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Brain Size Does Not Rescue Domestication Syndrome

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Brain Size Does Not Rescue Domestication Syndrome TREE 2763 No. of Pages 2 Trends in Ecology & Evolution Letter Brain Size Does Not making cross-species comparisons chal- show no significant difference relative to lenging. Many studies used modern modern wolves. Rescue Domestication breeds as the representatives of domes- Syndrome ticated populations, but trait differences The comparison of alpacas and llamas with in breed subpopulations are not related guanacos (Lama guanicoe)suggestsa 1,2 Kathryn A. Lord, to domestication, but instead to the later change in the ratio of brain weight to body Greger Larson ,3,@ and improvement process to which existing weight, but the choice of wild population is Elinor K. Karlsson ,1,2,4,*,@ domesticates have been subjected. suspect because alpacas are descended from vicunas (Vicugna vicugna)[8]. In sheep, two modern breeds (North To demonstrate that a trait is universal German moorland sheep and blackhead among almost all domestic animals, we sheep) were compared with European In a recent letter, Wright et al. question the would ideally compare modern domesticates ‘ wild sheep (Ovis ammon musimon), a conclusions of our opinion article The his- with their pre-domestic wild ancestors, but species that diverged from the closest tory of farm foxes undermines the animal this is not possible in any species. Most ’ modern relative of domesticated sheep, domestication syndrome [1,2]. We argue domestication syndrome traits cannot be Asiatic Mouflon (Ovis orientalis), more than that, while the hypothesis that a universal measured in ancient remains. Modern wild a million years ago [9]. Wild mink were set of traits accompanies domestication in populations are not representatives of compared with ranch mink [10,11], an arti- animal species is intriguing, there is, thus the ancestral pre-domesticated population, fi ficially selected wild population rather than far, insuf cient supporting data to meet as is sometimes implied, but are instead a true domesticate. Similarly, wild gerbils the burden of proof required to conclude sister taxa with their own evolutionary history. were compared with a bottlenecked labo- the domestication syndrome exists. Wright They are not even necessarily descendants ratory population established using wild et al. propose that by applying a less- of the lineage from which the species was fi gerbils [12]. restrictive de nition of the domestication domesticated (e.g., dogs, the wild Eurasian syndrome, an alternative conclusion can wolf ancestor of which is extinct [3]), and In pigs, a comparison of breeds of varying be reached. thus observed phenotypic differences may sizes with wild boar suggested a decrease predate domestication by hundreds of thou- fi in the ratio of brain weight to body weight We de ne a domestication syndrome trait sands of years. In some cases, populations [13]. Yet even here, the choice of an as one causally linked to the process of thought to represent the wild lineage are domestication. In populations experiencing appropriate comparison wild population instead feralized domestic populations. selective pressure that favors tameness, is confounded firstly by ancestry, since as in the Russian Farm Fox project, pigs were domesticated independently domestication syndrome traits would rise The work on reduced brain size, described from two geographically distinct subspe- in prevalence as a consequence. Wright by Wright et al. in Table 1 in that article, cies [14]. Secondly, a strict dichotomy et al. propose that domestication syndrome perfectly illustrates these difficulties [2,4]. between wild and domestic populations should be defined purely phenotypically, The comparison populations used to is undermined by long-term gene flow and if one does so, abundant evidence assess brain size reduction vary widely, within and between both domestic pigs exists for shared changes in behavior, and a critical assessment reveals that many and wild boar [15]. body size, brain size, and color across are invalid. For example, domestic horses almost all domesticated animals when were compared with modern Przewalski One trait, increased tameness, is shared compared with their wild relatives. horses [5]; a severely bottlenecked and across domesticated animals, because it heavily managed lineage that has recently is inherent in how we define a species as Even if a purely phenotypic definition been shown to be the feral descendants domesticated. For other traits, the evidence is used, however, we find little support of the first domestic horses, and thus is weak. Even when differences between for the domestication syndrome. We not wild in any sense [6]. In dogs, while populations are found, varying definitions restricted our analysis to mammals early work from Coppinger described a of ‘wild’ and ‘domestic’ make it impossible because of the difficulty of defining decrease in the ratio of brain volume to to conclude that the process of domestica- traits consistently across orders, yet still skull area in dogs, these findings were tion is the critical feature explaining the dif- foundwidevariationinhowtraitswere amended in a later rewrite [7]. Breeds ferentiation between those populations. measured, and in how the wild and do- selected for giant size do possess a The null hypothesis – thedegreeofpheno- mesticated populations were defined, smaller ratio, but average sized dogs typic change expected between similarly Trends in Ecology & Evolution, Month 2020, Vol. xx, No. xx 1 Trends in Ecology & Evolution genetically differentiated populations in the *Correspondence: 8. Kruska, D. (1988) Mammalian domestication and its effect on [email protected] (E.K. Karlsson). brain structure and behavior. In Intelligence and Evolutionary absence of domestication – has rarely @Twitter: @Greger_Larson (G. Larson) and @eenork Biology, pp. 211–250, Springer if ever been defined. A recent large-scale (E.K. Karlsson). 9. Hedges, S.B. et al. (2015) Tree of life reveals clock-like https://doi.org/10.1016/j.tree.2020.10.004 speciation and diversification. Mol. Biol. Evol. 32, 835–845 study failed to find the covariation between 10. Kruska, D. (1996) The effect of domestication on brain size morphology and behavior expected if the © 2020 Elsevier Ltd. All rights reserved. and composition in the mink (Mustela vison). J. Zool. 239, 645–661 domestication syndrome were real [16]. 11. Kruska, D. and Schreiber, A. (1999) Comparative Although it is a long-standing hypothesis, morphometrical and biochemical-genetic investigations in References wild and ranch mink (Mustela vison: Carnivora: Mammalia). the domestication syndrome has not yet 1. Lord, K.A. et al. (2020) The history of farm foxes undermines the Acta Theriol. 44, 377–392 – been rigorously tested, as any scientifichy- animal domestication syndrome. Trends Ecol. Evol. 35, 125 136 12. Stuermer, I.W. et al. (2003) Intraspecificallometriccompari- 2. Wright, D. et al. (2020) Defining the domestication son of laboratory gerbils with mongolian gerbils trapped in pothesis must be, and cannot be assumed syndrome: comment on Lord et al. 2020. Trends Ecol. the wild indicates domestication in Meriones unguiculatus to be true. Evol. Published online September 8, 2020. https://doi. (Milne-Edwards, 1867) (Rodentia: Gerbillinae). Zoologischer org/10.1016/j.tree.2020.08.009 Anzeiger J. Compar. Zool. 242, 249–266 3. Freedman, A.H. et al. (2014) Genome sequencing highlights 13. Kruska, D.C.T. (2005) On the evolutionary significance of the dynamic early history of dogs. PLoS Genet. 10, e1004016 encephalization in some eutherian mammals: effects of 1Bioinformatics and Integrative Biology, University of 4. Zeder, M.A. (2012) The domestication of animals. J. Anthropol. adaptive radiation, domestication, and feralization. Brain Massachusetts Medical School, 368 Plantation Street, Res. 68, 161–190 Behav. Evol. 65, 73–108 Worcester, MA 01605, USA 5. Röhrs, V.M. and Ebinger, P. (1993) Progressive und re- 14. Bosse, M. et al. (2014) Genomic analysis reveals selection 2Broad Institute of MIT and Harvard, 415 Main Street, Cambridge, gressive Hirngrößienveränderungen bei Equiden. J. Zool. for Asian genes in European pigs following human- MA 02142, USA Syst. Evol. Res. 31, 233–239 mediated introgression. Nat. Commun. 5, 4392 3The Palaeogenomics and Bio-Archaeology Research Network, 6. Gaunitz, C. et al. (2018) Ancient genomes revisit the ancestry 15. Frantz, L.A.F. et al. (2019) Ancient pigs reveal a near- Research Laboratory for Archaeology and History of Art, University of domestic and Przewalski’shorses.Science 360, 111–114 complete genomic turnover following their introduction to of Oxford,1 South Parks Road, Oxford OX1 3TG, UK 7. Lord, K. et al. (2016) Evolution of working dogs. In The Europe. Proc. Natl. Acad. Sci. U. S. A. 116, 17231–17238 4Program in Molecular Medicine, University of Massachusetts Domestic Dog: Its Evolution, Behavior and Interactions 16. Hansen Wheat, C. et al. (2020) Morphology does not covary Medical School, 368 Plantation Street, Worcester, MA 01605, with People 4 (Serpell, J., ed.), pp. 42–66, Cambridge with predicted behavioral correlations of the domestication USA University Press syndrome in dogs. Evol. Lett. 4, 189–199 2 Trends in Ecology & Evolution, Month 2020, Vol. xx, No. xx.
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