Received:	30	May	2018  |  Revised:	12	August	2018  |  Accepted:	17	August	2018
DOI: 10.1002/ece3.4513
O R I G I N A L  R E S E A R C H
Morphological adaptations for relatively larger brains in 
hummingbird skulls
Diego Ocampo1,2  | Gilbert Barrantes2 | J. Albert C. Uy1
1Department of Biology, University of 
Miami, Coral Gables, Florida Abstract
2Escuela de Biología, Universidad de Costa A	common	allometric	pattern	called	Haller’s	Rule	states	that	small	species	have	rela-
Rica, San José, Costa Rica tively larger brains and eyes than larger species of the same taxonomic group. This 
Correspondence pattern imposes drastic structural changes and energetic costs on small species to 
Diego Ocampo, Department of Biology, produce and maintain a disproportionate amount of nervous tissue. Indeed, several 
University of Miami, Coral Gables, Florida.
Email: ocampov.diego@gmail.com studies have shown the significant metabolic costs of having relatively larger brains; 
however, little is known about the structural constraints and adaptations required for 
housing these relatively larger brains and eyes. Because hummingbirds include the 
smallest birds, they are ideal for exploring how small species evolve morphological 
adaptations for housing relatively larger brain and eyes. We here present results from 
a comparative study of hummingbirds and show that the smallest species have the 
lowest levels of ossification, the most compact braincases, and relatively larger eye 
sockets, but lower eye/head proportion, than larger species. In contrast to Passerines, 
skull ossification in hummingbirds correlates with body and brain size but not with 
age. Correlation of these skull traits with body size might represent adaptations to 
facilitate housing relatively larger brain and eyes, rather than just heterochronic ef-
fects related to change in body size. These structural changes in skull traits allow 
small animals to accommodate disproportionately larger brains and eyes without fur-
ther increasing overall head size.
K E Y W O R D S
braincase, eye socket size, Haller’s rule, relative brain size, skull ossification
1  | INTRODUC TION proportionally large brains (Eberhard & Wcislo, 2011). Indeed, the 
current evidence suggests a significant increase in energetic costs 
Relative to body size, brain size is proportionately larger in small spe- associated with more nervous tissues (e.g., Kotrschal et al., 2013; 
cies than in large species, a widespread pattern known as Haller’s Niven & Laughlin, 2008); however, little is known about the struc-
Rule (Rensch, 1948). This allometric pattern is found in a wide range tural changes that have evolved to deal with housing relatively larger 
of vertebrate and invertebrate taxa (Eberhard & Wcislo, 2011; brains and eyes in small animals (e.g., Niven & Farris, 2012).
Huxley, 1932; Striedter, 2005). For instance, brain and eyes of small To provide space for larger brains, cephalized animals can evolve 
birds and mammals scale hypoallometrically with body size (Brooke, larger heads or evolve changes in shape or structure of the braincase 
Hanley, & Laughlin, 1999; Calder, 1984). Consequently, small animals (Eberhard & Wcislo, 2011). For example, in very small spiders, the 
with relatively large brain and eyes have to deal with the behavioral, brain overflows into the coxae and deforms the sternum, reducing 
physiological, and structural costs of producing and maintaining the space for prosomal muscles, and, in miniature insects, portions 
This	is	an	open	access	article	under	the	terms	of	the	Creative	Commons	Attribution	License,	which	permits	use,	distribution	and	reproduction	in	any	medium,	
provided the original work is properly cited.
©	2018	The	Authors.	Ecology and Evolution published by John Wiley & Sons Ltd.
Ecology and Evolution. 2018;1–7.	 	 www.ecolevol.org	 | 	1
2  |     OCAMPO et Al.
of their brain extend into the prothorax and even the abdomen size. We test for the effect of body mass and relative brain size on 
(Quesada et al., 2011). Similarly, small salamanders have lost some skull thickness (e.g., degree of ossification), braincase compactness, 
skull bones, reduced skull ossification, and adjusted the overall skull and relative eye socket size. We predict that small- bodied humming-
morphology to accommodate relatively larger brains (Hanken, 1983, birds, which are known to have relatively larger brains, will have less 
1984). These modifications in small arthropods and vertebrates sug- skull ossification (i.e., single- layered skull), more compact braincases, 
gest that relatively large brains impose a series of presumably costly and relatively larger eye sockets than large species.
modifications in small animals due to the large space required to ac-
commodate large brains. In small birds, adjustments in the skull to 
accommodate relatively larger brains without enlarging overall head 2  | METHODS
size are expected to be achieved in at least two ways. First, differ-
ential growth of some skull bones (allometric variation) could alter 2.1 | Skull and body measures
the shape of a skull to accommodate more neural tissue. In this case, 
having a more spherical braincase can accommodate the brain in a We collected the percentage of skull ossification as a proxy for 
more compact way, with deviations from sphericity requiring more skull thickness from 501 individuals in 96 hummingbird species, 
area to house the same volume of neural tissue. Second, evolving from museum specimens in the Louisiana State University Museum 
thinner or less ossified skulls could provide additional space in the of Natural Science (LSUMNS) and Museo de Zoología, Escuela de 
braincase because the second layer of bone grows internally, which Biología, Universidad de Costa Rica (MZUCR). Percentage of skull 
may be taking up space available for brain tissue. ossification was estimated from ossification pattern, which is the 
Although	 a	 correlation	 between	 the	 morphological	 varia- proportion of the braincase having a double layer of bone (i.e., 
tion of facial and braincase modules has been identified (Bright, pneumatized) (Harrison & Harrison, 1949; Miller, 1946), as recorded 
Marugán-L obón, Cobbe, & Rayfield, 2016; Marcucio, Young, Hu, & on specimen labels by curators at the moment of skin preparation 
Hallgrimsson, 2011; Young, Linde-M edina, Fondon, Hallgrimsson, & (Supporting Information Table S1). Likewise, body mass (g) of each 
Marcucio, 2017), most studies on avian skull morphology have ex- individual was taken from specimen labels recorded by curators. We 
plored the ecological and molecular factors underlining covariation calculated mean values from a sample ranging from 3 to 17 adult 
with	beak	morphology	(e.g.,	Abzhanov,	Protas,	Grant,	Grant,	&	Tabin,	 males per species, as confirmed by gonads and plumage patterns. 
2004; Mallarino et al., 2012; Wu, Jiang, Suksaweang, Widelitz, & For skulls/skeletons without body mass information, we use the 
Chuong, 2004). In contrast, not much is known about the evolution- mean body mass value for the species to test for the effect of body 
ary processes determining braincase shape, especially adaptations size on skull compactness (see below). Because brain size of hum-
in the smallest species. For instance, birds with rounded eye sock- mingbirds estimated from endocranial volume might be unreliable, 
ets have more rounded and flexed brains than those with elongated we used fresh brain mass and body mass from fresh specimens col-
orbits (Kawabe, Shimokawa, Miki, Matsuda, & Endo, 2013), which lected for a subset of 24 species of hummingbirds (Diego Ocampo, 
should affect the overall skull morphology. The current information César Sánchez, & Gilbert Barrantes data).
on hummingbird skull morphology is restricted to general descrip- We measured braincase compactness (i.e., circularity) and the 
tions of its shape (Zusi, 2013). area of the contour of the orbit eye socket (eye socket area here-
Under a phylogenetically controlled comparative framework, after) from scaled pictures of skulls for four to six males of 32 spe-
we here explore how shape and structure of the skull correlate cies of hummingbirds from the LSUMNS and MZUCR collections 
with body mass and relative brain size in hummingbirds (Figure 1). (Supporting Information Table S2). We estimated the relative size of 
Hummingbirds include the smallest species of birds and have likely the eye socket from pictures of the lateral view of the skull, mea-
been under strong selection to modify their skull morphology to ac- suring the ratio between eye socket area and the total area of the 
commodate larger brains and eyes without enlarging overall head skull from the lateral view (without the beak, Figure 2a). We then 
(a) (b) (c)
F IGURE  1 Some species of 
hummingbirds included in this study are 
(a) Selasphorus flammula, (picture Julio 
E. Sánchez†) (b) Amazilia tzacatl, and (c) 
Eugenes spectabilis
OCAMPO et Al.      |  3
took pictures of the dorsal view, perpendicularly (90° angle) to the 2.2 | Statistical analysis
junction between the suture of the frontal and nasal bones, and 
the paraoccipital process (Figure 2b). From this dorsal view, we es- To control for the nonindependence of closely related humming-
timated the compactness of the braincase based on the ratio be- bird species, we used phylogenetic generalized least square (PGLS) 
tween the area and perimeter of the braincase (Peura & Livarinen, analyses for correlations between variables. We controlled for the 
1997). We delimited the frontal border of the braincase by a straight phylogenetic relationship, within each subset of species (trees with 
line between the most indented point of the frontal bones at the 96, 32, and 24 hummingbird species, respectively), in each analy-
interorbital region (Figure 2c). We use the compactness (circularity) sis using on 5,000 molecular phylogenies built using the backbone 
index as a proxy of the three- dimensional skull’s sphericity. To take method (Hackett et al., 2008) and data obtained from www.bird-
standardized pictures, each skull was placed on a small platform, tree.org (Jetz, Thomas, Joy, Hartmann, & Mooers, 2012). We show 
maintaining the camera at the same position relative to either the the figures generated using the 50% majority rule tree (Supporting 
lateral	or	the	dorsal	plane	of	the	skull	and	at	20	cm	from	it.	All	high-	 Information Figure S1); however, to control for phylogenetic uncer-
resolution pictures were scaled in coplanarity and analyzed using tainty, we ran all our analyses using the total population of trees. We 
ImageJ	(Abramoff,	Magelhaes,	&	Ram,	2004),	and	we	used	the	“free- report the mean values and standard deviation (±SD) of the param-
hand selection” function to delimit the contour of the braincase and eters when pertinent.
eye socket to measure the areas and perimeters on the pictures. To test for the effect of body size or relative brain size on skull 
ossification, the PGLS models included the log10- transformed body 
mass or the ratio of brain/body mass as a predictor variable and the 
log10-t ransformed percentage of skull ossification as the response 
variable (log10 (percentage of skull ossification + 1), to avoid unde-
fined values). To control for scale effect (i.e., body mass), we ran a 
PGLS of the residuals of the linear model of the log-t ransformed 
body mass and the log- transformed brain mass (x- axis), against the 
residuals of the linear model of the log- transformed body mass and 
the log- transformed skull ossification model (y-	axis).	A	negative	cor-
relation would indicate that species with larger brains than expected 
by body size have skulls with lower ossification than expected.
To test for the effect of body size and skull ossification on braincase 
compactness, the PGLS model included either the log- transformed 
body mass or log- transformed skull ossification against the mean 
compactness index (Peura & Livarinen, 1997), as a two-d imensional 
proxy of the spherical shape of the braincase. We could not test for 
the effect of brain size on skull compactness due to the limited number 
of samples that included both variables (only 11 species) and the ex-
tremely high correlation between brain size and body size (R2 = 0.94; 
Diego Ocampo, César Sánchez, & Gilbert Barrantes, unpublished data). 
We also tested for the effect of log- transformed body mass on relative 
eye socket area with a PGLS. We conducted all analyses in R v.3.1.3 (R 
Core	Team,	2014)	using	the	APE	(Paradis,	Claude,	&	Strimmer,	2004)	
and	CAPER	(Orme,	2013)	libraries	for	the	analyses.
3  | RESULTS
3.1 | Skull ossification
F IGURE  2 Skull of Rufous-t ailed hummingbird (Amazilia tzacatl). All	PGLS	models	 showed	a	 significant	effect	of	body	 size	on	 skull	
(a) The lateral view, with the dashed line representing eye socket ossification, with little phylogenetic signal (F1,94 = 68.13; p < 0.001; 
area. (b) Lateral view of the skull, with the thick red arrows pointing R2 = 0.42; λ = 0; Figure 3a). For the 96 species of hummingbirds, 
to the paraoccipital process (PaOc) and the suture between frontal the percentage of ossification increased with body size (β = 0.78; 
and nasal bones (Fr- Na). The dashed line represents the angle of p < 0.001). For the 24 species with brain size data (58 individuals, 
the placement of the camera to capture the dorsal view. (c) Dorsal 
view of the skull, with the red arrows pointing at the most indented 1–6 individuals per species), the PGLS models also found an ef-
region of the frontal bone. The dashed line delimits the anterior fect of relative brain size on skull ossification (F1,22 = 9.98; p < 0.01; 
border of the braincase R2 = 0.32; λ = 0; Figure 3b), in which species with relatively larger 
4  |     OCAMPO et Al.
F IGURE  3 Patterns of skull ossification in hummingbirds. (a) Relationship between body mass and skull ossification for 96 species. 
(b) Relationship between the brain/body mass ratio and the skull ossification for 24 species. (c) Nonsignificant relationship between the 
residuals of body mass/brain mass and residuals of body mass/skull ossification (for coefficients and R2 values, see main text)
brains had lower percentage of ossification (β	=	−0.39;	 p < 0.01). (F1,30 = 10.68; β = 3.44; p < 0.005; R
2 = 0.31; λ = 0; Figure 4c), with 
However, when we removed the effect of body size, we did not find small species having relatively smaller eye sockets (44%) than larger 
a significant effect of brain size on skull ossification (F1,22 = 0.86; species (50%).
p = 0.36; R2 = 0.04; λ = 0; Figure 3c).
3.2 | Skull shape 4  | DISCUSSION
For a subset of 32 species (five males per species), we found a sig- Several studies have explored variation in relative brain size and eye 
nificant effect of mean body size on mean braincase compactness size at various ontogenic and evolutionary scales (Burton, 2008; 
(F1,30 = 32.97 ± 1.26; p < 0.001; R
2 = 0.52 ± 0.01; λ = 1; Figure 4a): Linke, Roth, & Rottluff, 1986; Nealen & Ricklefs, 2001), along with 
Smaller species had more circular braincases than larger species their association with ecological and behavioral factors (Dunbar 
(β	=	−0.011;	p < 0.001). In addition, more circular skulls correlated &	Shultz,	2007;	Maklakov,	 Immler,	Gonzalez-V	 oyer,	Rӧnn,	&	Kolm,	
with low levels of ossification (F1,30 = 10.33 ± 0.42; β	=	−0.004;	 2011; Martínez- Ortega, Santos, & Gil, 2014; Smaers, Dechmann, 
p < 0.005; R2 = 0.26 ± 0.01; λ = 1; Figure 4b), so that more circu- Goswami, Soligo, & Safi, 2012). However, little is known about how 
lar skulls had lower levels of ossification (β	=	−0.0044;	p < 0.005). the size of both brain and eyes affects overall skull structure and 
Finally, small species had relatively larger eyes (relative to the body) morphology to accommodate the changes in relative brain and eye 
than those of larger species (F1,30 = 144.44; β = 12.55; p < 0.001; size. We found that small hummingbirds had less ossified and more 
R2 = 0.85; λ = 0), but a positive relationship between body size and compact or circular braincases and lower eye/head proportion than 
percentage of the lateral head area occupied by the eye socket their large counterparts; these allometric patterns support two 
F IGURE  4 Patterns of skull shape across 32 hummingbird species. Relationship between (a) body mass and braincase compactness. 
(b) Braincase compactness and skull ossification. (c) Percentage of the skull’s lateral area occupied by the eye socket and body size (for 
coefficients and R2 values, see main text)
OCAMPO et Al.      |  5
nonmutually exclusive hypotheses. First, changes in skull shape and in the proportion of braincase and eyes could also result from a re-
size could be adaptations to accommodate the relatively larger brains arrangement of the three- dimensional morphological space, rather 
of smaller species. That is, changes in skull morphology could result than changes in volume.
from selection on distinct skeletal modules of the skull, which results 
in adaptive changes in shape and size to more effectively accom- 4.2 | Size-r elated constraint hypothesis
modate larger nervous tissue while mitigating the overall increase 
in	relative	head	size	(“adaptive	change	hypothesis”).	Second,	selec- Alternatively,	selection	on	traits	other	than	skull	morphology,	such	
tion acting on body size could change the overall allometric scaling as body size, might result in secondary nonadaptive changes in skull 
of other structures and organs on body size. For instance, selection morphology (McKinney, 1986) because the same developmental 
favoring small body sizes could also result in small- bodied species pathways link brain morphology and skull characteristics (Koyabu 
with proportionally larger brains through developmental mechanism et al., 2014). For example, changes in body size could be achieved 
(“size-r	elated	constraint	hypothesis”). through heterochronic changes in the ontogenetic trajectory of the 
ancestral	 group	 (Alberch,	 Gould,	 Oster,	 &	Wake,	 1979),	 and	 skull	
4.1 | Adaptive change hypothesis morphology likely represents adjustments to this new allometric 
scaling. For instance, the avian skull morphology has likely evolved 
Direct selection on brain size could affect several skull traits to through a paedomorphic process, because avian skulls retain char-
better accommodate relatively larger brains thus shaping cranial acteristics of juveniles of ancestral theropods (Bhullar et al., 2012). 
morphology in hummingbirds. For example, the space to encase Similarly, reduced ossification in the smallest of hummingbird spe-
the relatively large brain and eyes of plethodontid salamanders is cies may result from paedomorphosis.
limited, imposing structural changes in the surrounding structures In general, thirteen skeletal traits correlate with body mass in 
(Hanken, 1983). These structural changes include the loss and re- birds (Field, Lynner, Brown, & Darroch, 2013). However, an evolu-
duction in skull bones, which results in the brain being partially un- tionary trend of reduction in body size (e.g., miniaturization) has 
protected but able to house relatively larger brains (Hanken, 1984). several particular implications for physiological (Eberhard & Wcislo, 
Similarly, in hummingbirds, the orbitocranial fonticulus is fused with 2011), behavioral (Cole, 1985; but see Eberhard, 2011), and mor-
the optic foramen (Zusi, 2013), resulting in skulls that have an open phological traits, where the most common morphological outcome 
space between the interorbital septum and the parietal bone. is the reduction and fusion of bones (Hanken & Wake, 1993). Thus, 
Increasing compactness or sphericity of the braincase in the if miniaturization has shaped hummingbird skull morphology, hum-
smallest species of hummingbird may also allow for housing a rela- mingbirds may have convergently evolved anatomical traits that are 
tively larger brain without increasing overall head size. Evolutionary typically found in miniaturized species of other clades, such as rela-
changes in brain size correlate with changes in braincase morphol- tively larger head and eyes, poorly ossified skeleton, and reductions 
ogy, since presumably an enlargement of the brain in the early evo- or loss of bones (Gould, 1977).
lution of birds had strong consequences in skull shape (Fabbri et al., Reduced skull ossification in relatively large-b rained species and 
2017). Previous comparative studies across 60 orders of birds have the general enlargement of the head and eyes found in the small-
shown that when the brain becomes larger in relation to the cra- est species of hummingbirds are comparable with those changes 
nial base, the braincase becomes more spherical and the foramen observed in the skull of miniaturized plethodontid salamanders 
magnum is displaced to a more ventral position (Marugán- Lobón & (Hanken, 1983) and Geomyoid rodents (Hafner & Hafner, 1984). The 
Buscalioni, 2009). More spherical braincases are associated with reduction in ossification (i.e., thickness) and the loss of bones are 
species with high flight maneuverability, which likely require more also similar to the drastic changes observed in Danionella dracula, 
nervous tissue (Iwaniuk & Wylie, 2007). Our results in hummingbirds a miniaturized cyprinid fish that lacks 44 bones, as a consequence 
are consistent with this broadscale study in birds. miniaturization (Britz, Conway, & Rüber, 2009). Other examples 
In addition, hummingbirds have the highest mass- specific meta- of changes in skeletal traits correlated with miniaturization, as in-
bolic rate among vertebrates, which likely represents the upper evo- creased variability and the evolution of morphological novelties, are 
lutionary metabolic limit (Suarez, 1992). This high metabolic rate is well documented elsewhere (see Hanken, 1993).
directly correlated with several physiological and anatomical traits 
that demand high energy input, such as flight (Lasiewski, 1963) and 
a relatively large heart (Lasiewski, 1964), brain, and eyes. Therefore, 5  | CONCLUSIONS
producing and maintaining a disproportionately large amount of 
nervous tissue, which would include the brain and the retina, which The scaling pattern of relative brain size on skull morphological traits 
is an outgrowth of the brain itself (Kiltie, 2000), should result in a and body size is consistent with an evolutionary framework of direct 
trade-o ff between the relative eye and brain investment (Niven & and indirect selection acting on skull morphology. Skull compactness 
Laughlin, 2008). Because the smallest hummingbird species may re- and relative eye socket size likely reflect not just a structural effect 
quire relatively more space for brain, the space for the eyes may be of size due to heterochronic changes, but rather adaptations to re-
limited, compared to larger species. Further, the observed changes duce the costs of housing a relatively large brain and eyes. However, 
6  |     OCAMPO et Al.
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