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Insular dwarfism in hippos and a model for brain size reduction in Homo floresiensis

Nature volume 459, pages 8588 (07 May 2009) | Download Citation

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Abstract

Body size reduction in mammals is usually associated with only moderate brain size reduction, because the brain and sensory organs complete their growth before the rest of the body during ontogeny1,2. On this basis, ‘phyletic dwarfs’ are predicted to have a greater relative brain size than ‘phyletic giants’1,3. However, this trend has been questioned in the special case of dwarfism of mammals on islands4. Here we show that the endocranial capacities of extinct dwarf species of hippopotamus from Madagascar are up to 30% smaller than those of a mainland African ancestor scaled to equivalent body mass. These results show that brain size reduction is much greater than predicted from an intraspecific ‘late ontogenetic’ model of dwarfism in which brain size scales to body size with an exponent of 0.35. The nature of the proportional change or grade shift2,5 observed here indicates that selective pressures on brain size are potentially independent of those on body size. This study demonstrates empirically that it is mechanistically possible for dwarf mammals on islands to evolve significantly smaller brains than would be predicted from a model of dwarfing based on the intraspecific scaling of the mainland ancestor. Our findings challenge current understanding of brain–body allometric relationships in mammals and suggest that the process of dwarfism could in principle explain small brain size, a factor relevant to the interpretation of the small-brained hominin found on the Island of Flores, Indonesia6.

Main

Brain tissue is energetically expensive, and it has been suggested that a decrease in brain volume may be advantageous to an animal’s survival under the environmental conditions associated with islands4,7,8. This phenomenon, if real, can be difficult to test because not only are most examples of dwarf island mammals extinct and known only from incomplete subfossil material, but knowledge of the founding ancestor can also be difficult to ascertain. The strongest case previously documented is that of a fossil bovid Myotragus, isolated on the Mediterranean island of Majorca for more than 5 Myr (refs 4, 9). The brain mass of Myotragus was decreased by up to 50% relative to those of extant bovids of equivalent body mass4. However, a link between the relatively small brain of Myotragus and the process of dwarfism has been disputed10,11 in the light of the length of the bovid’s isolation and its uncertain ancestry9.

One aspect of the continuing debate12,13,14 over whether the small-brained hominin discovered on the Island of Flores, Indonesia6, evolved by insular dwarfism centres on scaling exponents between brain and body size10,11. For predicting the brain size of a mammal at a smaller body size, these ‘intraspecific’ scaling models are the most appropriate to accommodate the likely correlated effects of body size adjustment on brain size in closely related species10,15,16 (see Supplementary Discussion). However, here we show that two species of extinct dwarf hippopotamus do not correspond to such dwarfing models because even though the same scaling exponents relating brain size to body size apply, large intercept shifts (grade shifts2,5) distinguish these ‘phyletic dwarfs’ from their mainland ancestor (Fig. 1, Supplementary Table 1 and Supplementary Discussion).

Figure 1: Relationship between brain size and cranial size for an intraspecific ‘late ontogenetic’ model of dwarfing.
Figure 1

Major axis slopes (95% confidence intervals): thin line, H. amphibius, 0.3482 (0.28–0.41); thick line, H. lemerlei, 0.369 (0.15–0.63); dashed line, H. madagascariensis, 0.4587 (0.20–0.79). Filled diamonds, H. amphibius (n = 33); filled triangles, H. lemerlei (n = 12); open triangles, H. madagascariensis (n = 12); crosses, C. liberiensis (n = 6). For statistical comparisons see Supplementary Table 1.

To model the dwarfing process, we took the extant large H. amphibius, a generalized representative of the genus Hippopotamus, to be the probable ancestor of two recently extinct dwarfed hippos, H. lemerlei and H. madagascariensis, from the island of Madagascar17 (see Supplementary Discussion). These species can be unequivocally separated taxonomically17 but both share apomorphies with the modern genus Hippopotamus18. The modern pygmy hippopotamus Choeropsis liberiensis represents a lineage distinct from all other hippopotamids, diverging from its closest relative before 5 Myr ago (ref. 18). Madagascar is a large island of diverse habitats that has prehistorically supported up to three species of hippopotamus19, whose times of dispersal to Madagascar are unknown but whose remains persist to within the past 6,000 years20.

Brain–body scaling trends in hippos can be inferred from the relationship of brain to cranial size, because the relation between a volumetric estimate of cranial size and a postcranial estimate of body mass across the two living hippos and the Madagascan dwarf species is approximately isometric (Supplementary Figs 3–7, Supplementary Table 4 and Supplementary Discussion). Predictions of decrease in brain size given in Table 1 are thus based on observed cranial size data and not on estimates of body mass (the latter are provided for contextual purposes only). In Table 1 we evaluate predictions of brain–body scaling in insular dwarf hippos and a dwarf elephant by considering two intraspecific dwarfing models: ‘late ontogenetic’ and ‘ontogenetic’. In mammals that commonly dwarfed on islands, such as hippos, elephants and deer (see Supplementary Discussion), all of which have precocial young, there is generally thought to be a transition from rapid to slow growth of the brain that closely coincides with birth2,15,16. In H. amphibius, however, the rapid early phase of brain growth continues after birth for up to 2 years (Supplementary Fig. 1). The ‘late ontogenetic’ exponent (0.35) in this context is calculated from the late, slower phase of postnatal brain growth (2–40 years) and not just from static adult data. This distinction is important, because the ‘growth’ as opposed to the ‘static adult’ exponent will best characterize the size adjustments (developmental allometry) associated with the late phase of brain maturation1. However, because all late postnatal brain development in mammals typically involves a low exponent value (0.2–0.4 for intraspecific brain–body scaling)5, ‘late ontogenetic’ exponents should be similar to, or only moderately higher than, those derived from static adult data (see Supplementary Discussion). The higher ‘ontogenetic’ exponent (0.47) is derived from a complete postnatal series from birth to adulthood in which rapid and slow growth phases are combined.

Table 1: Estimates of brain size based on dwarfing models

If the endocranial capacity of H. lemerlei scaled as (cranial size)0.35 in accord with the ‘late ontogenetic’ model (Fig. 1 and Supplementary Table 1), an endocranial capacity of 544 cm3 would be predicted; that is, 62% of the value of an ancestor four times its cranial size (Tables 1 and 2). The observed mean endocranial capacity of H. lemerlei is 380 ± 7.25 cm3 (mean ± s.e.m.; Table 2), 30% smaller than that predicted from the ‘late ontogenetic’ model (Table 1). The observed mean endocranial capacity of H. madagascariensis is 421 ± 11.9 cm3 (Table 2), 24% smaller than that predicted from the ‘late ontogenetic’ model (Table 1). The ‘ontogenetic’ model, in which the endocranial capacity of H. lemerlei would scale as (cranial size)0.47 (Fig. 2 and Supplementary Table 1), predicts a endocranial capacity of 456 cm3, 52% of the value of the ancestor, but the observed endocranial capacity is still 17% smaller than that predicted under this model, and in H. madagascariensis it is 9% smaller (Table 1).

Table 2: Endocranial capacities, cranial sizes and body masses for species in Table 1
Figure 2: Relationship between brain size and cranial size for an intraspecific ‘ontogenetic’ model of dwarfing.
Figure 2

Major axis slopes (95% confidence intervals): thin line, H. amphibius, 0.468 (0.44–0.50); bold line, dwarf species pooled, 0.454 (0.27–0.67). Filled diamonds, H. amphibius (n = 37); filled triangles, H. lemerlei (n = 12); open triangles, H. madagascariensis (n = 12); crosses, C. liberiensis (n = 6). For statistical comparisons see Supplementary Table 1.

The Malagasy dwarf hippos do not correspond to either ‘intraspecific’ scaling model (Figs 1 and 2 and Table 1), indicating that ‘insular dwarfing’ does not necessarily comply with predictions based on the ontogenetic scaling of the mainland ancestor. The Malagasy dwarf hippos are roughly equivalent in body mass to a 1–2-year-old H. amphibius (353–544 kg), a stage in development that marks the completion of the first rapid phase of brain growth. In contrast, the extant pygmy hippopotamus (C. liberiensis), with a body mass one-sixth to one-eighth that of H. amphibius (ref. 19 and Table 2), has a mean endocranial capacity of 350 ± 12.7 cm3, approximately equal to the values predicted from the ‘ontogenetic’ scaling model (Table 1) but reduced by 17% relative to the values predicted from the ‘late ontogenetic’ model (Table 1). The extant pygmy hippopotamus is not an insular dwarf21 and is phylogenetically more basal than H. amphibius, its only extant sister taxon18 (see Supplementary Discussion). Adult C. liberiensis has a body mass equivalent to a 6-month-old H. amphibius (see Supplementary Discussion), a stage of development in which rapid early brain growth persists in the hippopotamus. In primates, too, a marked increase in relative brain size has been attributed to the prolongation of the rapid ‘prenatal’ phase of brain development3. In ‘phyletic dwarfs’ the opposite developmental adjustment, involving a decrease in the duration of rapid early brain growth, could potentially explain a ‘grade shift’ to a lower brain–body ratio, as demonstrated by the change in ratio of brain to cranial size in Fig. 1 (see Supplementary Discussion).

A further example is provided by Palaeoloxodon falconeri22,23, the smallest insular dwarf elephant from Sicily and Malta, derived from the mainland P. antiquus22,23. The brain of a modern elephant grows relatively little after birth (the brain of a newborn elephant is 50% of its adult brain weight, whereas that of a common hippopotamus is 22% and that of a human is 25%)24, indicating that rapid early brain growth is completed by the end of gestation. The adult P. falconeri is estimated to be approximately the size of a newborn modern elephant23, and hence brain mass is expected to scale to body mass with a ‘late ontogenetic’ exponent typical of a precocial mammal. With brain size scaled as (body mass)0.35, brain size matches the prediction of the ‘late ontogenetic’ model with a 100-fold estimated decrease in body mass (Table 1, second entry for P. falconeri; see also refs 10, 11). However, estimates of decrease in body mass in these elephants are imprecise, especially given the magnitude of the dwarfing (Table 2). Cranial volume, determined by direct measurement22, is reduced only 50-fold, and when scaled as (cranial volume)0.35, P. falconeri would have an endocranial capacity (2,250 cm3) 25% of the original value of its ancestor (P. antiquus) 50 times its size (Tables 1 and 2). The actual endocranial capacity of P. falconeri is 1,800 cm3 (ref. 22), 20% smaller than the value predicted from this ‘late ontogenetic’ model (Table 1, first entry for P. falconeri), in line with our results on the dwarf hippos. This discrepancy between the predictions based on cranial size22 and those based on estimates of body mass23,25 in these elephants gives grounds for caution in the use of the latter for the interpretation of brain-size scaling (see refs 7, 10, 11).

One argument put forward to rebut the idea that the small brain of H. floresiensis was linked to the process of insular dwarfism was that its small brain size could not be accommodated within predictions made from mammalian intraspecific brain–body scaling models10,11. Here we show empirically that it is mechanistically possible for dwarf mammals on islands to evolve significantly smaller brains in relation to their cranial size than would be predicted from models of dwarfing based on intraspecific scaling of the mainland ancestor. If the hippo model is applied to a typical H. erectus ancestor with a body mass of 60 kg (refs 10, 11, 26) and average endocranial capacity of 991 cm3 (refs 10, 11, 27) that reduced its body mass by 62% to 23 kg (the median of the 16–29 kg estimated body mass of H. floresiensis)6, an endocranial capacity of 704 cm3 (71% of the original value) would be predicted from scaling as (body mass)0.35. If the brain size were decreased by a further 30% of that value, as in the Malagasy hippo, H. lemerlei, an endocranial capacity of 493 cm3 would result. This is still larger than the actual value of H. floresiensis (380–430 cm3)6,28, but if the ancestor had an endocranial capacity of 804 cm3, as in the African H. erectus KNM-ER 3883 (ref. 27), scaling the body mass of the ancestor down to 23 kg and then decreasing the brain size by a further 30% of the scaled value gives an endocranial capacity of 405 cm3, comparable to that of H. floresiensis (see Supplementary Table 5). By the same analogy, if the Dmanisi adult Homo remains (skull D3444 cf. H. erectus)29, with an endocranial capacity 650 cm3 (ref. 29) and body mass of 40 kg (ref. 30) are considered, an endocranial capacity of 378 cm3 would result, a value close to that of H. floresiensis (see Supplementary Table 5). If cranial variables are used instead of body mass for scaling the endocranial capacity of these hominins, as in the hippo example, a similar result is obtained (see Supplementary Table 5).

Similar shifts in intercept to those illustrated in Fig. 1 have been reported from domesticated mammals that on average have smaller brains than their wild relatives16. Domesticated mammals provide proof of the developmental malleability of the brain among closely related species or within species, but there are some noteworthy distinctions between the phenomena of domestication and island dwarfism. The decrease in brain size of domestic mammals is not necessarily associated with decrease in body size, as it is in phyletic dwarfism, and domestication is usually associated with a decrease in the size of the sense organs16. H. floresiensis, unlike the bovid Myotragus and domesticated mammals, does not have reduced orbital dimensions11, although such skeletal variation does not necessarily correlate with the actual size of the sense organ. This is also evident in the Malagasy hippos, in which orbit area is actually larger in the dwarf hippos relative to H. amphibius (Supplementary Fig. 2). A pathological explanation for this condition in the Malagasy species can be ruled out through the existence of more than 40 individual dwarf hippo specimens with intact braincases (Supplementary Table 2). Whatever the explanation for the tiny brain of H. floresiensis relative to its body size, the evidence presented here suggests that the phenomenon of insular dwarfism could have played a part in its evolution.

Methods Summary

A cross-sectional postnatal series of crania of H. lemerlei, H. madagascariensis, H. amphibius and C. liberiensis (see Supplementary Tables 2 and 3) was digitized with a MicroScribe G2 and inter-landmark distances were calculated to compute a volumetric measure of the entire cranium. Endocranial capacity was used as a surrogate for brain size. Exponents derived from brain–body allometric scaling relationships in mammals are widely applied in analyses of relative brain size5, but here brain size has been regressed against cranial volume. Supplementary data are provided demonstrating that results generated from estimates of body mass are similar to those reported for cranial size (see Supplementary Figs 3–7 and Supplementary Discussion). The data and procedure used to determine body mass estimates from Malagasy dwarf postcrania are given in Supplementary Table 4 and in the Supplementary Discussion.

Online Methods

Sample size

The number of specimens included in different analyses is not constant as a result of missing data (MD); all relevant landmarks were not preserved on every specimen studied, and endocranial capacity could not be measured accurately on some specimens as a result of braincase damage or poor state of preservation (see Supplementary Tables 2 and 3). Sample sizes were: H. lemerlei, n = 29 (17 with MD); H. madagascariensis, n = 19 (7 with MD); H. amphibius, n = 50 (13 with MD); C. liberiensis n = 7 (1 with MD).

Estimation of cranial volume

A volumetric measure of the entire cranium was computed from the product of three variables: cranial length (the posteriormost point of the nuchal crest to the mesialmost point of the first incisor socket), cranial width (zygion to zygion) and cranial height (akrokranion (the median dorsal point of the occipital region) to basion). The static adult samples used to derive values given in Table 2 include specimens from dental ‘Age Group XI’ and above (see Supplementary Tables 2 and 3 and Supplementary Discussion).

Estimation of endocranial capacity

Endocranial capacity, the volume of the endocranial cavity, was measured by pouring precision plastic (polypropylene) balls 5.5 mm in diameter into the braincase cavity (after the large foramina had been plugged with plastazote foam), and then decanting the balls into a measuring cylinder.

Analysis of relative brain size

Brain size in mammals scales allometrically with body size and is described by the bivariate power function or, after logarithmic transformation, by the linear equation where y and x are variables, and k (exponent expressing slope) and b (y intercept) are constants. Slopes were determined by major-axis and least-squares regression (see Supplementary Table 1), but major-axis values define k in Table 1. In view of the absence of associated data on body mass for a growth series of modern H. amphibius skeletons, an analysis of cranial size versus global skeletal size (an estimate of body mass determined from postcranial evidence) has been provided in Supplementary Material (see Supplementary Discussion). For the subfossil taxa, body mass values were estimated from crania or from unassociated skeletal elements (see Supplementary Table 4 and Supplementary Discussion). The endocranial cavity (used to represent brain size), forms part of the cranium; cranial size is therefore a conservative estimator of change that can be measured directly from both fossil and modern material, and in hippos it is a good proxy for body size (see Supplementary Discussion).

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Acknowledgements

We thank A. Currant, C. Lefèvre, C. Sagne, E. Gilissen, F. Renoult, H. Chatterjee, J. Ashby, M. Nowak-Kemp, M. Harman, P. Jenkins, P. Tassy, R. Sabin, R. Symonds and S. Stuenes for facilitating access to museum collections; A. Rasoamiaramanana, G. Ravololonarivo, H. Andriamialison, T. Rakotondrazafy, M. Ramarolahy and S. Bourlat for permission and/or assistance with study of the subfossil material held in the University of Antananarivo and the Académie Malagache; B. Ramanivosoa, D. Gommery, C. Guérin and M. Faure for allowing the study of material at the Akiba Museum, Mahajanga, Madagascar; R. Portela Miguez for assistance with recording endocranial capacity measures from H. amphibius specimens in the Natural History Museum, London; A. Friday for assistance with data collection in the University Museum of Zoology, Cambridge; C. Anderung, J.-R. Boisserie, S. Walsh and V. Herridge for discussion and helpful comments; and J. Kappelman, J. Niven, D. Lieberman and A. Gordon for comments on earlier versions of this manuscript. This research was supported by the Biotechnology and Biological Sciences Research Council.

Author Contributions E.W. and A.L. designed the study. E.W. collected and analysed the data and drafted the paper. Both authors discussed the results and edited the manuscript.

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    • Eleanor M. Weston
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    This file contains Supplementary Data, Supplementary Tables 1-5, Supplementary Figures 1-8 with Legends a Supplementary Discussion and Supplementary References.

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