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A Conserved Pattern of Brain Scaling from Sharks to Primates

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A Conserved Pattern of Brain Scaling from Sharks to Primates A conserved pattern of brain scaling from sharks to primates Kara E. Yopaka,b,1, Thomas J. Lisneyc,d, Richard B. Darlingtone, Shaun P. Collind,f, John C. Montgomeryb, and Barbara L. Finlaye aCenter for Scientific Computation in Imaging, University of California, San Diego, CA 92037; bLeigh Marine Laboratory, University of Auckland, Leigh 0985, New Zealand; cDepartment of Animal Ecology, Evolutionary Biology Centre, Uppsala University, 752 36 Uppsala, Sweden; dSchool of Biomedical Sciences, University of Queensland, St. Lucia, Queensland 4072, Australia; eDepartment of Psychology, Cornell University, Ithaca, NY 14853; and fSchool of Animal Biology, University of Western Australia, Crawley, Western Australia 6009, Australia Edited by Charles F. Stevens, Salk Institute for Biological Studies, La Jolla, CA, and approved June 4, 2010 (received for review February 23, 2010) Several patterns of brain allometry previously observed in mam- 100,000 or more between the smallest and largest mammalian mals have been found to hold for sharks and related taxa brains, however. (chondrichthyans) as well. In each clade, the relative size of brain Cartilaginous fishes occupy a basal position in the evolutionary parts, with the notable exception of the olfactory bulbs, is highly tree of gnathostomes, and extending these analyses to species in predictable from the total brain size. Compared with total brain such a key phylogenetic position would be highly instructive re- mass, each part scales with a characteristic slope, which is highest garding the cross-vertebrate generality of the mammalian brain for the telencephalon and cerebellum. In addition, cerebellar foli- plan (13). For many reasons, brains of sharks, skates and rays ation reflects both absolute and relative cerebellar size, in a man- (batoids), and holocephalans—a group collectively referred to as ner analogous to mammalian cortical gyrification. This conserved chondrichthyans—could demonstrate more diversity in basic pattern of brain scaling suggests that the fundamental brain plan brain plans than is seen in the highly covarying mammals. As that evolved in early vertebrates permits appropriate scaling in a group, these species sit closer to the first divergence of verte- response to a range of factors, including phylogeny and ecology, brates, where multiple solutions to fundamental adaptive prob- where neural mass may be added and subtracted without com- lems might have emerged and been stabilized, with mammals promising basic function. representing only one branch of this early tree. Chondrichthyans EVOLUTION occupy a wide range of aquatic niches (14), have an extremely chondrichthyan | cerebellar foliation | allometry | mammal | wide range of body size (15), and exhibit substantial variations in neuroevolution brain size and brain organization (16–21). Because neurons are generated widely within the fish brain throughout life (22, 23), he allometric relationship of brain parts to overall brain size engagement of neurogenesis in some aspect of later life history, Thas been studied and debated extensively (1–7). At the core of which is not a major factor in mammals, also might alter numer- the debate lies the question of whether the brain is best charac- ical relationships established in early development (24). Conse- terized as a collection of independently varying structures/devices quently, we have examined the overall scaling relationships in evolved for particular behavioral requirements or niches or as chondrichthyan brains, duplicating the analytical techniques of a single coordinated processing structure/device in which adap- the mammalian work but also using other quantitative methods to tation for species-specific behavioral capacities occurs without the address some persistent problems in allometric analyses. production of delineable modules (8, 9). Many methodological issues have arisen as well, including what about a brain should be Results quantified [cells or volumes (10)], what should be compared and Basic Scaling by Order. Of the six major brain components (telen- how, and how to take into account the statistical dependence of cephalon, diencephalon, mesencephalon, cerebellum, medulla both structural and species relationships (11). oblongata, and olfactory bulbs), only the first five scaled strongly Until recently, a single data corpus comprising primates, bats, with one another. We studied this scaling in 10 orders of chon- and insectivorous mammals was the sole source for comparison drichthyans, totaling 81 species (Fig. 1A). These data are visual- (2), leaving the question of whether these mammals represented ized as a regression against either total brain mass or the medulla, all vertebrates, or even all other mammals, unresolved. The which allows the easiest visual comprehension of the data struc- addition of carnivorous mammals (including marine mammals), ture (not identical to the inferential statistical analysis, as detailed SI Materials and Methods SI Materials and Methods ungulates, xenarthrans, and the manatee demonstrated that the in ). also pro- original conclusions drawn from primates, bats, and insectivores vides details of the brain divisions, explanations of how data were – could be extended to this larger data set (8, 12). These studies collected from original reports (16 20) and how new data on the revealed that mammalian brain structure exhibits a pattern of mass of the olfactory bulbs were collected in a subset of these variation containing two principal components. The first com- species, and the phylogenetic relationships of the chondrichthyans ≈ used for independent contrast analyses. ponent, accounting for 96% of the total variance of related fi brain parts to total brain size, loads most highly on neocortex and Here we present ve major analyses. First, we explore co- cerebellum. The second component loads most highly on the variation in the volume of brain parts by factor analysis. Second, olfactory bulb and associated limbic structures and accounts for ≈3% of the original variance. Each brain part also has a characteristic slope with respect to absolute brain size, such Author contributions: K.E.Y., R.B.D., and B.F. designed research; K.E.Y., T.J.L., S.P.C., J.C.M., and B.L.F. performed research; K.E.Y. and T.J.L. collected data on chondrichthyan brain that every large mammalian brain is composed disproportion- organization; S.P.C. and J.C.M. supervised data collection on chondrichthyan brains; R.B.D. ately of neocortex and cerebellum. The remaining 1% of the analyzed data; and K.E.Y., T.J.L., R.B.D., and B.L.F. wrote the paper. variance must subsume all remaining sources, including niche, The authors declare no conflict of interest. sex and individual differences, and measurement error. This 1% This article is a PNAS Direct Submission. contribution is large in one sense: In two species with the same 1To whom correspondence should be addressed. E-mail: [email protected]. brain size, a single structure might differ by a factor of 2.5. This article contains supporting information online at www.pnas.org/lookup/suppl/doi:10. The total range of structure sizes may differ by a factor of 1073/pnas.1002195107/-/DCSupplemental. www.pnas.org/cgi/doi/10.1073/pnas.1002195107 PNAS Early Edition | 1of6 Downloaded by guest on September 25, 2021 Fig. 2. Relative loadings of the two factors of the principal components analysis on 6 major brain areas across chondrichthyans (A) and 11 major brain areas across mammals (B). For both groups, the first principal component is plotted (factor 1), which accounts for the vast majority of the variance. For mammals, the second principal component (the olfactory bulb and limbic system, accounting for 2.6% of the variance) is plotted and compared with the third principal component in chondrichthyans (accounting for 1.98% of the variance), both of which load high on the olfactory bulb(s). Fig. 1. Scaling of the relative sizes of five major brain structures plotted as a function of total brain mass across 81 chondrichthyan species (51 sharks, 24 batoids, and 6 holocephalans) (A) and plotted as a function of medulla size, correlate at a level of 0.820 with each other, but each correlates at comparing brain structure scaling in chondrichthyans and mammals (B). For only about 0.6 with the “olfactory factor.” The relative loading of the purpose of visualization, an arbitrary constant (in parentheses in each factor 1 versus the olfactory factor (factor 2 in mammals, factor 3 scatterplot) was added to each brain structure. Tel, telencephalon; cer, cer- in chondrichthyans) is shown in Fig. 2 A and B. ebellum; die, diencephalon; mes, mesencephalon; med, medulla oblongata. Hyperallometry. For all six structures examined in chondrichthyans, The slopes and intercepts (without arbitrary constants) for each regression we tested for hyperallometry between each pair of structures. are given in Table 1 for A and in Table 2 for B. How we accounted for multiple comparisons in these analyses is discussed in SI Materials and Methods. Ignoring the olfactory we investigate the incidence of hyperallometry (i.e., relatively bulbs initially, our results suggested the same division of struc- greater increase in the size of any one brain part with respect to tures that had been suggested by the factor analysis. Each of the the others), using a statistical test that has rarely, if ever, been three structures in factor 1 (see above) was significantly hyper- used by neuroscientists but is used widely in other areas of bi- allometric relative to each of the two
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