This is a repository copy of The shapes of birds’ eggs: evolutionary constraints andadaptations.
White Rose Research Online URL for this paper:https://eprints.whiterose.ac.uk/186835/
Version: Published Version
Article:Montgomerie, R., Hemmings, N., Thompson, J.E. et al. (1 more author) (2021) The shapesof birds’ eggs: evolutionary constraints and adaptations. The American Naturalist, 198 (6).
E215-E231. ISSN 0003-0147
https://doi.org/10.1086/716928© 2021 The University of Chicago. Reproduced in accordance with the publisher's selfarchiving policy. This version is distributed under the terms of the Creative Commons
Attribution-NonCommercial Licence (http://creativecommons.org/licenses/by-nc/4.0/). You
may not use the material for commercial purposes.

Reuse
This article is distributed under the terms of the Creative Commons Attribution-NonCommercial (CC BY-NC)
licence. This licence allows you to remix, tweak, and build upon this work non-commercially, and any newworks must also acknowledge the authors and be non-commercial. You don’t have to license any derivative
works on the same terms. More information and the full terms of the licence here:
https://creativecommons.org/licenses/
Takedown
If you consider content in White Rose Research Online to be in breach of UK law, please notify us byemailing eprints@whiterose.ac.uk including the URL of the record and the reason for the withdrawal request.

eprints@whiterose.ac.uk
https://eprints.whiterose.ac.uk/

vol. 198, no. 6

the american naturalist

december 2021

E-Article

The Shapes of Birds’ Eggs: Evolutionary
Constraints and Adaptations
Robert Montgomerie,1,* Nicola Hemmings,2 Jamie E. Thompson,2 and Tim R. Birkhead2
1. Department of Biology, Queen’s University, Kingston, Ontario K7L 3N6, Canada; 2. School of Biosciences, University of Shefﬁeld,
Shefﬁeld S10 2TN, United Kingdom
Submitted August 26, 2020; Accepted June 29, 2021; Electronically published October 26, 2021
Online enhancements: supplemental PDF. Dryad data: https://doi.org/10.5061/dryad.sj3tx9648.

abstract: We studied the shapes of eggs from 955 extant bird species across the avian phylogeny, including 39 of 40 orders and 78%
of 249 families. We show that the elongation component of egg shape(length relative to width) is largely the result of constraints imposedby the female’s anatomy during egg formation, whereas asymmetry(pointedness) is mainly an adaptation to conditions during the incubation period. Thus, egg elongation is associated with the size of theegg in relation to both the size of the female’s oviduct and her generalbody conformation and mode of locomotion correlated with pelvis
shape. Egg asymmetry is related mainly to clutch size and the structure of the incubation site, factors that inﬂuence thermal efﬁciency
during incubation and the risk of breakage. Importantly, general patterns across the avian phylogeny do not always reﬂect the trends withinlower taxonomic levels. We argue that the analysis of avian egg shapeis most proﬁtably conducted within taxa where all species share similar life histories and ecologies, as there is no single factor that inﬂuences egg shape in the same way in all bird species.
Keywords: birds, egg shape, oviduct, pelvis shape, clutch size, relative
egg size.

Introduction
For centuries, naturalists have marveled at the diversity ofsizes, colors, and shapes of what Thomas Wentworth Higginson, in 1862, called the most perfect things in the universe (Birkhead 2016)—the eggs of birds. The diversity ofegg size—spanning ﬁve orders of magnitude from the eggsof Mellisuga helenae (bee hummingbird, at 0.5 g) to thoseof Aepyornis maximus (elephant bird, at 8 kg)—is largely
explained by life histories and body size allometries (Lack1968). The colors and shapes of birds’ eggs also vary amongorders, families, genera, species, populations, and even in* Corresponding author; email: mont@queensu.ca.
ORCIDs: Montgomerie, https://orcid.org/0000-0003-4701-4525; Hemmings,
https://orcid.org/0000-0003-2418-3625; Thompson, https://orcid.org/0000-0003-0048-7886; Birkhead, https://orcid.org/0000-0003-2916-4976.

dividuals, but the causes of variation in these traits remain
somewhat elusive.
The study of egg shape has progressed along two fronts:(i) quantiﬁcation and (ii) attempts to explain variation. Since
D’Arcy Wentworth Thompson (1908, 1917) ﬁrst tackled
the quantiﬁcation problem in 1908, more than 20 studies
have attempted both mathematical and practical descriptions of avian egg shape with mixed success, especially forthe most asymmetric eggs (Biggins et al. 2018). Preston’s(1953, 1968, 1969) mathematical formulations provided an
accurate descriptor of all avian egg shapes using four parameters but have rarely been used to assess interspeciﬁc variation in shape. Simpler measures have not been as accurate
as Preston’s for all species, but a new software tool (Biggins
et al. 2018) uses Preston’s parameters to derive three accurate indexes of egg shape—elongation, pointedness, and polar asymmetry—that are readily obtained from digital images(Birkhead et al. 2018).
The ﬁrst studies on the adaptive signiﬁcance of egg shapefocused on species that laid the most asymmetric (pointed)
eggs: Uria murres (Uria guillemots in Europe; Tschanz et al.
1969) and waders (Andersson 1978), both in the order Charadriiformes. The earliest studies of murre eggs suggested that
their pear-like shape was an adaptation that made their eggs
spin or roll in a tight circle when knocked, thus reducing thechance of rolling off the bare cliff ledges where those birds
incubate their eggs (Tschanz et al. 1969). More recent work
has shown instead that this shape makes the murres’ eggs
more stable and less likely to move during incubation changeovers (Birkhead et al. 2018). The pointed shape of wader
eggs, on the other hand, allows eggs in their typical four-egg
clutches to pack more closely together, presumably enhancing incubation efﬁciency (Andersson 1978).
We embarked on this study with the primary goal ofidentifying the evolutionary pressures and anatomical/

American Naturalist, volume 198, number 6, December 2021. q 2021 The University of Chicago. All rights reserved. Published by The University of Chicago Press
for The American Society of Naturalists. https://doi.org/10.1086/716928

E216

The American Naturalist

physiological constraints that inﬂuence avian egg shapeacross the entire range of variation in extant species. We
had four objectives.
First, we sought to replicate a recent comprehensive studyof egg shape across the avian phylogeny (Stoddard et al.
2017) by (i) using more accurate measures of egg shapebased on standardized photographs and a new method forquantifying the shapes of all birds’ eggs (Biggins et al. 2018),(ii) achieving a slightly broader taxonomic coverage by targeting species from diverse sources, (iii) analyzing independent measures of the elongation and asymmetry components of egg shape so that we could evaluate the factors
affecting each of these traits separately, and (iv) categorizing incubation sites according to structural features thatmight be expected to inﬂuence egg shape by optimizing thermal efﬁciency—maximizing heat gain during incubationand minimizing heat loss when parents are absent. We feelthat such replication is useful as we used a different data set
with many different species, a different method of quantifying egg shape, and some different predictors in our models(table S1; tables S1–S22 are available online) but also because
we have raised questions about the generality of previous
conclusions (Birkhead et al. 2019b; but see Stoddard et al.
2019).
Second, to identify and quantify potential constraints on
egg shape, we examined oviductal anatomy in a large anddiverse family of birds (Galliformes) as well as the available
data on pelvis anatomy from a taxonomically broad rangeof species (Shatkovska et al. 2018). The diameter of the oviduct could plausibly limit egg diameter, and we present
new data here to assess how the oviduct inﬂuences egg shape.
Pelvis anatomy has been previously implicated as inﬂuencing egg shape (Rensch 1959; Warham 1990; Deeming andMayr 2018; Shatkovska et al. 2018), although the underlying mechanisms are unknown.
Third, we explored variation in the factors inﬂuencing
egg shape within avian families and orders. Our previous
work on the evolution of egg shape in the families Alcidae(auks, guillemots, murres) and Spheniscidae (penguins) revealed interesting within-family variation in egg shape thatwas correlated with incubation site (Birkhead et al. 2018;see also table S3-C in Stoddard et al. 2017). Our exploratory analyses also revealed that the trends within many
avian families and orders did not match the general trends
across all birds, suggesting that a more comprehensive understanding of the evolution of egg shape required a focus
on different clades within the class Aves (see also Stoddard
et al. 2019).
We focus most of our analyses at the level of avian families because this is the lowest taxonomic level at which
we were able to measure the eggs of enough species to makestatistically useful analyses for comparison among and withintaxa. These family-level patterns will not always be consis-

tent with patterns at lower taxonomic ranks (subfamily,
genus, subgenus) within those families. Thus, without further analysis, we cannot be sure that all of the potential
drivers of variation in egg shape are to be found at the levelof family. Families in the class Aves also differ in functional
morphologies and ecologies, forming clades that are well
supported by comprehensive molecular phylogenies (Hackett
et al. 2008; Jetz et al. 2012; Jarvis et al. 2014; Prum et al. 2015;
Kimball et al. 2019). There is ample evidence that familiesof birds differ markedly in ecologies and life histories (Lack
1968; Bennett and Owens 2002), with considerably morevariation in those traits among than within families. Thus,
analyses at the family level control for variation in traits thatare not expected to inﬂuence egg shape (e.g., foraging ecology, diet, age at ﬁrst breeding, longevity).
Fourth, we provide—and test predictions from—a conceptual framework for the study of egg shape that focuseson the underlying mechanisms that might either constrain
egg shape or select for different shapes that maximize thermal efﬁciency and minimize breakage. In this context, wedeﬁne a constraint as a factor that limits optimal shape because of an adaptation to some other aspect of a bird’s lifestyle. For example, the optimization of underwater locomotion for foraging favors a streamlined, elongated body shape
to reduce drag (Nesteruk et al. 2014), resulting in a relatively
narrow pelvis that might constrain egg width (Shatkovska
et al. 2018).

Conceptual Framework
Constraints
We looked speciﬁcally at two possible constraints on egg
shape, one imposed by the size of the female’s oviduct andthe other imposed by the shape of the female’s pelvis. First,
as Thompson (1917) suggested more than a century ago,
oviduct diameter might inﬂuence egg elongation as the unshelled egg is squeezed by the walls of the oviduct.
To assess the possibility of such a constraint on egg shape,
we measured several oviduct dimensions in 28 species ofGalliformes (land fowl) and found that all were positively
related to female mass with negative allometry (slope ! 1:0;
table S10). The maximum diameter of the isthmus—wherean egg expands to its ﬁnal shape before the shell is addedin the uterus—scales with female body size with an exponent of 0.38 (see “Constraints: Oviduct Anatomy”) suchthat larger birds have a much narrower isthmus for theirbody size than do smaller birds. Thus, if the diameter ofthe isthmus limits egg width, we expected a positive effectof both female size and relative egg size (controlling for female size) on the elongation of eggs.
Second, almost two centuries ago, Thienemann (1825)
suggested that the shapes of birds’ eggs might be inﬂuenced

Evolution of Avian Egg Shapeby the shape of the female’s body, with species having
more elongated bodies laying more elongated eggs. Pelvis
anatomy has since been implicated as the causal mechanism (Rensch 1959; Warham 1990) but only recently has
this relationship been analyzed quantitatively (Shatkovska
et al. 2018). Thus, in 173 species, pelvis shape was correlated with an index of egg elongation but not with an index
of egg asymmetry (Shatkovska et al. 2018).
Because almost all extant bird species have an unfused
pelvis—unlike their Jurassic and Cretaceous ancestors (andthe ostriches and possibly other ratites; Deeming and Mayr
2018)—the pelvis is unlikely to be a hard constraint thatprevents the passage of a too-wide egg (Kaiser 2010). Birds
with relatively narrow pelvises do have relatively narrow
bodies streamlined to enhance locomotion (Shatkovska et al.
2018). Thus, narrow pelvises might simply be correlated withsome aspect of abdominal anatomy that moderates egg width.
These effects should be pronounced in species with particularly large eggs for their body size.
An index of wing shape—the hand-wing index (HWI)—that is related to ﬂight efﬁciency (Claramunt et al. 2017)
was recently found to be correlated with egg shape (Stoddard et al. 2017) but accounted for only 5% of the interspeciﬁc variation in indexes of elongation and asymmetry.
In that study, the indexes of elongation and asymmetry
were moderately correlated (with family as random effect,r p 0:53 [95% conﬁdence limits (CLs): 0.49, 0.56], n p
1,400 species means), preventing the independent assessment of the factors affecting those two aspects of shape.
Species with high HWI are more dispersive and migratory(Sheard et al. 2020), presumably requiring more efﬁcient
ﬂight that might in turn be associated with a more streamlined body shape (Stoddard et al. 2017).
Adaptations
The evidence for egg shape being adaptive has so far been
restricted to selection acting during the incubation period,
with shape inﬂuencing egg strength (Bain 1991), egg stability during incubation on different substrates (Birkhead
et al. 2019b), and incubation efﬁciency (Andersson 1978),as well as being related to nest microclimate (Duursma et al.
2018). For example, perfect spheres offer the strongest shellstructure (Bain 1991) and lowest surface-to-volume ratio(Paganelli et al. 1974), everything else being equal. Thus,
eggs are expected to be more spherical in species with larger
clutch sizes (14 eggs), both to take advantage of closer packing to increase incubation efﬁciency and reduce heat loss
(Andersson 1978) and to reduce the chance of breakage(Bain 1991). Conversely, eggs that are prolate spheroids(elongated spheres) have a relatively larger surface area thanperfect spheres and thus allow for a larger region of contact incubation on their long axis such that they heat up

E217

more efﬁciently during incubation, even though they cool
down more quickly when no parent is incubating.
Two components of egg shape that represent asymmetry(polar asymmetry and pointedness; ﬁg. 1A, 1B) are likely
determined during egg formation by (i) some as yet unidentiﬁed structural characteristic of the magnum-isthmus
junction (Mao et al. 2006) or (ii) variation in the thickness
and structure of the shell membrane (Mallock 1925; Stoddard et al. 2017; Birkhead et al. 2019a) as the albumen
takes up water and expands before the ovum moves to theuterus where the shell is applied. Either way, the question
remains whether these mechanisms represent anatomical
constraints or evolved mechanisms to produce asymmetrical eggs for some adaptive purpose.
Finally, incubation efﬁciency is thought to be an important selective force on egg shape because any increase in
efﬁciency that enhances heat transfer from the incubating
adult—or decreases heat loss when the eggs are not being
incubated—reduces the time that eggs and chicks are conﬁned to the incubation site (Martin et al. 2015). For example, asymmetric eggs allow closer packing than prolate spheroids in clutches of three and four in open nests (Andersson
1978), thereby increasing incubation efﬁciency and reducing heat loss. Such close packing seems to be the clearest
explanation for the extremely asymmetric eggs of waders(families Charadriidae, Jacanidae, Pedionomidae, Recurvirostridae, Rostratulidae, Scolopacidae, Thinocoridae), where
the clutch size is almost always four and eggs are incubatedin open scrapes and platforms. This incubation advantage
is predicted to decline as clutch size increases above four(Andersson 1978), so less asymmetric eggs are expectedin species with larger clutches, everything else being equal.

Methods
Measuring Oviduct Size
To study oviductal anatomy, we obtained 70 specimensof 28 species of Galliformes euthanized during their egglaying period. The oviduct (including cloaca and ovary)
was removed intact, unraveled, stripped of connective tissue, and cleaned in phosphate buffered saline.
These freshly dissected oviducts were pinned out, photographed, and measured. The entire length of the oviductwas measured (51 mm) from the infundibulum to thecloaca, as well as the individual lengths of the magnum,
isthmus, uterus (shell gland), and vagina. The oviduct wasthen transferred to a tray, where each section was pinned
straight and submerged in 10% formalin to ﬁx the tissue forhistological examination. After 148 h in ﬁxative, segments
were cut from the vagina, uterus, isthmus, and magnum,
then sectioned and stained with hematoxylin and eosin before

Elongation

A

Pointedness

Polar Asymmetry

L
dL

W

L
LP

dS

0.6

r = 0.33

0.5
1.0

Galloanserae

1.4

1.2

1.6

Elongation (RC2EL)

paleognaths

Coraciiformes

1.5

1.0

1.8

r = 0.18
1

2

3

Charadriiformes

Trochilidae

4

3
2
1

4

Polar Asymmetry

Elongation

C 4

wadersPolar Asymmetry

Pointedness

AlcidaeElongation

paleognaths

B

Galliformes

r = 0.80
0.50

0.60

Pointedness

Anseriformes

2

0

−2

−4
−2

0

2

4

Asymmetry (RC1AS)
Figure 1: Egg shape parameters and morphospaces. A, Three parameters that describe the shapes of all birds’ eggs (Biggins et al. 2018):
elongation p length (L)/width (W), polar asymmetry p dL/dS, and pointedness p LP/L, where dL and dS are the diameters of the largest
circles that ﬁt within the large and small ends of the egg, respectively; L is the maximum length of the egg; and LP is the distance from the
maximum width of the egg to the small end. B, Morphospaces deﬁned by the three parameters in A. As shown by the correlation coefﬁcients,
these parameters are not independent. Silhouettes, all shown to the same length, illustrate the range of shapes represented by each parameter.
From left to right: pink-headed duck, Australian golden whistler, rufous-breasted hermit, striped kingﬁsher, Bell’s vireo, European golden plover,
ostrich, twelve-wired bird of paradise, and plains wanderer. C, Egg shape morphospace based on variables calculated as the varimax-rotated principal components of the parameters in B with asymmetry (RC1AS) representing the variation in pointedness and polar asymmetry independentof variation in elongation (RC2EL). Symbols show the mean values for each of the 955 species studied, with some representative taxa identiﬁed.

E218

Evolution of Avian Egg Shapebeing mounted on slides and imaged using a #100 optical
microscope with integrated camera.
To estimate the maximum diameter of the isthmus, wemeasured the invaginated inner wall of its lumen on composite digital photomicrographs of histological cross sections
using the segmented line tool in ImageJ software (Schindelin
et al. 2015). We used that measurement as an index of the
maximum perimeter of the fully stretched isthmus, fromwhich we calculated the maximum diameter. We recognizethat this index probably underestimates the actual diameterof the fully stretched isthmus.

Sources of Anatomical and Life History Data
We used published data sets for body mass (Dunning 2007),
pelvis anatomy (Shatkovska et al. 2018), clutch size (Myhrvold et al. 2015), structure of the incubation site (usuallya nest; Fang et al. 2018), and HWI (Sheard et al. 2020), corrected and enhanced as needed using Billerman et al. (2020).
We also used a standard reference for the developmental
mode of chicks (Nice 1962), classifying each species simply as either altricial or precocial, and we categorized thedominant mode of locomotion during foraging for each species as aerial, cursorial, perching, or swimming according
to descriptions in Billerman et al. (2020).

Measuring Egg Shape
We analyzed the images of 5,378 eggs of 955 species madefrom digital photographs taken in the ﬁeld (408 eggs of
20 species) or museum collections (2,546 eggs of 306 species) as well as from images in books (2,425 eggs of 725 species) when we could be certain that the eggs were photographed or painted to scale with the long axis of the egg
parallel to the plane of the image. To ensure the integrityof photographs in books, we contacted the photographers(Harry Taylor for Walters 1994; Douglas Elford for Johnstone and Storr 1998). We also examined correlations between measurements from real eggs and illustrations inbooks (all r 1 0:95) to ensure that published illustrations
were oriented correctly.
Following established protocols (Birkhead et al. 2019b),
we used an R script (Biggins et al. 2018) to analyze a silhouette image of each egg (e.g., ﬁgs. 1B, 6B) and calculate
elongation, polar asymmetry, and pointedness (as deﬁned
in Biggins et al. 2018; ﬁg. 1A, 1B). The values calculated
from each image were checked for accuracy by comparing
measures of the actual egg to the output from the script.
Errors were always due to anomalies on the silhouettes,
which were then corrected and reanalyzed to ensure thatany measurement errors were within 4% of the actual egg
measurements.

E219

We used principal components analysis (PCA; table S2)
with varimax rotation to reduce the three mean egg shapemeasures for each species (ﬁg. 1A, 1B) to two rotated variables (ﬁg. 1C) that are independent: RC1AS representing asymmetry (accounting for 60% of the total variationand correlated with both polar asymmetry, r p 0:96, andpointedness, r p 0:92), and RC2EL representing elongation (accounting for 35% of the total variation and correlated with elongation, r p 0:99). We used these two indexes
in all analyses of egg shape to minimize spurious correlations between egg shape indexes.
Bird and Egg Size
Where possible, we used female mass as a measure ofbird size when that was available but otherwise used average mass for either both sexes or males (in that order ofpreference). The density of birds’ eggs is close to the density of water (Paganelli et al. 1974), so egg volume is a reasonable index of egg mass and has the same dimensionality.
We also used PCA to create variables for adult mass
(PC1mass) and relative egg size (PC2relegg) that would be
independent of one another (r p 0:004, P p :999) for use
in all analyses (table S3; ﬁg. S2; ﬁgs. S1–S9 are available
online). PC1mass is highly correlated with log(adult mass)(r p 0:99). PC2relegg is highly correlated with the residualsof the regression of log(egg volume) on log(adult mass)(r p 0:99, n p mean values from 944 species; see also ﬁg. S3)
and avoids the statistical issues associated with analyses thatuse residuals as predictors (Freckleton 2002).
To analyze pelvis anatomy, we used varimax-rotated
PCA to reduce the available data (from Shatkovska et al.
2018) to two orthogonal variables (table S4), one representing pelvis size (RC1meas) and the other representing
pelvis shape (RC2ratios). RC1meas is positively correlated(r 1 0:92) with three pelvis measurements such that larger
values indicate a larger pelvis. RC2ratios is positively correlated (r p 0:67–0:89) with two ratios from different measurements than those described by RC1meas such thatlarger values indicate a more elongated pelvis.
Allometries
For the analyses of oviduct size and egg size in relation tofemale body size, we used standardized major axis (SMA)
regressions (smatr package in R) on log10-transformed variables. The slopes of these regressions were compared with
one another and with slopes of 0 and 1.0 (Warton et al. 2012).
Statistical Models
All data were analyzed using R version 4.0.4 (R Development Core Team 2021). To assess and control for the inﬂuence

E220

The American Naturalistof phylogeny in general analyses across all species, we constructed phylogenetic general least squares (PGLS) regressions using the phylolm package and a phylogeny basedon the Ericsson backbone downloaded from BirdTree (https://birdtree.org/; ﬁg. S1).
We also generated linear models (using the lm functionin the base package) for each family with 15 species in ourdata set, excluding models that did not converge or had
singularities. To reduce the effect of overﬁtting, we included
only a few predictors of interest in each of these models.
All continuous variables used as predictors in statisticalmodels were standardized (z-scores) using the scale function in R so that effect sizes (b) could be compared on thesame scale. We report this effect size and 95% CLs for eachpredictor to illustrate the magnitude and variability of theeffects across all species.

Results
General Patterns
To evaluate the generality of previous models to explain
egg shape (Stoddard et al. 2017), we constructed PGLS models (details in the supplemental PDF, available online). We
did not include diet, latitude, developmental mode, temperature, or precipitation in these general models, as noneof these factors were previously identiﬁed as having an appreciable effect on egg shape (Stoddard et al. 2017) and there
is not a plausible mechanism relating those factors to theshapes of birds’ eggs.
Stoddard et al. (2017, p. 1249) suggested that “adaptations for ﬂight may have been critical drivers of egg-shapevariation in birds,” so we sought to evaluate that prediction
in birds that use their wings for locomotion. To that end, we
focused these general analyses on the large clade of neognaths (921 species in 188 families and 34 orders in our dataset) to reduce bias from species that are ﬂightless (orders
Struthioniformes, Rheiformes, Casuariiformes, and Apterygiformes) or largely cursorial (Tinamiformes). Inclusion of
the paleognaths does not affect our conclusions (table S6).
Elongation (RC2EL). Egg elongation is signiﬁcantly associated with female mass (PC1mass; positive), HWI (positive), clutch size (negative), and incubation site across all
species of neognaths (ﬁg. 2A; table S5). The full model explains about 14% of the variation in elongation, with female mass (PC1mass) having the largest effect, about twicethat of either HWI or clutch size. Eggs in domed nests ormounds are the most elongated, while those laid in cavities, burrows, and scrapes are the most spherical. These
results are consistent with those of Stoddard et al. (2017)with respect to female mass and HWI, but that study founda signiﬁcant effect of a measure of relative egg size and no

signiﬁcant effects of incubation site or clutch size acrossall species.
Asymmetry (RC1AS). Across species of neognaths, egg asymmetry is positively related to female mass (PC1mass), clutchsize, HWI, and incubation site (ﬁg. 2B; table S5). The fullmodel, however, explains only 8% of the variation in asymmetry. HWI had the largest effect on asymmetry, approximately double the effects of either clutch size or female
mass. Eggs laid in scrapes are the most asymmetrical, whereas
those laid in mounds have the lowest asymmetry values.
These results are also consistent with those of Stoddard
et al. (2017) with respect to female mass and HWI, butthat study found no signiﬁcant effects of incubation site or
clutch size across all species.
Complications. These general across-species analyses of egg
elongation and asymmetry are complicated by model complexity and some multicollinearity among predictors thatsometimes obscures the patterns within families. Thus, evenpredictors with small and nonsigniﬁcant effects in thesegeneral models across all species are important predictorsof egg shape in some families of birds (table S9), with somewithin-family relationships positive and some negative, often opposite to the sign or magnitude of the effect in the
global model (ﬁg. 2C–2J).
Among the 55 families with ≥5 species in our data set,for example, 24%–64% of the linear model relationships
predicting elongation had signs that differed from that in
the global model (ﬁg. 2A) with respect to female mass
(PC1mass, 13/55; ﬁg. 2C), relative egg volume (PC2relegg,
35/55; ﬁg. 2D), clutch size (20/51; ﬁg. 2E), and HWI (27/55;
ﬁg. 2F; for details, see table S9a). Similarly, linear models to
predict asymmetry within families had different signs fromthat in the global model (ﬁg. 2B) with respect to female mass
(23/55; ﬁg. 2G), relative egg volume (21/55; ﬁg. 2H), clutch
size (20/51; ﬁg. 2I), and HWI (27/55; ﬁg. 2J; for details, seetable S9b).
Most of these within-family effects are based on small
numbers of species and thus have low statistical power andwide CLs (table S9). Nonetheless, closer inspection at thefamily level reveals some interesting patterns and suggests
avenues for further research. A complete family-by-family
assessment of the factors inﬂuencing egg shape is beyond
the scope of this article, but we provide a few illustrative
examples of different within-family patterns (ﬁgs. S4–S6),
providing mixed support for each predictor inﬂuencing elongation in the manner suggested by the global model.
Constraints: Oviduct Anatomy
In the 18 species of Galliformes for which we have measurements of both eggs and oviducts from the same females,

Evolution of Avian Egg Shape

E221

response: Asymmetry (RC1AS)
response: Elongation (RC2EL)
B
A

Continuous variables
Female size
Relative egg size
Clutch size
HWI
Incubation sites
Mound
Domed
Burrow
CavityCup
Platform
Scrape

2.70
–1.40

1

0

2

0

−0.5

0.5

Asymmetry (RC1AS)

Elongation (RC2EL)

Effect size (std beta±95%CL)
2

C

D

E

F

G

H

I

J

0

−2

2

0

−2
−2

0

2

Female mass (PC1mass)

−2

0

2

4 −2

Relative egg size (PC2relegg)

0

Clutch size

2

−2

0

2

Hand-wing index

Figure 2: Models to predict egg elongation and asymmetry across the avian phylogeny. A, B, Effect sizes (b with 95% conﬁdence limits [CLs])from phylogenetic linear regressions with the same set of predictors, controlling for the effects of phylogeny (for statistical details, see table S5).
C–J, Relationships between either elongation (C–F) or asymmetry (G–J) and continuous predictors in each of 55 families with ≥5 species basedon linear models with family # focal predictor interactions, controlling for the other three predictors (all predictors are standardized so thatslopes can be compared on the same scale). On all graphs, red lines and open triangles indicate negative slopes, and blue lines and ﬁlled triangles
indicate positive slopes. In C–J, dotted purple lines show slopes close to zero.

there is a clear allometric relationship between the diameter of the maximally stretched isthmus and the width of
the shelled egg (SMA slope p 0:61 [95% CLs: 0.49, 0.77],
R2 p 0:81). The negative allometry here suggests that theisthmus (and the oviduct in general; table S10) constrains
egg width, resulting in more elongated eggs in species withlarger females.
Data for the family Phasianidae support the predictionthat egg elongation increases with female size (ﬁg. 3B), controlling for relative egg size (PC2relegg). In the Megapodiidae and Cracidae (both Galliformes), however, elongation
increases with relative egg size (PC2relegg; ﬁg. 3C, 3D) but
not with female mass (PC1mass; table S11). These threefamilies differ in that the Phasianidae have relatively small

eggs (mean relative egg size [PC2relegg] p –1.14 [95%CLs: –1.39, –0.89], n p 34 species), whereas the Cracidae(0.68 [95% CLs: 0.43, 0.93], n p 20 species) and Megapodiidae (2.25 [95% CLs: 1.92, 2.59], n p 14 species) haverelatively large eggs for their body size (ﬁg. S2). These differences between the families of Galliformes suggest thatwhen species have relatively large eggs, then egg size has thelargest inﬂuence on elongation, whereas in species with relatively small eggs, the size of the female (and her oviduct)
has the largest inﬂuence on elongation.
The Megapodiidae provide the clearest example of an effect of relative egg size on elongation (ﬁg. 3C), as their eggs
are particularly large relative to female size and they are theonly birds whose eggs are incubated in mounds of rottingThe American Naturalist
Numididae
80
60

Odontophoridae

A

40

20

Residual elongation (RC2EL)

Isthmus lumen diameter (mm)

E222

1.0

B

0.0

−1.0

Galliformes
50 100500 1000

Phasianidae
−1.0

5000

1.0

0.0

1.0

Residual female mass (PC1mass)

Female mass (g)Residual elongation (RC2EL)

Phasianidae

D

C
1.0

0.5
0.0

0.0

−0.5

Megapodiidae
− 0.5

0.0

0.5

−1.0

Cracidae
−1.0

0.0

1.0

Residual relative egg volume (PC2relegg)
Figure 3: Constraints on egg shape due to oviduct anatomy in the Galliformes. A, Allometric relationship between the diameter of the isthmus
lumen and female body mass in 28 species of Galliformes in three families (allometric slope p 0:38 [95% conﬁdence limits: 0.31, 0.46]). Dashedgray line has slope p 1 (isometry). B–D, Partial regression (add-variable) plots of the relationship between residual elongation (RC2EL), residual
female mass (PC1mass; B), and residual relative egg volume (PC2relegg; C, D) in three families based on linear models (for details and models
controlling for phylogeny, see tables S10–S11).

vegetation or warm volcanic soil without contact with either the parent or other eggs. Thus, the shape of their eggs
is unlikely to be inﬂuenced by selection for increased shellstrength or parental contact during incubation, as the eggs
are warmed from all sides and are rarely exposed to heatloss.
This oviductal constraints hypothesis is supported by
two additional lines of evidence. First, within two ordersof birds that lay relatively large eggs, elongation is significantly predicted by both female mass (PC1mass) and relative egg size (PC2relegg), whereas in two orders of birds
that lay relatively small eggs, elongation is not related torelative egg size (ﬁg. 4A; table S18). Both patterns are expected as a result of the negative allometry of oviduct width
constraining egg diameter when birds lay relatively large
eggs.
Second, within the paleognaths (ostriches, rheas, cassowaries, kiwis, tinamous), relative egg size is the only variable
that predicts elongation (ﬁg. 4B; table S19). All paleognaths

are cursorial, but the pattern is the same for both ﬂightlessand ﬂying species in this clade.

Constraints: Pelvis Anatomy
The relationships between egg elongation (RC2EL) andpelvis shape (RC2ratios) are positive in species using cursorial, perching, and swimming modes of locomotion(ﬁg. 5B; tables S12, S13). The slopes of these relationships (0.20–0.29) are remarkably consistent across modesof locomotion (ﬁg. 5B; table S13). Thus, elongation increases with the relative narrowness of the pelvis (RC2ratios),
as expected from a previous study (Shatkovska et al. 2018),
although the mechanism underlying this relationship is
not known.
The relationships between egg elongation (RC2EL) andrelative pelvis size (RC1meas) for those three modes of locomotion are negative and also remarkably similar (–0.40

Evolution of Avian Egg Shape

E223

Relatively large eggs Relatively small eggs

A

Charadriiformes

Procellariformes

Accipitriformes

Passeriformes

Female mass
Relative egg size
Clutch size

NA

HWI

−0.5 00.5−0.5 0 0.5 1.0 −0.5

00.5 −0.500.5Standardized effect
Apterygidae

B

Casuariidae

Rheidae

Struthionidae

3

Tinamidae

Southern Brown Kiwi

Elongation (RC2EL)

North Island Brown Kiwi

2
Elegant Crested Tinamou

10Southern
Cassowary

Spotted Nothura

Highland Tinamou

Dwarf Cassowary

Emu

Little Tinamou
Lesser Rhea

Red-winged Tinamou
Grey Tinamou

Greater Rhea

Thicket Tinamou−1−2
Common Ostrich

−3

−2

−1

0

1

2

3

Relative egg volume (PC2relegg)
Figure 4: Further evidence for oviductal constraints on elongation. A, Elongation is inﬂuenced by female size (and its relationship to oviduct diameter) and relative egg size (PC2relegg) within two orders in which species lay relatively large eggs but not within two orders inwhich species lay relatively small eggs. Standardized effects (95% conﬁdence limits) are shown, controlling for phylogeny, with red indicating negative and blue indicating positive. B, In 15 paleognaths, elongation increases with relative egg size (PC2relegg) across all species(black line) and within the Tinamiformes, all of which can ﬂy (dashed blue line, adjusted data not shown for that regression). Regression
lines and data are predicted from linear models controlling for female mass and phylogeny (table S19).

to –0.47; ﬁg. 5A; table S13). Thus, elongation decreases as
relative pelvis size increases, as expected if pelvis size—or
something correlated with it—constrains egg width, sincethose negative relationships control for both female size

and relative egg size. In aerial birds, the signs of the relationships between elongation and both pelvis size and shape
are in the opposite directions (ﬁg. 5A, 5B; table S13), but
the reasons for this are not known.

E224

The American Naturalist

cursorial

perchingAswimming

B

2

E

Wacet
Wantr

0

Lpre

Elongation (RC2EL)

aerial

Lil
Ls
Lpost

−2

Asymmetry (R1AS)

C

D

2

0

Wish

−2
−2

0

2

–2

Relative pelvis size (RC1meas)

0

2

4

Pelvis shape (RC2ratios)

Figure 5: Predicted regression plots for the relationships between components of egg shape (elongation [RC2EL] and asymmetry [RC1AS])and both relative pelvis size (RC1meas) and pelvis shape (RC2ratios) for species with different modes of locomotion. Models control for
female size (log transformed) and phylogeny. Number of species: 37 aerial, 28 cursorial, 72 perching, and 24 swimming. A, B, Each regression
line shown is from a separate model because the interaction terms were signiﬁcant. C, D, Predicted regressions are from models with mode oflocomotion as a nonsigniﬁcant interaction with pelvis size or shape. E, Avian pelvis, modiﬁed from Shatkovska et al. (2018), showing the dimensions used in our analyses.

The asymmetry component of egg shape is not clearly
related to relative pelvis size or shape across species (ﬁg. 5C,
5D; table S12). Moreover, the statistical models to predict
asymmetry explain only 6%–9% of the variation, whereas
the models to predict elongation from pelvis size and shape
explain 27%–30% of the variation.
Pelvis shape may also explain the relationship that Stoddard et al. (2017) found between egg shape and HWI, if
HWI is related to pelvis anatomy. To assess this, we lookedat the relationships between HWI and measures of pelvis
size and shape available for 173 species (Shatkovska et al.
2018). Both the maximum distance between ischial bones(Wish in ﬁg. 5E) and the size of the pelvis (RC1meas) aresigniﬁcantly and positively correlated with HWI (table S14).
Among species with the different modes of locomotion, HWI
is not consistently related to relative pelvis size (RC1meas)or shape (RC1ratios; tables S15, S16; ﬁg. S7). Thus, HWI
is not signiﬁcantly related to pelvis size or shape in cursorial
or swimming birds, but the relationship between HWI andpelvis size is signiﬁcantly positive for perching birds andsigniﬁcantly negative for aerial birds (table S16; ﬁg. S7).
The nonsigniﬁcant relationships between HWI and pelvis

shape are positive for aerial birds and negative for perching and swimming birds (table S16; ﬁg. S7).
Revisiting General Patterns
Our analysis of the relationship between HWI and pelvis
shape (table S16; ﬁg. S7) suggests that mode of locomotion should be included in general models for egg elongation and asymmetry when HWI is also a predictor (ﬁg. 2A,
2B). In the revised models, the relationship between HWI(as an index of pelvis shape) and elongation is signiﬁcantand consistent across modes of locomotion (table 1). In themodel to predict asymmetry, however, HWI is not significant (table 1), but the signiﬁcant interactions with mode oflocomotion renders that main effect uninterpretable. Within
locomotion modes, HWI remains a signiﬁcant predictor ofasymmetry in both cursorial and perching birds but not for
aerial and swimming species (table S17).
Adaptations: Clutch Size
Across species, the effect of clutch size on elongation isnegative (table 1; ﬁg. 2A) as expected if more sphericalEvolution of Avian Egg Shape

E225

Table 1: Models to predict egg elongation (RC2EL) and asymmetry (RC1AS) from factors thought to inﬂuence
egg shape in 921 species of neognath birds, controlling for phylogeny, mode of locomotion (LOCO), and theinteraction between LOCO and hand-wing index (HWI)
Predictorsa
Intercept
Female mass (PC1mass)
Relative egg size (PC2relegg)
Clutch size
HWI
Incubation site (cup)c
Incubation site (cavity)c
Incubation site (dome)c
Incubation site (mound)c
Incubation site (platform)c
Incubation site (scrape)c
LOCO (cursorial)
LOCO (ﬂightless)
LOCO (perching)
LOCO (swimming)
LOCO (cursorial) # HWI
LOCO (ﬂightless) # HWI
LOCO (perching) # HWI
LOCO (swimming) # HWIl (bootstrapped)dR2eElongationb

Asymmetryb

2.74 (21.44, .13) [.05].40 (.28, .49) [!.0001].003 (2.06, .06) [.94]2.18 (2.24, 2.11) [!.0001].25 (.02, .48), [.03].41 (.13, .72) [.02].02 (2.28, .30) [.89].53 (.25, .86) [.006]
2.22 (1.34, 3.17) [!.0001].44 (.14, .67) [.009].17 (2.17, .56) [.36].14 (2.39, .59) [.55]
21.02 (25.88, 5.84) [.75].005 (2.52, .51) [.98]1.28 (.74, 1.79) [!.0001].03 (2.23, .28) [.84]2.08 (23.68, 3.44) [.96]2.13 (2.38, .11) [.32]
2.28 (2.56, .03) [.16].75 (.69, .82)
.18

2.65 (21.32, 2.12) [.09].10 (2.01, .21) [.08]2.03 (2.11, .05) [.42].13 (.05, .18) [.0007].01 (2.26, .20) [.91].33 (.04, .60) [.05].27 (.006, .51) [.08].33 (2.01, .67) [.08]2.42 (21.35, .68) [.44].10 (2.21, .35) [.53].48 (.07, .84) [.01]2.17 (2.61, .24) [.47]
21.64 (27.80, 3.78) [.59]2.26 (2.72, .24) [.29]
2.17 (2.68, .33) [.57].40 (.17, .70) [.005]
21.35 (24.85, 1.50) [.46].20 (2.07, .49) [.14].21 (2.15, .48) [.27].80 (.71, .84)
.09

aContinuous predictors were all standardized to facilitate comparison of effects on the same scale.
Effects are b, with 95% conﬁdence limits in parentheses and P values in brackets. Signiﬁcant effects are in bold.
cEffects are compared with eggs laid in burrows (effect p 0).
d
Measure of the phylogenetic signal.
e
Proportion of variance explained controlling for phylogeny speciﬁed by l.
beggs are favored in larger clutches because of their thermal properties (lower rate of heat loss due to lower surfaceto-volume ratio) and resistance to breakage. In simple linear models for each of 51 families with 15 species in ourdata set (table S9a), there are both positive (20) and negative(31) effects of clutch size on elongation.
While the linear effect of clutch size on asymmetry acrossall neognaths is negligible (table 1), clutch size is positively
associated with asymmetry for mean clutch sizes of one tofour eggs laid in scrapes (ﬁg. 6A; table S21), as predicted(Andersson 1978). There is also a positive trend acrossneognaths that do not lay eggs in scrapes, with asymmetry increasing across the full range of clutch sizes. Even within the
Passeriformes, where most species do not have particularly
asymmetric eggs, asymmetry increases weakly with clutch size
across all species up to clutches of six eggs (ﬁg. 6B; table S20),
although there are many exceptions with some of the withinfamily slopes being negative (ﬁg. 6B; table S9b).
Adaptations: Incubation Site
The most elongated eggs are laid singly in mounds of vegetation or soil, with elongation decreasing from domed nests

to cups, platforms, and scrapes (ﬁg. 2A; table 1). These incubation sites are progressively less well insulated. Species
laying eggs in cavities and burrows do not ﬁt this pattern,as those sites are not exposed, yet their eggs are the least
elongated, possibly to reduce the chance of breakage in dark,
cramped quarters with little or no nesting material or toincrease thermal efﬁciency when clutch size is large. We
used general categories for incubation site for this analysis
such that there was no within-family variation, potentiallylimiting the statistical power, especially as the insulating
properties of nests and the potential for egg breakage mustvary within these broad categories of incubation site.
Eggs that are closer to being perfect prolate spheroids—from perfect spheres to symmetrical ovoids, with polar asymmetry close to 1 and pointedness close to 0.5—are relatively
uncommon in birds (ﬁg. 1A, 1B), conﬁned to a few families with small clutches and well-insulated incubation sites(Trochilidae [hummingbirds], Megapodiidae [mound builders]). Eggs that are near-perfect spheres are found in species with larger clutches laid in cavities without lined nests,
where the eggs might be more susceptible to breakage (Coraciiformes [kingﬁshers and their allies] and some species ofStrigidae [owls] and Anatidae [waterfowl]).

E226

The American Naturalist
scrape ≤4 eggs

other

A

4

Asymmetry (RC1AS)

scrape >4 eggs

20Discussion
−2
0

4

8

12

16

20

Clutch size

Asymmetry (RC1AS)

posed in incubation sites ranging from mounds and burrows to cavities, cups, and domed nests to scrapes (ﬁg. 2B;
table 1) in general, as well as within neognath orders that
include species with more than one type of incubation site(ﬁg. 7; table S22). While several of these comparisons among
the asymmetry of eggs laid in different incubation sites are
not statistically signiﬁcant, the patterns are remarkably consistent within some orders of birds.

1.5

B

1.0

t

0.5
0

−0.5
0

2

4

6

Clutch size
Figure 6: A, Relationships between egg asymmetry (RC1AS) andclutch sizes of neognath species that lay their eggs in scrapes withclutch sizes ≤4 (solid red line and circles; 108 species) or 14 (red triangles; 8 species) and for species laying eggs in all other incubation sites (dashed blue line and dots; 811 species). Each regression
is predicted from a phylogenetic general least squares (PGLS) model
controlling for female mass (PC1mass), relative egg size (PC2relegg),mode of locomotion, hand-wing index (HWI), and incubation site,
as well as controlling for phylogeny (table S21). B, Relationship between egg asymmetry and clutch size in 16 families of Passeriformesthat lay average clutches of ≤6 eggs in cup nests. Shown here are
predicted relationships from linear models for each family, controlling for female size (PC1mass), relative egg size (PC2relegg), and HWI.
Silhouettes show the full range of asymmetries scaled to the samelength in order from top to bottom: common chafﬁnch, horned lark,
and yellowhammer. Solid blue lines have positive slopes, and dotted
red lines have negative slopes. The dashed blue line is predicted with
95% conﬁdence limits from a PGLS model on all Passeriformes inour data set that laid eggs in cup nests with clutch size ≤6 (235 species), using the same model structure as for the separate family-levellinear models (table S20).

Egg asymmetry is also related to incubation site in thatspecies having the least asymmetric eggs incubate them insites most protected from heat loss (mounds and burrows).
Asymmetry increases as eggs become generally more ex-

Across a broad panoply of birds of the world, we foundthat egg shape is largely determined by (i) anatomical constraints imposed by the oviduct and pelvis and (ii) adaptations that are likely to reduce breakage and increase
thermal efﬁciency of eggs at the incubation site. It is also
possible that some of the anatomical constraints that wehave identiﬁed evolve in response to selection on egg size.
For example, when selection favors larger eggs in precocial
species (e.g., Boersma 1982) or in species where managing
cooling rates is critical (e.g., Martin 2008), we might expect
a coevolutionary response in the oviduct and pelvis. In addition to this general conceptual framework, we have documented four key advances over previous work on this
topic.
First, while our analyses also provide some support forthe conclusion of Stoddard et al. (2017, p. 1253) that “adaptations for high-powered ﬂight . . . may have considerable
effects on egg shape,” our study suggests that adaptations of
the pelvis (or general body conformation) to different formsof locomotion may be more relevant than simply adaptations to high-powered ﬂight. Thus, while HWI is positively related to elongation (table 1) across all bird species,
egg shape is not positively correlated with HWI withinmany avian families and orders (ﬁgs. 2F, 2J, S4–S6; tables S9, S18–S20, S22 ). One source of this variability islikely the different relationships between HWI and pelvis
anatomy in species that use different modes of locomotion (table S16; ﬁg. S7).
Second, the structure of both the oviduct and the pelvis
appears to constrain egg shape in a predictable manner(ﬁgs. 3–5). Thus, we argue that egg elongation, in particular, is the result of constraints on shape imposed by adaptive responses to selection on body size or mode of locomotion. The occasional occurrence of runt and double-yolked
eggs in the clutches of many species (Koenig 1980; Birkhead
et al., forthcoming) provides additional support for this idea.
Runt eggs are abnormally small eggs, often lacking a yolk,
and are invariably more spherical (less elongated) than is
typical for the species, just as expected if oviduct or pelvis
anatomy limits the diameter of eggs. Similarly, double-yolked
eggs are larger than is typical for the species, and those eggs

Evolution of Avian Egg Shape

African Scops Owl

E227

4

Pheasant-tailed Jacana0

Eurasian Scops Owl

62

Asymmetry (RC1AS)

2

38

1
11

3
−1

1

0

21

Strigiformes
Burrow

CavityPlatform Scrape

White Tern
−2

Burrow

1

2

Charadriiformes

Platform

ScrapeSpotted Wood Kingﬁsher

5
0

55

6

0

16

23

−1

−2

Galliformes
Mound

Platform

Coraciiformes

ScrapeBurrow

CavityIncubation Site
Figure 7: Asymmetry increases with openness of the incubation site within four orders that display a range of incubation sites. Data shown are
species means as well as Tukey boxplots summarizing medians, interquartile ranges (IQRs; boxes), and 1.5 times the IQR (whiskers). Sample sizes
are shown at the top of each box. For an exception to this pattern, see ﬁgure S9.

are, on average, more elongated in the common murre (Uriaaalge; Birkhead et al., forthcoming).
This study is the ﬁrst to measure oviductal anatomy inbirds, and the data were hard-won because of the need forspecimens that were laying eggs. Thus, we quantiﬁed oviduct allometry only in the Galliformes and have assumed
that the relationships between oviduct size and female size
would be similar for all birds, as has been found for otheraspects of avian anatomy and physiology (Calder 1984;
Burton 2008; Field et al. 2013). Our results support thisassumption as elongation increases (i) with female mass
(PC1mass; due to negative allometry with oviduct diameter;ﬁg. 3A) across all species (ﬁg. 2A; tables 1, S5, S6) and withinsome families and orders (ﬁg. 3B; tables S9, S18–S20) and(ii) with relative egg size (PC2relegg) within families andorders in which species lay particularly large eggs (ﬁgs. 3C,
3D, 4A, 4B; table S18a).
Two recent studies have also looked at the relationship between nest design and egg shape in large avifaunas.
Duursma et al. (2018) identiﬁed both climate and nest
structure as inﬂuencing egg elongation in 308 Australianpasserine species. Their ﬁnding that a warmer within-nest

microclimate selects for more elongated eggs is consistent
with our results (table 1). Nagy et al. (2019) looked at correlations between nest and egg characteristics in 855 European birds, simply categorizing nest design as open, semiopen, or closed and quantifying egg shape only in termsof elongation (width/length). Their analyses suggest thateggs evolved to be more spherical in closed nests but more
elliptical in open nests. This is supported by our ﬁndingthat eggs laid in cup nests are more elongated than thoselaid in cavities (table 1) but is not consistent with our resultsfor other incubation sites. Unlike our study and Duursma
et al. (2018), Nagy et al. (2019) did not classify nest designin functional terms (with respect to stability, breakage, thermal efﬁciency, clutch sizes), and this may account for thedifferences in our ﬁndings. Neither Duursma et al. (2018)
nor Nagy et al. (2019) looked at asymmetry or any othermeasure of egg shape.
Our analysis of pelvic anatomy suggests that pelvis shape
also constrains egg diameter, although the underlying mechanism is unclear. Thus, the relationship between elongation and pelvis shape is supported by both a direct relationship between these two variables in a sample of 141 species

E228

The American Naturalist(ﬁg. 5B; table S12) and an indirect relationship using HWI
as a proxy for pelvis shape for all species in our sample(table 1), as well as in within some orders and families(ﬁg. S6A, S6B).
Shatkovska et al. (2018) looked at the relationship between various measures of pelvis shape and egg shape in
173 species in 25 avian orders and 49 families. They foundthat pelvis shape was related to both habitat and the modeof chick development, concluding that those factors in turninﬂuenced egg shape. The mode of chick development, however, has no effect on either elongation or asymmetry whencontrolling for relative egg size (table S8), and mode of locomotion is probably the underlying mechanism—rather
than habitat—related to both pelvis shape and egg elongation (table 1). While Shatkovska et al. (2018, p. 10) focusedon pelvis size and shape, they concluded that “the shape of
pelvis mainly determines body shape, and thus the shape ofabdominal cavity and interposition of viscera in it,” suggesting that the pelvis itself may not be the underlying causeof egg shape. Further work is needed to determine how
pelvis shape or general body conformation inﬂuences elongation independent of relative oviduct size.
Third, egg asymmetry increases with both clutch size andthe openness of incubation sites across species (ﬁgs. 2B, 6,
7; tables 1, S5–S7, S21, S22), as expected from both theory(Andersson 1978; Barta and Szekely 1997) and an empirical study (Birkhead et al. 2019b), respectively. However,asymmetry is also related to pelvis shape (ﬁg. 5D) andHWI (as an index of pelvis shape) in perching species (table S17b), but the underlying mechanism is unknown andneeds further study.
Finally, the broad patterns across all bird species conceal an underlying complexity wherein the sign and magnitudes of those patterns vary among the ~50 families that
we analyzed separately. Thus, within each family of birds,
egg shape is inﬂuenced by a variety of anatomical and environmental factors, with often little consistency among
even closely related taxa (ﬁgs. 2C–2J, 4, 6, 7). Such taxonspeciﬁc patterns have been uncovered in a variety of life
history and behavioral traits (Bennett and Owens 2002).
As we have shown, global cross-species patterns of egg
shape in relation to anatomical and environmental variables
sometimes mask other biologically interesting within-taxon
patterns (but see Stoddard et al. 2017, 2019). Thus, we foundwell-supported trends within families and orders (ﬁgs. 3B–
3D, 4A, 6, S4–S6; tables S9, S19, S20) that are not consistent
with general trends across all species (table 1). General statistical models based on data across a wide diversity of species often tacitly assume that there is no variation in slopes
among constituent groups. As a result, small effect sizes inbroadscale comparative studies can mask useful insights
into the underlying mechanisms, whether these be adaptations or constraints. Such global analyses may often be

subject to Simpson’s paradox (Samuel et al. 2000) wherein
within-taxon trends sometimes have the opposite sign toglobal trends (ﬁgs. 2C–2J, 4A, 6B).
The only other study of egg shape across a large taxon
looked at the shapes of eggs in 6,706 insect species from526 families and all extant orders (Church et al. 2019).
As in the present study, they concluded that egg shape in
the insects cannot be explained by a single factor across
such a diverse array of species and that “where eggs arelaid . . . underlies the evolution of insect egg size and shape”(p. 58).
Unexplained Variation
Our exploration of the factors inﬂuencing egg shape within
avian families and orders explained considerably more of
the variation in egg asymmetry and elongation than statistical models based on species across the avian phylogeny(e.g., tables 1, S5–S8). Such an increase in explanatory powerof models is not unexpected when dealing with traits thatvary among taxa in their inﬂuence on egg shape (see also
Stoddard et al. 2019). Within orders and families, for example, the variables that we studied explained as much as
85% of the variation in elongation and 77% of the variationin asymmetry (tables S18, S22).
While our statistical models are sometimes able to explain much of the interspeciﬁc variation in egg shape, there
remains considerable unexplained variation that is likely
due to measurement error. For example, our measure of female size (body mass) may often be inaccurate because it
was based on few samples, on combined values for the twosexes, or on unknown sexes and was rarely restricted tothe breeding season. Despite an excellent compilation ofavian body masses for almost 85% of extant bird species(Dunning 2007) that is widely used in comparative studies, 10% of those species are represented by a single measurement, and 25% are represented by ≤5 samples, with data
explicitly on females for only 400 species. For the analysisof allometric patterns of egg shape and anatomy related tobody size, accurate measurements of female size and shape
are crucial.
Unanswered Questions
The approach we have taken for understanding the variation in avian egg shapes requires a logical link to the underlying mechanisms. Even though birds’ eggs have been
intensively studied for more than a century, relatively little is known about the anatomical and physiological mechanisms that we have focused on in this study. How does
the isthmus of the oviduct constrain elongation, and how
does that constraint vary among families? How does theshape of the pelvis inﬂuence egg shape (Shatkovska et al.

Evolution of Avian Egg Shape2018)? How does the incubation environment (Deeming
and Reynolds 2015), the behavior and morphology of theparents (Boulton and Cassey 2012; Deeming 2016), and thecomposition and shape of the egg itself (Sotherland andRahn 1987; Deeming 2018) inﬂuence how an egg gains heat
when a parent is incubating and loses heat when that parent is absent? And how does the thermal efﬁciency of an
egg in a normal clutch size inﬂuence chick development
and survival (Boulton and Cassey 2012) and thus selectfor particular egg shapes? In this article, we provide a broad
framework in which to address those questions, recognizing that the answers are likely to be complex and often
taxon speciﬁc. We have also made a fair start at quantifying the shapes of birds’ eggs in an accurate, repeatablefashion, but a more complete database from both museum
and ﬁeld studies is essential to understand why birds’ eggs
are so variable in shape both within and between species.
Acknowledgments
We are particularly grateful to the following museums (andpeople) for access and permission to photograph eggs intheir collections: Natural History at Tring (Douglas Russell),Manchester Museum (Henry McGhie), Natural History
Museum of Denmark (Jon Feldså), National Museum ofWales (Julian Carter, Jennifer Gallichan), Tromsø University Museum (Robert Barrett), Tyne and Wear Archives andMuseums (Dan Gordon), University of California Berkeley
Museum of Vertebrate Zoology (Carla Cicero, Michael Nachman), Royal Ontario Museum (Mark Peck, Santiago Claramunt), American Museum of Natural History (Paul Sweet,
Joel Cracraft), and Delaware Museum of Natural History(Jean Woods). This work was supported by research grants
from the Leverhulme Trust (RPG-2015-221) and the European Research Council PCSSIB (grant 268688) awarded to
T.R.B. and from the Natural Sciences and Engineering Research Council of Canada (RGPIN/05711-2014) awarded to
R.M. Ben Bolker, Douglas Elford, George and Mark Peck,
Harry Taylor, and Joe Tobias responded to our inquiries
about specimens, photographs, data, and statistical analysis.
Haley Kenyon, Danielle Montgomerie, and Jie Yuen assistedwith the collection of images from museum specimens andpublished photographs; Ian Clark, Emily Glendenning, andAlex Ball assisted with galliform dissections; and Bruce Lyon,
David Winkler, Russell Bonduriansky, Tony Williams, and an
anonymous reviewer provided valuable feedback on draftsof the manuscript.
Statement of Authorship
R.M. and T.R.B. conceptualized the research; R.M., T.R.B.,
and J.E.T. photographed eggs; R.M. and J.E.T. analyzed egg
shapes; N.H. and T.R.B. collected and measured oviducts;

E229

R.M. performed all statistical analyses; R.M. and T.R.B.
wrote the ﬁrst draft of the manuscript; all authors contrib
uted to and approved the ﬁnal version of the manuscript.

Data and Code Availability
All code and data sets required to replicate these analyses
are available in the Dryad Digital Repository (https://doi.org/10.5061/dryad.sj3tx9648; Montgomerie et al. 2021).

Literature Cited
Andersson, M. 1978. Optimal egg shape in waders. Ornis Fennica
55:105–109.
Bain, M. M. 1991. A reinterpretation of eggshell strength. Pages 131–
145 in S. E. Solomon, ed. Egg and eggshell quality. Wolfe, London.
Barta, Z., and T. Szekely. 1997. The optimal shape of avian eggs.
Functional Ecology 11:656–662.
Bennett, P. M., and I. P. F. Owens. 2002. Evolutionary ecology ofbirds: life histories, mating systems and extinction. Oxford University Press, New York.
Biggins, J. D., J. E. Thompson, and T. R. Birkhead. 2018. Accurately
quantifying the shape of birds’ eggs. Ecology and Evolution 8:9728–
9738.
Billerman, S. A., B. K. Keeney, P. G. Rodewald, and S. T. Editors.
2020. Birds of the world. Cornell Laboratory of Ornithology,
Ithaca, NY.
Birkhead, T. 2016. The most perfect thing: inside (and outside) abird’s egg. Bloomsbury, London.
Birkhead, T. R., M. Attard, and A. Pilastro. 2019a. Subtle egg-shellmembrane structures in birds’ eggs. Molecular Reproduction andDevelopment 86:353.
Birkhead, T. R., D. R. Russell, and J. E. Thompson. Forthcoming.
Abnormal eggs of the common guillemot Uria aalge: the role ofstress. Seabird.
Birkhead, T. R., J. E. Thompson, and R. Montgomerie. 2018. The
pyriform egg of the common murre (Uria aalge) is more stable on
sloping surfaces. Auk 135:1020–1032.
———. 2019b. The evolution of egg shape in birds: selection during
the incubation period. Ibis 161:605–618.
Boersma, P. D. 1982. Why some birds take so long to hatch. American Naturalist 120:733–750.
Boulton, R. L., and P. Cassey. 2012. How avian incubation behaviour inﬂuences egg surface temperatures: relationships with egg
position, development and clutch size. Journal of Avian Biology
43:289–296.
Burton, R. F. 2008. The scaling of eye size in adult birds: relationshipto brain, head and body sizes. Vision Research 48:2345–2351.
Calder, W. A. 1984. Size, function, and life history. Harvard University Press, Cambridge, MA.
Church, S. H., S. Donoughe, B. A. S. de Medeiros, and C. G.
Extavour. 2019. Insect egg size and shape evolve with ecology but
not developmental rate. Nature 571:58–62.
Claramunt, S., N. A. Wright, and M. S. Webster. 2017. Using museum specimens to study ﬂight and dispersal. Pages 127–141 in
M. S. Webster, ed. The extended specimen: emerging frontiers incollections-based ornithological research. CRC, Boca Raton, FL.

E230

The American Naturalist

Deeming, D. C. 2016. How does the bird-nest incubation unit
work? Avian Biology Research 9:103–113.
———. 2018. Effect of composition on shape of bird eggs. Journal of
Avian Biology 49:jav-01528.
Deeming, D. C., and G. Mayr. 2018. Pelvis morphology suggeststhat early Mesozoic birds were too heavy to contact incubate theireggs. Journal of Evolutionary Biology 31:701–709.
Deeming, D. C., and J. S. Reynolds, eds. 2015. Nests, eggs, and incubation: new ideas about avian reproduction. Oxford University
Press, Oxford.
Dunning, J. B., Jr., ed. 2007. CRC handbook of avian body masses.
CRC, Boca Raton, FL.
Duursma, D. E., R. V. Gallagher, J. J. Price, and S. C. Grifﬁth. 2018.
Variation in avian egg shape and nest structure is explained byclimatic conditions. Scientiﬁc Reports 8:4141.
Fang, Y.-T., M.-N. Tuanmu, and C.-M. Hung. 2018. Asynchronous evolution of interdependent nest characters across the avian
phylogeny. Nature Communications 9:1863.
Field, D. J., C. Lynner, C. Brown, and S. A. F. Darroch. 2013. Skeletal correlates for body mass estimation in modern and fossil
ﬂying birds. PLoS ONE 8:e82000.
Freckleton, R. 2002. On the misuse of residuals in ecology: regression of residuals vs. multiple regression. Journal of Animal Ecology 71:542-545.
Hackett, S. J., R. T. Kimball, S. Reddy, R. C. K. Bowie, E. L. Braun,
M. J. Braun, J. L. Chojnowski, et al. 2008. A phylogenomic studyof birds reveals their evolutionary history. Science 320:1763–
1768.
Jarvis, E. D., S. Mirarab, A. J. Aberer, B. Li, P. Houde, C. Li, S. Y. W.
Ho, et al. 2014. Whole-genome analyses resolve early branches inthe tree of life of modern birds. Science 346:1320–1331.
Jetz, W., G. H. Thomas, J. B. Joy, K. Hartmann, and A. O. Mooers.
2012. The global diversity of birds in space and time. Nature
491:444–448.
Johnstone, R. E., and G. M. Storr. 1998. Handbook of Western
Australian birds. Vols. 1–2. Western Australian Museum, Perth.
Kaiser, G. W. 2010. The inner bird: anatomy and evolution. University of British Columbia Press, Vancouver.
Kimball, R. T., C. H. Oliveros, N. Wang, N. D. White, F. K. Barker,
D. J. Field, D. T. Ksepka, et al. 2019. A phylogenomic supertreeof birds. Diversity 11:109.
Koenig, W. D. 1980. The determination of runt eggs in birds.
Wilson Bulletin 92:103–107.
Lack, D. 1968. Ecological adaptations for breeding in birds. Chapman & Hall, London.
Mallock, A. 1925. The shapes of birds’ eggs. Nature 116:311–312.
Mao, K. M., F. Sultana, M. A. R. Howlider, A. Iwasawa, andN. Yoshizaki. 2006. The magnum-isthmus junction of the fowl
oviduct participates in the formation of the avian-type shellmembrane. Zoological Science 23:41–47.
Martin, T. E. 2008. Egg size variation among tropical and temperate songbirds: an embryonic temperature hypothesis. Proceedingsof the National Academy of Sciences of the USA 105:9268–9271.
Martin, T. E., J. C. Oteyza, A. J. Boyce, P. Lloyd, and R. Ton. 2015.
Adult mortality probability and nest predation rates explain parental effort in warming eggs with consequences for embryonicdevelopment time. American Naturalist 186:223–236. https://doi.org/10.1086/681986.
Montgomerie, R., N. Hemmings, J. E. Thompson, and T. R.
Birkhead. 2021. Data from: The shapes of birds’ eggs: evolutionary

constraints and adaptations. American Naturalist, Dryad Digital
Repository, https://doi.org/10.5061/dryad.sj3tx9648.
Myhrvold, N. P., E. Baldridge, B. Chan, D. Sivam, D. L. Freeman,
and S. K. M. Ernest. 2015. An amniote life-history database toperform comparative analyses with birds, mammals, and reptiles.
Ecology 96:3109–3109.
Nagy, J., M. E. Hauber, I. R. Hartley, and M. C. Mainwaring. 2019.
Correlated evolution of nest and egg characteristics in birds.
Animal Behaviour 158:211–225.
Nesteruk, I., G. Passoni, and A. Redaelli. 2014. Shape of aquatic
animals and their swimming efﬁciency. Journal of Marine Biology 2014:470715.
Nice, M. M. 1962. Development of behavior in precocial birds.
Linnean Society of New York, New York.
Paganelli, C. V., A. Olszowka, and A. Ar. 1974. The avian egg: surface
area, volume, and density. Condor 76:319–325.
Preston, F. W. 1953. The shapes of birds’ eggs. Auk 70:160–182.
———. 1968. The shapes of birds’ eggs: mathematical aspects. Auk
85:454–463.
———. 1969. Shapes of birds’ eggs: extant North American families. Auk 246–264.
Prum, R. O., J. S. Berv, A. Dornburg, D. J. Field, J. P. Townsend,
E. M. Lemmon, and A. R. Lemmon. 2015. A comprehensive
phylogeny of birds (Aves) using targeted next-generation DNA sequencing. Nature 526:569–573.
R Development Core Team. 2021. R: a language and environment
for statistical computing. R Foundation for Statistical Computing,
Vienna.
Rensch, B. 1959. Evolution above the species level. Methuen,
London.
Samuel, M., S. B. Cox, M. Willig, G. G. Mittelbach, C. Osenberg,and M. Kaspari. 2000. Species richness, species-area curves andSimpson’s paradox. Evolutionary Ecology Research 2:791–802.
Schindelin, J., C. T. Rueden, M. C. Hiner, and K. W. Eliceiri. 2015.
The ImageJ ecosystem: an open platform for biomedical image analysis. Molecular Reproduction and Development 82:518–
529.
Shatkovska, O. V., M. Ghazali, I. S. Mytiai, and N. Druz. 2018. Sizeand shape correlation of birds’ pelvis and egg: impact of developmental mode, habitat, and phylogeny. Journal of Morphology
279:1590–1602.
Sheard, C., M. H. C. Neate-Clegg, N. Alioravainen, S. E. I. Jones,
C. Vincent, H. E. A. MacGregor, T. P. Bregman, S. Claramunt,and J. A. Tobias. 2020. Ecological drivers of global gradients inavian dispersal inferred from wing morphology. Nature Communications 11:2463.
Sotherland, P. R., and H. Rahn. 1987. On the composition of bird
eggs. Condor 89:48–65.
Stoddard, M. C., C. Sheard, D. Akkaynak, E. H. Yong, L.
Mahadevan, and J. A. Tobias. 2019. Evolution of avian egg shape:
underlying mechanisms and the importance of taxonomic scale.
Ibis 161:922–925.
Stoddard, M. C., E. H. Yong, D. Akkaynak, C. Sheard, J. A. Tobias,
and L. Mahadevan. 2017. Avian egg shape: form, function, andevolution. Science 356:1249–1254.
Thienemann, F. A. W. 1825. Systematische Darstellung der Fortpﬂanzung der Vögel Europa’s mit Abbildung der Eier. J. A. Barth,Leipzig.
Thompson, D. W. 1908. On the shapes of eggs, and the causes
which determine them. Nature 78:111–113.

Evolution of Avian Egg Shape———. 1917. On the shapes of eggs, and of certain other hollow
structures. Pages 652–669 in D. W. Thompson, ed. On growthand form. Cambridge University Press, Cambridge.
Tschanz, B., P. Ingold, and H. Lengacher. 1969. Eiform undBruterfolg bei Trottellummen. Der Ornithologische Beobachter
66:25–42.
Walters, M. 1994. Birds’ eggs. Dorling Kindersley, London.
Warham, J. 1990. The petrels: their ecology and breeding systems.
Academic Press, San Diego, CA.
Warton, D. I., R. A. Duursma, D. S. Falster, and S. Taskinen. 2012.
smatr 3—an R package for estimation and inference about allometric lines. Ecology and Evolution 3:257–259.

E231

References Cited Only in the Online Enhancements
Björklund, M. 2019. Be careful with your principal components.
Evolution 73:2151–2158.
Jetz, W., C. H. Sekercioglu, and K. Böhning-Gaese. 2008. The
worldwide variation in avian clutch size across species and space.
PLoS Biology 6:2650–2657.
Liker, A., J. D. Reynolds, and T. Szekely. 2001. The evolution ofegg size in socially polyandrous shorebirds. Oikos 95:3–14.
Associate Editor: Tony D. Williams
Editor: Russell Bonduriansky

From left to right: band-rumped storm petrel; Bulwer’s petrel; Audubon’s shearwater; wedge-tailed shearwater; Atlantic yellow-nosed albatross; short-tailed shearwater; white-chinned petrel; southern giant petrel; sooty shearwater; wandering albatross. Credit: Tim Birkhead.