Testing hypotheses of marsupial brain size variation using phylogenetic multiple imputations and a Bayesian comparative framework

. 2021 Mar 31 ; 288 (1947) : 20210394. [epub] 20210331

Jazyk angličtina Země Velká Británie, Anglie Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid33784860

Considerable controversy exists about which hypotheses and variables best explain mammalian brain size variation. We use a new, high-coverage dataset of marsupial brain and body sizes, and the first phylogenetically imputed full datasets of 16 predictor variables, to model the prevalent hypotheses explaining brain size evolution using phylogenetically corrected Bayesian generalized linear mixed-effects modelling. Despite this comprehensive analysis, litter size emerges as the only significant predictor. Marsupials differ from the more frequently studied placentals in displaying a much lower diversity of reproductive traits, which are known to interact extensively with many behavioural and ecological predictors of brain size. Our results therefore suggest that studies of relative brain size evolution in placental mammals may require targeted co-analysis or adjustment of reproductive parameters like litter size, weaning age or gestation length. This supports suggestions that significant associations between behavioural or ecological variables with relative brain size may be due to a confounding influence of the extensive reproductive diversity of placental mammals.

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Jerison HJ. 1973. Evolution of the brain and intelligence. New York, NY: Academic Press.

Tsuboi M, et al. 2018. Breakdown of brain-body allometry and the encephalization of birds and mammals. Nat. Ecol. Evol. 2, 1492-1500. (10.1038/s41559-018-0632-1) PubMed DOI

Reader SM, Laland KN. 2002. Social intelligence, innovation, and enhanced brain size in primates. Proc. Natl Acad. Sci. USA 99, 4436-4441. (10.1073/pnas.062041299) PubMed DOI PMC

Sol D, Bacher S, Reader SM, Lefebvre L. 2008. Brain size predicts the success of mammal species introduced into novel environments. Am. Nat. 172(Suppl. 1(S1)), S63-S71. (10.1086/588304) PubMed DOI

Benson-Amram S, Dantzer B, Stricker G, Swanson EM, Holekamp KE. 2016. Brain size predicts problem-solving ability in mammalian carnivores. Proc. Natl Acad. Sci. USA 113, 2532-2537. (10.1073/pnas.1505913113) PubMed DOI PMC

van Woerden JT, Willems EP, van Schaik CP, Isler K. 2012. Large brains buffer energetic effects of seasonal habitats in catarrhine primates. Evolution 66, 191-199. (10.1111/j.1558-5646.2011.01434.x) PubMed DOI

Milton K. 1981. Distribution patterns of tropical plant foods as an evolutionary stimulus to primate mental development. Am. Anthropol. 83, 534-548. (10.1525/aa.1981.83.3.02a00020) DOI

Rosati AG. 2017. Foraging cognition: reviving the ecological intelligence hypothesis. Trends Cogn. Sci. 21, 691-702. (10.1016/j.tics.2017.05.011) PubMed DOI

Fox KCR, Muthukrishna M, Shultz S. 2017. The social and cultural roots of whale and dolphin brains. Nat. Ecol. Evol. 1, 1699-1705. (10.1038/s41559-017-0336-y) PubMed DOI

Holekamp KE, Benson-Amram S. 2017. The evolution of intelligence in mammalian carnivores. Interface Focus 7, 20160108. (10.1098/rsfs.2016.0108) PubMed DOI PMC

DeCasien AR, Williams SA, Higham JP. 2017. Primate brain size is predicted by diet but not sociality. Nat. Ecol. Evol. 1, 112. (10.1038/s41559-017-0112) PubMed DOI

Todorov OS, Weisbecker V, Gilissen E, Zilles K, Sousa A. 2019. Primate hippocampus size and organization are predicted by sociality but not diet. Proc. R. Soc. B 286, 20191712. (10.1098/rspb.2019.1712) PubMed DOI PMC

Dunbar RIM. 1998. The social brain hypothesis. Evol. Anthropol. Issues News Rev. 6, 178-190. (10.1002/(sici)1520-6505(1998)6:5<178::Aid-evan5>3.0.Co;2-8) DOI

Sol D. 2009. Revisiting the cognitive buffer hypothesis for the evolution of large brains. Biol. Lett. 5, 130-133. (10.1098/rsbl.2008.0621) PubMed DOI PMC

Healy SD, Rowe C. 2007. A critique of comparative studies of brain size. Proc. Biol. Sci. 274, 453-464. (10.1098/rspb.2006.3748) PubMed DOI PMC

Barton RA, Montgomery SH. 2019. Proportional versus relative size as metrics in human brain evolution. Proc. Natl Acad. Sci. USA 116, 3-4. (10.1073/pnas.1817200116) PubMed DOI PMC

Wartel A, Lindenfors P, Lind J. 2019. Whatever you want: inconsistent results are the rule, not the exception, in the study of primate brain evolution. PLoS ONE 14, e0218655. (10.1371/journal.pone.0218655) PubMed DOI PMC

Nakagawa S, Freckleton RP. 2008. Missing inaction: the dangers of ignoring missing data. Trends Ecol. Evol. 23, 592-596. (10.1016/j.tree.2008.06.014) PubMed DOI

Weisbecker V, Blomberg S, Goldizen AW, Brown M, Fisher D. 2015. The evolution of relative brain size in marsupials is energetically constrained but not driven by behavioral complexity. Brain Behav. Evol. 85, 125-135. (10.1159/000377666) PubMed DOI

Isler K, van Schaik C. 2006. Costs of encephalization: the energy trade-off hypothesis tested on birds. J. Hum. Evol. 51, 228-243. (10.1016/j.jhevol.2006.03.006) PubMed DOI

Isler K, van Schaik CP. 2012. Allomaternal care, life history and brain size evolution in mammals. J. Hum. Evol. 63, 52-63. (10.1016/j.jhevol.2012.03.009) PubMed DOI

Tsuboi M, Husby A, Kotrschal A, Hayward A, Buechel SD, Zidar J, Lovlie H, Kolm N. 2015. Comparative support for the expensive tissue hypothesis: big brains are correlated with smaller gut and greater parental investment in Lake Tanganyika cichlids. Evolution 69, 190-200. (10.1111/evo.12556) PubMed DOI PMC

Street SE, Navarrete AF, Reader SM, Laland KN. 2017. Coevolution of cultural intelligence, extended life history, sociality, and brain size in primates. Proc. Natl Acad. Sci. USA 114, 7908-7914. (10.1073/pnas.1620734114) PubMed DOI PMC

Aiello LC, Wheeler P. 1995. The expensive-tissue hypothesis: the brain and the digestive system in human and primate evolution. Curr. Anthropol. 36, 199-221. (10.1086/204350) DOI

Isler K, van Schaik CP. 2009. The expensive brain: a framework for explaining evolutionary changes in brain size. J. Hum. Evol. 57, 392-400. (10.1016/j.jhevol.2009.04.009) PubMed DOI

Weisbecker V, Goswami A. 2014. Reassessing the relationship between brain size, life history, and metabolism at the marsupial/placental dichotomy. Zoolog. Sci. 31, 608-612. (10.2108/zs140022) PubMed DOI

Weisbecker V, Goswami A. 2011. Neonatal maturity as the key to understanding brain size evolution in homeothermic vertebrates. Bioessays 33, 155-158. (10.1002/bies.201000128) PubMed DOI

Lukas D, Clutton-Brock T. 2014. Evolution of social monogamy in primates is not consistently associated with male infanticide. Proc. Natl Acad. Sci. USA 111, E1674. (10.1073/pnas.1401012111) PubMed DOI PMC

Hintz WD, Lonzarich DG. 2018. Maximizing foraging success: the roles of group size, predation risk, competition, and ontogeny. Ecosphere 9, e02456. (10.1002/ecs2.2456) DOI

Shuster SM. 2009. Sexual selection and mating systems. Proc. Natl Acad. Sci. USA 106(Suppl. 1), 10 009-10 016. (10.1073/pnas.0901132106) PubMed DOI PMC

Weisbecker V, Goswami A. 2011. Marsupials indeed confirm an ancestral mammalian pattern: a reply to Isler. Bioessays 33, 358-361. (10.1002/bies.201100013) PubMed DOI

Smith KK. 2006. Craniofacial development in marsupial mammals: developmental origins of evolutionary change. Dev. Dyn. 235, 1181-1193. (10.1002/dvdy.20676) PubMed DOI

Logan CJ, et al. 2018. Beyond brain size: uncovering the neural correlates of behavioral and cognitive specialization. Comp. Cogn. Behav. Rev. 13, 55-89. (10.3819/ccbr.2018.130008) DOI

Guernsey MW, Chuong EB, Cornelis G, Renfree MB, Baker JC. 2017. Molecular conservation of marsupial and eutherian placentation and lactation. Elife 6, e27450. (10.7554/eLife.27450) PubMed DOI PMC

Hinds LA. 1988. Hormonal Control of Lactation. In The developing marsupial: models for biomedical research (eds Tyndale-Biscoe CH, Janssens PA), pp. 55-67. Berlin, Germany: Springer.

Weisbecker V, Goswami A. 2010. Brain size, life history, and metabolism at the marsupial/placental dichotomy. Proc. Natl Acad. Sci. USA 107, 16 216-16 221. (10.1073/pnas.0906486107) PubMed DOI PMC

Carlisle A, Selwood L, Hinds LA, Saunders N, Habgood M, Mardon K, Weisbecker V. 2017. Testing hypotheses of developmental constraints on mammalian brain partition evolution, using marsupials. Sci. Rep. 7, 4241. (10.1038/s41598-017-02726-9) PubMed DOI PMC

Todorov OS. 2019. Marsupial Cognition. In Encyclopedia of animal cognition and behavior (eds Vonk J, Shackelford T), pp. 1-8. Cham, Switzerland: Springer International Publishing.

Ashwell KW. 2008. Encephalization of Australian and New Guinean marsupials. Brain Behav. Evol. 71, 181-199. (10.1159/000114406) PubMed DOI

Suarez R, Paolino A, Fenlon LR, Morcom LR, Kozulin P, Kurniawan ND, Richards LJ. 2018. A pan-mammalian map of interhemispheric brain connections predates the evolution of the corpus callosum. Proc. Natl Acad. Sci. USA 115, 9622-9627. (10.1073/pnas.1808262115) PubMed DOI PMC

Sikes RS, Ylönen H. 1998. Considerations of optimal litter size in mammals. Oikos 83, 452-465. (10.2307/3546673) DOI

Werner J, Griebeler EM. 2011. Reproductive biology and its impact on body size: comparative analysis of mammalian, avian and dinosaurian reproduction. PLoS ONE 6, e28442. (10.1371/journal.pone.0028442) PubMed DOI PMC

Mundry R. 2014. Statistical Issues and Assumptions of Phylogenetic Generalized Least Squares. In Modern phylogenetic comparative methods and their application in evolutionary biology: concepts and practice (ed. Garamszegi LZ), pp. 131-153. Berlin, Germany: Springer.

Resche-Rigon M, White IR. 2018. Multiple imputation by chained equations for systematically and sporadically missing multilevel data. Stat. Methods Med. Res. 27, 1634-1649. (10.1177/0962280216666564) PubMed DOI PMC

Rubin DB. 1987. Multiple imputation for nonresponse in surveys. New York, NY: John Wiley.

Hadfield JD. 2010. MCMC methods for multi-response generalized linear mixed models: TheMCMCglmmRPackage. J. Stat. Softw. 33, 1-22. (10.18637/jss.v033.i02) PubMed DOI

R Core Team. 2017. R: a language and environment for statistical computing. Vienna, Austria: R Foundation for Statistical Computing.

Revell LJ. 2012. phytools: an R package for phylogenetic comparative biology (and other things). Methods Ecol. Evol. 3, 217-223. (10.1111/j.2041-210X.2011.00169.x) DOI

Orme CDL. 2012. The caper package: comparative analyses in phylogenetics and evolution in R. See https://cran.r-project.org/web/packages/caper.

Guillerme T, Healy K. 2014. mulTree: a package for running MCMCglmm analysis on multiple trees. Zonodo. (10.5281/zenodo.12902). DOI

Buuren S, Groothuis-Oudshoorn K. 2011. mice: multivariate imputation by chained equations inR. J. Stat. Softw. 45, 1-67. (10.18637/jss.v045.i03) DOI

Drhlik P, Blomberg SP. 2021. Phylomice. See https://github.com/pdrhlik/phylomice.

Harmon LJ, Weir JT, Brock CD, Glor RE, Challenger W. 2007. GEIGER: investigating evolutionary radiations. Bioinformatics 24, 129-131. (10.1093/bioinformatics/btm538) PubMed DOI

Wickham H. 2016. Ggplot2: elegant graphics for data analysis. Berlin, Germany: Springer.

Hyndman RJ, Einbeck J, Wand MP. 2021. hdrcde: highest density regions and conditional density estimation. R package version 3.4. See https://pkg.robjhyndman.com/hdrcde.

Weisbecker V, Ashwell K, Fisher D. 2013. An improved body mass dataset for the study of marsupial brain size evolution. Brain Behav. Evol. 82, 81-82. (10.1159/000348647) PubMed DOI

Gynther I, Baker A, Van Dyck S. 2013. Field companion to the mammals of Australia. London, UK: New Holland Publishers.

Taylor J, Rühli FJ, Brown G, De Miguel C, Henneberg M. 2006. Mr imaging of brain morphology, vascularisation and encephalization in the koala. Austral. Mammal. 28, 243-247. (10.1071/AM06034) DOI

Kumar S, Stecher G, Suleski M, Hedges SB. 2017. TimeTree: a resource for timelines, timetrees, and divergence times. Mol. Biol. Evol. 34, 1812-1819. (10.1093/molbev/msx116) PubMed DOI

Mitchell KJ, et al. 2014. Molecular phylogeny, biogeography, and habitat preference evolution of marsupials. Mol. Biol. Evol. 31, 2322-2330. (10.1093/molbev/msu176) PubMed DOI

Weisbecker V, Speck C, Baker AM. 2019. A tail of evolution: evaluating body length, weight and locomotion as potential drivers of tail length scaling in Australian marsupial mammals. Zool. J. Linn. Soc. 188, 242-254. (10.1093/zoolinnean/zlz055) DOI

Demirtas H. 2018. Flexible imputation of missing data. Boca Raton, FL: CRC Press.

Little RJA. 1988. Missing-data adjustments in large surveys. J. Business Econ. Stat. 6, 287-296. (10.1080/07350015.1988.10509663) DOI

Tierney N, Cook D, McBain M, Fay C, O'Hara-Wild M, Hester J. 2019. Naniar: Data structures, summaries, and visualisations for missing data. R Package.

White IR, Royston P, Wood AM. 2011. Multiple imputation using chained equations: issues and guidance for practice. Statist. Med. 30, 377-399. (10.1002/sim.4067) PubMed DOI

Barnard J, Rubin DB. 1999. Small-sample degrees of freedom with multiple imputation. Biometrika 86, 948-955. (10.1093/biomet/86.4.948) DOI

Housworth EA, Martins EP, Lynch M. 2004. The phylogenetic mixed model. Am. Nat. 163, 84-96. (10.1086/380570) PubMed DOI

Navarrete A, van Schaik CP, Isler K. 2011. Energetics and the evolution of human brain size. Nature 480, 91-93. (10.1038/nature10629) PubMed DOI

Sol D, Garcia N, Iwaniuk A, Davis K, Meade A, Boyle WA, Szekely T. 2010. Evolutionary divergence in brain size between migratory and resident birds. PLoS ONE 5, e9617. (10.1371/journal.pone.0009617) PubMed DOI PMC

Barton RA, Capellini I. 2011. Maternal investment, life histories, and the costs of brain growth in mammals. Proc. Natl Acad. Sci. USA 108, 6169-6174. (10.1073/pnas.1019140108) PubMed DOI PMC

Barrickman NL, Lin MJ. 2010. Encephalization, expensive tissues, and energetics: an examination of the relative costs of brain size in strepsirrhines. Am. J. Phys. Anthropol. 143, 579-590. (10.1002/ajpa.21354) PubMed DOI

Isler K. 2011. Energetic trade-offs between brain size and offspring production: marsupials confirm a general mammalian pattern. Bioessays 33, 173-179. (10.1002/bies.201000123) PubMed DOI

Smaers JB, Dechmann DK, Goswami A, Soligo C, Safi K. 2012. Comparative analyses of evolutionary rates reveal different pathways to encephalization in bats, carnivorans, and primates. Proc. Natl Acad. Sci. USA 109, 18 006-18 011. (10.1073/pnas.1212181109) PubMed DOI PMC

Hudson LN, Isaac NJ, Reuman DC. 2013. The relationship between body mass and field metabolic rate among individual birds and mammals. J. Anim. Ecol. 82, 1009-1020. (10.1111/1365-2656.12086) PubMed DOI PMC

Heldstab SA, Isler K, van Schaik CP. 2018. Hibernation constrains brain size evolution in mammals. J. Evol. Biol. 31, 1582-1588. (10.1111/jeb.13353) PubMed DOI

Riek A, Bruggeman J. 2013. Estimating field metabolic rates for Australian marsupials using phylogeny. Comp. Biochem. Physiol. A Mol. Integr. Physiol. 164, 598-604. (10.1016/j.cbpa.2013.01.007) PubMed DOI

Luo Y, Zhong MJ, Huang Y, Li F, Liao WB, Kotrschal A. 2017. Seasonality and brain size are negatively associated in frogs: evidence for the expensive brain framework. Sci. Rep. 7, 16629. (10.1038/s41598-017-16921-1) PubMed DOI PMC

Reddon AR, Chouinard-Thuly L, Leris I, Reader SM, Leroux S. 2018. Wild and laboratory exposure to cues of predation risk increases relative brain mass in male guppies. Funct. Ecol. 32, 1847-1856. (10.1111/1365-2435.13128) DOI

Jaatinen K, Møller AP, Öst M. 2019. Annual variation in predation risk is related to the direction of selection for brain size in the wild. Sci. Rep. 9, 11847. (10.1038/s41598-019-48153-w) PubMed DOI PMC

Dunlap KD, Corbo JH, Vergara MM, Beston SM, Walsh MR. 2019. Predation drives the evolution of brain cell proliferation and brain allometry in male Trinidadian killifish, Rivulus hartii. Proc. R. Soc. B 286, 20191485. (10.1098/rspb.2019.1485) PubMed DOI PMC

Mitchell DJ, Vega-Trejo R, Kotrschal A. 2020. Experimental translocations to low predation lead to non-parallel increases in relative brain size. Biol. Lett. 16, 20190654. (10.1098/rsbl.2019.0654) PubMed DOI PMC

Iwaniuk AN, Nelson JE, Pellis SM. 2001. Do big-brained animals play more? Comparative analyses of play and relative brain size in mammals. J. Comp. Psychol. 115, 29-41. (10.1037/0735-7036.115.1.29) PubMed DOI

Byers JA. 1999. The distribution of play behaviour among Australian marsupials. J. Zool. 247, 349-356. (10.1111/j.1469-7998.1999.tb00997.x) DOI

Montgomery SH. 2014. The relationship between play, brain growth and behavioural flexibility in primates. Anim. Behav. 90, 281-286. (10.1016/j.anbehav.2014.02.004) DOI

Abelson ES. 2016. Brain size is correlated with endangerment status in mammals. Proc. R. Soc. B 283, 20152772. (10.1098/rspb.2015.2772) PubMed DOI PMC

Gonzalez-Voyer A, Gonzalez-Suarez M, Vila C, Revilla E. 2016. Larger brain size indirectly increases vulnerability to extinction in mammals. Evolution 70, 1364-1375. (10.1111/evo.12943) PubMed DOI

Sol D, Szekely T, Liker A, Lefebvre L. 2007. Big-brained birds survive better in nature. Proc. R. Soc. B 274, 763-769. (10.1098/rspb.2006.3765) PubMed DOI PMC

Snell-Rood EC, Wick N. 2013. Anthropogenic environments exert variable selection on cranial capacity in mammals. Proc. R. Soc. B 280, 20131384. (10.1098/rspb.2013.1384) PubMed DOI PMC

White EP, Ernest SKM, Kerkhoff AJ, Enquist BJ. 2007. Relationships between body size and abundance in ecology. Trends Ecol. Evol. 22, 323-330. (10.1016/j.tree.2007.03.007) PubMed DOI

Sibly RM, Brown JH. 2009. Mammal reproductive strategies driven by offspring mortality-size relationships. Am. Nat. 173, E185-E199. (10.1086/598680) PubMed DOI PMC

Shultz S, Dunbar RIM. 2010. Social bonds in birds are associated with brain size and contingent on the correlated evolution of life-history and increased parental investment. Biol. J. Linnean Soc. 100, 111-123. (10.1111/j.1095-8312.2010.01427.x) DOI

Weisbecker V, et al. In press. Global elongation and high shape flexibility as an evolutionary hypothesis of accommodating mammalian brains into skulls. Evolution. (10.1111/evo.14163) PubMed DOI

Todorov OS, Blomberg SP, Goswami A, Sears K, Drhlík P, Peters J, Weisbecker V. 2021. Data from: Testing hypotheses of marsupial brain size variation using phylogenetic multiple imputations and a Bayesian comparative framework. Dryad Digital Repository. (10.5061/dryad.jh9w0vt9h) PubMed DOI PMC

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