Canadian Journal of Zoology
Size and shape of Neognathae's eggs: Effects of developmental mode and phylogeny
Journal: Canadian Journal of Zoology
Manuscript ID cjz-2016-0142.R1
Manuscript Type: Article
Date Submitted by the Author: 20-Dec-2016
Complete List of Authors: Mytiai, Ivan; National University of Life and Environmental Science of Ukraine Shatkovska, Oksana; Schmalhausen Institute of Zoology Ghazali, Maria;Draft Schmalhausen Institute of Zoology
Keyword: birds, developmental mode, precocial, altricial, eggs shape
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Title: Size and shape of Neognathae's eggs: Effects of developmental mode and phylogeny
Authors: I. S. Mytiai *1 , O. V. Shatkovska **2 , M. Ghazali **3
Addresses:
* - National University of Life and Environmental Science of Ukraine, Vul. General
Rodimtsev, 19, building 1, Kyiv, 03041, Ukraine
** – Schmalhausen Institute of Zoology of NAS of Ukraine, Vul. B. Khmelnytskogo, 15, Kyiv,
01030, Ukraine
E-mails: 1 – [email protected] Draft 2 – [email protected]
Corresponding author:
Oksana Shatkovska,
Schmalhausen Institute of Zoology of NAS of Ukraine, Vul. B. Khmelnytskogo, 15, Kyiv,
01030, Ukraine;
Phone: + 38 044 234 30 93
E-mail: [email protected]
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Abstract:
We evaluated the variation in absolute size and shape of birds' eggs and the effects of developmental mode and phylogenetic relatedness on these traits. Eggs were characterized by length, diameter, and three indices of egg shape. Indices of egg shape were calculated as the ratio of radii which described the curvature of pointed end (cloacal zone), blunt end (infundibular zone) and lateral zone to egg diameter. We found that eggs shape was less variable than the absolute size of eggs. Index of the cloacal zone was the most changeable and index of the infundibular zone was very conservative. Size and shape of eggs could be better explained with phylogenetic relatedness than developmental mode.
Key words : birds, egg shape, developmental mode, precocial, altricial
Draft
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Developmental modes in birds are determined on the basis of anatomical and
physiological traits of the neonates, nest attendance, feeding behavior, and parent-chick
relationship (Portmann 1935; Nice 1962; Ricklefs 1983; O’Connor 1984; Starck 1993; Starck
and Ricklefs 1998). There are several classifications of altricial – precocial spectrum in birds
(Portmann 1935; Nice 1962; Skutch 1976; Starck 1993). Categories of developmental modes
range from altricial birds whose hatchlings are completely helpless to superprecocial that can fly
from the first day of postnatal life as megapodes. There are many intermediate states between
these extreme categories. Researchers usually distinguish from four to eight categories of
developmental modes (Portmann 1935; Nice 1962; Skutch 1976; Starck 1993; Dial 2003).
Developmental modes are often considered in connection with egg traits: egg mass
(Heinroth 1922; Amadon 1943; Nice 1962; Starck and Ricklefs 1998; Tullberg et al. 2002; Deeming 2007 a: Deeming 2007 b; DraftDyke and Kaiser 2010) and egg composition (Nice 1962; Ricklefs 1977; Starck and Ricklefs 1998; Deeming 2007 b; Sibly et al. 2012). Olsen et al. (1994)
found that eggs become proportionally longer with increase of body weight; once the effect of
body weight was removed, elongation of the egg positively correlated with clutch size in semi-
precocial Caprimulgiformes, but not in other birds (altricial or precocial). The egg shape was
calculated as the ratio of length to diameter. In our opinion, this formula is insufficient to
describe the egg shape. There are three zones in the egg: blunt end (infundibular zone), pointed
end (cloacal zone) and lateral zone (Kostin 1977). Preston (1953; 1968; 1969; 1974) was the first
who drew attention to the need to use characteristics of polar zones to describe the egg shape.
However, the method offered by Preston for determining the radius of polar zones did not
spread, probably, due to the complexity of the application.
One of us proposed an original method for determining radii of surface curvature of egg
areas based on using digital photography of eggs and computer programs (Mytiai 2008) that
made possible comprehensively analyze the shape of birds’ eggs. Indices of egg shape were
https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 4 of 24 proposed to avoid the influence of size in analysis of egg shape and to make the comparable shape of eggs of different sizes.
In our study, we aimed to focus on the variation of the egg shapes across different developmental modes and to test differences between them.
Materials and methods
Geometrically, bird's egg is asymmetric oval (ovoid) that consists of three zones: blunt end (infundibular zone), pointed end (cloacal zone) and lateral zone. Each zone could be presented with a specific circle. The contour of the egg is drawn from the combination of the arcs (Fig. 1). Radii of infundibular (circle O3, Fig. 1), lateral (circle O2) and cloacal (circle O1) zones, diameter, and length are initial independent parameters which were used to calculate indices of the egg shape. Scheme ofDraft egg measurements proposed by Mytiai (2003) is shown on Fig. 1.
Length ( L) and maximum breadth, hereinafter called diameter ( D) of eggs, were measured using a caliper to the nearest 0.1 mm. Radii of infundibular ( ri ), lateral ( rl ) and cloacal
(rc ) zones were measured by digital photos using computer programs written especially by
Shelestyuk, Trotsenko, Demchenko and Mytiai (Mytiai 2003; Mytiai 2008). In total 13060 eggs were described for 557 species of birds from 28 orders. Taxonomy and nomenclature of the studied birds were given according to Jetz et al. (2012). Egg parameters were averaged for each species (Supplementary Material: Table S1).
Indices of egg shape were calculated as follows: Iiz = ri / D , Ilz = rl / D , Iсz = rс / D , where Iiz, Iсz, Ilz are indices of infundibular, lateral and cloacal zones; ri, rl , rc are radii of infundibular, lateral and cloacal zones, D is diameter. Asymmetry of polar zones of egg was estimated with the ratio of rc / ri ; eggs with rc / ri more than 0.75 were considered to be symmetrical. Spherical eggs were distinguished as eggs with elongation ratio (D / L) more than
0.75.
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According to Mytiai (2014), eggs with Iiz close to 0.5 (i.e. ri close to half of D) are called
normal ovoids (in terms of Fig. 1 these eggs have coincident O3 and O circles). Otherwise, Iiz <
0.5, eggs are called pseudo-ovoids; symmetric or asymmetric pseudo-ovoids according to the
relative size of polar zones (Iiz and Icz ). Besides, large values of Icz correlate with the blunt
cloacal end and small values of Icz correspond to the sharp cloacal zone; large values of Ilz
correlate with elongation of the egg.
Material (raw measurements and photographs) was gathered in field and museum
collections: National Natural Science Museum of NAN of Ukraine, Zoological Museum of Taras
Shevchenko National University of Kyiv (Ukraine), Zoological Museum of Ivan Franko
National University of Lviv (Ukraine), State Museum of Natural History (Lviv, Ukraine), State
Museum of Nature of V. N. Karazin Kharkiv National University (Ukraine) and Zoological Museum of Moscow State UniversityDraft (Russian). We used 5000 trees from the database at http://birdtree.org to make a phylogenetic
reconstruction (Jetz et al. 2012). Hackett All Species subset was chosen (Hackett et al. 2008).
Maximum clade-credibility tree was produced with TreeAnnotator (Drumond et al. 2012).
Developmental modes were defined according to Starck and Ricklefs (1998) with some
simplification of classification. We identified four developmental categories: precocial
(according to Starck and Ricklefs (1998) superprecocial, precocial 1-3), altricial (altricial 1-2),
semiprecocial and semialtricial. The developmental mode was rather conservative and rarely
changed within orders (Fig. 2). Exceptions among studied birds were representatives of
Charadriiformes which can be precocial (representatives of Burhinidae, Charadriidae,
Glareolidae, Haematopodidae, Recurvirostridae, Scolopacidae, Turnicidae) or semiprecocial
(representatives of Alcidae, Laridae, Stercorariidae) and Pelecaniformes which can be altricial
(Pelecanidae) or semialtricial (Threskiornithidae, Ardeidae).
All statistical calculations were conducted in R (R Core Team 2016). The portion of
multivariate variation that could be explained with taxonomical order of birds or developmental
https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 6 of 24 mode was estimated with non-parametric permutational NPMANOVA with Euclidean distance matrix and 1000 permutations (function adonis in vegan R package; Oksanen et al. 2016). The partial coefficient of determination ( R2) was used as a measure of additional variance that could be explained when developmental mode (or order) was included in the analysis. Nonparametric methods were chosen since the statistical distribution of the traits deviated from normality
(Shapiro – Wilks test, p << 0.001).
The phylogenetic signal was significant for all traits; Pagel's lambda (Pagel 1999) ranged between 0.7 and 0.96, p << 0.001 (tested with phylosig function of phytools R package; Revell
2012). Thus, phylogenetic MANOVA with Wilk's Λ summarizing statistic (function aov.phylo of
R package geiger; Harmon et al. 2008) was applied to check for multivariate differences between developmental groups. Trait by trait comparisons were conducted with phylogenetic t-test implemented in R function phylANOVADraft of package phytools (Revell 2012). Significance of all phylogenetic tests was estimated by randomization test with 1000 simulations.
Correlation structure of egg traits ( L, D, Iiz , Ilz , Icz ) was evaluated with phylogenetic principal component analysis on correlation matrix and assuming Brownian motion model of evolutionary change of traits (function phyl.pca of R package phytools; Revell 2009: Revell
2012). Correlation between principal components and elongation and asymmetry indices was estimated with Kendall's tau correlation test. Phylogenetic MANOVA with Wilk's Λ summarizing statistic (function aov.phylo of R package geiger; Harmon et al. 2008) was applied to check for multivariate differences between developmental groups.
Results
Differences among developmental modes
Basic statistic estimates (number of species, mean, range, standard deviation, and coefficient of variation) of egg traits are given in Table 1. The highest variability was observed in traits of the absolute size of eggs (length and diameter). Eggs shape was much less variable.
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Index of the cloacal zone was the most changeable and index of the infundibular zone was very
conservative with CV around 5.5 % (Table 1).
We found significant multivariate differences in egg traits (L, D, Icz , Ilz , Iiz ) for orders
and developmental modes (NPMANOVA, p < 0.001). When comparison was made for
developmental modes and order of birds was treated as an additional term, almost half of the
variance was explained by developmental mode (51 %), and order of birds added 24 % of the
variance. Changing the sequence of terms, order of birds explained 71 %, and developmental
mode added only 4 % of the variance.
When accounting for phylogeny, multivariate differences between developmental groups
were marginally significant (phylogenetic MANOVA: Wilks' Λ = 0.243, p = 0.030). Pairwise
phylogenetic MANOVA found differences only in altricial – precocial ( p = 0.007) and altricial – semialtricial ( p = 0.001) comparisons.Draft The phylogenetic pairwise t-test of developmental groups found that altricial birds might
be smaller in L and D from all other groups, but the significance was not preserved after
Bonferroni correction for multiple tests (Table 2).
Variation of egg shape of Neognathae
Developmental mode groups highly overlapped in the shape and size of eggs as could be
seen from the scatter plots of principal components (Fig. 3, Table S1). The first three
phylogenetic principal components described 86 % of the variance. PC1 explained 43 % of total
variance and was connected mainly with the size of eggs ( L and D) and associated changes of the
cloacal zone (Fig. 3, Table 3, Fig. S1). Most of the altricial birds were associated with small egg
size and relatively large Icz (right side of PC1 axis), whereas other developmental groups were
spread along the PC1 axis more or less equally (Fig.3). Large eggs with the pointed shape of the
cloacal zone located at the left side of the PC1 axis. PC2 and PC3 were associated with the shape
indices (Fig. 3, Table 3; species are colored by orders in Fig. S2 – S11). Negative values of PC2
https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 8 of 24 correlated with relatively large lateral and infundibular radii of eggs. Thus, PC2 showed variation from normal ovoids to nearly spherical eggs (Fig. S1). PC3 was associated with the relative size of the cloacal zone and, thus, showed variation in the asymmetry of polar zones of eggs (Fig. S1).
Both PC1 and PC2 moderately correlated with the elongation ratio, D / L (Kendall's tau correlation = 0.325 and 0.201, respectively; p < 0.001). Elongated eggs ( D / L less than 0.75) were mostly observed in precocial (127 of 157 species) and semiprecocial (63 of 70) birds (Figs.
5, S4, S6). Spherical eggs were mostly seen in semialtricials (61 of 75 species) (Figs. 4, S5).
Altricial birds were equally presented with nearly spherical and elongated eggs mostly due to the high diversity of egg shape in Passeriformes (Figs. 4, S3): 114 out of 212 species were considered to have nearly spherical eggs. Symmetry of polar zones ( rcDraft / ri ) correlated with PC2 (Kendall's tau correlation = 0.505, p < 0.001) and PC3 (Kendall's tau correlation = -0.528, p < 0.001). Most of the studied species had asymmetric polar zones (433 of 557), although almost half of the semialtricial birds (39 of
61) had similar polar zones.
Developmental modes differed significantly only by PC1 (phylogenetic ANOVA, p =
0.008); it was caused by significant differences of altricials from other groups. Most of the altricial birds had small but highly variable in shape eggs (Figs. 3, 4, S3, S8). Eggs of precocial
(Figs. S4, S9), semialtricial (Figs. S5, S10), and semiprecocial (Figs. S6, S11) birds were medium to large size (Figs. 3, 5). Semialtricials had nearly spherical eggs or biconical eggs with both polar zones blunt (Figs. 3, 4, S5, S10).
The position of different orders of birds with different developmental strategies in the morphospace of first and second principal components is shown at Figs. 4, 5, and S2. Three of eleven orders of altricial birds (Fig. 4) occupied separate regions in the morphospace
(Pelecanidae, Phoenicopteriformes, and Suliformes): they had large and relatively symmetrical eggs. Passerine birds were especially interesting; their eggs are the most diverse in the values of
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shape (by PC2): cloacal zones of passerines range from sharp to blunt (Figs. 4, S8). Semialtricial
birds were presented with five orders (Fig. 4), which eggs were almost symmetrical and medium
to large in size: Falconiformes, Strigiformes, Pelecaniformes (Ardeidae and Threskiornithidae),
Ciconiiformes, and Accipitriformes. Among all birds, they are distinguished by relatively large
cloacal zone.
None of the bird orders with precocial or semiprecocial developmental mode occupied a
distinct region in the morphospace of first three principal components (Fig. 5, S4, S6, S9, S11).
Caprimulgiformes had eggs with symmetrical shape. Both precocial and semiprecocial
Charadriiformes had a tendency for asymmetrical eggs, and many of their eggs had normal ovoid
shape (Fig. 5: lower part of PC2). Anseriformes tend to have more symmetrical eggs than
Galliformes (Fig. 5). Draft Discussion
Birds of the altricial – precocial spectrum were similar in the egg shape. Though, altricial
eggs were significantly smaller. Size and shape of eggs could be better explained with phylogeny
than the developmental mode. It was shown previously with standard linear discriminant
function analysis of eggs' length, diameter, and indices of shape that eggs were well separated by
orders (Mytiai and Shatkovska 2015).
Though most orders overlapped each other, some of the orders were placed in specific
regions in the morphospace of first two principal components (Fig. 4, 5). In other words,
members of various orders have specific size and shape of eggs. This is probably due to the fact
that size and shape of the egg could be determined by features of female's morphology, i.e. size
and shape of the body, volume of the abdominal cavity, width, and openness of pelvis. Shape of
birds' body related to their habitat and lifestyle. We believe that birds within one order are closer
ecologically, and thus have similar size and shape of eggs. Developmental modes include several
https://mc06.manuscriptcentral.com/cjz-pubs Canadian Journal of Zoology Page 10 of 24 orders which could differ ecologically. Therefore, phylogenetic relatedness more affected size and shape of eggs than reproductive strategy.
The elongated shape of eggs occurs in many waterfowl and, especially, diving birds.
These are precocial Anseriformes, Gaviiformes, Podicipediformes and some Gruiformes, semiprecocial Sphenisciformes, Procellariiformes, semialtricial and altricial Pelicaniformes and
Suliformes. Specialization to diving is associated with the elongated shape of the body
(Kurochkin 1971). Diving birds have especially narrow and elongated pelvis (Kurochkin 1971;
Bogdanovich 2014) that probably affects egg shape (Thompson 1942). However, there are exceptions that require more detailed investigation. For example, among the studied penguins, the largest species Aptenodytes forsteri has the elongated egg shape with elongation ratio around
0.65 while species with average body weight ( Pygoscelis adeliae and P. papua ) have eggs nearly spherical form with the index of elongationDraft about 0.8. Taking into account mapping of developmental modes onto the phylogenetic hypothesis of Hackett et al. (2008) (Fig. 2), we assume that precociality and altriciality repeatedly occurred in the evolution of birds. Multiple origins of developmental modes in avian evolution also were noted by Starck and Ricklefs (1998) and Deeming (2007 a; 2007 b). The same developmental mode can be observed in ecologically various birds. Among precocials, there are Terrestrornithes and Natatores (Dyke and Kaiser 2010). We showed that Natatores (Anseriformes,
Podicipediformes, Gaviiformes) tend to have large and elongated eggs, whereas Terrestrornithes
(Galliformes, many Gruiformes) are mostly small to medium in size and asymmetrical in shape.
Some features of altriciality appeared in many orders of birds with intermediate developmental strategies. However, “fully altricial” birds are observed in Dendroornithes (Dyke and Kaiser 2010). Most of the studied altricial birds are Dendroornithes. They differ from others by small body size. Their eggs are also small in size with relatively blunt cloacal end. Due to the high variation of eggs' shape of passerines, the majority of altricials do not differ from them.
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Some similarity in eggs' shape is observed between species that do not have any close
phylogenetic relatedness or the same ecological habitat. For example, many Charadriiformes,
half of Galliformes, and some Passeriformes eggs could be described as normal ovoids (high Iiz
index). The maximum size of the infundibular zone probably associated with the maximum
volume of the air chamber. Generally, normal ovoids could be observed in almost 20 % of the
birds, especially in those which are evolutionary successful, Passeriformes and Charadriiformes
(Mytiai 2014). The presence of normal ovoids mainly among evolutionarily successful groups of
birds could indicate the general trend of evolution of egg shape to the normal ovoid shape.
However, this issue requires more detailed study.
Acknowledgments Draft The authors thank I. Dzeverin and I.A. Bogdanovich for valuable comments and
discussion.
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Table 1. Basic statistic estimates of eggs characteristics in birds with different developmental modes: N – number of species, SD – standard deviation, CV – coefficient of variation.
Trait Group N Mean Min Max SD CV , % All 557 39.90 12.30 117.62 22.268 55.81 altricial 255 22.98 12.30 94.15 11.755 51.16 L, mm precocial 157 54.47 22.70 115.00 20.585 37.79 semialtricial 75 53.07 28.50 96.48 14.923 28.12 semiprecocial 70 54.78 24.80 117.62 18.318 33.44 All 557 28.83 10.10 76.75 15.058 52.22 altricial 255 16.78 10.10 60.53 7.256 43.23 D, mm precocial 157 38.23 18.73 76.50 12.753 33.36 semialtricial 75 40.99 22.90 73.71 10.819 26.40 semiprecocial 70 38.63 18.90 76.75 12.034 31.15 All 557 0.289 0.120 0.451 0.062 21.42 altricial 255 0.298 0.155 0.451 0.048 16.00 Icz precocial 157 0.261 0.120 0.428 0.072 27.40 semialtricial 75 0.340 0.206 0.430 0.041 12.01 semiprecocial 70 0.267 0.160 0.427 0.062 23.29 All 557 0.917 0.613 1.593 0.143 15.60 altricial 255 0.905 0.640 1.458 0.126 13.90 Ilz precocial 157 Draft 0.979 0.635 1.279 0.140 14.28 semialtricial 75 0.769 0.613 1.051 0.069 8.91 semiprecocial 70 0.978 0.665 1.593 0.145 14.79 All 557 0.462 0.364 0.500 0.026 5.58 altricial 255 0.465 0.386 0.500 0.021 4.48 Iiz precocial 157 0.461 0.364 0.500 0.033 7.19 semialtricial 75 0.451 0.378 0.483 0.024 5.30 semiprecocial 70 0.465 0.409 0.500 0.022 4.72
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Table 2. Comparison of egg traits between developmental modes. Values marked with *
remained significant after Bonferroni correction for multiple tests.
Phylogenetic t-test L D Icz Ilz Iiz PC1 PC2 PC3 altricial – precocial 0.021 0.009 0.470 0.522 0.858 0.008* 1.000 0.448 altricial – semialtricial 0.017 0.001* 0.362 0.192 0.516 0.022 0.114 0.045 altricial – semiprecocial 0.046 0.024 0.598 0.567 0.991 0.028 0.921 0.461 precocial – semialtricial 0.917 0.719 0.057 0.035 0.591 0.755 0.082 0.242 precocial – semiprecocial 0.982 0.958 0.890 0.993 0.829 1.000 0.924 0.922 semialtricial – semiprecocial 0.910 0.800 0.148 0.066 0.530 0.765 0.138 0.375
Draft
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Table 3. Results of phylogenetic principal components analysis of egg traits.
PC1 PC2 PC3 PC4 PC5 Eigenvalues 2.153 1.260 0.869 0.699 0.018 Portion of 0.431 0.252 0.174 0.140 0.004 variance Loadings L -0.980 0.031 -0.167 0.043 0.097 D -0.938 0.084 -0.187 0.263 -0.090 Icz 0.477 0.092 -0.863 0.141 0.008 Ilz -0.248 -0.769 -0.230 -0.542 -0.020 Iiz 0.155 -0.807 0.095 0.561 0.014
Draft
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Figure 1. Generalized scheme of egg measurements: О–О3 – centers of arcs; ri – radius of
infundibular zone, rl – radius of lateral zone, rc – radius of cloacal zone; D – diameter; L –
length.
Figure 2. Phylogenetic relationship between orders of the studied birds with modes of
development shown near tips.
Figure 3. Position of developmental mode groups and traits loadings in the morphospace of first
three phylogenetic principal components. Egg shape associated with minimal and maximal
values of specific principal components are shown. See also Fig. S1 for schematic representation
of the associated wih principal components shapes. Draft Figure 4. Position of the orders with altricial (top) and semialtricial (bottom) developmental
mode in the morphospace of first and second phylogenetic principal components. Outlines of the
eggs for each order are given around the perimeter of the plots. Axis to the left of eggs' outlines
represent scale. Distance between tick marks is 10 mm.
Figure 5. Position of the orders with precocial (top) and semiprecocial (bottom) developmental
mode in the morphospace of first and second phylogenetic principal components. Outlines of the
eggs for each order are given around the perimeter of the plots. Axis to the left of eggs' outlines
represent scale. Distance between tick marks is 10 mm.
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Draft Figure 1. Generalized scheme of egg measurements: О–О3 centers of arcs; ri radius of infundibular zone, rl radius of lateral zone, rc radius of cloacal zone; D diameter; L length.
109x69mm (300 x 300 DPI)
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