1932

Abstract

Instances of multicellularity across the tree of life have fostered the evolution of complex organs composed of distinct cell types that cooperate, producing emergent biological functions. How organs originate is a fundamental evolutionary problem that has eluded deep mechanistic and conceptual understanding. Here I propose a cell- to organ-level transitions framework, whereby cooperative division of labor originates and becomes entrenched between cell types through a process of functional niche creation, cell-type subfunctionalization, and irreversible ratcheting of cell interdependencies. Comprehending this transition hinges on explaining how these processes unfold molecularly in evolving populations. Recent single-cell transcriptomic studies and analyses of terminal fate specification indicate that cellular functions are conferred by modular gene expression programs. These discrete components of functional variation may be deployed or combined within cells to introduce new properties into multicellular niches, or partitioned across cells to establish division of labor. Tracing gene expression program evolution at the level of single cells in populations may reveal transitions toward organ complexity.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-cellbio-111822-121620
2024-10-02
2024-10-15
Loading full text...

Full text loading...

/deliver/fulltext/cellbio/40/1/annurev-cellbio-111822-121620.html?itemId=/content/journals/10.1146/annurev-cellbio-111822-121620&mimeType=html&fmt=ahah

Literature Cited

  1. Adler M, Chavan AR, Medzhitov R. 2023.. Tissue biology: in search of a new paradigm. . Annu. Rev. Cell Dev. Biol. 39::6789
    [Crossref] [Google Scholar]
  2. Adler M, Kohanim YK, Tendler A, Mayo A, Alon U. 2019.. Continuum of gene-expression profiles provides spatial division of labor within a differentiated cell type. . Cell Syst. 8:(1):4352.e5
    [Crossref] [Google Scholar]
  3. Aldridge S, Teichmann SA. 2020.. Single cell transcriptomics comes of age. . Nat. Commun. 11:(1):4307
    [Crossref] [Google Scholar]
  4. Aneshansley DJ, Eisner T, Widom JM, Widom B. 1969.. Biochemistry at 100°C: explosive secretory discharge of bombardier beetles (Brachinus). . Science 165:(3888):6163
    [Crossref] [Google Scholar]
  5. Arendt D. 2008.. The evolution of cell types in animals: emerging principles from molecular studies. . Nat. Rev. Genet. 9:(11):86882
    [Crossref] [Google Scholar]
  6. Arendt D, Hausen H, Purschke G. 2009.. The division of labour model of eye evolution. . Philos. Trans. R. Soc. B 364:(1531):280917
    [Crossref] [Google Scholar]
  7. Arendt D, Musser JM, Baker CVH, Bergman A, Cepko C, et al. 2016a.. The origin and evolution of cell types. . Nat. Rev. Genet. 17:(12):74457
    [Crossref] [Google Scholar]
  8. Arendt D, Tosches MA, Marlow H. 2016b.. From nerve net to nerve ring, nerve cord and brain—evolution of the nervous system. . Nat. Rev. Neurosci. 17:(1):6172
    [Crossref] [Google Scholar]
  9. Arlotta P, Hobert O. 2015.. Homeotic transformations of neuronal cell identities. . Trends Neurosci. 38:(12):75162
    [Crossref] [Google Scholar]
  10. Arrese EL, Soulages JL. 2010.. Insect fat body: energy, metabolism, and regulation. . Annu. Rev. Entomol. 55::20725
    [Crossref] [Google Scholar]
  11. Arthur W. 2002.. The emerging conceptual framework of evolutionary developmental biology. . Nature 415:(6873):75764
    [Crossref] [Google Scholar]
  12. Asano T, Seto Y, Hashimoto K, Kurushima H. 2019.. Mini-review an insect-specific system for terrestrialization: laccase-mediated cuticle formation. . Insect Biochem. Mol. Biol. 108::6170
    [Crossref] [Google Scholar]
  13. Baldwin MW, Ko M-C. 2020.. Functional evolution of vertebrate sensory receptors. . Horm. Behav. 124::104771
    [Crossref] [Google Scholar]
  14. Bayram H, Sayadi A, Immonen E, Arnqvist G. 2018.. Identification of novel ejaculate proteins in a seed beetle and division of labour across male accessory reproductive glands. . Insect Biochem. Mol. 104::5057
    [Crossref] [Google Scholar]
  15. Ben-Moshe S, Itzkovitz S. 2019.. Spatial heterogeneity in the mammalian liver. . Nat. Rev. Gastroenterol. Hepatol. 16:(7):395410
    [Crossref] [Google Scholar]
  16. Bontonou G, Saint-Leandre B, Kafle T, Baticle T, Hassan A, et al. 2024.. Evolution of chemosensory tissues and cells across ecologically diverse Drosophilids. . Nat. Commun. 15::1047
    [Crossref] [Google Scholar]
  17. Borg M, Krueger-Hadfield SA, Destombe C, Collén J, Lipinska A, Coelho SM. 2023.. Red macroalgae in the genomic era. . New Phytol. 240:(2):47188
    [Crossref] [Google Scholar]
  18. Bourguignon T, Šobotník J, Brabcová J, Sillam-Dussès D, Buček A, et al. 2016.. Molecular mechanism of the two-component suicidal weapon of Neocapritermes taracua old workers. . Mol. Biol. Evol. 33:(3):80919
    [Crossref] [Google Scholar]
  19. Bowman JL. 2022.. The origin of a land flora. . Nat. Plants 8:(12):135269
    [Crossref] [Google Scholar]
  20. Bringloe TT, Starko S, Wade RM, Vieira C, Kawai H, et al. 2020.. Phylogeny and evolution of the brown algae. . Crit. Rev. Plant Sci. 39:(4):281321
    [Crossref] [Google Scholar]
  21. Brückner A, Badroos JM, Learsch RW, Yousefelahiyeh M, Kitchen SA, Parker J. 2021.. Evolutionary assembly of cooperating cell types in an animal chemical defense system. . Cell 184:(25):613856.e28
    [Crossref] [Google Scholar]
  22. Brückner A, Parker J. 2020.. Molecular evolution of gland cell types and chemical interactions in animals. . J. Exp. Biol. 223:(Suppl. 1):jeb211938
    [Crossref] [Google Scholar]
  23. Brunet T, King N. 2017.. The origin of animal multicellularity and cell differentiation. . Dev. Cell 43:(2):12440
    [Crossref] [Google Scholar]
  24. Brunet TDP. 2022.. Higher level constructive neutral evolution. . Biol. Philos. 37:(4):23
    [Crossref] [Google Scholar]
  25. Buss LW. 1987.. The Evolution of Individuality. Princeton, NJ:: Princeton Univ. Press
    [Google Scholar]
  26. Charrier B, Bail AL, de Reviers B. 2012.. Plant Proteus: brown algal morphological plasticity and underlying developmental mechanisms. . Trends Plant Sci. 17:(8):46877
    [Crossref] [Google Scholar]
  27. Clark RI, Tan SWS, Péan CB, Roostalu U, Vivancos V, et al. 2013.. MEF2 is an in vivo immune-metabolic switch. . Cell 155:(2):43547
    [Crossref] [Google Scholar]
  28. Cock JM, Godfroy O, Macaisne N, Peters AF, Coelho SM. 2014.. Evolution and regulation of complex life cycles: a brown algal perspective. . Curr. Opin. Plant Biol. 17::16
    [Crossref] [Google Scholar]
  29. Cock JM, Sterck L, Rouzé P, Scornet D, Allen AE, et al. 2010.. The Ectocarpus genome and the independent evolution of multicellularity in brown algae. . Nature 465:(7298):61721
    [Crossref] [Google Scholar]
  30. Cole AG, Jahnel SM, Kaul S, Steger J, Hagauer J, et al. 2023.. Muscle cell-type diversification is driven by bHLH transcription factor expansion and extensive effector gene duplications. . Nat. Commun. 14:(1):1747
    [Crossref] [Google Scholar]
  31. Cooper GA, Frost H, Liu M, West SA. 2021.. The evolution of division of labour in structured and unstructured groups. . eLife 10::e71968
    [Crossref] [Google Scholar]
  32. Cooper GA, West SA. 2018.. Division of labour and the evolution of extreme specialization. . Nat. Ecol. Evol. 2:(7):116167
    [Crossref] [Google Scholar]
  33. Darwin C. 1859.. On the Origin of Species by Means of Natural Selection, or, the Preservation of Favoured Races in the Struggle for Life. London:: John Murray
    [Google Scholar]
  34. Dassanayake M, Larkin JC. 2017.. Making plants break a sweat: the structure, function, and evolution of plant salt glands. . Front. Plant Sci. 8::406
    [Google Scholar]
  35. de Ceglia R, Ledonne A, Litvin DG, Lind BL, Carriero G, et al. 2023.. Specialized astrocytes mediate glutamatergic gliotransmission in the CNS. . Nature 622:(7981):12029
    [Crossref] [Google Scholar]
  36. Dettner K. 1993.. Defensive secretions and exocrine glands in free-living staphylinid beetles—their bearing on phylogeny (Coleoptera: Staphylinidae). . Biochem. Syst. Ecol. 21:(1):14362
    [Crossref] [Google Scholar]
  37. Douglas AE. 2020.. Housing microbial symbionts: evolutionary origins and diversification of symbiotic organs in animals. . Philos. Trans. R. Soc. B 375:(1808):20190603
    [Crossref] [Google Scholar]
  38. Dutertre S, Jin A-H, Vetter I, Hamilton B, Sunagar K, et al. 2014.. Evolution of separate predation- and defence-evoked venoms in carnivorous cone snails. . Nat. Commun. 5:(1):3521
    [Crossref] [Google Scholar]
  39. Eisner T, Meinwald J. 1966.. Defensive secretions of arthropods. . Science 153:(3742):134150
    [Crossref] [Google Scholar]
  40. Finnigan GC, Hanson-Smith V, Stevens TH, Thornton JW. 2012.. Evolution of increased complexity in a molecular machine. . Nature 481:(7381):36064
    [Crossref] [Google Scholar]
  41. Fisher RM, Cornwallis CK, West SA. 2013.. Group formation, relatedness, and the evolution of multicellularity. . Curr. Biol. 23:(12):112025
    [Crossref] [Google Scholar]
  42. Force A, Lynch M, Pickett FB, Amores A, Yan YL, Postlethwait J. 1999.. Preservation of duplicate genes by complementary, degenerative mutations. . Genetics 151:(4):153145
    [Crossref] [Google Scholar]
  43. Fritzsch B, Beisel KW, Bermingham NA. 2000.. Developmental evolutionary biology of the vertebrate ear: conserving mechanoelectric transduction and developmental pathways in diverging morphologies. . NeuroReport 11:(17):R3544
    [Crossref] [Google Scholar]
  44. Fritzsch B, Beisel KW, Jones K, Fariñas I, Maklad A, et al. 2002.. Development and evolution of inner ear sensory epithelia and their innervation. . J. Neurobiol. 53:(2):14356
    [Crossref] [Google Scholar]
  45. Fritzsch B, Straka H. 2014.. Evolution of vertebrate mechanosensory hair cells and inner ears: toward identifying stimuli that select mutation driven altered morphologies. . J. Comp. Physiol. A 200:(1):518
    [Crossref] [Google Scholar]
  46. Fukushima K, Fang X, Alvarez-Ponce D, Cai H, Carretero-Paulet L, et al. 2017.. Genome of the pitcher plant Cephalotus reveals genetic changes associated with carnivory. . Nat. Ecol. Evol. 1:(3):0059
    [Crossref] [Google Scholar]
  47. Gilbert C. 1994.. Form and function of stemmata in larvae of holometabolous insects. . Annu. Rev. Entomol. 39::32349
    [Crossref] [Google Scholar]
  48. Gray MW, Lukeš J, Archibald JM, Keeling PJ, Doolittle WF. 2010.. Irremediable complexity?. Science 330:(6006):92021
    [Crossref] [Google Scholar]
  49. Gregory TR. 2008.. The evolution of complex organs. . Evol. Educ. Outreach 1:(4):35889
    [Crossref] [Google Scholar]
  50. Griffith OW, Wagner GP. 2017.. The placenta as a model for understanding the origin and evolution of vertebrate organs. . Nat. Ecol. Evol. 1:(4):72
    [Crossref] [Google Scholar]
  51. Gupta V, Frank AM, Matolka N, Lazzaro BP. 2022.. Inherent constraints on a polyfunctional tissue lead to a reproduction-immunity tradeoff. . BMC Biol. 20:(1):127
    [Crossref] [Google Scholar]
  52. Halpern KB, Shenhav R, Matcovitch-Natan O, Tóth B, Lemze D, et al. 2017.. Single-cell spatial reconstruction reveals global division of labour in the mammalian liver. . Nature 542:(7641):35256
    [Crossref] [Google Scholar]
  53. Hamilton BR, Marshall DL, Casewell NR, Harrison RA, Blanksby SJ, Undheim EAB. 2020.. Mapping enzyme activity on tissue by functional mass spectrometry imaging. . Angew. Chem. 132:(10):388386
    [Crossref] [Google Scholar]
  54. Harrison CJ. 2017.. Development and genetics in the evolution of land plant body plans. . Philos. Trans. R. Soc. B 372:(1713):20150490
    [Crossref] [Google Scholar]
  55. Heavner W, Pevny L. 2012.. Eye development and retinogenesis. . Cold Spring Harb. Perspect. Biol. 4:(12):a008391
    [Crossref] [Google Scholar]
  56. Hobert O. 2016.. Terminal selectors of neuronal identity. . Curr. Top. Dev. Biol. 116::45575
    [Crossref] [Google Scholar]
  57. Hobert O. 2021.. Homeobox genes and the specification of neuronal identity. . Nat. Rev. Neurosci. 22:(10):62736
    [Crossref] [Google Scholar]
  58. Hochberg GKA, Liu Y, Marklund EG, Metzger BPH, Laganowsky A, Thornton JW. 2020.. A hydrophobic ratchet entrenches molecular complexes. . Nature 588:(7838):5038
    [Crossref] [Google Scholar]
  59. Hopkins BR, Sepil I, Bonham S, Miller T, Charles PD, et al. 2019.. BMP signaling inhibition in Drosophila secondary cells remodels the seminal proteome and self and rival ejaculate functions. . PNAS 116:(49):2471928
    [Crossref] [Google Scholar]
  60. Ibarra Y, Blair NT. 2013.. Benzoquinone reveals a cysteine-dependent desensitization mechanism of TRPA1. . Mol. Pharmacol. 83:(5):112032
    [Crossref] [Google Scholar]
  61. Innan H, Kondrashov F. 2010.. The evolution of gene duplications: classifying and distinguishing between models. . Nat. Rev. Genet. 11:(2):97108
    [Crossref] [Google Scholar]
  62. Jacobs DK, Nakanishi N, Yuan D, Camara A, Nichols SA, Hartenstein V. 2007.. Evolution of sensory structures in basal metazoa. . Integr. Comp. Biol. 47:(5):71223
    [Crossref] [Google Scholar]
  63. Jékely G. 2011.. Origin and early evolution of neural circuits for the control of ciliary locomotion. . Proc. R. Soc. B 278:(1707):91422
    [Crossref] [Google Scholar]
  64. Jiang J, Chen S, Tsou T, McGinnis CS, Khazaei T, et al. 2023.. D-SPIN constructs gene regulatory network models from multiplexed scRNA-seq data revealing organizing principles of cellular perturbation response. . bioRxiv 2023.04.19.537364. https://doi.org/10.1101/2023.04.19.537364
  65. Jordan K. 1913.. Zur Morphologie und Biologie der myrmecophilen Gattungen Lomechusa und Atemeles und einiger verwandter Formen. . Z. Wiss. Zool. 107::34686
    [Google Scholar]
  66. Kazandjian TD, Hamilton BR, Robinson SD, Hall SR, Bartlett KE, et al. 2022.. Physiological constraints dictate toxin spatial heterogeneity in snake venom glands. . BMC Biol. 20:(1):148
    [Crossref] [Google Scholar]
  67. Kishi Y, Parker J. 2021.. Cell type innovation at the tips of the animal tree. . Curr. Opin. Genet. Dev. 69::11221
    [Crossref] [Google Scholar]
  68. Kitchen SA, Naragon TH, Brückner A, Ladinsky MS, Quinodoz S, et al. 2024.. The genomic and cellular basis of biosynthetic innovation in rove beetles. . Cell 187::356384.e26
    [Crossref] [Google Scholar]
  69. Kmieć Z. 2001.. Cooperation of Liver Cells in Health and Disease. Berlin:: Springer
    [Google Scholar]
  70. Knoll AH. 2011.. The multiple origins of complex multicellularity. . Annu. Rev. Earth Planet. Sci. 39::21739
    [Crossref] [Google Scholar]
  71. Kotliar D, Veres A, Nagy MA, Tabrizi S, Hodis E, et al. 2019.. Identifying gene expression programs of cell-type identity and cellular activity with single-cell RNA-Seq. . eLife 8::e43803
    [Crossref] [Google Scholar]
  72. Krausgruber T, Fortelny N, Fife-Gernedl V, Senekowitsch M, Schuster LC, et al. 2020.. Structural cells are key regulators of organ-specific immune responses. . Nature 583:(7815):296302
    [Crossref] [Google Scholar]
  73. Kuwabara T, Kohno H, Hatakeyama M, Kubo T. 2023.. Evolutionary dynamics of mushroom body Kenyon cell types in hymenopteran brains from multifunctional type to functionally specialized types. . Sci. Adv. 9:(18):eadd4201
    [Crossref] [Google Scholar]
  74. Lamb TD. 2013.. Evolution of phototransduction, vertebrate photoreceptors and retina. . Prog. Retin. Eye Res. 36::52119
    [Crossref] [Google Scholar]
  75. Levinger R, Tussia-Cohen D, Friedman S, Lender Y, Nissan Y, et al. 2023.. Spatial and single-cell transcriptomics illuminate bat immunity and barrier tissue evolution. . bioRxiv 2023.10.30.564705. https://doi.org/10.1101/2023.10.30.564705
  76. Leys SP, Degnan BM. 2001.. Cytological basis of photoresponsive behavior in a sponge larva. . Biol. Bull. 201:(3):32338
    [Crossref] [Google Scholar]
  77. Libby E, Conlin PL, Kerr B, Ratcliff WC. 2016.. Stabilizing multicellularity through ratcheting. . Philos. Trans. R. Soc. B 371:(1701):20150444
    [Crossref] [Google Scholar]
  78. Libby E, Ratcliff WC. 2014.. Ratcheting the evolution of multicellularity. . Science 346:(6208):42627
    [Crossref] [Google Scholar]
  79. Litviňuková M, Talavera-López C, Maatz H, Reichart D, Worth CL, et al. 2020.. Cells of the adult human heart. . Nature 588:(7838):46672
    [Crossref] [Google Scholar]
  80. Love AC, Wagner GP. 2022.. Co-option of stress mechanisms in the origin of evolutionary novelties. . Evolution 76:(3):394413
    [Crossref] [Google Scholar]
  81. Lynch M. 2007.. The frailty of adaptive hypotheses for the origins of organismal complexity. . PNAS 104:(Suppl. 1):8597604
    [Crossref] [Google Scholar]
  82. Mackie GO. 1999.. Coelenterate organs. . Mar. Freshw. Behav. Physiol. 32:(2–3):11327
    [Crossref] [Google Scholar]
  83. Mah JL, Dunn CW. 2023.. Reconstructing cell type evolution across species through cell phylogenies of single-cell RNAseq data. . bioRxiv 2023.05.18.541372. https://doi.org/10.1101/2023.05.18.541372
  84. Makki R, Cinnamon E, Gould AP. 2014.. The development and functions of oenocytes. . Annu. Rev. Entomol. 59::40525
    [Crossref] [Google Scholar]
  85. Marais DLD, Rausher MD. 2008.. Escape from adaptive conflict after duplication in an anthocyanin pathway gene. . Nature 454:(7205):76265
    [Crossref] [Google Scholar]
  86. Marshall WF. 2020.. Pattern formation and complexity in single cells. . Curr. Biol. 30:(10):R54452
    [Crossref] [Google Scholar]
  87. McShea DW. 2002.. A complexity drain on cells in the evolution of multicellularity. . Evolution 56:(3):44152
    [Google Scholar]
  88. Michod RE. 1999.. Darwinian Dynamics: Evolutionary Transitions in Fitness and Individuality. Princeton, NJ:: Princeton Univ. Press
    [Google Scholar]
  89. Michod RE. 2007.. Evolution of individuality during the transition from unicellular to multicellular life. . PNAS 104:(Suppl. 1):861318
    [Crossref] [Google Scholar]
  90. Mikhailov KV, Konstantinova AV, Nikitin MA, Troshin PV, Rusin LY, et al. 2009.. The origin of Metazoa: a transition from temporal to spatial cell differentiation. . BioEssays 31:(7):75868
    [Crossref] [Google Scholar]
  91. Minelli A. 2021.. On the nature of organs and organ systems – a chapter in the history and philosophy of biology. . Front. Ecol. Evol. 9::745564
    [Crossref] [Google Scholar]
  92. Moor AE, Harnik Y, Ben-Moshe S, Massasa EE, Rozenberg M, et al. 2018.. Spatial reconstruction of single enterocytes uncovers broad zonation along the intestinal villus axis. . Cell 175:(4):115667.e15
    [Crossref] [Google Scholar]
  93. Moreau MX, Saillour Y, Elorriaga V, Bouloudi B, Delberghe E, et al. 2023.. Repurposing of the multiciliation gene regulatory network in fate specification of Cajal-Retzius neurons. . Dev. Cell 58:(15):136582.e6
    [Crossref] [Google Scholar]
  94. Moriano J, Leonardi O, Vitriolo A, Testa G, Boeckx C. 2023.. A multi-layered integrative analysis reveals a cholesterol metabolic program in outer radial glia with implications for human brain evolution. . bioRxiv 2023.06.23.546307. https://doi.org/10.1101/2023.06.23.546307
  95. Muñoz-Gómez SA, Bilolikar G, Wideman JG, Geiler-Samerotte K. 2021.. Constructive neutral evolution 20 years later. . J. Mol. Evol. 89:(3):17282
    [Crossref] [Google Scholar]
  96. Murphy DP, Hughes AE, Lawrence KA, Myers CA, Corbo JC. 2019.. Cis-regulatory basis of sister cell type divergence in the vertebrate retina. . eLife 8::e48216
    [Crossref] [Google Scholar]
  97. Nagy LG, Kovács GM, Krizsán K. 2018.. Complex multicellularity in fungi: evolutionary convergence, single origin, or both?. Biol. Rev. 93:(4):177894
    [Crossref] [Google Scholar]
  98. Najle SR, Grau-Bové X, Elek A, Navarrete C, Cianferoni D, et al. 2023.. Stepwise emergence of the neuronal gene expression program in early animal evolution. . Cell 186:(21):467693.e29
    [Crossref] [Google Scholar]
  99. 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):95163
    [Crossref] [Google Scholar]
  100. Nilsson D-E. 2009.. The evolution of eyes and visually guided behaviour. . Philos. Trans. R. Soc. B 364:(1531):283347
    [Crossref] [Google Scholar]
  101. Nordstrom K, Wallén R, Seymour J, Nilsson D. 2003.. A simple visual system without neurons in jellyfish larvae. . Proc. R. Soc. B 270:(1531):234954
    [Crossref] [Google Scholar]
  102. Oakley TH, Speiser DI. 2012.. How complexity originates: the evolution of animal eyes. . Annu. Rev. Ecol. Evol. Syst. 46::23760
    [Crossref] [Google Scholar]
  103. Ogawa Y, Corbo JC. 2021.. Partitioning of gene expression among zebrafish photoreceptor subtypes. . Sci. Rep. 11:(1):17340
    [Crossref] [Google Scholar]
  104. Ohno S. 1970.. Evolution by Gene Duplication. Berlin:: Springer
    [Google Scholar]
  105. Okasha S. 2005.. Multilevel selection and the major transitions in evolution. . Philos. Sci. 72:(5):101325
    [Crossref] [Google Scholar]
  106. Olson EN. 2006.. Gene regulatory networks in the evolution and development of the heart. . Science 313:(5795):192227
    [Crossref] [Google Scholar]
  107. Oteiza P, Baldwin MW. 2021.. Evolution of sensory systems. . Curr. Opin. Neurobiol. 71::5259
    [Crossref] [Google Scholar]
  108. Parker J. 2017.. Staphylinids. . Curr. Biol. 27:(2):R4951
    [Crossref] [Google Scholar]
  109. Post Y, Puschhof J, Beumer J, Kerkkamp HM, de Bakker MAG, et al. 2020.. Snake venom gland organoids. . Cell 180:(2):23347.e21
    [Crossref] [Google Scholar]
  110. Randel N, Jékely G. 2016.. Phototaxis and the origin of visual eyes. . Philos. Trans. R. Soc. B 371:( 1685.):20150042
    [Crossref] [Google Scholar]
  111. Ribeiro JMC. 1995.. Insect saliva: function, biochemistry, and physiology. . In Regulatory Mechanisms in Insect Feeding, ed. RF Chapman, G de Boer , pp. 7497. Boston:: Springer
    [Google Scholar]
  112. Ros-Rocher N, Pérez-Posada A, Leger MM, Ruiz-Trillo I. 2021.. The origin of animals: an ancestral reconstruction of the unicellular-to-multicellular transition. . Open Biol. 11:(2):200359
    [Crossref] [Google Scholar]
  113. Roy R, Schmitt AJ, Thomas JB, Carter CJ. 2017.. Nectar biology: from molecules to ecosystems. . Plant Sci. 262::14864
    [Crossref] [Google Scholar]
  114. Rueffler C, Hermisson J, Wagner GP. 2012.. Evolution of functional specialization and division of labor. . PNAS 109:(6):E32635
    [Crossref] [Google Scholar]
  115. Schmidt-Rhaesa A. 2007.. The Evolution of Organ Systems. Oxford, UK:: Oxford Univ. Press
    [Google Scholar]
  116. Shafer MER, Sawh AN, Schier AF. 2022.. Gene family evolution underlies cell-type diversification in the hypothalamus of teleosts. . Nat. Ecol. Evol. 6:(1):6376
    [Crossref] [Google Scholar]
  117. Shields VDC. 2004.. Ultrastructure of insect sensilla. . In Encyclopedia of Entomology, ed. JL Capinera , pp. 240820. Dordrecht, Neth:.: Springer
    [Google Scholar]
  118. Shoval O, Sheftel H, Shinar G, Hart Y, Ramote O, et al. 2012.. Evolutionary trade-offs, Pareto optimality, and the geometry of phenotype space. . Science 336:(6085):115760
    [Crossref] [Google Scholar]
  119. Smith JM, Szathmáry E. 1997.. The Major Transitions in Evolution. Oxford, UK:: Oxford Univ. Press
    [Google Scholar]
  120. Specht CD, Bartlett ME. 2009.. Flower evolution: the origin and subsequent diversification of the angiosperm flower. . Annu. Rev. Ecol. Evol. Syst. 40::21743
    [Crossref] [Google Scholar]
  121. Steidle JLM, Dettner K. 1993.. Chemistry and morphology of the tergal gland of freeliving adult Aleocharinae (Coleoptera: Staphylinidae) and its phylogenetic significance. . Syst. Entomol. 18:(2):14968
    [Crossref] [Google Scholar]
  122. Stoltzfus A. 1999.. On the possibility of constructive neutral evolution. . J. Mol. Evol. 49:(2):16981
    [Crossref] [Google Scholar]
  123. Surm JM, Moran Y. 2021.. Insights into how development and life-history dynamics shape the evolution of venom. . EvoDevo 12:(1):1
    [Crossref] [Google Scholar]
  124. Suzuki Y, Obara T, Takiya S, Hui C, Matsuno K, et al. 1990.. Differential transcription of the fibroin and sericin-1 genes in cell-free extracts. . Dev. Growth Differ. 32:(2):17987
    [Crossref] [Google Scholar]
  125. Swart CC, Deaton LE, Felgenhauer BE. 2006.. The salivary gland and salivary enzymes of the giant waterbugs (Heteroptera; Belostomatidae). . Comp. Biochem. Physiol. Part A 145:(1):11422
    [Crossref] [Google Scholar]
  126. Szathmáry E. 2015.. Toward major evolutionary transitions theory 2.0. . PNAS 112:(33):1010411
    [Crossref] [Google Scholar]
  127. Szövényi P, Waller M, Kirbis A. 2018.. Evolution of the plant body plan. . Curr. Top. Dev. Biol. 131::134
    [Google Scholar]
  128. Thayer MK. 2005.. Staphylinidae Latreille, 1802. . In Handbook of Zoology, Vol. IV (Arthropoda: Insecta), Part 38 Coleoptera, Beetles. Volume 1: Morphology and Systematics (Archostemata, Adephaga, Myxophaga, Polyphaga Partim), ed. RG Beutel, RAB Leschen , pp. 296344. Berlin:: de Gruyter
    [Google Scholar]
  129. Tosches MA. 2017.. Developmental and genetic mechanisms of neural circuit evolution. . Dev. Biol. 431:(1):1625
    [Crossref] [Google Scholar]
  130. Tosches MA, Yamawaki TM, Naumann RK, Jacobi AA, Tushev G, Laurent G. 2018.. Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. . Science 360:(6391):eaar4237
    [Crossref] [Google Scholar]
  131. Undheim EAB, Hamilton BR, Kurniawan ND, Bowlay G, Cribb BW, et al. 2015.. Production and packaging of a biological arsenal: evolution of centipede venoms under morphological constraint. . PNAS 112:(13):402631
    [Crossref] [Google Scholar]
  132. van der Kooi CJ, Stavenga DG, Arikawa K, Belušič G, Kelber A. 2020.. Evolution of insect color vision: from spectral sensitivity to visual ecology. . Annu. Rev. Entomol. 66::43561
    [Crossref] [Google Scholar]
  133. Vanlandewijck M, He L, Mäe MA, Andrae J, Ando K, et al. 2018.. A molecular atlas of cell types and zonation in the brain vasculature. . Nature 554:(7693):47580
    [Crossref] [Google Scholar]
  134. Wagner GJ. 1991.. Secreting glandular trichomes: more than just hairs. . Plant Physiol. 96:(3):67579
    [Crossref] [Google Scholar]
  135. Walker AA, Mayhew ML, Jin J, Herzig V, Undheim EAB, et al. 2018.. The assassin bug Pristhesancus plagipennis produces two distinct venoms in separate gland lumens. . Nat. Commun. 9:(1):755
    [Crossref] [Google Scholar]
  136. West SA, Cooper GA. 2016.. Division of labour in microorganisms: an evolutionary perspective. . Nat. Rev. Microbiol. 14:(11):71623
    [Crossref] [Google Scholar]
  137. West SA, Fisher RM, Gardner A, Kiers ET. 2015.. Major evolutionary transitions in individuality. . PNAS 112:(33):1011219
    [Crossref] [Google Scholar]
  138. Xiao N, Xu S, Li Z-K, Tang M, Mao R, et al. 2023.. A single photoreceptor splits perception and entrainment by cotransmission. . Nature 623:(7987):56270
    [Crossref] [Google Scholar]
  139. Yang X, Poelmans W, Grones C, Lakehal A, Pevernagie J, et al. 2023.. Spatial transcriptomics of a lycophyte root sheds light on root evolution. . Curr. Biol. 33:(19):406984.e8
    [Crossref] [Google Scholar]
  140. Yanni D, Jacobeen S, Márquez-Zacarías P, Weitz JS, Ratcliff WC, Yunker PJ. 2020.. Topological constraints in early multicellularity favor reproductive division of labor. . eLife 9::e54348
    [Crossref] [Google Scholar]
  141. Zancolli G, Casewell NR. 2020.. Venom systems as models for studying the origin and regulation of evolutionary novelties. . Mol. Biol. Evol. 37:(10):277790
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-cellbio-111822-121620
Loading
/content/journals/10.1146/annurev-cellbio-111822-121620
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error