Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Review article
  • Published:

Evolution of central neural circuits: state of the art and perspectives

Nature Reviews Neuroscience volume 23, pages 725–743 (2022)Cite this article

Subjects

Abstract

The wide variety of animal behaviours that can be observed today arose through the evolution of their underlying neural circuits. Advances in understanding the mechanisms through which neural circuits change over evolutionary timescales have lagged behind our knowledge of circuit function and development. This is particularly true for central neural circuits, which are experimentally less accessible than peripheral circuit elements. However, recent technological developments — including cross-species genetic modifications, connectomics and transcriptomics — have facilitated comparative neuroscience studies with a mechanistic outlook. These advances enable knowledge from two classically separate disciplines — neuroscience and evolutionary biology — to merge, accelerating our understanding of the principles of neural circuit evolution. Here we synthesize progress on this topic, focusing on three aspects of neural circuits that change over evolutionary time: synaptic connectivity, neuromodulation and neurons. By drawing examples from a wide variety of animal phyla, we reveal emerging principles of neural circuit evolution.

This is a preview of subscription content, access via your institution

Access options

Buy this article

  • Purchase on Springer Link
  • Instant access to full article PDF
Buy now

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: Overview of evolutionary forces and outcomes.
Fig. 2: Evolution of neural circuits through connectivity changes.
Fig. 3: Evolution of neural circuits through changes in neuromodulation.
Fig. 4: Evolution of neuronal circuits through changes in neuronal physiology.
Fig. 5: Evolution through changes in neuron number.

Similar content being viewed by others

References

  1. Knudsen, E. I. & Konishi, M. Mechanisms of sound localization in the barn owl (Tyto alba). J. Comp. Physiol. 133, 13–21 (1979).

    Article  Google Scholar 

  2. Sperry, R. W. Effect of 180 degree rotation of the retinal field on visuomotor coordination. J. Exp. Zool. 92, 263–279 (1943).

    Article  Google Scholar 

  3. Laurent, G. On the value of model diversity in neuroscience. Nat. Rev. Neurosci. 21, 395–396 (2020).

    Article  CAS  PubMed  Google Scholar 

  4. Seeholzer, L. F., Seppo, M., Stern, D. L. & Ruta, V. Evolution of a central neural circuit underlies Drosophila mate preferences. Nature 559, 564–569 (2018). Landmark article showing that species-specific pheromone responses can emerge through conservation of peripheral sensory neuron responses and changes in central circuitry.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Ding, Y., Berrocal, A., Morita, T., Longden, K. D. & Stern, D. L. Natural courtship song variation caused by an intronic retroelement in an ion channel gene. Nature 536, 329–332 (2016).

    Article  CAS  PubMed  Google Scholar 

  6. Ding, Y. et al. Neural evolution of context-dependent fly song. Curr. Biol. 29, 1089–1099.e7 (2019). Quantitative trait locus study identifying the genetic bases of divergence in courtship songs between two Drosophila species.

    Article  CAS  PubMed  Google Scholar 

  7. Elipot, Y. et al. A mutation in the enzyme monoamine oxidase explains part of the Astyanax cavefish behavioural syndrome. Nat. Commun. 5, 3647 (2014).

    Article  PubMed  Google Scholar 

  8. Yoshizawa, M., Gorički, Š., Soares, D. & Jeffery, W. R. Evolution of a behavioral shift mediated by superficial neuromasts helps cavefish find food in darkness. Curr. Biol. 20, 1631–1636 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Alié, A. et al. Developmental evolution of the forebrain in cavefish, from natural variations in neuropeptides to behavior. Elife 7, e32808 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  10. Newcomb, J. M., Sakurai, A., Lillvis, J. L., Gunaratne, C. A. & Katz, P. S. Homology and homoplasy of swimming behaviors and neural circuits in the Nudipleura (Mollusca, Gastropoda, Opisthobranchia). Proc. Natl Acad. Sci. USA 109, 10669–10676 (2012). Review article on the evolution of swimming circuits in nudibranchs.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Prieto-Godino, L. L. et al. Evolution of acid-sensing olfactory circuits in drosophilids. Neuron 93, 661–676 (2017).

    Article  CAS  PubMed  Google Scholar 

  12. Prieto-Godino, L. L. et al. Olfactory receptor pseudo-pseudogenes. Nature 539, 93–97 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Auer, T. O. et al. Olfactory receptor and circuit evolution promote host specialization. Nature 579, 402–408 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Hart, N. S. Vision in sharks and rays: opsin diversity and colour vision. Semin. Cell Dev. Biol. 106, 12–19 (2020).

    Article  PubMed  Google Scholar 

  15. Yokoyama, S. & Yokoyama, R. Adaptive evolution of photoreceptors and visual pigments in vertebrates. Annu. Rev. Ecol. Syst. 27, 543–567 (1996).

    Article  Google Scholar 

  16. Prieto-Godino, L. L., Schmidt, H. R. & Benton, R. Molecular reconstruction of recurrent evolutionary switching in olfactory receptor specificity. Elife 10, 69732 (2021).

    Article  Google Scholar 

  17. Baldwin, M. W. et al. Evolution of sweet taste perception in hummingbirds by transformation of the ancestral umami receptor. Science 345, 929–933 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  18. Marques, D. A. et al. Convergent evolution of SWS2 opsin facilitates adaptive radiation of threespine stickleback into different light environments. PLoS Biol. 15, e2001627 (2017).

    Article  PubMed  PubMed Central  Google Scholar 

  19. Bowmaker, J. K. Evolution of vertebrate visual pigments. Vis. Res. 48, 2022–2041 (2008).

    Article  CAS  PubMed  Google Scholar 

  20. Herron, J.C. & Freeman, S. Evolutionary Analysis 5th edn (Pearson Education, 2015).

  21. Futuyma, D. J. Evolution 3rd edn (Sinauer Associates, 2013).

  22. Lynch, M. & Hill, W. G. Phenotypic evolution by neutral mutation. Evolution 40, 915 (1986).

    Article  PubMed  Google Scholar 

  23. Zhang, J. Neutral theory and phenotypic evolution. Mol. Biol. Evol. 35, 1327–1331 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  24. Arguello, J. R. et al. Extensive local adaptation within the chemosensory system following Drosophila melanogaster’s global expansion. Nat. Commun. 7, 11855 (2016).

    Article  Google Scholar 

  25. Long, M., Betrán, E., Thornton, K. & Wang, W. The origin of new genes: glimpses from the young and old. Nat. Rev. Genet. 4, 865–875 (2003).

    Article  CAS  PubMed  Google Scholar 

  26. Long, M., Vankuren, N. W., Chen, S. & Vibranovski, M. D. New gene evolution: little did we know. Annu. Rev. Genet. 47, 307–333 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Lynch, M. & Conery, J. S. The evolutionary fate and consequences of duplicate genes. Science 290, 1151–1155 (2000).

    Article  CAS  PubMed  Google Scholar 

  28. Pollen, A. A. et al. Establishing cerebral organoids as models of human-specific brain evolution. Cell 176, 743–756 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Tosches, M. A. Developmental and genetic mechanisms of neural circuit evolution. Dev. Biol. 431, 16–25 (2017).

    Article  CAS  PubMed  Google Scholar 

  30. Suryanarayana, S. M., Pérez-Fernández, J., Robertson, B. & Grillner, S. The evolutionary origin of visual and somatosensory representation in the vertebrate pallium. Nat. Ecol. Evol. 4, 639–651 (2020).

    Article  PubMed  Google Scholar 

  31. Chakraborty, M. & Jarvis, E. D. Brain evolution by brain pathway duplication. Philos. Trans. R. Soc. B Biol. Sci. 370, 20150056 (2015).

    Article  Google Scholar 

  32. Arendt, D. The evolution of cell types in animals: emerging principles from molecular studies. Nat. Rev. Genet. 9, 868–882 (2008).

    Article  CAS  PubMed  Google Scholar 

  33. Nilsson, D.-E. & Arendt, D. Eye evolution: the blurry beginning. Curr. Biol. 18, 1096–1098 (2008).

    Article  Google Scholar 

  34. Silbering, A. F. et al. Complementary function and integrated wiring of the evolutionarily distinct Drosophila olfactory subsystems. J. Neurosci. 31, 13357–13375 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Couto, A., Alenius, M. & Dickson, B. J. Molecular, anatomical, and functional organization of the Drosophila olfactory system. Curr. Biol. 15, 1535–1547 (2005).

    Article  CAS  PubMed  Google Scholar 

  36. Ramdya, P. & Benton, R. Evolving olfactory systems on the fly. Trends Genet. 26, 307–316 (2010).

    Article  CAS  PubMed  Google Scholar 

  37. Sukhum, K. V., Shen, J. & Carlson, B. A. Extreme enlargement of the cerebellum in a clade of teleost fishes that evolved a novel active sensory system. Curr. Biol. 28, 3857–3863.e3 (2018).

    Article  CAS  PubMed  Google Scholar 

  38. Marder, E. & Prinz, A. A. Modeling stability in neuron and network function: the role of activity in homeostasis. Bioessays 24, 1145–1154 (2002).

    Article  CAS  PubMed  Google Scholar 

  39. McLennan, D. A. The concept of co-option: why evolution often looks miraculous. Evol. Educ. Outreach 1, 247–258 (2008).

    Article  Google Scholar 

  40. Chapman, P. D. et al. Co-option of a motor-to-sensory histaminergic circuit correlates with insect flight biomechanics. Proc. R. Soc. B Biol. Sci. 284, 20170339 (2017).

    Article  Google Scholar 

  41. Fischer, E. K. et al. Mechanisms of convergent egg provisioning in poison frogs. Curr. Biol. 29, 4145–4151.e3 (2019). Study on poison frogs showing that two different species evolved egg provisioning convergently by independently recruiting the same brain area — the preoptic area — but that the activity patterns in this area are different across the two species.

    Article  CAS  PubMed  Google Scholar 

  42. Tosches, M. A. et al. Evolution of pallium, hippocampus, and cortical cell types revealed by single-cell transcriptomics in reptiles. Science 360, 881–888 (2018).

    Article  CAS  PubMed  Google Scholar 

  43. Colquitt, B. M., Merullo, D. P., Konopka, G., Roberts, T. F. & Brainard, M. S. Cellular transcriptomics reveals evolutionary identities of songbird vocal circuits. Science 371, eabd9704 (2021). Single-cell transcriptomics study of the songbird motor pathway suggesting that the mammalian neocortex and the dorsal ventricular ridge of birds and reptiles are not homologous.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. Storz, J. F. Causes of molecular convergence and parallelism in protein evolution. Nat. Rev. Genet. 17, 239–250 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  45. Magalhaes, I. S. et al. Intercontinental genomic parallelism in multiple three-spined stickleback adaptive radiations. Nat. Ecol. Evol. 5, 251–261 (2021).

    Article  PubMed  Google Scholar 

  46. Stuart, Y. E. Divergent uses of “parallel evolution” during the history of The American Naturalist. Am. Nat. 193, 11–19 (2019).

    Article  PubMed  Google Scholar 

  47. Arendt, J. & Reznick, D. Convergence and parallelism reconsidered: what have we learned about the genetics of adaptation? Trends Ecol. Evol. 23, 26–32 (2008).

    Article  PubMed  Google Scholar 

  48. Elmer, K. R. & Meyer, A. Adaptation in the age of ecological genomics: Insights from parallelism and convergence. Trends Ecol. Evol. 26, 298–306 (2011).

    Article  PubMed  Google Scholar 

  49. Torres-Méndez, A. et al. Parallel evolution of a splicing program controlling neuronal excitability in flies and mammals. Sci. Adv. 8, eabk0445 (2022).

    Article  PubMed  PubMed Central  Google Scholar 

  50. Bumbarger, D. J., Riebesell, M., Rödelsperger, C. & Sommer, R. J. System-wide rewiring underlies behavioral differences in predatory and bacterial-feeding nematodes. Cell 152, 109–119 (2013). Electron microscopy-based connectomic reconstruction of the motor pharyngeal system of the nematode P. pacificus and comparison with that of C. elegans. The study reveals extensive rewiring of homologous neurons across the two species.

    Article  CAS  PubMed  Google Scholar 

  51. Hong, R. L. et al. Evolution of neuronal anatomy and circuitry in two highly divergent nematode species. Elife 8, e47155 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  52. Cook, S. J., Crouse, C. M., Hall, D. H., Emmons, S. W. & Hobert, O. The connectome of the Caenorhabditis elegans pharynx. J. Comp. Neurol. 528, 2767–2784 (2020).

  53. Suzuki, H. et al. Functional asymmetry in Caenorhabditis elegans taste neurons and its computational role in chemotaxis. Nature 454, 114–117 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Johnston, R. J. & Hobert, O. A microRNA controlling left/right neuronal asymmetry in Caenorhabditis elegans. Nature 426, 845–849 (2003).

    Article  CAS  PubMed  Google Scholar 

  55. Chesmore, K. N., Bartlett, J., Cheng, C. & Williams, S. M. Complex patterns of association between pleiotropy and transcription factor evolution. Genome Biol. Evol. 8, 3159–3170 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  56. Pérez-Escudero, A. & De Polavieja, G. G. Optimally wired subnetwork determines neuroanatomy of Caenorhabditis elegans. Proc. Natl Acad. Sci. USA 104, 1–6 (2007).

    Article  Google Scholar 

  57. Chen, B. L., Hall, D. H. & Chklovskii, D. B. Wiring optimization can relate neuronal structure and function. Proc. Natl Acad. Sci. USA 103, 4723–4728 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Barabási, D. L. & Barabási, A. L. A genetic model of the connectome. Neuron 105, 435–445 (2020).

    Article  PubMed  Google Scholar 

  59. Seth, R. et al. Molecular topography of an entire nervous system. Cell 184, 4329–4347.e23 (2021).

    Article  Google Scholar 

  60. Auer, T. O. & Benton, R. Sexual circuitry in Drosophila. Curr. Opin. Neurobiol. 38, 18–26 (2016).

    Article  CAS  PubMed  Google Scholar 

  61. Ahmed, O. M. et al. Evolution of mechanisms that control mating in Drosophila males. Cell Rep. 27, 2527–2536.e4 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  62. Fan, P. et al. Genetic and neural mechanisms that inhibit Drosophila from mating with other species. Cell 154, 89–102 (2013).

    Article  CAS  PubMed  Google Scholar 

  63. Khallaf, M. A. et al. Mate discrimination among subspecies through a conserved olfactory pathway. Sci. Adv. 6, eaba5279 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Hong, W., Mosca, T. J. & Luo, L. Teneurins instruct synaptic partner matching in an olfactory map. Nature 484, 1–9 (2012).

    Article  Google Scholar 

  65. Martin-Pena, A. et al. Age-independent synaptogenesis by phosphoinositide 3 kinase. J. Neurosci. 26, 10199–10208 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Fossati, M. et al. SRGAP2 and its human-specific paralog co-regulate the development of excitatory and inhibitory synapses. Neuron 91, 356–369 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Schmidt, E. R. E. et al. A human-specific modifier of cortical connectivity and circuit function. Nature 599, 640–644 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  68. Charrier, C. et al. Inhibition of SRGAP2 function by its human-specific paralogs induces neoteny during spine maturation. Cell 149, 923–935 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  69. Tosches, M. A. & Laurent, G. Evolution of neuronal identity in the cerebral cortex. Curr. Opin. Neurobiol. 56, 199–208 (2019).

    Article  CAS  PubMed  Google Scholar 

  70. Bakken, T. E. et al. Comparative cellular analysis of motor cortex in human, marmoset and mouse. Nature 598, 111–119 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  71. Krienen, F. M. et al. Innovations present in the primate interneuron repertoire. Nature 586, 262–269 (2020). Single-cell transcriptomics study of the neocortex, hippocampus and striatum of ferrets, mice, marmosets, macaques and humans. The study uncovers a human-specific cell type.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  72. Baden, T. Vertebrate vision: lessons from non-model species. Semin. Cell Dev. Biol. 106, 1–4 (2020). Editorial in a special issue on the evolution of retinal circuits across vertebrates.

    Article  PubMed  Google Scholar 

  73. Schwartz, G. Retinal Computation (Elsevier, 2021).

  74. Kim, T., Shen, N., Hsiang, J. C., Johnson, K. P. & Kerschensteiner, D. Dendritic and parallel processing of visual threats in the retina control defensive responses. Sci. Adv. 6, eabc9920 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  75. Kölsch, Y. et al. Molecular classification of zebrafish retinal ganglion cells links genes to cell types to behavior. Neuron 109, 645–662 (2021).

    Article  PubMed  Google Scholar 

  76. Yoshimatsu, T., Schröder, C., Nevala, N. E., Berens, P. & Baden, T. Fovea-like photoreceptor specializations underlie single UV cone driven prey-capture behavior in zebrafish. Neuron 107, 320–337.e6 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  77. Ding, H., Smith, R. G., Poleg-Polsky, A., Diamond, J. S. & Briggman, K. L. Species-specific wiring for direction selectivity in the mammalian retina. Nature 535, 105–110 (2016). Study in mice and rabbits showing that their retinal direction selectivity circuits are differentially wired in a way that compensates for the different eye sizes of the two species.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  78. Baden, T. & Osorio, D. The retinal basis of vertebrate color vision. Annu. Rev. Vis. Sci. 5, 177–200 (2019).

    Article  CAS  PubMed  Google Scholar 

  79. Lamb, T. D., Collin, S. P. & Pugh, E. N. Evolution of the vertebrate eye: opsins, photoreceptors, retina and eye cup. Nat. Rev. Neurosci. 8, 960–976 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  80. Nilsson, D. E. The diversity of eyes and vision. Annu. Rev. Vis. Sci. 7, 19–41 (2021).

    Article  PubMed  Google Scholar 

  81. Yoshimatsu, T. et al. Ancestral circuits for vertebrate color vision emerge at the first retinal synapse. Sci. Adv. 7, eabj6815 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Euler, T., Haverkamp, S., Schubert, T. & Baden, T. Retinal bipolar cells: elementary building blocks of vision. Nat. Rev. Neurosci. 15, 507–519 (2014).

    Article  CAS  PubMed  Google Scholar 

  83. Yamagata, M., Yan, W. & Sanes, J. R. A cell atlas of the chick retina based on single-cell transcriptomics. Elife 10, e63907 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  84. Sakurai, A. & Katz, P. S. Artificial synaptic rewiring demonstrates that distinct neural circuit configurations underlie homologous behaviors. Curr. Biol. 27, 1721–1734.e3 (2017). Study suggesting that homologous circuits for swimming behaviour in two nudibranch species evolved through neuronal drift.

    Article  CAS  PubMed  Google Scholar 

  85. Jing, J. & Gillette, R. Central pattern generator for escape swimming in the notaspid sea slug Pleurobranchaea californica. J. Neurophysiol. 81, 654–667 (1999).

    Article  CAS  PubMed  Google Scholar 

  86. Gunaratne, C. A., Sakurai, A. & Katz, P. S. Variations on a theme: species differences in synaptic connectivity do not predict central pattern generator activity. J. Neurophysiol. 118, 1123–1132 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  87. Borst, A. & Euler, T. Seeing things in motion: models, circuits, and mechanisms. Neuron 71, 974–994 (2011).

    Article  CAS  PubMed  Google Scholar 

  88. Kim, Y. J. et al. Origins of direction selectivity in the primate retina. Nat. Commun. 13, 2862 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  89. Patterson, S. S. et al. Conserved circuits for direction selectivity in the primate retina. Curr. Biol. 32, 2529–2538 (2022).

    Article  CAS  PubMed  Google Scholar 

  90. Johnson, B. R., Peck, J. H. & Harris-Warrick, R. M. Differential modulation of chemical and electrical components of mixed synapses in the lobster stomatogastric ganglion. J. Comp. Physiol. A 175, 233–249 (1994).

    Article  CAS  PubMed  Google Scholar 

  91. Katz, P. S. & Lillvis, J. L. Reconciling the deep homology of neuromodulation with the evolution of behavior. Curr. Opin. Neurobiol. 29, 39–47 (2014).

    Article  CAS  PubMed  Google Scholar 

  92. Bendesky, A. & Bargmann, C. I. Genetic contributions to behavioural diversity at the gene–environment interface. Nat. Rev. Genet. 12, 809–820 (2011).

    Article  CAS  PubMed  Google Scholar 

  93. Lim, M. M. et al. Enhanced partner preference in a promiscuous species by manipulating the expression of a single gene. Nature 429, 754–757 (2004).

    Article  CAS  PubMed  Google Scholar 

  94. Young, L. J., Nilsen, R., Waymire, K. G., MacGregor, G. R. & Insel, T. R. Increased affiliative response to vasopressin in mice expressing the V1a receptor from a monogamous vole. Nature 400, 766–768 (1999).

    Article  CAS  PubMed  Google Scholar 

  95. Bendesky, A. et al. The genetic basis of parental care evolution in monogamous mice. Nature 544, 434–439 (2017). Quantitative trait locus study investigating the genetic bases of parental care in mice. The study uncovers the role of AVP in the evolution of nest-building behaviour.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Elipot, Y., Hinaux, H., Callebert, J. & Rétaux, S. Evolutionary shift from fighting to foraging in blind cavefish through changes in the serotonin network. Curr. Biol. 23, 1–10 (2013).

    Article  CAS  PubMed  Google Scholar 

  97. Jaggard, J. B. et al. Hypocretin underlies the evolution of sleep loss in the Mexican cavefish. Elife 7, e32637 (2018).

    Article  PubMed  PubMed Central  Google Scholar 

  98. Duboué, E. R., Borowsky, R. L. & Keene, A. C. β-adrenergic signaling regulates evolutionarily derived sleep loss in the Mexican cavefish. Brain. Behav. Evol. 80, 233–243 (2012).

    Article  PubMed  Google Scholar 

  99. Shafer, M. E. R., Sawh, A. N. & Schier, A. F. Gene family evolution underlies cell-type diversification in the hypothalamus of teleosts. Nat. Ecol. Evol. 6, 63–76 (2022). Single-cell transcriptomics study comparing the hypothalamus of zebrafish with that of surface and cave forms of Mexican tetra. The findings suggest that in homologous cell types, terminal differentiation genes can remain conserved while the underlying transcription factor regulatory network evolves.

    Article  PubMed  Google Scholar 

  100. Barkan, C. L., Kelley, D. B. & Zornik, E. Premotor neuron divergence reflects vocal evolution. J. Neurosci. 38, 5325–5337 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Barkan, C. L., Zornik, E. & Kelley, D. B. Evolution of vocal patterns: tuning hindbrain circuits during species divergence. J. Exp. Biol. 220, 856–867 (2017).

    PubMed  PubMed Central  Google Scholar 

  102. Carlson, B. A. & Gallant, J. R. From sequence to spike to spark: evo-devo-neuroethology of electric communication in mormyrid fishes. J. Neurogenet. 27, 106–129 (2013).

    Article  PubMed  Google Scholar 

  103. Osborne, K. A. et al. Natural behavior polymorphism due to a cGMP-dependent protein kinase of Drosophila. Science 277, 834–836 (1997).

    Article  CAS  PubMed  Google Scholar 

  104. Renger, J. J., Yao, W. D., Sokolowski, M. B. & Wu, C. F. Neuronal polymorphism among natural alleles of a cGMP-dependent kinase gene, foraging, in Drosophila. J. Neurosci. 19, RC28 (1999).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  105. Fitzpatrick, M. J., Feder, E., Rowe, L. & Sokolowski, M. B. Maintaining a behaviour polymorphism by frequency-dependent selection on a single gene. Nature 447, 210–212 (2007).

    Article  CAS  PubMed  Google Scholar 

  106. Mery, F., Belay, A. T., So, A. K. C., Sokolowski, M. B. & Kawecki, T. J. Natural polymorphism affecting learning and memory in Drosophila. Proc. Natl Acad. Sci. USA 104, 13051–13055 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  107. Ben-Shahar, Y., Robichon, A., Sokolowski, M. B. & Robinson, G. E. Influence of gene action across different time scales on behavior. Science 296, 741–744 (2002).

    Article  CAS  PubMed  Google Scholar 

  108. Ingram, K. K., Oefner, P. & Gordon, D. M. Task-specific expression of the foraging gene in harvester ants. Mol. Ecol. 14, 813–818 (2005).

    Article  CAS  PubMed  Google Scholar 

  109. Hong, R. L., Witte, H. & Sommer, R. J. Natural variation in Pristionchus pacificus insect pheromone attraction involves the protein kinase EGL-4. Proc. Natl Acad. Sci. USA 105, 7779–7784 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Allen, A. M. & Sokolowski, M. B. Expression of the foraging gene in adult Drosophila melanogaster. J. Neurogenet. 35, 192–212 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Dason, J. S. & Sokolowski, M. B. A cGMP-dependent protein kinase, encoded by the Drosophila foraging gene, regulates neurotransmission through changes in synaptic structure and function. J. Neurogenet. 35, 213–220 (2021).

    Article  CAS  PubMed  Google Scholar 

  112. LaPotin, S. et al. Divergent cis-regulatory evolution underlies the convergent loss of sodium channel expression in electric fish. Sci. Adv. 8, eabm2970 (2022).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  113. Arnegard, M. E., Zwickl, D. J., Lu, Y. & Zakon, H. H. Old gene duplication facilitates origin and diversification of an innovative communication system - twice. Proc. Natl Acad. Sci. USA 107, 22172–22177 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  114. Liscovitch-Brauer, N. et al. Trade-off between transcriptome plasticity and genome evolution in cephalopods. Cell 169, 191–202 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  115. Wang, Z. Y. & Ragsdale, C. W. Cadherin genes and evolutionary novelties in the octopus. Semin. Cell Dev. Biol. 69, 151–157 (2017).

    Article  CAS  PubMed  Google Scholar 

  116. Lamb, T. D. Evolution of vertebrate retinal photoreception. Philos. Trans. R. Soc. B Biol. Sci. 364, 2911–2924 (2009).

    Article  CAS  Google Scholar 

  117. Baden, T. & Euler, T. Early vision: where (some of) the magic happens. Curr. Biol. 23, R1096–R1098 (2013).

    Article  CAS  PubMed  Google Scholar 

  118. Sinha, R. et al. Cellular and circuit mechanisms shaping the perceptual properties of the primate fovea. Cell 168, 413–426 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  119. Truman, J. W. & Ball, E. E. Patterns of embryonic neurogenesis in a primitive wingless insect, the silverfish, Ctenolepisma longicaudata: comparison with those seen in flying insects. Dev. Genes Evol. 208, 357–368 (1998).

    Article  CAS  PubMed  Google Scholar 

  120. LaMonica, B. E., Lui, J. H., Wang, X. & Kriegstein, A. R. OSVZ progenitors in the human cortex: an updated perspective on neurodevelopmental disease. Curr. Opin. Neurobiol. 22, 747–753 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. Florio, M. et al. Human-specific gene ARHGAP11B promotes basal progenitor amplification and neocortex expansion. Science 347, 1465–1470 (2015).

    Article  CAS  PubMed  Google Scholar 

  122. Florio, M., Namba, T., Paabo, S., Hiller, M. & Huttner, W. B. A single splice site mutation in human-specific ARHGAP11B causes basal progenitor amplification. Sci. Adv. 2, e1601941 (2016). Work performing ancestral molecular reconstruction of a hominid-specific gene and misexpressing it in mice to show that a single-nucleotide substitution in this gene in the human lineage conferred it with its current function in neuronal progenitor amplification.

    Article  PubMed  PubMed Central  Google Scholar 

  123. Pop, S. et al. Extensive and diverse patterns of cell death sculpt neural networks in insects. Elife 9, e59566 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Prieto-Godino, L. L. et al. Functional integration of “undead” neurons in the olfactory system. Sci. Adv. 6, eaaz7238 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Cayirlioglu, P. et al. Hybrid neurons in a microRNA mutant are putative evolutionary intermediates in insect CO2 sensory systems. Science 319, 1256–1260 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Prieto-Godino, L. L. L. L., Diegelmann, S. & Bate, M. Embryonic origin of olfactory circuitry in Drosophila: contact and activity-mediated interactions pattern connectivity in the antennal lobe. PLoS Biol. 10, e1001400 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  127. Willett, R. T. et al. Cerebellar nuclei excitatory neurons regulate developmental scaling of presynaptic Purkinje cell number and organ growth. Elife 8, e50617 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  128. Tierney, A. J. Evolutionary implications of neural circuit structure and function. Behav. Process. 35, 173–182 (1995).

    Article  CAS  Google Scholar 

  129. Cande, J., Prud’homme, B. & Gompel, N. Smells like evolution: the role of chemoreceptor evolution in behavioral change. Curr. Opin. Neurobiol. 23, 152–158 (2013).

    Article  CAS  PubMed  Google Scholar 

  130. Jacobs, G. H., Williams, G. A., Cahill, H. & Nathans, J. Emergence of novel color vision in mice engineered to express a human cone photopigment. Science 315, 1723–1725 (2007).

    Article  CAS  PubMed  Google Scholar 

  131. Frangeul, L. et al. A cross-modal genetic framework for the development and plasticity of sensory pathways. Nature 538, 96–98 (2016).

    Article  CAS  PubMed  Google Scholar 

  132. Ramdya, P. & Engert, F. Emergence of binocular functional properties in a monocular neural circuit. Nat. Neurosci. 11, 1083–1090 (2008).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  133. Ramaekers, A. et al. Altering the temporal regulation of one transcription factor drives evolutionary trade-offs between head sensory organs. Dev. Cell 50, 780–792 (2019).

    Article  CAS  PubMed  Google Scholar 

  134. Jourjine, N. & Hoekstra, H. E. Expanding evolutionary neuroscience: insights from comparing variation in behavior. Neuron 109, 1084–1099 (2021). Article that introduced the concept of ‘model clades’ for evolutionary neuroscience studies.

    Article  CAS  PubMed  Google Scholar 

  135. Herman, A. et al. The role of gene flow in rapid and repeated evolution of cave-related traits in Mexican tetra, Astyanax mexicanus. Mol. Ecol. 27, 4397–4416 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  136. Torres-Méndez, A. et al. A novel protein domain in an ancestral splicing factor drove the evolution of neural microexons. Nat. Ecol. Evol. 3, 691–701 (2019).

    Article  PubMed  Google Scholar 

  137. Lillvis, J. L. & Katz, P. S. Parallel evolution of serotonergic neuromodulation underlies independent evolution of rhythmic motor behavior. J. Neurosci. 33, 2709–2717 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  138. Euler, T. & Baden, T. Computational neuroscience: species-specific motion detectors. Nature 535, 45–46 (2016).

    Article  CAS  PubMed  Google Scholar 

  139. Loomis, C. et al. An adult brain atlas reveals broad neuroanatomical changes in independently evolved populations of Mexican cavefish. Front. Neuroanat. 13, 88 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  140. Zakon, H. H., Lu, Y., Zwickl, D. J. & Hillis, D. M. Sodium channel genes and the evolution of diversity in communication signals of electric fishes: convergent molecular evolution. Proc. Natl Acad. Sci. USA 103, 3675–3680 (2006).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  141. Lui, J. H., Hansen, D. V. & Kriegstein, A. R. Development and evolution of the human neocortex. Cell 46, 18–36 (2011).

    Article  Google Scholar 

  142. Haalck, L., Mangan, M., Webb, B. & Risse, B. Towards image-based animal tracking in natural environments using a freely moving camera. J. Neurosci. Methods 330, 108455 (2020).

    Article  PubMed  Google Scholar 

  143. Berck, M. E. et al. The wiring diagram of a glomerular olfactory system. Elife 5, e14859 (2016).

    Article  PubMed  PubMed Central  Google Scholar 

  144. Eichler, K. et al. The complete connectome of a learning and memory centre in an insect brain. Nature 548, 175–182 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  145. Mackay, T. F. C. C. et al. The Drosophila melanogaster genetic reference panel. Nature 482, 173–178 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  146. Brown, E. B., Layne, J. E., Zhu, C., Jegga, A. G. & Rollmann, S. M. Genome-wide association mapping of natural variation in odour-guided behaviour in Drosophila. Genes Brain Behav. 12, 503–515 (2013).

    Article  CAS  PubMed  Google Scholar 

  147. Harbison, S. T., McCoy, L. J. & Mackay, T. F. C. Genome-wide association study of sleep in Drosophila melanogaster. BMC Genomics 14, 281 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  148. Andersson, L. L. S. et al. Mutations in DMRT3 affect locomotion in horses and spinal circuit function in mice. Nature 488, 642–646 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  149. Chen, S. et al. Frequent recent origination of brain genes shaped the evolution of foraging behavior in Drosophila. Cell Rep. 1, 118–132 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  150. Capra, J. A., Erwin, G. D., Mckinsey, G., Rubenstein, J. L. R. & Pollard, K. S. Many human accelerated regions are developmental enhancers. Philos. Trans. R. Soc. B Biol. Sci. 368, 20130025 (2013).

    Article  Google Scholar 

  151. Pollard, K. S. et al. Forces shaping the fastest evolving regions in the human genome. PLoS Genet. 2, e168 (2006).

    Article  PubMed  PubMed Central  Google Scholar 

  152. Dennis, M. Y. et al. Evolution of human-specific neural SRGAP2 genes by incomplete segmental duplication. Cell 149, 912–922 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  153. Boyd, J. L. et al. Human-chimpanzee differences in a FZD8 enhancer alter cell-cycle dynamics in the developing neocortex. Curr. Biol. 16, 772–779 (2015).

    Article  Google Scholar 

  154. Kawecki, T. J. et al. Experimental evolution. Trends Ecol. Evol. 27, 547–560 (2012).

    Article  PubMed  Google Scholar 

  155. Mery, F. & Kawecki, T. J. Experimental evolution of learning ability in fruit flies. Proc. Natl Acad. Sci. USA 99, 14274–14279 (2002).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  156. Mackay, T. F. C. et al. Genetics and genomics of Drosophila mating behavior. Proc. Natl Acad. Sci. USA 102, 6622–6629 (2005).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  157. Jaksic, A. M. et al. Neuronal function and dopamine signaling evolve at high temperature in Drosophila. Mol. Biol. Evol. 37, 2630–2640 (2020).

    Article  CAS  PubMed  Google Scholar 

  158. Turner, T. L., Stewart, A. D., Fields, A. T., Rice, W. R. & Tarone, A. M. Population-based resequencing of experimentally evolved populations reveals the genetic basis of body size variation in Drosophila melanogaster. PLoS Genet. 7, e1001336 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  159. Versace, E. Experimental evolution, behavior and genetics: associative learning as a case study. Curr. Zool. 61, 226–241 (2015).

    Article  Google Scholar 

  160. Schlötterer, C., Kofler, R., Versace, E., Tobler, R. & Franssen, S. U. Combining experimental evolution with next-generation sequencing: a powerful tool to study adaptation from standing genetic variation. Heredity 114, 431–440 (2015).

    Article  PubMed  Google Scholar 

Download references

Acknowledgements

The authors thank T. Baden from the University of Sussex, R. Arguello from the University of Lausanne and J. L. Ramos from the L.L.P.-G. laboratory for discussions and comments on the manuscript. They thank J. Brock at the Francis Crick Institute for help with illustrations. R.J.V.R. is supported by a Boehringer Ingelheim Fonds Ph.D. fellowship. L.L.P.-G.’s laboratory is supported by a European Research Council Starting Investigator Grant (802531), an Allen Distinguished Investigator Award, a Human Frontiers Science Grant (RGY0052/2022) and the Francis Crick Institute, which receives its core funding from Cancer Research UK (FC001594), the UK Medical Research Council (FC001594) and the Wellcome Trust (FC001594).

Author information

Author notes

  1. These authors contributed equally: Ruairí J. V. Roberts, Sinziana Pop.

Authors and Affiliations

  1. The Francis Crick Institute, London, UK

    Ruairí J. V. Roberts, Sinziana Pop & Lucia L. Prieto-Godino

Authors
  1. Ruairí J. V. Roberts
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sinziana Pop
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Lucia L. Prieto-Godino
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

The authors contributed equally to all aspects of the article.

Corresponding author

Correspondence to Lucia L. Prieto-Godino.

Ethics declarations

Competing interests

The authors declare no competing interests.

Peer review

Peer review information

Nature Reviews Neuroscience thanks P. Katz and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Additional information

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Related links

Retinal Functomics: http://retinal-functomics.net/

Supplementary information

Glossary

Alleles

Different versions of a DNA sequence found in a particular genomic location.

Alternative splicing

The process that, during pre-mRNA processing, rearranges exons (coding sequences) and thus allows a single gene to encode multiple proteins.

Clades

Groups of organisms that are derived from a common ancestor.

Comparative studies

Research work where two or more species are compared side by side to identify differences between them.

Connectomics

The generation of comprehensive synaptic resolution maps of the connections among the neurons of an organism’s nervous system.

Corollary discharge

Internal activity generated by nervous systems that carries information about a motor command and is used to estimate the outcomes of executed movements (for example, to help distinguish between self-generated and externally induced sensory input).

Evolvability

Here, the ability of particular features of a system to facilitate change.

Extant species

Species that can be found alive today, as opposed to species that were extinguished at some time in the past.

Functomics

High-throughput investigation of neuronal circuit function.

Homologues

Structures that share a common ancestral origin.

Neural circuit blueprint

The assembly of characters that determine the general organization of a brain, including the number and/or type of neurons, organization of cell bodies and mesoscale connectivity.

Phylogenetic distances

The amounts of time that elapsed between the divergence of pairs of species from their most recent common ancestor.

Pleiotropy

The phenomenon in which a gene affects multiple unrelated phenotypic traits. In evolution, pleiotropy is considered to limit the potential for change because modifications in a gene could simultaneously affect one trait in an adaptive way but cause maladaptive changes in another.

RNA editing

The process that modifies specific nucleotides of RNAs potentially altering their function.

Retroelement

Genome sequences that can be transcribed into RNA, can be reverse transcribed into DNA and can be inserted at another genome location.

Single-cell transcriptomics

The study of the gene expression of individual cells.

Terminal differentiation genes

Genes that confer cellular properties through their function, rather than influencing the expression of other genes.

Transcription factor genes

Genes that function by regulating the expression of other genes.

Wiring economy theory

A theory that proposes that nervous systems have evolved to minimize neurite length to minimize the energetic cost of the maintenance of neuronal extensions.

Rights and permissions

Springer Nature or its licensor 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.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Roberts, R.J.V., Pop, S. & Prieto-Godino, L.L. Evolution of central neural circuits: state of the art and perspectives. Nat Rev Neurosci 23, 725–743 (2022). https://doi.org/10.1038/s41583-022-00644-y

Download citation

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41583-022-00644-y

This article is cited by

Search

Advanced search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing