Neuron numbers link innovativeness with both absolute and relative brain size in birds.
Journal
Nature ecology & evolution
ISSN: 2397-334X
Titre abrégé: Nat Ecol Evol
Pays: England
ID NLM: 101698577
Informations de publication
Date de publication:
09 2022
09 2022
Historique:
received:
31
07
2021
accepted:
19
05
2022
pubmed:
12
7
2022
medline:
9
9
2022
entrez:
11
7
2022
Statut:
ppublish
Résumé
A longstanding issue in biology is whether the intelligence of animals can be predicted by absolute or relative brain size. However, progress has been hampered by an insufficient understanding of how neuron numbers shape internal brain organization and cognitive performance. On the basis of estimations of neuron numbers for 111 bird species, we show here that the number of neurons in the pallial telencephalon is positively associated with a major expression of intelligence: innovation propensity. The number of pallial neurons, in turn, is greater in brains that are larger in both absolute and relative terms and positively covaries with longer post-hatching development periods. Thus, our analyses show that neuron numbers link cognitive performance to both absolute and relative brain size through developmental adjustments. These findings help unify neuro-anatomical measures at multiple levels, reconciling contradictory views over the biological significance of brain expansion. The results also highlight the value of a life history perspective to advance our understanding of the evolutionary bases of the connections between brain and cognition.
Identifiants
pubmed: 35817825
doi: 10.1038/s41559-022-01815-x
pii: 10.1038/s41559-022-01815-x
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
1381-1389Informations de copyright
© 2022. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Shultz, S. & Dunbar, R. Encephalization is not a universal macroevolutionary phenomenon in mammals but is associated with sociality. Proc. Natl Acad. Sci. USA 107, 21582–21586 (2010).
pubmed: 21098277
pmcid: 3003036
doi: 10.1073/pnas.1005246107
Jerison, H. J. Animal intelligence as encephalization. Phil. Trans. R. Soc. Lond. B 308, 21–35 (1985).
doi: 10.1098/rstb.1985.0007
Roth, G. & Dicke, U. Evolution of the brain and intelligence. Trends Cogn. Sci. 9, 250–257 (2005).
pubmed: 15866152
doi: 10.1016/j.tics.2005.03.005
Lefebvre, L., Whitle, P., Lascaris, E. & Finkelstein, A. Feeding innovations and forebrain size in birds. Anim. Behav. 53, 549–560 (1997).
doi: 10.1006/anbe.1996.0330
Overington, S. E., Morand-Ferron, J., Boogert, N. J. & Lefebvre, L. Technical innovations drive the relationship between innovativeness and residual brain size in birds. Anim. Behav. 78, 1001–1010 (2009).
doi: 10.1016/j.anbehav.2009.06.033
Reader, S. M., Hager, Y. & Laland, K. N. The evolution of primate general and cultural intelligence. Phil. Trans. R. Soc. B 366, 1017–1027 (2011).
pubmed: 21357224
pmcid: 3049098
doi: 10.1098/rstb.2010.0342
Benson-Amram, S., Dantzer, B., Stricker, G., Swanson, E. M. & Holekamp, K. E. Brain size predicts problem-solving ability in mammalian carnivores. Proc Natl Acad. Sci. USA 113, 2532–2537 (2016).
pubmed: 26811470
pmcid: 4780594
doi: 10.1073/pnas.1505913113
Reader, S. M. & Laland, K. N. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA 99, 4436–4441 (2002).
pubmed: 11891325
pmcid: 123666
doi: 10.1073/pnas.062041299
Fristoe, T. S., Iwaniuk, A. N. & Botero, C. A. Big brains stabilize populations and facilitate colonization of variable habitats in birds. Nat. Ecol. Evol. 1, 1706–1715 (2017).
pubmed: 28963479
doi: 10.1038/s41559-017-0316-2
van Woerden, J. T., van Schaik, C. P. & Isler, K. Effects of seasonality on brain size evolution: evidence from Strepsirrhine primates. Am. Nat. 176, 758–767 (2010).
pubmed: 21043783
doi: 10.1086/657045
Ducatez, S., Sol, D., Sayol, F. & Lefebvre, L. Behavioural plasticity is associated with reduced extinction risk in birds. Nat. Ecol. Evol. 4, 788–793 (2020).
pubmed: 32251379
doi: 10.1038/s41559-020-1168-8
Herculano-Houzel, S. Brains matter, bodies maybe not: the case for examining neuron numbers irrespective of body size. Ann. NY Acad. Sci. 1225, 191–199 (2011).
pubmed: 21535005
doi: 10.1111/j.1749-6632.2011.05976.x
Logan, C. J. et al. Beyond brain size: uncovering the neural correlates of behavioral and cognitive specialization. Comp. Cogn. Behav. Rev. 13, 55–89 (2018).
doi: 10.3819/CCBR.2018.130008
Jerison, H. Evolution of the Brain and Intelligence (Academic Press, 1973).
Herculano-Houzel, S. Numbers of neurons as biological correlates of cognitive capability. Curr. Opin. Behav. Sci. 16, 1–7 (2017).
doi: 10.1016/j.cobeha.2017.02.004
Van Schaik, C. P., Triki, Z., Bshary, R. & Heldstab, S. A. A farewell to the encephalization quotient: a new brain size measure for comparative primate cognition. Brain Behav. Evol. 96, 1–12 (2021).
pubmed: 34247154
doi: 10.1159/000517013
Striedter, G. F. Principles of Brain Evolution (Sinauer Associates, 2005).
MacLean, E. L. et al. The evolution of self-control. Proc. Natl Acad. Sci. USA 111, E2140–E2148 (2014).
pubmed: 24753565
pmcid: 4034204
doi: 10.1073/pnas.1323533111
Matějů, J. et al. Absolute, not relative brain size correlates with sociality in ground squirrels. Proc. R. Soc. B 283, 20152725 (2016).
pubmed: 27009231
pmcid: 4822454
doi: 10.1098/rspb.2015.2725
Deaner, R. O., Isler, K., Burkart, J. & Van Schaik, C. Overall brain size, and not encephalization quotient, best predicts cognitive ability across non-human primates. Brain Behav. Evol. 70, 115–124 (2007).
pubmed: 17510549
doi: 10.1159/000102973
Smaers, J. B., Dechmann, D. K. N., Goswami, A., Soligo, C. & Safi, K. Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates. Proc. Natl Acad. Sci. USA 109, 18006–18011 (2012).
pubmed: 23071335
pmcid: 3497830
doi: 10.1073/pnas.1212181109
Smaers, J. B. et al. The evolution of mammalian brain size. Sci. Adv. 7, eabe2101 (2021).
pubmed: 33910907
pmcid: 8081360
doi: 10.1126/sciadv.abe2101
Němec, P. & Osten, P. The evolution of brain structure captured in stereotyped cell count and cell type distributions. Curr. Opin. Neurobiol. 60, 176–183 (2020).
pubmed: 31945723
pmcid: 7191610
doi: 10.1016/j.conb.2019.12.005
Olkowicz, S. et al. Birds have primate-like numbers of neurons in the forebrain. Proc. Natl Acad. Sci. USA 113, 7255–7260 (2016).
pubmed: 27298365
pmcid: 4932926
doi: 10.1073/pnas.1517131113
Kverková, K. et al. The evolution of brain neuron numbers in amniotes. Proc. Natl Acad. Sci. USA 119, e2121624119 (2022).
pubmed: 35254911
pmcid: 8931369
doi: 10.1073/pnas.2121624119
Iwaniuk, A. N. & Hurd, P. L. The evolution of cerebrotypes in birds. Brain Behav. Evol. 65, 215–230 (2005).
pubmed: 15761215
doi: 10.1159/000084313
Timmermans, S., Lefebvre, L., Boire, D. & Basu, P. Relative size of the hyperstriatum ventrale is the best predictor of feeding innovation rate in birds. Brain Behav. Evol. 56, 196–203 (2000).
pubmed: 11154998
doi: 10.1159/000047204
Sayol, F., Lefebvre, L. & Sol, D. Relative brain size and its relation with the associative pallium in birds. Brain Behav. Evol. 87, 69–77 (2016).
pubmed: 27089472
doi: 10.1159/000444670
Healy, K. et al. Ecology and mode-of-life explain lifespan variation in birds and mammals. Proc. R. Soc. B 281, 20140298 (2014).
Deaner, R. O., Barton, R. A. & van Schaik, C. P. in Primate Life Histories and Socioecology (eds Kappeler, P. M. & Pereira, M. E.) 233–265 (Univ. of Chicago Press, 2003).
Sol, D., Sayol, F., Ducatez, S. & Lefebvre, L. The life-history basis of behavioural innovations. Phil. Trans. R. Soc. B 371, 20150187 (2016).
pubmed: 26926277
pmcid: 4780529
doi: 10.1098/rstb.2015.0187
Dukas, R. Evolutionary biology of animal cognition. Ann. Rev. Ecol. Evol. Syst. 35, 347–374 (2004).
doi: 10.1146/annurev.ecolsys.35.112202.130152
Ricklefs, R. E. The cognitive face of life histories. Wilson Bull. 116, 119–133 (2004).
doi: 10.1676/04-054
Martin, T. E., Oteyza, J. C., Boyce, A. J., Lloyd, P. & Ton, R. Adult mortality probability and nest predation rates explain parental effort in warming eggs with consequences for embryonic development time. Am. Nat. 186, 223–236 (2015).
pubmed: 26655151
doi: 10.1086/681986
Unzeta, M., Martin, T. E. & Sol, D. Daily nest predation rates decrease with body size in passerine birds. Am. Nat. 196, 743–754 (2020).
pubmed: 33211569
doi: 10.1086/711413
Charvet, C. J. & Striedter, G. F. Developmental modes and developmental mechanisms can channel brain evolution. Front. Neuroanat. 5, 4 (2011).
Finlay, B. L. & Darlington, R. B. Linked regularities in the development and evolution of mammalian brains. Science 268, 1578–1584 (1995).
pubmed: 7777856
doi: 10.1126/science.7777856
Herculano-Houzel, S. Isotropic fractionator: a simple, rapid method for the quantification of total cell and neuron numbers in the brain. J. Neurosci. 25, 2518–2521 (2005).
pubmed: 15758160
pmcid: 6725175
doi: 10.1523/JNEUROSCI.4526-04.2005
Massen, J. J. M. et al. Brain size and neuron numbers drive differences in yawn duration across mammals and birds. Commun. Biol. 4, 1–10 (2021).
doi: 10.1038/s42003-021-02019-y
Ramsey, G., Bastian, M. L. & Schaik, C. Van Animal innovation defined and operationalized. Behav. Brain Sci. 30, 393–437 (2007).
pubmed: 18081967
doi: 10.1017/S0140525X07002373
Lefebvre, L. A global database of feeding innovations in birds. Wilson J. Ornithol. 132, 803–809 (2021).
doi: 10.1676/20-00101
Barton, R. A. Embodied cognitive evolution and the cerebellum. Phil. Trans. R. Soc. B 367, 2097–2107 (2012).
pubmed: 22734053
pmcid: 3385677
doi: 10.1098/rstb.2012.0112
Gutiérrez-Ibáñez, C., Iwaniuk, A. N. & Wylie, D. R. Parrots have evolved a primate-like telencephalic–midbrain–cerebellar circuit. Sci. Rep. 8, 9960 (2018).
pubmed: 29967361
pmcid: 6028647
doi: 10.1038/s41598-018-28301-4
Brieuc, M. S. O. O., Waters, C. D., Drinan, D. P. & Naish, K. A. A practical introduction to random forest for genetic association studies in ecology and evolution. Mol. Ecol. Res. 18, 755–766 (2018).
doi: 10.1111/1755-0998.12773
Hadfield, J. D. & Nakagawa, S. General quantitative genetic methods for comparative biology: phylogenies, taxonomies and multi-trait models for continuous and categorical characters. J. Evol. Biol. 23, 494–508 (2010).
pubmed: 20070460
doi: 10.1111/j.1420-9101.2009.01915.x
Güntürkün, O., Ströckens, F., Scarf, D. & Colombo, M. Apes, feathered apes, and pigeons: differences and similarities. Curr. Opin. Behav. Sci. 16, 35–40 (2017).
doi: 10.1016/j.cobeha.2017.03.003
Ströckens, F. et al. High associative neuron numbers could drive cognitive performance in corvid species. J. Comp. Neurol. 530, 1588–1605 (2022).
pubmed: 34997767
doi: 10.1002/cne.25298
Shanahan, M., Bingman, V. P., Shimizu, T., Wild, M. & Güntürkün, O. Large-scale network organisation in the avian forebrain: a connectivity matrix and theoretical analysis. Front. Comput. Neurosci. 7, 89 (2013).
Emery, N. J. Cognitive ornithology: the evolution of avian intelligence. Phil. Trans. R. Soc. B 361, 23–43 (2006).
pubmed: 16553307
doi: 10.1098/rstb.2005.1736
Lambert, M. L., Jacobs, I., Osvath, M. & von Bayern, A. M. P. Birds of a feather? Parrot and corvid cognition compared. Behaviour 156, 505–594 (2019).
doi: 10.1163/1568539X-00003527
Ksepka, D. T. et al. Tempo and pattern of avian brain size evolution. Curr. Biol. 30, 2026–2036 (2020).
pubmed: 32330422
doi: 10.1016/j.cub.2020.03.060
Herculano-Houzel, S., Manger, P. R. & Kaas, J. H. Brain scaling in mammalian evolution as a consequence of concerted and mosaic changes in numbers of neurons and average neuronal cell size. Front. Neuroanat. 8, 77 (2014).
Smaers, J. B., Mongle, C. S., Safi, K. & Dechmann, D. K. N. Allometry, evolution and development of neocortex size in mammals. Prog. Brain Res. 250, 83–107 (2019).
pubmed: 31703910
doi: 10.1016/bs.pbr.2019.05.002
Cárdenas, A. & Borrell, V. Molecular and cellular evolution of corticogenesis in amniotes. Cell Mol. Life Sci. 77, 435–1460 (2020).
doi: 10.1007/s00018-019-03315-x
García-Moreno, F. & Molnár, Z. Variations of telencephalic development that paved the way for neocortical evolution. Prog. Neurobiol. 194, 101865 (2020).
pubmed: 32526253
pmcid: 7656292
doi: 10.1016/j.pneurobio.2020.101865
Charvet, C. J. & Striedter, G. F. Developmental basis for telencephalon expansion in waterfowl: enlargement prior to neurogenesis. Proc. R. Soc. B 276, 3421–3427 (2009).
pubmed: 19605398
pmcid: 2817193
doi: 10.1098/rspb.2009.0888
Striedter, G. F. & Charvet, C. J. Developmental origins of species differences in telencephalon and tectum size: morphometric comparisons between a parakeet (Melopsittacus undulatus) and a quail (Colinus virgianus). J. Comp. Neurol. 507, 1663–1675 (2008).
pubmed: 18241052
doi: 10.1002/cne.21640
Sibly, R. M. & Brown, J. H. Effects of body size and lifestyle on evolution of mammal life histories. Proc. Natl Acad. Sci. USA 104, 17707–17712 (2007).
pubmed: 17940028
pmcid: 2077039
doi: 10.1073/pnas.0707725104
Uomini, N., Fairlie, J., Gray, R. D. & Griesser, M. Extended parenting and the evolution of cognition. Phil. Trans. R. Soc. Lond. B 375, 20190495 (2020).
doi: 10.1098/rstb.2019.0495
Reiner, A. et al. Revised nomenclature for avian telencephalon and some related brainstem nuclei. J. Comp. Neurol. 473, 377–414 (2004).
pubmed: 15116397
pmcid: 2518311
doi: 10.1002/cne.20118
Mullen, R. J., Buck, C. R. & Smith, A. M. NeuN, a neuronal specific nuclear protein in vertebrates. Development 116, 201–211 (1992).
pubmed: 1483388
doi: 10.1242/dev.116.1.201
Mezey, S. et al. Postnatal changes in the distribution and density of neuronal nuclei and doublecortin antigens in domestic chicks (Gallus domesticus). J. Comp. Neurol. 520, 100–116 (2012).
pubmed: 21674497
doi: 10.1002/cne.22696
Revell, L. J. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217–223 (2012).
doi: 10.1111/j.2041-210X.2011.00169.x
Ducatez, S. & Lefebvre, L. Patterns of research effort in birds. PLoS ONE 9, e89955 (2014).
pubmed: 24587149
pmcid: 3935962
doi: 10.1371/journal.pone.0089955
Sheard, C. et al. Ecological drivers of global gradients in avian dispersal inferred from wing morphology. Nat. Commun. 11, 2463 (2020).
Cooney, C. R. et al. Ecology and allometry predict the evolution of avian developmental durations. Nat. Commun. 11, 2383 (2020).
pubmed: 32409662
pmcid: 7224302
doi: 10.1038/s41467-020-16257-x
Botelho, J. F. & Faunes, M. The evolution of developmental modes in the new avian phylogenetic tree. Evol. Dev. 17, 221–223 (2015).
pubmed: 26174097
doi: 10.1111/ede.12126
Bürkner, P.-C. Brms: an R package for Bayesian multilevel models using Stan. J. Stat. Softw. 80, 1–28 (2017).
doi: 10.18637/jss.v080.i01
Pigot, A. L. et al. Macroevolutionary convergence connects morphological form to ecological function in birds. Nat. Ecol. Evol. 4, 230–239 (2020).
pubmed: 31932703
doi: 10.1038/s41559-019-1070-4
Jetz, W., Thomas, G. H., Joy, J. B., Hartmann, K. & Mooers, A. O. The global diversity of birds in space and time. Nature 491, 444–448 (2012).
pubmed: 23123857
doi: 10.1038/nature11631
Berk, R. A. Statistical Learning from a Regression Perspective (Springer International, 2017).
Liaw, A. & Wiener, M. Classification and regression by randomForest. R News 2, 18–22 (2002).
Lleonart, J., Salat, J. & Torres, G. J. Removing allometric effects of body size in morphological analysis. J. Theor. Biol. 205, 85–93 (2000).
pubmed: 10860702
doi: 10.1006/jtbi.2000.2043
Sayol, F., Downing, P. A., Iwaniuk, A. N., Maspons, J. & Sol, D. Predictable evolution towards larger brains in birds colonizing oceanic islands. Nat. Commun. 9, 2820 (2018).
pubmed: 30065283
pmcid: 6068123
doi: 10.1038/s41467-018-05280-8
Torres, C. R., Norell, M. A. & Clarke, J. A. Bird neurocranial and body mass evolution across the end-Cretaceous mass extinction: the avian brain shape left other dinosaurs behind. Sci. Adv. 7, eabg7099 (2021).