of phenotypic diversity and is also the subject of much evolutionary genetics research. This article is intended to both highlight recent advances in the field and also to be a primer for learning about evolutionary genetics and genomics.
Similar content being viewed by others
Data availability
No datasets were generated or re-analyzed for this work.
References
Adams MD, Celniker SE, Holt RA, Evans CA, Gocayne JD, Amanatides PG, Scherer SE et al (2000) The genome sequence of Drosophila melanogaster. Science 287(5461):2185–2195. https://doi.org/10.1126/science.287.5461.2185
Albalat R, Cañestro C (2016) Evolution by gene loss. Nat Rev Genet 17(7):379–391. https://doi.org/10.1038/nrg.2016.39
Andersen EA (1982) The semiaquatic bugs (Hemiptera, Gerromorpha): phylogeny, adaptations, biogeography and classification. Brill https://brill.com/display/title/576
Andersen JF, Joseph Hinnebusch B, Lucas DA, Conrads TP, Veenstra TD, Pham VM, Ribeiro JMC (2007) An insight into the sialome of the oriental rat flea, Xenopsylla cheopis (Rots). BMC Genomics 8(1):102. https://doi.org/10.1186/1471-2164-8-102
Andersson SG, Kurland CG (1998) Reductive evolution of resident genomes. Trends Microbiol 6(7):263–268. https://doi.org/10.1016/s0966-842x(98)01312-2
Barrangou R, Doudna JA (2016) Applications of CRISPR technologies in research and beyond. Nat Biotechnol 34(9):933–941. https://doi.org/10.1038/nbt.3659
Behura SK, Haugen M, Flannery E, Sarro J, Tessier CR, Severson DW, Duman-Scheel M (2011) Comparative genomic analysis of Drosophila melanogaster and vector mosquito developmental genes. PloS One 6(7):e21504. https://doi.org/10.1371/journal.pone.0021504
Benoit JB, Adelman ZN, Reinhardt K, Dolan A, Poelchau M, Jennings EC, Szuter EM et al (2016) Unique features of a global human ectoparasite identified through sequencing of the bed bug genome. Nat Commun 7(1):10165. https://doi.org/10.1038/ncomms10165
Blondel L, Jones TEM, Extavour CG (2020) Bacterial contribution to genesis of the novel germ line determinant Oskar. eLife 9:e45539. https://doi.org/10.7554/eLife.45539
Boulain H, Legeai F, Guy E, Morlière S, Douglas NE, Jonghee O, Murugan M et al (2018) Fast evolution and lineage-specific gene family expansions of aphid salivary effectors driven by interactions with host-plants. Genome Biol Evol 10(6):1554–1572. https://doi.org/10.1093/gbe/evy097
Brand P, Hinojosa-Díaz IA, Ayala R, Daigle M, Yurrita CL, Obiols TE, Ramírez SR (2020) The evolution of sexual signaling is linked to odorant receptor tuning in perfume-collecting orchid bees. Nat Commun 11(1):244. https://doi.org/10.1038/s41467-019-14162-6
Brand P, Ramírez SR (2017) The evolutionary dynamics of the odorant receptor gene family in corbiculate bees. Genome Biol Evol 9(8):2023–2036. https://doi.org/10.1093/gbe/evx149
Camacho JPM, Ruiz-Ruano FJ, Martín-Blázquez R, López-León MD, Cabrero J, Lorite P, Cabral-de-Mello DC, Bakkali M (2015) A step to the gigantic genome of the desert locust: chromosome sizes and repeated DNAs. Chromosoma 124(2):263–275. https://doi.org/10.1007/s00412-014-0499-0
Cañestro C, Catchen JM, Rodríguez-Marí A, Yokoi H, Postlethwait JH (2009) Consequences of lineage-specific gene loss on functional evolution of surviving paralogs: ALDH1A and retinoic acid signaling in vertebrate genomes. PLoS Genet 5(5):e1000496. https://doi.org/10.1371/journal.pgen.1000496
Carroll SB (2005) Evolution at two levels: on genes and form. PLoS Biol 3(7):e245. https://doi.org/10.1371/journal.pbio.0030245
Carroll SB (2008) Evo-devo and an expanding evolutionary synthesis: a genetic theory of morphological evolution. Cell 134(1):25–36. https://doi.org/10.1016/j.cell.2008.06.030
Casewell NR, Wüster W, Vonk FJ, Harrison RA, Fry BG (2013) Complex cocktails: the evolutionary novelty of venoms. Trends Ecol Evol 28(4):219–229. https://doi.org/10.1016/j.tree.2012.10.020
Chaverra-Rodriguez D, Macias VM, Hughes GL, Pujhari S, Suzuki Y, Peterson DR, Kim D, McKeand S, Rasgon JL (2018) Targeted delivery of CRISPR-Cas9 ribonucleoprotein into arthropod ovaries for heritable germline gene editing. Nat Commun 9(1):3008. https://doi.org/10.1038/s41467-018-05425-9
Choi JY, Yuh CG, Lee. (2020) Double-edged sword: the evolutionary consequences of the epigenetic silencing of transposable elements. PLoS Genet 16(7):e1008872. https://doi.org/10.1371/journal.pgen.1008872
Clark AG, Eisen MB, Smith DR, Bergman CM, Oliver B, Markow TA, Kaufman TC et al (2007) Evolution of genes and genomes on the Drosophila phylogeny. Nature 450(7167):203–218. https://doi.org/10.1038/nature06341
Clark E, Peel AD, Akam M (2019) Arthropod segmentation. Development 146(dev170480). https://doi.org/10.1242/dev.170480
Clarke TH, Garb JE, Hayashi CY, Arensburger P, Ayoub NA (2015) Spider transcriptomes identify ancient large-scale gene duplication event potentially important in silk gland evolution. Genome Biol Evol 7(7):1856–1870. https://doi.org/10.1093/gbe/evv110
Clements AN (1992) The biology of mosquitoes: development, nutrition, and reproduction. Chapman & Hall
Columbus-Shenkar YY, Sachkova MY, Macrander J, Fridrich A, Modepalli V, Reitzel AM, Sunagar K, Moran Y (2018) Dynamics of venom composition across a complex life cycle. eLife 7:e35014. https://doi.org/10.7554/eLife.35014
Cornelis G, Vernochet C, Carradec Q, Souquere S, Mulot B, Catzeflis F, Nilsson MA et al (2015) Retroviral envelope gene captures and syncytin exaptation for placentation in marsupials. Proc Natl Acad Sci 112(5):E487–E496. https://doi.org/10.1073/pnas.1417000112
Croset V, Rytz R, Cummins SF, Budd A, Brawand D, Kaessmann H, Gibson TJ, Benton R (2010) Ancient protostome origin of chemosensory ionotropic glutamate receptors and the evolution of insect taste and olfaction. PLoS Genet 6(8):e1001064. https://doi.org/10.1371/journal.pgen.1001064
Damen WGM (2007) Evolutionary conservation and divergence of the segmentation process in arthropods. Dev Dyn 236(6):1379–1391. https://doi.org/10.1002/dvdy.21157
Damen WGM, Hausdorf M, Seyfarth E-A, Tautz D (1998) A conserved mode of head segmentation in arthropods revealed by the expression pattern of hox genes in a spider. Proc Natl Acad Sci 95(18):10665–10670. https://doi.org/10.1073/pnas.95.18.10665
Darlington CD, Mather K (1949) The elements of genetics. In: The Elements of Genetics. https://www.cabdirect.org/cabdirect/abstract/19490101678
Davidson EH, Erwin DH (2006) Gene regulatory networks and the evolution of animal body plans. Science (New York, NY) 311(5762):796–800. https://doi.org/10.1126/science.1113832
Davis GK, Patel NH (2002) Short, long, and beyond: molecular and embryological approaches to insect segmentation. Annu Rev Entomol 47(1):669–699. https://doi.org/10.1146/annurev.ento.47.091201.145251
Dearden PK, Akam M (2001) Early embryo patterning in the grasshopper, Schistocerca gregaria: wingless, decapentaplegic and caudal expression. Development 128(18):3435–3444
Deppisch P, Kirsch V, Helfrich-Förster C, Senthilan PR (2023) Contribution of cryptochromes and photolyases for insect life under sunlight. J Comp Physiol A 209(3):373–389. https://doi.org/10.1007/s00359-022-01607-5
Der Zee V, Maurijn NB, Roth S (2005) Distinct functions of the Tribolium zerknu¨llt genes in serosa specification and dorsal closure. Curr Biol 15(7):624–636. https://doi.org/10.1016/j.cub.2005.02.057
Dönitz J, Gerischer L, Hahnke S, Pfeiffer S, Bucher G (2018) Expanded and updated data and a query pipeline for iBeetle-Base. Nucleic Acids Res 46(D1):D831–D835. https://doi.org/10.1093/nar/gkx984
Farkas Z, Kovács K, Sarkadi Z, Kalapis D, Fekete G, Birtyik F, Ayaydin F et al (2022) Gene loss and compensatory evolution promotes the emergence of morphological novelties in budding yeast. Nat Ecol Evol 6(6):763–773. https://doi.org/10.1038/s41559-022-01730-1
Feiner N, Motone F, Meyer A, Kuraku S (2019) Asymmetric paralog evolution between the ‘cryptic’ Gene Bmp16 and its well-studied sister genes Bmp2 and Bmp4. Sci Rep 9(1):1–13. https://doi.org/10.1038/s41598-019-40055-1
Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J (1999) Preservation of duplicate genes by complementary, degenerative mutations. Genetics 151(4):1531–1545
Fry BG, Roelants K, Champagne DE, Scheib H, Tyndall JDA, King GF, Nevalainen TJ et al (2009) The toxicogenomic multiverse: convergent recruitment of proteins into animal venoms. Annu Rev Genomics Hum Genet 10(1):483–511. https://doi.org/10.1146/annurev.genom.9.081307.164356
Giraldo-Calderón GI, Emrich SJ, MacCallum RM, Maslen G, Dialynas E, Topalis P, Ho N et al (2015) VectorBase: an updated bioinformatics resource for invertebrate vectors and other organisms related with human diseases. Nucleic Acids Res 43:D707–D713. https://doi.org/10.1093/nar/gku1117
Gitelman I (2007) Evolution of the vertebrate twist family and synfunctionalization: a mechanism for differential gene loss through merging of expression domains. Mol Biol Evol 24(9):1912–1925. https://doi.org/10.1093/molbev/msm120
González VL, Devine AM, Trizna M, Mulcahy DG, Barker KB, Coddington JA (2018) Open access genomic resources for terrestrial arthropods. Curr Opin Insect Sci 25:91–98. https://doi.org/10.1016/j.cois.2017.12.003
Gramates LS, Agapite J, Attrill H, Calvi BR, Crosby MA, dos Santos G, Goodman JL et al (2022) FlyBase: a guided tour of highlighted features. Genetics 220(4):iyac035. https://doi.org/10.1093/genetics/iyac035
Gurska D, Vargas IM, Jentzsch, and Kristen A. Panfilio. (2020) Unexpected mutual regulation underlies paralogue functional diversification and promotes epithelial tissue maturation in tribolium. Commun Biol 3(1):1–15. https://doi.org/10.1038/s42003-020-01250-3
Heger P, Zheng W, Rottmann A, Panfilio KA, Wiehe T (2020) The genetic factors of bilaterian evolution. eLife 9:e45530. https://doi.org/10.7554/eLife.45530
Herndon N, Shelton J, Gerischer L, Ioannidis P, Ninova M, Dönitz J, Waterhouse RM et al (2020) Enhanced genome assembly and a new official gene set for Tribolium castaneum. BMC Genomics 21(1):47. https://doi.org/10.1186/s12864-019-6394-6
Herzig V, Sunagar K, Wilson DTR, Pineda SS, Israel MR, Dutertre S, McFarland BS et al (2020) Australian funnel-web spiders evolved human-lethal δ-hexatoxins for defense against vertebrate predators. Proc Natl Acad Sci U S A 117(40):24920–24928. https://doi.org/10.1073/pnas.2004516117
Holt RA, Mani Subramanian G, Halpern A, Sutton GG, Charlab R, Nusskern DR, Wincker P et al (2002) The genome sequence of the malaria mosquito Anopheles gambiae. Science 298(5591):129–149. https://doi.org/10.1126/science.1076181
Horn T, Hilbrant M, Panfilio KA (2015) Evolution of epithelial morphogenesis: phenotypic integration across multiple levels of biological organization. Front Genet 6 https://www.frontiersin.org/articles/10.3389/fgene.2015.00303
Hotaling S, Sproul JS, Heckenhauer J, Powell A, Larracuente AM, Pauls SU, Kelley JL, Frandsen PB (2021) Long reads are revolutionizing 20 years of insect genome sequencing. Genome Biol Evol 13(8):evab138. https://doi.org/10.1093/gbe/evab138
i5K Consortium (2013) The i5K initiative: advancing arthropod genomics for knowledge, human health, agriculture, and the environment. J Hered 104(5):595–600. https://doi.org/10.1093/jhered/est050
Jacobs CGC, Rezende GL, Lamers GEM, van der Zee M (2013) The extraembryonic serosa protects the insect egg against desiccation. Proc R Soc B: Biol Sci 280(1764):20131082. https://doi.org/10.1098/rspb.2013.1082
Janssen R, Pechmann M, Turetzek N (2021) A chelicerate Wnt gene expression atlas: novel insights into the complexity of arthropod Wnt-patterning. EvoDevo 12(1):12. https://doi.org/10.1186/s13227-021-00182-1
Jarvela C, Alys M, Pick L (2016) Evo-devo: discovery of diverse mechanisms regulating development. Curr Top Dev Biol 117:253–274. https://doi.org/10.1016/bs.ctdb.2015.11.014
Jarvela C, Alys M, Trelstad CS, Pick L (2020) Regulatory gene function handoff allows essential gene loss in mosquitoes. Communications Biology 3(1):1–10. https://doi.org/10.1038/s42003-020-01203-w
Jockusch EL, Fisher CR (2021) Something old, something new, something borrowed, something red: the origin of ecologically relevant novelties in Hemiptera. Curr Opin Genet Dev 69:154–162. https://doi.org/10.1016/j.gde.2021.04.003
Kelley JL, Peyton JT, Fiston-Lavier A-S, Teets NM, Muh-Ching Yee J, Johnston S, Bustamante CD, Lee RE, Denlinger DL (2014) Compact genome of the Antarctic midge is likely an adaptation to an extreme environment. Nat Commun 5(1):4611. https://doi.org/10.1038/ncomms5611
Khalturin K, Hemmrich G, Fraune S, Augustin R, Bosch TCG (2009) More than just orphans: are taxonomically-restricted genes important in evolution? Trends Genet 25(9):404–413. https://doi.org/10.1016/j.tig.2009.07.006
Klomp J, Athy D, Kwan CW, Bloch NI, Sandmann T, Lemke S, Schmidt-Ott U (2015) Embryo development. a cysteine-clamp gene drives embryo polarity in the midge chironomus. Science 348(6238):1040–1042. https://doi.org/10.1126/science.aaa7105
Komata S, Yoda S, KonDo Y, Shinozaki S, Tamai K, Fujiwara H (2023) Functional Unit of supergene in female-limited Batesian mimicry of Papilio polytes. Genetics 223(2):iyac177. https://doi.org/10.1093/genetics/iyac177
Korgaonkar A, Han C, Lemire AL, Siwanowicz I, Bennouna D, Kopec RE, Andolfatto P, Shigenobu S, Stern DL (2021) A novel family of secreted insect proteins linked to plant gall development. Curr Biol 31(9):1836–1849.e12. https://doi.org/10.1016/j.cub.2021.01.104
Krieger MJB, Ross KG (2002) Identification of a major gene regulating complex social behavior. Science 295(5553):328–332. https://doi.org/10.1126/science.1065247
Kunte K, Zhang W, Tenger-Trolander A, Palmer DH, Martin A, Reed RD, Mullen SP, Kronforst MR (2014) Doublesex is a mimicry supergene. Nature 507(7491):229–232. https://doi.org/10.1038/nature13112
Lariviere PJ, Leonard SP, Horak RD, Elijah Powell J, Barrick JE (2023) Honey bee functional genomics using symbiont-mediated RNAi. Nat Protoc 18(3):902–928. https://doi.org/10.1038/s41596-022-00778-4
Leclercq S, Thézé J, Chebbi MA, Giraud I, Moumen B, Ernenwein L, Grève P, Gilbert C, Cordaux R (2016) Birth of a W sex chromosome by horizontal transfer of Wolbachia bacterial symbiont genome. Proc Natl Acad Sci 113(52):15036–15041. https://doi.org/10.1073/pnas.1608979113
Lehmann R (2016) Chapter thirty-nine - germ plasm biogenesis—an Oskar-centric perspective. In: Wassarman PM (ed) Current Topics in Developmental Biology, Essays on Developmental Biology, Part A, vol 116. Academic Press, pp 679–707. https://doi.org/10.1016/bs.ctdb.2015.11.024
Leys R, Cooper SJB, Strecker U, Wilkens H (2005) Regressive evolution of an eye pigment gene in independently evolved eyeless subterranean diving beetles. Biol Lett 1(4):496–499. https://doi.org/10.1098/rsbl.2005.0358
Li F, Zhao X, Li M, He K, Huang C, Zhou Y, Li Z, Walters JR (2019) Insect genomes: progress and challenges. Insect Mol Biol 28(6):739–758. https://doi.org/10.1111/imb.12599
Li Z, Tiley GP, Galuska SR, Reardon CR, Kidder TI, Rundell RJ, Barker MS (2018) Multiple large-scale gene and genome duplications during the evolution of hexapods. Proc Natl Acad Sci 115(18):4713–4718. https://doi.org/10.1073/pnas.1710791115
Losey JE, Harmon J, Ballantyne F, Brown C (1997) A polymorphism maintained by opposite patterns of parasitism and predation. Nature 388(6639):269–272. https://doi.org/10.1038/40849
Maderspacher F, Bucher G, Klingler M (1998) Pair-rule and gap gene mutants in the flour beetle Tribolium castaneum. Dev Genes Evol 208(10):558–568. https://doi.org/10.1007/s004270050215
Mans BJ, Andersen JF, Francischetti IMB, Valenzuela JG, Schwan TG, Pham VM, Garfield MK, Hammer CH, Ribeiro JMC (2008) Comparative sialomics between hard and soft ticks: implications for the evolution of blood-feeding behavior. Insect Biochem Mol Biol 38(1):42–58. https://doi.org/10.1016/j.ibmb.2007.09.003
Mans BJ, Ribeiro JMC (2008) Function, mechanism and evolution of the moubatin-clade of soft tick lipocalins. Insect Biochem Mol Biol 38(9):841–852. https://doi.org/10.1016/j.ibmb.2008.06.007
Marx JL (1986) The continuing saga of ‘homeo-madness. Science 232(4747):158–159. https://doi.org/10.1126/science.3082010
Matthews BJ, Dudchenko O, Kingan SB, Koren S, Antoshechkin I, Crawford JE, Glassford WJ et al (2018) Improved reference genome of Aedes aegypti informs arbovirus vector control. Nature 563(7732):501–507. https://doi.org/10.1038/s41586-018-0692-z
McBride CS, Roman Arguello J, O’Meara BC (2007) Five Drosophila genomes reveal nonneutral evolution and the signature of host specialization in the chemoreceptor superfamily. Genetics 177(3):1395–1416. https://doi.org/10.1534/genetics.107.078683
McClintock B (1950) The origin and behavior of mutable loci in maize. Proc Natl Acad Sci 36(6):344–355. https://doi.org/10.1073/pnas.36.6.344
McGinnis W, Garber RL, Wirz J, Kuroiwa A, Gehring WJ (1984a) A homologous protein-coding sequence in Drosophila Homeotic Genes and its conservation in other metazoans. Cell 37(2):403–408. https://doi.org/10.1016/0092-8674(84)90370-2
McGinnis W, Hart CP, Gehring WJ, Ruddle FH (1984b) Molecular cloning and chromosome mapping of a mouse DNA sequence homologous to homeotic genes of Drosophila. Cell 38(3):675–680. https://doi.org/10.1016/0092-8674(84)90262-9
Misof B, Liu S, Meusemann K, Peters RS, Donath A, Mayer C, Frandsen PB et al (2014) Phylogenomics resolves the timing and pattern of insect evolution. Science 346(6210):763–767. https://doi.org/10.1126/science.1257570
Moran NA, Jarvik T (2010) Lateral transfer of genes from fungi underlies carotenoid production in aphids. Science. https://doi.org/10.1126/science.1187113
Moriyama Y, Koshiba-Takeuchi K (2018) Significance of whole-genome duplications on the emergence of evolutionary novelties. Brief Funct Genomics 17(5):329–338. https://doi.org/10.1093/bfgp/ely007
Nakatani Y, McLysaght A (2019) Macrosynteny analysis shows the absence of ancient whole-genome duplication in Lepidopteran insects. Proc Natl Acad Sci 116(6):1816–1818. https://doi.org/10.1073/pnas.1817937116
Nei M, Niimura Y, Nozawa M (2008) The evolution of animal chemosensory receptor gene repertoires: roles of chance and necessity. Nat Rev Genet 9(12):951–963. https://doi.org/10.1038/nrg2480
Nene V, Wortman JR, Lawson D, Haas B, Kodira C, Zhijian Jake T, Loftus B et al (2007) Genome sequence of Aedes aegypti, a major arbovirus vector. Science 316(5832):1718–1723. https://doi.org/10.1126/science.1138878
Nong W, Zhe Q, Li Y, Barton-Owen T, Wong AYP, Yip HY, Lee HT et al (2021) Horseshoe crab genomes reveal the evolution of genes and microRNAs after three rounds of whole genome duplication. Communications Biology 4(1):1–11. https://doi.org/10.1038/s42003-020-01637-2
Nüsslein-Volhard C, Wieschaus E (1980a) Mutations affecting segment number and polarity in Drosophila. Nature 287(5785):795–801. https://doi.org/10.1038/287795a0
Nüsslein-Volhard C, Wieschaus E (1980b) Mutations affecting segment number and polarity in Drosophila. Nature 287(5785):795–801. https://doi.org/10.1038/287795a0
Ohno S (1970) Evolution by gene duplication, 1st edn. Springer-Verlag, London, New York
Oliver KM, Moran NA, Hunter MS (2005) Variation in resistance to parasitism in aphids is due to symbionts not host genotype. Proc Natl Acad Sci 102(36):12795–12800. https://doi.org/10.1073/pnas.0506131102
Palopoli MF, Patel NH (1996) Neo-Darwinian developmental evolution: can we bridge the gap between pattern and process? Curr Opin Genet Dev 6(4):502–508. https://doi.org/10.1016/S0959-437X(96)80074-8
Panfilio KA, Chuva de Sousa Lopes SM (2022) The extended analogy of extraembryonic development in insects and amniotes. Philos Trans R Soc Lond B Biol Sci 377(1865):20210268 https://doi.org/10.1098/rstb.2021.0268
Panfilio KA, Vargas IM, Jentzsch JB, Benoit DE, Suzuki Y, Colella S, Robertson HM et al (2019) Molecular evolutionary trends and feeding ecology diversification in the Hemiptera, anchored by the milkweed bug genome. Genome Biol 20(1):64. https://doi.org/10.1186/s13059-019-1660-0
Pechmann M, Kenny NJ, Pott L, Heger P, Chen Y-T, Buchta T, Özüak O, Lynch J, Roth S (2021) Striking parallels between dorsoventral patterning in Drosophila and Gryllus reveal a complex evolutionary history behind a model gene regulatory network. eLife 10:e68287. https://doi.org/10.7554/eLife.68287
Peel AD, Chipman AD, Akam M (2005) Arthropod segmentation: beyond the Drosophila paradigm. Nat Rev Genet 6(12):905–916. https://doi.org/10.1038/nrg1724
Pellegrino M, Nakagawa T, Vosshall LB (2010) Single sensillum recordings in the insects Drosophila melanogaster and Anopheles gambiae. JoVE (J Vis Exp) (36):e1725. https://doi.org/10.3791/1725
Pers D, Buchta T, Özüak O, Wolff S, Pietsch JM, Memon MB, Roth S, Lynch JA (2016) Global analysis of dorsoventral patterning in the wasp Nasonia reveals extensive incorporation of novelty in a regulatory network. BMC Biol 14(1):63. https://doi.org/10.1186/s12915-016-0285-y
Pers D, Lynch JA (2018) Ankyrin domain encoding genes from an ancient horizontal transfer are functionally integrated into Nasonia developmental gene regulatory networks. Genome Biol 19(1):148. https://doi.org/10.1186/s13059-018-1526-x
Protas ME, Trontelj P, Patel NH (2011) Genetic basis of eye and pigment loss in the cave Crustacean, Asellus aquaticus. Proc Natl Acad Sci 108(14):5702–5707. https://doi.org/10.1073/pnas.1013850108
Prud’homme B, Gompel N, Carroll SB (2007) Emerging principles of regulatory evolution. Proc Natl Acad Sci U S A 104:8605–8612. https://doi.org/10.1073/pnas.0700488104
Reding K, Chen M, Lu Y, Cheatle Jarvela AM, Pick L (2019) Shifting roles of Drosophila pair-rule gene orthologs: segmental expression and function in the milkweed bug Oncopeltus fasciatus. Development 146(17). https://doi.org/10.1242/dev.181453
Reding K, Pick L (2020) High-efficiency CRISPR/Cas9 mutagenesis of the white Gene in the milkweed bug Oncopeltus fasciatus. Genetics 215(4):1027–1037. https://doi.org/10.1534/genetics.120.303269
Rezende GL, Martins AJ, Gentile C, Farnesi LC, Pelajo-Machado M, Peixoto AA, Valle D (2008) Embryonic desiccation resistance in Aedes aegypti: presumptive role of the chitinized serosal cuticle. BMC Dev Biol 8(1):82. https://doi.org/10.1186/1471-213X-8-82
Ribeiro JMC, Andersen J, Silva-Neto MAC, Pham VM, Garfield MK, Valenzuela JG (2004) Exploring the sialome of the blood-sucking bug Rhodnius prolixus. Insect Biochem Mol Biol 34(1):61–79. https://doi.org/10.1016/j.ibmb.2003.09.004
Ribeiro JMC, Mans BJ (2020) TickSialoFam (TSFam): a database that helps to classify tick salivary proteins, a review on tick salivary protein function and evolution, with considerations on the tick sialome switching phenomenon. Front Cell Infect Microbiol 10 https://www.frontiersin.org/articles/10.3389/fcimb.2020.00374
Ribeiro RO, Chaim OM, da Silveira RB, Gremski LH, Sade YB, Paludo KS, Senff-Ribeiro A, de Moura J, Chávez-Olórtegui C, Gremski W, Nader HB (2007) Biological and structural comparison of recombinant phospholipase D toxins from Loxosceles intermedia (Brown Spider) venom. Toxicon 50(8):1162–1174. https://doi.org/10.1016/j.toxicon.2007.08.001
Richards S, Gibbs RA, Weinstock GM, Brown SJ, Denell R, Beeman RW, Gibbs R et al (2008) The genome of the model beetle and pest Tribolium castaneum. Nature 452(7190):949–955. https://doi.org/10.1038/nature06784
Robertson HM, Baits RL, Walden KKO, Wada-Katsumata A, Schal C (2018) Enormous expansion of the chemosensory gene repertoire in the omnivorous German cockroach Blattella germanica. J Exp Zool B Mol Dev Evol 330(5):265–278. https://doi.org/10.1002/jez.b.22797
Ross KG, Keller L (1998) Genetic control of social organization in an ant. Proc Natl Acad Sci 95(24):14232–14237. https://doi.org/10.1073/pnas.95.24.14232
Sachkova MY, Singer SA, Macrander J, Reitzel AM, Peigneur S, Tytgat J, Moran Y (2019) The birth and death of toxins with distinct functions: a case study in the sea anemone Nematostella. Mol Biol Evol 36(9):2001–2012. https://doi.org/10.1093/molbev/msz132
Santos ME, Le Bouquin A, Crumière AJJ, Khila A (2017) Taxon-restricted genes at the origin of a novel trait allowing access to a new environment. Science 358(6361):386–390. https://doi.org/10.1126/science.aan2748
Sayers EW, Cavanaugh M, Clark K, Pruitt KD, Schoch CL, Sherry ST, Karsch-Mizrachi I (2021) GenBank. Nucleic Acids Res 49(D1):D92–D96. https://doi.org/10.1093/nar/gkaa1023
Schierwater B, Murtha M, Dick M, Ruddle FH, Buss LW (1991) Homeoboxes in Cnidarians. J Exp Zool 260(3):413–416. https://doi.org/10.1002/jez.1402600316
Schwager EE, Sharma PP, Clarke T, Leite DJ, Wierschin T, Pechmann M, Akiyama-Oda Y et al (2017) The house spider genome reveals an ancient whole-genome duplication during arachnid evolution. BMC Biol 15(1):62. https://doi.org/10.1186/s12915-017-0399-x
Sequenced arthropod genomes. i5K 2023. Accessed January 22, 2023. http://i5k.github.io/arthropod_genomes_at_ncbi.
Sharma A, Pham MN, Reyes JB, Chana R, Yim WC, Heu CC, Kim D et al (2022) Cas9-mediated gene editing in the black-legged tick, Ixodes scapularis, by embryo injection and ReMOT control. iScience 25(3):103781. https://doi.org/10.1016/j.isci.2022.103781
Sharma PP (2023) The impact of whole genome duplication on the evolution of the arachnids. Integr Comp Biol:icad050. https://doi.org/10.1093/icb/icad050
Sharma PP, Schwager EE, Extavour CG, Wheeler WC (2014) Hox gene duplications correlate with posterior heteronomy in scorpions. Proc R Soc B: Biol Sci 281(1792):20140661. https://doi.org/10.1098/rspb.2014.0661
Shirai Y, Piulachs M-D, Belles X, Daimon T (2022) DIPA-CRISPR is a simple and accessible method for insect gene editing. Cell Rep Methods 2(5):100215. https://doi.org/10.1016/j.crmeth.2022.100215
Somorjai IML, Martí-Solans J, Diaz-Gracia M, Nishida H, Imai KS, Escrivà H, Cañestro C, Albalat R (2018) Wnt evolution and function shuffling in liberal and conservative chordate genomes. Genome Biol 19(1):98. https://doi.org/10.1186/s13059-018-1468-3
Stauber M, Taubert H, Schmidt-Ott U (2000) Function of bicoid and hunchback homologs in the basal Cyclorrhaphan Fly Megaselia (Phoridae). Proc Natl Acad Sci 97(20):10844–10849. https://doi.org/10.1073/pnas.190095397
Stern DL, Han C (2022) Gene structure-based homology search identifies highly divergent putative effector gene family. Genome Biol Evol 14(6):evac069. https://doi.org/10.1093/gbe/evac069
Surm JM, Smith HL, Madio B, Undheim EAB, King GF, Hamilton BR, van der Burg CA, Pavasovic A, Prentis PJ (2019) A process of convergent amplification and tissue-specific expression dominates the evolution of toxin and toxin-like genes in sea anemones. Mol Ecol 28(9):2272–2289. https://doi.org/10.1111/mec.15084
Takada H (1981) Inheritance of body colors in Myzus persicae (SULZER)(Homoptera : Aphididae). Appl Entomol Zool 16(3):242–246. https://doi.org/10.1303/aez.16.242
Tautz D, Friedrich M, Schröder R (1994) Insect embryogenesis - what is ancestral and what is derived? Development 1994:193–199. https://doi.org/10.1242/dev.1994.Supplement.193
Thomas GWC, Dohmen E, Hughes DST, Murali SC, Poelchau M, Glastad K, Anstead CA et al (2020) Gene content evolution in the arthropods. Genome Biol 21(1):15. https://doi.org/10.1186/s13059-019-1925-7
Thompson MJ, Jiggins CD (2014) Supergenes and their role in evolution. Heredity 113(1):1–8. https://doi.org/10.1038/hdy.2014.20
True JR, Haag ES (2001) Developmental system drift and flexibility in evolutionary trajectories. Evol Dev 3(2):109–119
Villoutreix R, Ayala D, Joron M, Gompert Z, Feder JL, Nosil P (2021) Inversion breakpoints and the evolution of supergenes. Mol Ecol 30(12):2738–2755. https://doi.org/10.1111/mec.15907
Villoutreix R, de Carvalho CF, Soria-Carrasco V, Lindtke D, De-la-Mora M, Muschick M, Feder JL, Parchman TL, Gompert Z, Nosil P (2020) Large-scale mutation in the evolution of a gene complex for cryptic coloration. Science 369(6502):460–466. https://doi.org/10.1126/science.aaz4351
Waddington CH (1940) Organisers and genes. Organisers and Genes https://www.cabdirect.org/cabdirect/abstract/19412202515
Wang B, Liu Y, He K, Wang G (2016) Comparison of research methods for functional characterization of insect olfactory receptors. Sci Rep 6(1):32806. https://doi.org/10.1038/srep32806
Weinstock GM, Robinson GE, Gibbs RA, Weinstock GM, Weinstock GM, Robinson GE, Worley KC et al (2006) Insights into social insects from the genome of the honeybee Apis mellifera. Nature 443(7114):931–949. https://doi.org/10.1038/nature05260
Wellmeyer B, Böhringer AC, Rösner J, Merzendorfer H (2023) Analyses of ecdysteroid transporters in the fat body of Tribolium castaneum. Insect Mol Biol 32(4):400–411. https://doi.org/10.1111/imb.12839
Wissler L, Gadau J, Simola DF, Helmkampf M, Bornberg-Bauer E (2013) Mechanisms and dynamics of orphan gene emergence in insect genomes. Genome Biol Evol 5(2):439–455. https://doi.org/10.1093/gbe/evt009
Wolf YI, Koonin EV (2013) Genome reduction as the dominant mode of evolution. Bioessays 35(9):829–837. https://doi.org/10.1002/bies.201300037
Xia Q, Zhou Z, Cheng L, Cheng D, Dai F, Li B, Zhao P et al (2004) A draft sequence for the genome of the domesticated silkworm (Bombyx mori). Science 306(5703):1937–1940. https://doi.org/10.1126/science.1102210
Xue L, Li X, Noll M (2001) Multiple protein functions of paired in Drosophila development and their conservation in the gooseberry and Pax3 homologs. Development 128(3):395–405
Yan Z, Martin SH, Gotzek D, Arsenault SV, Duchen P, Helleu Q, Riba-Grognuz O et al (2020) Evolution of a supergene that regulates a trans-species social polymorphism. Nat Ecol Evol 4(2):240–249. https://doi.org/10.1038/s41559-019-1081-1
Yates AD, Allen J, Amode RM, Azov AG, Barba M, Becerra A, Bhai J et al (2022) Ensembl Genomes 2022: an expanding genome resource for non-vertebrates. Nucleic Acids Res 50(D1):D996–D1003. https://doi.org/10.1093/nar/gkab1007
Ylla G, Nakamura T, Itoh T, Kajitani R, Toyoda A, Tomonari S, Bando T et al (2021) Insights into the Genomic Evolution of Insects from Cricket Genomes. Commun Biol 4(1):1–12. https://doi.org/10.1038/s42003-021-02197-9
You Y, Smith DP, Lv M, Zhang L (2016) A broadly tuned odorant receptor in neurons of trichoid sensilla in Locust, Locusta migratoria. Insect Biochem Mol Biol 79:66–72. https://doi.org/10.1016/j.ibmb.2016.10.008
Yuan Q, Metterville D, Briscoe AD, Reppert SM (2007) Insect cryptochromes: gene duplication and loss define diverse ways to construct insect circadian clocks. Mol Biol Evol 24(4):948–955. https://doi.org/10.1093/molbev/msm011
Zhou K, Huang B, Zou M, Dandan L, He S, Wang G (2015) Genome-wide identification of lineage-specific genes within Caenorhabditis elegans. Genomics. https://doi.org/10.1016/j.ygeno.2015.07.002
Zug R, Hammerstein P (2012) Still a host of hosts for Wolbachia: analysis of recent data suggests that 40% of terrestrial arthropod species are infected. PloS One 7(6):e38544. https://doi.org/10.1371/journal.pone.0038544
Funding
Alys Cheatle Jarvela was supported by NIH grant R01GM113230 (awarded to Leslie Pick, University of Maryland, College Park). Judith R. Wexler was supported by the Zuckerman STEM Leadership program and by the Rector of Hebrew University in Jerusalem.
Author information
Authors and Affiliations
Contributions
Alys Cheatle Jarvela and Judith R. Wexler wrote and revised the manuscript and arranged the figures.
Corresponding authors
Ethics declarations
Ethics approval
Not applicable. No human or animal studies were conducted.
Competing interests
The authors declare no competing interests
Additional information
Communicated by Kristen Panfilio
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
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
Cheatle Jarvela, A.M., Wexler, J.R. Advances in genome sequencing reveal changes in gene content that contribute to arthropod macroevolution. Dev Genes Evol 233, 59–76 (2023). https://doi.org/10.1007/s00427-023-00712-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00427-023-00712-y