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Female Brain Size and Parental Care in Carnivores (Mammal) JOHN L

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Female Brain Size and Parental Care in Carnivores (Mammal) JOHN L Proc. Natd. Acad. Sci. USA Vol. 91, pp. 5495-5497, June 1994 Evolution Female brain size and parental care in carnivores (mammal) JOHN L. GITTLEMAN Department of Zoology, University of Tennessee, Knoxville, TN 37996-0810 Communicated by George C. Williams, February 24, 1994 (receivedfor review October 12, 1993) ABSTRACT Comparative studies indicate that species dif- 26) and African lions (27), a mother is assisted by multiple ferences in mammalian brain size relate to body size, ecology, males and/or females. Communal duties include similar and life-history traits. Previous analyses failed to show intra- parental behaviors as shown in biparental systems, except sexual or behavioral patterns ofbrain size in mammals. Across that communal nursing is an added feature occasionally the terrestrial Carnivora, I find to the contrary. Differences in shown in some species. A crucial difference is that in both female, but not male, brain size associate with a fundamental biparental and communal species, parental care by an adult ecological and evolutionary characteristic of female behavior. other than the mother confers significant reduction in time Other factors equal, females that provide the sole parental care and energy ofmaternal feeding, guarding, and den attendance have larger brains than those of biparental or communal (28-30). Of the three parental systems in carnivores, single species. For females, more parental investment accompanies female care reflects the most intensive behavioral and ener- larger brains. Future comparative studies of mammalian brain getic demands. size must recognize that some patterns arise independently in Thus, assuming that brain size is associated with increased the two sexes. information processing (1, 4-6, 31), it is predicted that females of species that care for young exclusively on their Among mammal species, brain weight reflects differences in own will have larger brains relative to their body weight than body size, ecology, and life histories (1). Body size might be those in biparental or communal systems. Since other com- either a causal or constraining allometric variable of brain parative studies of mammals indicate that dietary specialists weight (2, 3). After removing the effects ofbody weight, brain have larger brains, dietary categories (meat-eating; om- weight is greater in dietary specialists across bats (4), rodents nivory; frugivory; insectivory) are examined across the Car- (5), and primates (6). Protracted gestation length coupled nivora. Further, to allow for any possible effect of life with small litter sizes is associated with large neonatal brain histories on female brain size, particularly those that index size, which in turn correlates with adult brain size (7). Two precociality/altriciality in mammals (32), correlates of ges- factors have eluded and confounded comparative study de- tation length and the age at which eyes first open in neonates spite such consistent patterns across diverse taxa. First, are also analyzed. patterns of variation need not be the same in males and females. Second, despite considerable effort to find behav- ioral correlates of brain size (1), no variables have emerged METHODS that are independent of phylogeny. By recognizing these Brain-size measurements are from braincase volumes of factors, I show that relative female brain size is larger in adult females in 71 carnivore species and are presented species with strictly maternal care than in biparental or elsewhere (14, 33, 51). Data on body weight, diet, and life communal taxa. This finding is independent of allometry, histories are those of Gittleman (34-36); the data were ecology, neonatal development, phylogeny, and covariation logarithmically transformed before analysis. By use of infor- of male brain size. mation in the literature, each species was classified according The terrestrial Carnivora exhibit three general forms of care (see the legend to female parental care. (i) The majority ofcarnivore species, as to the above definitions of parental in most other mammalian taxa, display solitary female pa- Fig. 1). Autocorrelation and Moran's I statistics were used, rental care independent ofa male or other adult helpers (8, 9). respectively, for estimating (i) whether and (ii) at what As exemplified by raccoons and all species of ursids (10, 11) taxonomic level cross-taxonomic variation in brain size is and small felids (12, 13), a solitary female locates or builds a related to phylogenetic distance (37, 38). Many statistical natal den site, nurses and grooms young, defends the young methods are available for incorporating and/or removing from potential threats, procures solid food after lactation, phylogenetic pattern in comparative tests (37, 38). For con- facilitates the development of food preferences and/or ac- tinuous traits, two methods in particular are appropriate quisition, and influences patterns and areas of dispersal. though different in statistical properties and assumptions Further, given the amount of time necessary for young to concerning rates of trait evolution. The "phylogenetic auto- reach age at independence in relation to female life-span, a correlation" method assumes an autoregressive process single adult female typically spends 80%o of her life attending whereby trait variation is correlated with phylogeny, and this young (14, 15). (ii) In biparental systems, as shown in many correlation declines with phylogenetic distance (37-39). The canids (16-19) and the brown hyena (20), mothers give similar "independent comparisons" method assumes a specific care as in the solitary system, but assistance is provided by model of trait evolution by calculating expected contrast an attendant male who will feed, guard, and retrieve young as values in accord with phylogenetic distance (40, 41). Both much as, and sometimes more than, the mother. (iii) In methods are used in the present analysis as a conservative communal systems, such as observed in grey wolves (16, 17, approach to presumed inaccuracy of phylogenetic informa- 19), coatis (21), dwarf mongooses (22), spotted hyenas (23- tion (42) and uncertainty of a model of trait evolution (39). A least-squares (model 1) regression is used to describe allo- The publication costs ofthis article were defrayed in part by page charge metric relations. Even though this model is inappropriate payment. This article must therefore be hereby marked "advertisement" with error variance in the x variable, it is acceptable in the in accordance with 18 U.S.C. §1734 solely to indicate this fact. present study because estimates of slope do not effect 5495 Downloaded by guest on September 27, 2021 54% Evolution: Gittleman Proc. Natl. Acad. Sci. USA 91 (1994) following traits: female brain weight, r2 = 0.63; female body weight, r2 = 0.49; gestation length, r2 = 0.65. Across taxonomic ranks, observed phylogenetic relations of brain weight are specifically due to correlation among species IcC within genera (z values of Moran's I = 6.42) and among genera within families (z = 5.37), as expected with greater .C phenotypic similarity usually observed in more related taxa. These diagnostic statistics therefore indicate that it is nec- essary to apply the above-mentioned comparative methods .0 ~~~~~~~0Maternal for hypothesis testing. Female brain weight increases significantly with increasing female body weight for absolute species data (y = 2.47x° 65, r = 0.97; n = 71), autoregressed data (y = 9.29x 92, r2 = 0.90; n = 71), and independent comparisons (y = -0.05x.64, 2cio Blparental r2 = 0.89; n = 20); all analyses are significant at the 0.001 -4 -1 level. I remove these allometric effects by the regression of Female body weight (in) female brain size on female body weight and then use the residuals for the following comparative tests. U) 20 As predicted, carnivore species in which females exclu- sively take care oftheir young have larger relative brain sizes than females of species with either biparental or communal (U care [species data are F(2,68) = 5.20, P < 0.008; autore- 1o gressed data are F(2,68) = 6.72, P < 0.002; see also Fig. 1]. Ln 1.5- Mean deviations from a common slope (using autoregressed values) across the order show that exclusively maternal species have the highest elevation (0.28) followed by bipa- , 5 rental (-0.52) and communal (-0.60) species. Pairwise com- parisons reveal significant differences in deviation between 0 0 Maternal the maternal and biparental species [t(28) = 2.21, P < 0.05] 5 X Biparental and maternal and communal species [t(32) = 3.25, P < 0.01]. 0 Communal Differences in relative female brain size are not observed 00 among dietary categories across carnivores (F(3,61) = 2.06, not significant), nor do the relative life histories of gestation length (r2 = 0.05) or the days on which eyes first open in -1 5 E -2 -I.5 -1I .5 0 .5 1.5 2 young (r2 = 0.04) correlate. 0 U. Female body weight (in)- autoregressed values To employ the independent comparisons method, I coded types of parental care into numerical categories and exam- FIG. 1. Female brain weight regressed on female body weight ined their correlations with female brain size while control- (wt.) among different modes of parental care across the terrestrial ling for body size (40, 41); the correlation coefficient is Carnivora. Bivariate plots include original species data (Upper) and significant (r2 = 0.28, n = 20; P < 0.05). autoregressed data (Lower) that are statistically independent from phylogenetic correlation. Species classification of parental care are
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