Chapter One – Review of Analytical Techniques

4.1 – An Introduction to Shape Analysis

Humans have a natural talent for shape recognition, as demonstrated by the ability of a

newborn infant to recognise faces (de Haan et al., 2002). However, this is a qualitative and

subjective assessment of shape that is not amenable to scientific analysis. To overcome this

subjectivity, methods of shape analysis have been developed that allow for an objective

quantification of shape. These methods encompass such approaches as the statistical analysis

of univariate, bivariate or multivariate metric data (linear measurements, areas, volumes and

angles) acquired from the organisms comprising a sample, to the multivariate analysis of two-

or three-dimensional coordinate landmark data that incorporates the statistical analysis and

also includes a representation of the shape of the specimens under study.

These forms of analysis fall under the general heading of morphometrics, the quantitative

description and statistical analysis of biological shapes, forms and patterns (Oxnard, 1978).

Morphometrics can also be defined as the study of the shape variation (as represented by

landmark sets) and its covariation with other variables such as environmental influences

(Bookstein, 1991, Adams et al., 2004). Broadly speaking, morphometric analysis comes in

two forms: traditional morphometrics and geometric morphometrics. While there are some

common concepts to each and the latter builds upon and borrows from the former, there are

also some marked differences.

This chapter will introduce some concepts that are basic to the field of shape analysis,

describe the techniques of traditional morphometrics, give a brief history of shape analysis

and how early techniques in this field led to the modern method of geometric morphometrics,

and describe the techniques of geometric morphometric analysis.

4.2 – Traditional Morphometric Analysis

The ‘traditional’ morphometric approach to shape analysis comprises the statistical analysis

of univariate, bivariate or multivariate morphometric data in the form of linear measurements,

areas, volumes indices, ratios and/or angles taken from the anatomy of biological specimens

to investigate patterns of variation within and among groups (Adams et al., 2004). Univariate

morphometric analysis comprises the use of linear measurements, areas and volumes, to gain

a preliminary understanding of variation in a sample. (NB: strictly speaking, a linear

measurement, area or volume is a measure of size but not shape: a single dimensional

measurement cannot of itself provide any information regarding shape for the object from

which it was taken). Bivariate morphometric analysis begins the process of understanding

variation in the shape of biological structures. Two linear measurements can be used to

calculate an angle, index or ratio that describes proportional features for the structure under

study (i.e. whether a structure is relatively narrow for its length or is more flexed when

compared to another individual).

The analysis of more than two variables simultaneously requires multivariate statistics such

as factor analysis, principal components analysis (PCA), discriminant function analysis or

canonical variates analysis for purposes such as determining group membership or other

issues of biological interest (Reyment et al., 1984, Adams et al., 2004). These variables may

be directly measured or may be calculated as interlandmark distances (ILDs). As an example

of a statistical analytical technique used in multivariate morphometrics that offers a means of

exploring shape variation, PCA will be the focus of the remainder of this section.

Measurements that are derived from living (or once-living) organisms are neither biologically

or statistically independent. Indeed, these shape variables are expected to be interrelated

because they describe features of an organism that are functionally, developmentally or

genetically connected, and the manner in which these shape features vary and co-vary can be

complex and difficult to understand (Zelditch et al., 2004). Principal component analysis is a

mathematical procedure that simplifies the patterns of shape variation and their interpretation

by replacing these interrelated variables with new variables (the principal components) that

are independent of one another (Zelditch et al., 2004).

When using PCA, a relatively large number of the original variables can be reduced to a

smaller number of principal components (PCs). Moreover, the first principal component will

describe the largest amount of variance in the sample, with each subsequent PC describing

the largest amount of variance remaining that has not been described by the preceding PCs.

Thus, instead of having to consider a large number of interrelated variables when exploring

patterns of shape variation, a PCA gives the investigator a small number of unrelated PCs that

together account for the majority of variation in a sample. Furthermore, a scatter plot using

pairs of these PCs as axes on a graph can identify clusters of individuals that belong to

distinct groups among the sample (based on anatomical or other properties) that are difficult

to identify when plotting the original data. These clusters can be independently verified by

statistical means to test whether or not they represent a priori groups (Zelditch et al., 2004).

The hierarchical nature of the PCs (with respect to the amount of variance each PC describes

for the sample) creates a matrix that can be thought of as a multi-dimensional space occupied

by the number of individuals that comprises the sample; each PC represents a straight-line

axis in this multidimensional space. The ‘direction’ in which the axis of each PC points is a

vector with a length of one (this constraint is necessary to keep the total amount of variance

in the sample unchanged). Furthermore, all of the PC axes must have covariances of zero.

This requires each of the axes to be orthogonal (at right angles) to all of the others in

multidimensional space.
The “direction” of the vector represented by each PC is described by the eigenvectors (or

loadings) which indicate the extent to which each variable contributes to each PC. Each PC

is the sum of the product of each eigenvector and each of the original measurements.

Therefore, particular aspects of morphology for the sample are described by each PC which

can be understood by an examination of the eigenvectors. If all the eigenvectors have the

same magnitude and sign then the PC is coding for size, but if some eigenvectors are positive

and others negative then the PC is coding for some aspect of shape. For example if the length

measurements have positive eigenvectors and the width measurements have negative

eigenvectors then specimens with a high score on that PC are long and slender while those

with a low score are short and wide. It is by this technique that shape differences in the

sample are understood, but it has the disadvantage that the investigator must interpret each

PC by an examination of the eigenvectors, and to varying extents the PC are confounded by

the influence of size. This has led to the attempts to develop analytical techniques that are

able to describe shape independently of size.

4.3 – Geometric Morphometric Analysis

Traditional morphometrics deals with linear measurements of biological structures, and with

angles indices, areas and other parameters calculated from the landmark coordinates

(Blackith and Reyment, 1971, Reyment et al., 1984). This allows for a quantification of

shape and for the exploration of patterns of covariance between variables, but the geometric

configuration of the objects studied is lost, and the original shapes cannot be reconstructed

with the generated variables. In a geometric morphometric analysis (GMA), the data is

collected as two- or three-dimensional Cartesian coordinate data in the form of a set of

landmarks. This data is manipulated in ways that preserve the geometry of its original

configuration, allowing a reconstruction of the actual form (or a simplified representation of

it) during the process of analysis and in the stages of presentation and interpretation of results

(O'Higgins, 2000b).

Geometric morphometric methodology utilises ways of data acquisition and manipulation,

statistical analysis and presentation of results that were described as ‘revolutionary’ when

first introduced (Rohlf, 1993, Adams et al., 2004), but several techniques developed in the

early part of the twentieth century foreshadowed some aspects of GMA. A brief review of

these techniques will follow.

4.3.1 – Early Approaches to Shape Analysis

The quantitative approach to shape analysis formally began in the early twentieth century

with pioneers such as Boas (1905, form superposition technique), Galton (1907, portrait

numeralisation) and Thompson (1917, Cartesian transformation grids) offering approaches to

shape analysis that could be statistically analysed and were reproducible on different

specimens and by different investigators. Galton’s approach using shape coordinates that

could be analysed by rectangles or triangulation was ‘rediscovered’ by Bookstein in the

1980s (Bookstein, 1982, 1984, 1986). Each of these approaches will be discussed briefly

below.

The pioneering anthropologist Franz Boas published a paper in 1905 wherein he suggested

that when comparing the shapes of objects with variable forms (such as the human cranium),

every point must be given equal weighting and that “the nearest approach of all points must

be attempted” (Boas, 1905: 862). The best comparative method minimises “the sum of the

squares of the distances between all pairs of homologous points” (Boas, 1905: 862). These

homologous points are rotated and translated (but not scaled) and their geometric centres of

gravity positioned so that they coincide (Boas, 1905). This method was almost identical with
Sneath’s (1967) method of least squares superimposition except that no allowances were

made for variations in size between organisms (Cole, 1996).

In his analysis of the facial features of humans, Galton (1907) took six landmarks from side-

view facial portraits and described the position of these landmarks as coordinates on a

rectangle or by triangulation. These coordinates were used in interlandmark distance and

angle comparisons to characterise and classify the shapes from which they were derived.

This approach was found to be efficient for identifying the race of individuals from their

portraits (Galton, 1907). Galton’s was an early approach in the use of coordinate data for the

analysis and classification of biological shapes, but used landmarks with only weak (or no)

homology between individuals. The Galton approach was reinvented and refined by

Bookstein in the 1980s after rigorous statistical testing and modelling (Bookstein, 1982,

1984, 1986).

D’Arcy Wentworth Thompson was another early investigator in the field of shape analysis

whose ideas have contributed to modern morphometric research. Thompson created the

Cartesian transformation grid, a regular grid pattern that is superimposed on a reference

object is deformed so that corresponding points on a target object contact the same points on

the grid (Thompson, 1917). The degree of difference between the two objects can be

visualised by the degree of deformation of the grid on the target object. The following

example (Figure 4.1) is drawn from Thompson’s (1917) own work. There were however

limitations to the Thompson method: the figures were usually hand-drawn without any

quantifiable data, so that the accuracy of the two figures was unreliable, and that differences

in shape between the target and reference objects could not be quantitatively described (Chen,

2005).
Figure 4.1 – Cartesian Transformation Grid of Fish from Diodon (left) to Orthagoriscus (right)
(Adapted from Thompson, 1917)

Developed during the 1980s, Bookstein’s two-point registration method of shape analysis

standardises the position of all the landmarks in a dataset to a baseline fixed by two

landmarks that are assigned the coordinates (0, 0) and (0, 1) in a Cartesian coordinate system.

The coordinate data for each specimen is then rotated, translated and scaled to the common

baseline, as illustrated below in Figure 4.2. This removes all variation in size, position and

orientation between specimens, leaving only the variation pertaining to shape.

In Figure 4.2A, two triangles with vertices (A, B and C) and (A’, B’ and C’) are presented.

In Figure 4.2B, the points A and A’ are assigned the coordinates (0, 0), putting the triangles

in the same position, and the lines AB and A’B’ are both aligned horizontally, giving the

triangles the same orientation. The baselines AB and A’B’ are now scaled so they both have

the length (1, 0), while the other lines comprising the two triangles are scaled by the same

degree. The two triangles in Figure 4.2B now have the same position, orientation and base

line size, so that the only differences that are left (between the points C and C’) are
differences in the shape of the triangles. The coordinates of the points C and C’ completely

describe the shape of the two triangles.

Figure 4.2 – Two triangles before (A) and after (B) two-point registration
(From Klingenberg 2006)

Bookstein’s two-point registration method can be applied to a landmark set with any number

of landmarks by designating two of the landmarks of each set as the baseline points A and B,

and a third point as the free vertex of the triangle C. The same steps of translation, rotation

and scaling are applied, with the subsequent scatter of C points indicating the amount of

shape variation in a sample. Plotting the other landmarks in the dataset for each individual

gives information about variation of these other landmarks across the whole sample, allowing

the identification of where in a structure the most variation occurs (Klingenberg, 2006). This

approach analyses landmarks in sets of three at a time, but cannot analyse a multi-landmark

set such as that routinely used in a geometric morphometric analysis.

These early methods of shape analysis have all in some way contributed to modern geometric

morphometric methods. The following sections will explain the theoretical aspects of

geometric morphometric analyses that are relevant to the current study.

4.3.2 – Landmarks and Homology

The terms ‘landmark’ and ‘homology’ have particular meanings in GMA that are

fundamental to the method. Each of these terms is defined below.

4.3.2.1 – Landmarks

Landmarks in the morphometric sense are points that have a specific location that is

equivalent among all specimens and are easily locatable and identified on the biological

structures under consideration (Bookstein, 1991, O'Higgins, 2000b). A set of landmarks

collected from a biological structure is a geometric representation of the morphological

features of that structure, and preserves the spatial relationships among the landmarks

throughout the processes of analysis (Klingenberg, 2006). Thus, landmark sets are geometric

representations of biological phenomena. Preferably, some form of homology (see below) is

present in the landmark set used to represent the biological structures under study.

Landmarks can be classified into three different categories. Type I landmarks are those that

are represented by discrete anatomical features such as the meeting points of sutures, the

juxtaposition of tissues, or the centre-point of a foramen. Type II landmarks include the tips

of extrusions on a structure (such as a bony spur that serves as a site of muscle attachment)

and are identified by geometric rather than anatomical evidence. Type III landmarks are

those that can be located on an outline or a surface but not at a specific point, such as the tip

of a nodule of bone (Bookstein, 1991, O'Higgins, 2000b, Klingenberg, 2006). With respect
to homology between specimens, the greatest amount of confidence can be attached to Type I

landmarks and the least to Type III (O'Higgins, 2000b).

4.3.2.2 – Homology

Homology in its simplest definition is a matter of correspondence between parts (Bookstein,

1991). However, there are different types of homology that are dependent upon the sort of

research question being posed. In evolutionary studies, homology is the matching of parts

between organisms based on common evolutionary origins. In developmental studies,

homology refers to the matching of structures throughout ontogenetic stages. In studies of

biomechanical function, homology refers to matching of structures based upon an

equivalence of function between organisms that have long been separated from their common

ancestor in evolutionary time. Geometric homology refers to the situation where homology is

caused by the equivalence of points in three-dimensional space, such as the apex of a pyramid

(O'Higgins, 2000b).

In the current study, the form of homology will be that of comparative anatomy (Brigandt,

2003). This form of homology uses the relative position of the salient feature(s) with respect

to adjacent structures, similarity in structural detail and histology, and correspondence of

developmental origin as the key criteria to identify homologous landmarks across the sample.

For a sample comprising just one species (Homo sapiens), anatomical features will be

standard across the sample, making the homologous nature of the landmarks relatively simple

to define.

4.3.3 – The Modern Paradigm of Geometric Morphometric Analysis

Geometric morphometric analysis (GMA) is a relatively recent synthesis of techniques that

were developed over the course of the twentieth century. This technique uses coordinate
landmark data derived from points that are homologous across the specimens under study,

and preserves the main geometric relationships between these landmarks as reflected by their

positions in two- or three-dimensional Cartesian coordinate shape space (Cole, 1996). A

GMA registers the coordinate data for all of the specimens in an analysis by scaling it to an

average size for each specimen, translating it to a common plane of reference, and rotating it

to a common orientation (O'Higgins and Jones, 1998, O'Higgins, 2000a, O'Higgins, 2000b).

These steps remove all size, positional and orientation-related differences from the specimens

comprising a study sample so that all that is left for examination are the shape differences.

Theoretical developments and advances in the tools of analysis have made it possible to

manipulate large sets of coordinate landmark data in ways that were not previously possible.

Thus, samples comprising many individuals with large numbers of landmark sets can be

analysed and displayed using powerful computers in a way that was heretofore impossible.

What also sets GMA apart from its forerunners is its focus upon landmark coordinates and

the geometric information about their relative positions, allowing configurations of

landmarks to visually display differences between individuals or groups, in addition to these

differences being displayed in the form of statistical plots (Adams et al., 2004). Data is

analysed in geometric morphometric research by registration and superimposition techniques,

by principal components analysis, and by deformation methods (O'Higgins, 2000b). A brief

explanation of each of these tools will now follow.

4.3.3.1 – Registration by Procrustes Superimposition

A superimposition method registers all the forms within the sample with respect to one

another by such approaches as two point registration (discussed above) or Procrustes

superimposition (O'Higgins, 2000b). The Procrustes superimposition method (also known as

generalised Procrustes analysis or GPA) involves the following steps:

 1. The centroid (central point of the landmark dataset for each individual) is calculated

as the mean of the landmarks representing each object, and each object is translated

so that the centroid is at the origin of the coordinate system;

2. The centroid size of each object is calculated as the square root of the sum of squared

Euclidean distances from each landmark to the centroid, and all the objects are scaled

to a unit size by dividing all the landmark coordinates by the centroid size (the

centroid size value is retained as a measure of the original size); and

3. The Procrustes analysis then rotates each shape/object to the same orientation by

minimising the sum of squared distances between the equivalent landmarks of all the

shapes in the sample.

4.3.3.2 – Kendall’s Shape Space

After the registration process, a principal component analysis (PCA) is conducted upon the

whole dataset to convert the interrelated components of biological shape variation that are

present into independent principal components (PCs) of shape variation. As with any PCA,

the axes of all the PCs are orthogonal to one another, and fulfil all of the other requirements

necessary to form a multidimensional shape space. Thus, each shape (i.e. configuration of

landmarks) is represented as a point in a ‘shape space’ (Kendall, 1984, O'Higgins, 2000b).

Each landmark set is represented as an ‘independent isotropic distribution’ of shapes that

results in an even distribution of the specimens in the shape space (O'Higgins, 2000b). To

present an example of this, Kendall’s shape space for triangles is illustrated in Figure 4.3

below.

For triangles, Kendall’s shape space is curved like the surface of a sphere, but for shapes that

are represented by more than three points the shape space is more complex and
multidimensional (a hypersphere). The PCA in the space that is tangential to Kendall’s shape

space is capable of handling this complexity (O'Higgins, 2000b). For triangles this involves

projecting the scatter of points on the hypersphere’s surface that represents variation the

sample onto a flat Euclidean plane (as seen in Figure 4.3B), with the axes that define the

plane being a pair of PCs. The coordinates for the points representing each specimen are now

given as coordinates on a plane rather than as coordinates on the surface of a sphere. This

allows for an examination of the PCs of shape variation. Clusters of points can be identified

and tested for biological significance, such as whether they represent groupings by size, sex,

or age. The actual shape variation can be visualised by warping the mean shape along the

PCs of interest (O'Higgins, 2000b) (see Section 4.3.3.3 below).

Figure 4.3 – Kendall’s Shape Space

(A) – Representation of Kendall’s shape space for triangles; Equilateral triangles are located at the poles;
the southern hemisphere reflects the northern hemisphere. (B) – A schematic projection of the points
representing triangles in the shape space onto a plane tangent to the mean shape with the principal
components of shape variation (PCI, PCII) in this tangent space. Steps involved are; (i) registration of
figures by generalised Procrustes analysis; (ii) projection of points into a space tangential to the mean and
extraction of the principal components in this space; and (iii) reconstruction of the figures to examine the
shape variation represented by the principal components (O'Higgins, 2000b).

4.3.3.3 – Visualisation of Shape Variation

In a traditional morphometric analysis the shape variation associated with each PC is

interpreted by examining the eigenvectors of each measurement. However in GMA there is

an eigenvector for each of the X, Y and Z coordinates for each landmark, making

interpretation of the PCs by examination of the eigenvectors problematic. Instead, the shape

differences can be visualised by plotting the coordinates of the mean shape in a viewer. The

user can define lines joining particular points to produce a wire frame model of the object, or

define triplets of points to form surfaces for a surface model. The mean shape can be warped

along any particular PC of interest by adding the coordinates of the mean shape to the product

of the eigenvectors for that PC and the score on the PC (Kent, 1994). This process changes

each coordinate value for the mean shape to a new value that sits somewhere along the

relevant PC’s axis. If the warping is done to one extreme or other of that PC, the wireframe

will then illustrate the shape difference described by that PC. If this PC is associated with

some biological difference that results in clustering of the sample (e.g. sex), each end of the

PC axis will depict the extreme male shape (as represented by the landmark configuration)

and the extreme female shape.

Thin plate splines (the mathematical equivalent of the transformation grids developed by

D’arcy Thompson) can be applied to compare two shapes, such as the positive and negative

extremes of a PC of interest. This approach offers a means of visualising which regions of

the object of study differ between the two shapes by the deformations of the grid around a

reference shape as it is warped to a target shape (O'Higgins, 2000b). This involves the

deformation of the whole configuration of reference landmarks coordinates into target object

coordinates, using a thin plate spline (TPS) that is mapped onto the reference object. The

TPS grid shows how the space in the region of a reference object is deformed when the

landmarks are mapped into their corresponding position in a target object. The bending

energy (amount of grid deformation) is an indicator of how different the two objects are in
shape (O'Higgins, 2000b). The locations of the deformations indicate where (in terms of

anatomical location) the two objects differ.

4.3.3.4 – Multivariate Regression Analysis

A PC may be of interest because it has a strong correlation with some independent variable

that has biological relevance to the question being posed, such as variation within a sample

that is associated with differences in size, sex or age. However, while very strong

correlations do occur between PCs and independent variables, there is nothing inherent in a

PCA that seeks this biological variation; and it is more likely that the variation associated

with (e.g.) sex differences will be dispersed among many of the PCs. A multivariate

regression analysis (MRA) can identify the extent to which each PC is associated with the

independent biological factors under consideration.

For a geometric morphometric analysis, multivariate regression analysis is a statistical tool

that considers the relationship between a number of dependent variables (i.e. the principal

components of shape variation from a PCA) and an independent variable (a factor that may

cause biological variation in a sample). The PCs are regressed against the independent

variable, and the results of this test are examined to determine which PCs are significantly

associated with the independent variable. It is these PCs that are then examined to see what

differences may be present in the sample are associated with (e.g.) allometric variation,

sexual dimorphism, changes/degeneration with age, regional variation, or whatever other

biological or environmental factor may cause there to be a morphological difference in the

study sample.

Shape differences in a sample that are associated with the independent variable may be

illustrated through the use of wireframe models and thin plate splines. A wireframe model
that combines the total PC output can be constructed and a TPS grid imposed on this image.

The image is warped from one extreme to the other to illustrate all of the shape differences

associated with the independent variable, with each PC affecting the image according to the

significance of its regression value – those PCs that have a non-significant association with

the independent variable will have minimal effects on the image, while those PCs that have a

significant association with the independent variable will affect the image in orders of

magnitude ranging from subtle to gross. If desired, individual PCs that have a significant

association with the independent variable can be identified and examined to see what aspect

of shape variation they have detected, by use of the procedures described in Section 4.3.3.3

above.

* * * * * * *
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