The shadow of forgotten ancestors differently constraints the fate of Alligatoroidea and...

DOI: 10.1111/j.1466-8238.2008.00426.x © 2008 The Authors

30

Journal compilation © 2008 Blackwell Publishing Ltd www.blackwellpublishing.com/geb

Global Ecology and Biogeography, (Global Ecol. Biogeogr.)

(2009)

18

, 30–40

RESEARCHPAPER

Blackwell Publishing Ltd

The shadow of forgotten ancestors differently constrains the fate of Alligatoroidea and Crocodyloidea

Paolo Piras

1,2

*, Luciano Teresi

3

, Angela D. Buscalioni

4

and Jorge Cubo

1

*

ABSTRACT

Aim

We tested the hypothesis that the evolutionary fates of two sister groups(Alligatoroidea and Crocodyloidea) are differently constrained by phylogenetic andecological (functional) factors in the face of climatic change.

Location

Global.

Methods

We quantified disparity in skull rostrum shape by means of geometricmorphometrics. Mechanical performance of the rostrum was analyzed by applyingbeam theory calculations to morphological data and experimentally measured biteforce. The phylogeny was expressed in the form of principal coordinates, the firstones of which were used as a set of explanatory variables. Extents of species occurrencewere computed using species distribution maps. Finally, species maximum skull sizewere measured and considered as a proxy of maximum body size. We performedvariation partitioning analyses in order to compare differential contributions ofphylogenetic and ecological factors in Alligatoroidea and Crocodyloidea.

Results

Alligatoroidea show higher ‘pure’ historical components than Crocodyloideain explaining both rostrum shape and extent of occurrence (after controlling forbody size). On the contrary, geometric variation of skull rostra of Crocodyloideaunequivocally shows a higher ‘pure’ functional component (linked to performanceon prey capture) and a higher phylogenetically structured environmental variationthan those found in Alligatoroidea. Results obtained for body size variation are con-sistent with these patterns. In Alligatoroidea, body size variation contains a higherphylogenetic signal than in Crocodyloidea.

Main Conclusions

Our results suggest that Crocodyloidea and Alligatoroideamay react differently when faced with significant environmental changes. We predictthat global climatic changes will have a more important effect on Crocodyloideathan in Alligatoroidea by (1) promoting trait shift, adaptation to the new diet andspeciation and (2) modifying the geographical range distribution of species (whichmay track favourable ecological conditions).

Keywords

Alligatoroidea, climatic change, Crocodyloidea, functional performance, geometric

morphometrics, rostral shape, variation partitioning.

*Correspondence: Paolo Piras & Jorge Cubo, Université Pierre et Marie Curie, UMR CNRS 7179, 4 Pl Jussieu, BC 19, Paris 75005, France. E-mail: [email protected]; [email protected]

1

Université Pierre et Marie Curie, UMR CNRS

7179, 4 Pl Jussieu, BC 19, Paris 75005, France,

2

Center for Evolutionary Ecology, Largo San

Leonardo Murialdo, 1, 00146 Roma, Italy,

3

Department of Studies on Structures,

Mathematical Structures of Materials Physics,

Universita degli Studi ‘Roma Tre’ Via Corrado

Segre 6, I-00146 Roma,Italy,

4

Departamento de

Biología, Unidad de Paleontología, Facultad de

Ciencias Universidad Autónoma de Madrid,

28049 Cantoblanco, Madrid, Spain

INTRODUCTION

Diniz-Filho & Bini (2008) published a stimulating paper suggest-

ing that the structure of the variation of traits among related

species may contain keys for predicting their evolutionary fate.

In their own words, ‘the shadow of forgotten ancestors’ could

strongly constrain the possibilities of overcoming environmental

transformations like the current global climatic change. In this

paper we make predictions on how Crocodyloidea and Alli-

gatoroidea may react when faced with climatic change by analys-

ing rostral shape, rostral structural performance, geographical

extent of occurrence and body size in a phylogenetic context.

The proposal of Diniz-Filho & Bini (2008) is based on a new

(phylogenetic) comparative method allowing quantification of

fractions of character variation explained by different factors:

a fraction exclusively explained by ecology, a fraction of phylo-

genetically structured environmental variation and a fraction

exclusively explained by phylogeny. The first fraction refers to

Phylogenetic effects and climatic change

© 2008 The Authors

Global Ecology and Biogeography

,

18

, 30–40, Journal compilation © 2008 Blackwell Publishing Ltd

31

responses of species traits to environmental conditions,

regardless of trait values in closely related species. This fraction

has been considered to match the cladistic concept of auta-

pomorphies at the species level (Cubo, 2004; Cubo

et al

., 2005).

The fraction of phylogenetically structured environmental varia-

tion corresponds to the portion of character variation explained

by ecology

and

phylogeny (Desdevises

et al

., 2003). This fraction

may reflect niche conservatism: closely related species share

character states because they tend to occupy similar ecological

niches (Desdevises

et al

., 2003). Therefore, a high fraction of

character variation explained by ecology

and

phylogeny may sug-

gest that closely related species were tracking the environmental

conditions in which their last common ancestor originally

evolved (Diniz-Filho & Bini, 2008). This fraction matches the

cladistic concept of synapomorphies with functional (ecological)

significance (Cubo, 2004; Cubo

et al

., 2005). Finally, the ‘pure’

phylogenetic fraction refers to character states that were adapted

to the past environment and are now in a suboptimal condition

(this is possible when the feature is not tightly linked to fitness).

In cladistic terminology, this fraction may correspond to syna-

pomorphies without a clear functional significance in extant species

(Cubo, 2004; Cubo

et al

., 2005). According to Diniz-Filho & Bini

(2008), species with a high fraction of character variation

exclusively explained by ecology may react differently to climatic

change (through trait shift and adaptation to the new conditions)

than either species with a high fraction exclusively explained by

phylogeny or species with a high fraction of phylogenetically

structured environmental variation. Although these authors

explicitly used the species level, herein we use their approach at

the level of clades.

Extant species of Crocodylia constitute a suitable group to

which to apply the above model. This clade contains two sister

groups (Crocodyloidea and Alligatoroidea) showing many

specificities (in terms of species richness, ecological diversity and

morphological disparity) that, according to the model proposed

by Diniz-Filho & Bini (2008), may predispose them to react

differently to climatic change. We choose the crocodilian ros-

trum as the best morphological structure to test predictions

made by Diniz-Filho & Bini (2008). It is involved in prey capture,

killing and manipulation, and for this reason it is suitable

for testing the relative importance of functional performance in

the two clades in a phylogenetic context.

MATERIAL AND METHODS

Material

The variation of skull shape explained in terms of functional per-

formance and phylogenetic signal of all extant Crocodyloidea

and Alligatoroidea was used to predict the evolutionary fate of

these clades. Shape data came from a geometric morphometric

analysis of rostra, and mechanical performance was evaluated by

applying beam theory calculations to morphological data and

experimentally measured bite forces (Erickson

et al

., 2003,

2005). Detailed species extents of occurrence were taken from

the IUCN Crocodile Specialist Group official website (http://

iucncsg.org/ph1/modules/Home/), and phylogeny from the

most recent published studies (Brochu, 2000; McAliley

et al

.,

2006; Janke

et al

., 2006). We analysed all living species of

Alligatoroidea (157 individuals, 8 species) and Crocodyloidea

(224 individuals, 14 extant species plus three extinct species –

Crocodylus robustus

from the Pleistocene of Madagascar,

Crocodylus

ossifragus

from the Pleistocene of Java and

Dollosuchus dixoni

from the Early Eocene of Belgium). Perfect three-dimensional

skulls were available for this sample. No undeformed three-

dimensional fossils for Alligatoroidea have been found. Details

about specimens are available in Appendix S1 in Supporting

Information.

Phylogeny

The modern phylogeny of Crocodylia is characterized by a

conflict between molecular studies and morphological/palaeon-

tological studies (see Brochu, 2003, McAliley

et al

., 2006, and

Janke

et al

., 2006, with references for a review). This conflict

regards the position of Gavialoidea within which is placed the

sole extant species belonging to this group,

Gavialis gangeticus

.

In morphological/palaeontological studies, Gavialoidea is placed

outside all other species (as a sister taxon of the remaining

members of the crown group Crocodylia) with a Late Cretaceous

divergence time (Brochu, 2003), while according to molecular

studies it is a sister taxon of

Tomistoma

with their separation

estimated, at the very earliest, in the Late Eocene (Janke

et al

.,

2006).

The remaining extant crocodilian species are unambiguously

grouped into two clades: Alligatoroidea and Crocodyloidea.

Some uncertainties still exist within the genus

Crocodylus

, but the

phylogeny of the group is rather stable. Here we took into

consideration a ‘consensus’ phylogeny mainly deriving from

molecular data (Brochu, 2000; McAliley

et al

., 2006; Janke

et al

.,

2006; Fig. 1). We specifically avoided considering

Gavialis

because of its uncertain position. The consensus tree was

calibrated estimating the branch lengths in millions of

years according to Brochu’s (2003) fossil calibration. We built a

phylogenetic distance matrix for the whole sample (Fig. 1) using

topology and divergence times in Mesquite 2.0 (Maddison &

Maddison, 2007). The matrix was exported using the

Stratigraphic Tools additional module for Mesquite (Josse

et al

.,

2006). Then, following Diniz-Filho

et al

. (1998), phylogeny was

expressed in the form of principal coordinates (PC), which were

subjected to a broken stick analysis (Legendre & Legendre, 1998)

to select a number of them (representative of phylogeny) to be

used in variation partitioning analyses as independent variables.

Geographical extent of occurrence

The geographical extent of occurrence is defined by the IUCN

‘... as the area contained within the shortest continuous imagi-

nary boundary which can be drawn to encompass all the known,

inferred or projected sites of present occurrence of a species,

excluding cases of vagrancy’. We calculated these areas starting

from the maps available for all extant species from the IUCN

http://iucncsg.org/ph1/modules/Home/


P. Piras

et al.

© 2008 The Authors

32


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Crocodile Specialist Group official website (http://iucncsg.org/

ph1/modules/Home/). We used a single map source to avoid

problems linked to heterogeneity of error measurements.

Another source of uncertainty may be linked to the fact that all

species inhabit fresh to brackish waters. Only land areas have

been computed to partially circumvent this problem.

Geometric morphometrics (analysis of rostrum shape disparity)

Twenty-one unilateral three-dimensional landmarks were digi-

tized on the left side of skull rostra to quantify morphospace

occupation for all living Alligatoroidea and Crocodyloidea. Data

collection was performed with an Immersion Microscribe G2®.

Rostrum configuration and landmark definitions are shown in

Fig. 2. These landmark configurations accurately reflect subtle

shape differences among Alligatoroidea and Crocodyloidea over

other typological rostral categories (e.g. slender-snout, blunt-snout

or generalized as used by other authors; see Brochu, 2001).

Landmarks allow precise tests on whether rostral variation is

constricted by phylogeny, by ecology or by both, since they

capture the overall contour, shape details and size.

Generalized Procrustes analysis (Bookstein, 1991) has been

selected for the analysis of shape. This technique can perform a

full investigation of shape differences eliminating the effect of

position, rotation and size. All homologous landmarks of any

configuration are superimposed, minimizing the Procrustes

distance, which is defined as ‘the square root of the sum of

squared differences between the positions of the landmarks in

two optimally (by least-squares procedure) superimposed

configurations at centroid size.’ (Bookstein, 1991). The generalized

least squares method has been used for the superimposition

procedure. All configurations are scaled at the same size unit, i.e.

the centroid size, which is defined as ‘the square root of the sum

of squared distances of a set of landmarks from their centroid.’

The centroid is ‘that point, in a given configuration, whose

coordinates of any dimension are represented by the arithmetic

mean of corresponding dimension coordinates of all landmarks

of that configuration’ (Bookstein, 1991). Procrustes residuals

were subjected to a principal components analysis and the scores

(PCs) were subjected to a broken stick analysis (Legendre &

Legendre, 1998) to select a number of them (representative of

shape) to use in successive comparative analyses. Procrustes

analysis and successive principal components analyses were

performed in Morphologika 2.5 (O’Higgins & Jones, 2007).

Two separate Procrustes superimpositions (Rohlf & Slice,

1990) were performed for Alligatoroidea and Crocodyloidea.

In order to eliminate intraspecific allometric effects, for each

species all individuals were standardized at their maximum

recorded size using IMP series software (Sheets, 2006). The

goodness of standardization was tested by per species multivariate

regressions of original log CS (log

10

centroid size) against shape

variables of standardized data.

Beam theory (analysis of rostral mechanical performance)

Beam theory was adopted to analyse rostral mechanical performance.

The rostrum was modelled as a hollow semi-circular conic trunk

cantilevered at its larger section, corresponding to the antorbital

diameter (Fig. 3). This geometry was considered as a good

approximation of the crocodilian rostrum, probably better

than that of Metzger

et al

. (2005) that used a full tapered ellipsoid

as a model. Dimensions of the model came directly from the

Figure 1 Phylogeny of Crocodylia used in this work. Geological time scale in millions of years.




© 2008 The Authors


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33

height and width of each single specimen at three precise coronal

section levels: premaxillary constriction diameter, fourth

alveolus diameter and pre-orbital diameter. To build the final

geometry, sagittal distances between sections were calculated

and the thickness of the whole object was assumed to represent

10% of the vertical axis of the corresponding section. A Matlab

routine (Trave; Teresi, 2006) read our geometric database,

implemented and solved a beam problem under different load

conditions and eventually computed the stress states in the beam

wall. Linear measurements were computed directly from geo-

metric morphometrics data, projecting on the proper planes

appropriate landmarks through the program Jcocco (Iocchi &

Piras, 2006). The geometric properties of the solid were specified

before any calculation under load conditions.

Bite force was calculated and scaled for each specimen

according to the equation of Erickson

et al

. (2003): log

10

(biteforce) =

−

0.46 + 2.57 log

10

(head length). Head length was calculated by

projecting the distance between the tip of the premaxilla and the

posterior-most tip of the quadrate articular surface on the

sagittal plane. This equated the measurements used by Erickson

et al

. (2003), namely the projected jaw length from jaw tip to

articular surface. Erickson

et al

. (2003) measured the maximum

bite force on one side only for

Alligator mississippiensis

at the level

of fourth maxillary alveolus. Then, a symmetric bite was inferred

with a double force. Moreover, given that this model is a beam

simulation based on steady force distribution, the values of bite force

corresponding to the first section (at the premaxillo-maxillary

Figure 2 Landmark configuration. Landmarks are: 1, medial dorsal anterior projection of frontal; 2, medial dorsal anterior projection of nasals; 3, posterolateral tip of external nares opening; 4, anterior tip of external nares opening (in Alligator and Osteolaemus it just corresponds to anterior profile); 5, posterolateral tip of premaxilla; 6, lateral skull margin at antero-orbital diameter; 7, distal tip of premaxilla; 8, distal tip of external nares contour; 9, anterior tip of premaxilla; 10, posterior-most ventral tip of maxillary–premaxillary contact; 11, anterior-most tip maxillo-palatine contact; 12, premaxillary constriction just on premaxillary–maxillary suture, along the alveolar margin; 13, lateral tip of fourth alveolus; 14, lateral tip of fifth alveolus; 15, medial tip of fifth alveolus; 16, medial tip of fourth alveolus; 17, lateral tip of seventh alveolus; 18, lateral tip of eighth alveolus; 19, lateral tip of eleventh alveolus; 20, lateral tip of twelfth alveolus; 21, anterior tip of incisive foramen.

Figure 3 Geometric model for beam theory analysis built to analyse rostral mechanical performance using the actual skull morphology.

P. Piras

et al.

© 2008 The Authors

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constriction) were calculated as F1 = F2

×

L_23/(L_12 + L_23),

where L_

ij

is the distance between section

i

and

j

, with section

1 the shortest and F2 is the force calculated experimentally by

Erickson

et al

. (2003). Erickson

et al

. (2005) directly measured

the maximal bite force from all extant crocodilian species.

These authors did not publish quantitative results but they stated

that, for all species, both absolute values and values scaled to

allometric change followed the pattern published by Erickson

et al

. (2003) for

A. mississippiensis

. They also stated that this

was true both for brevirostral and longirostral forms.

Six loading conditions were simulated (Fig. 4). They were

chosen as representatives of a great variety of biting circum-

stances. Basically, we can distinguish between symmetrical and

asymmetrical positions that imply very different torsional and

bending responses for various rostral morphologies. Bites with

force exerted on the first and/or the second section level were

considered. Details about mechanical quantities and their

computation are given in Appendix S2.

Material properties were set with a Poisson’s ratio of 0.3 and

with a Young elastic modulus of 10 GPa. These values correspond

to the properties of trabecular bone reported in the reference list

of McGowan (1999). However, given the comparative aim of this

investigation (that is not strictly ‘validative’), possible differences

for these constants with other studies are not relevant and should

not affect the results. The basic idea was to correlate the shape

variables obtained from geometric morphometric analysis with

the simulated rostral mechanical response. Even though six

loading conditions were simulated, sigmas of simulation 5

were only considered as a proxy of functional performance. In

fact, simulation 5 represents a somewhat more realistic bite.

Other conditions revealed identical results relative to species

differences, just scaled in intensity. Thus they would be

redundant in successive statistical analyses. Sigma represents

the maximum normal stress on the section. This parameter is

often used to predict the failure of brittle material; thus, we

considered it to be linked to the overall mechanical performance

of the rostrum.

Comparative methods

The use of classical regression methods requires that the values of

each variable be independent of each other but, in an interspecific

study, the phylogenetic relationships between species imply that

these values are non-independent (Felsenstein, 1985; Harvey &

Pagel, 1991; Garland

et al

., 1992). To overcome this problem, we

used variation partitioning analyses including the phylogeny as

an explanatory factor (Desdevises

et al

., 2003). This method

allows an assessment of the portions of variation of a dependent

variable: (1) explained exclusively by phylogeny; (2) explained

exclusively by ecology (function); or (3) explained by the overlap

of these two sets of variables. It is an extension of the partitioning

method proposed in ecology (Borcard

et al

., 1992; Borcard &

Legendre, 1994; Legendre & Legendre, 1998). Similarly, a method

of variation partitioning among three factors, including the

phylogeny as a set of explanatory variables (Cubo

et al

., 2008) has

been used as an extension of previous developments in ecology

(Anderson & Gribble, 1998; Cushman & McGarigal, 2002;

Økland, 2003). Details about steps of the variation partitioning

method can be found in Desdevises

et al

. (2003) and Cubo

et al

.

(2008). We first applied variation partitioning analysis to a model

involving rostrum shape as a matrix of dependent variables and

two sets of explanatory variables: log

10

(sigmas) (as proxy of

biomechanical performance or rostrum function) and the

selected phylogenetic principal coordinates (as proxy of phylogeny).

This analysis was performed separately in Alligatoroidea and

Crocodyloidea to check the differential contribution of function

and phylogeny to variation of rostrum shape in the two groups.

In a second analysis, we tested the influence of rostrum shape

(as a proxy for degree of trophic specialization) on geographical

extent of species occurrence, controlling for phylogenetic

background, and maximum recorded body size. This exploratory

analysis was also performed separately for Alligatoroidea and

Crocodyloidea. Lastly we quantified the fraction of interspecific

maximum body size variation explained by phylogeny. This

analysis aimed to see whether, in the two groups, this trait

contained a differential degree of phylogenetic signal.

RESULTS

Analysis of rostrum shape disparity using geometric morphometrics

Our standardization procedure eliminated any allometric effect.

Per species multivariate regressions between the original log CS

and shape variables coming from standardized data returned

neither significant Wilk’s lambda nor singular correlations.

The broken stick model returned the first two PCs as significant

for Crocodyloidea, explaining, respectively, 65.99% and 10.83%

of total variation, and the first three for Alligatoroidea,

explaining, respectively, 39.21%, 19.79% and 8.43% of total

variation.

Figure 4 Loading conditions studied for the beam analysis. Schematic drawings show sections of rostrum corresponding to the described anatomical levels (see text). Arrows indicate forces (F) applied.


© 2008 The Authors


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For Alligatoroidea (Fig. 5a), PC1 explains a moderate

lengthening of the rostrum. At positive values, we find

Melanosuchus

niger

and

Caiman latirostris

possessing particularly wide rostra

while at the negative values we find

Caiman crocodylus

and

Paleosuchus

spp. that show, among Alligatoroidea, the most

slender rostra. Both PC2 and PC3 are related mainly to the

relationship between nasals and external nares. At negative

values we found

Alligator

spp. in which nasals enter and bisect

the external nares. At positive extremes,

C. latirostris

and

M. niger

possess the shortest nasals.

For Crocodyloidea (Fig. 5c), PC1 is related to rostrum

lengthening by means of maxillary bone modification; it is

particularly long in

Tomistoma

at positive values, while the

widest morphology can be observed in

Crocodylus porosus

at

negative values. Also for Crocodyloidea, PC2 is associated with

the position of nasals relative to external nares. At extreme

Figure 5 Plots of principal components (PC) of rostral shape analyses. (a) PC1/PC2 scatterplot for shape analysis involving Alligatoroidea. (b) PC1/log10(sigma) for Alligatoroidea. (c) PC1/PC2 scatterplot for shape analysis involving Crocodyloidea. (d) PC1/log10(sigma) for Crocodyloidea. Screenshot morphologies refer to axis extremes. Species abbreviations: Am, Alligator mississippiensis; As, Alligator sinensis; Cc, Caiman crocodylus; Cl, Caiman latirostris; Cy, Caiman yacare; Mn, Melanosuchus niger; Pp, Paleosuchus palpebrosus; Pt, Paleosuchus trigonatus; Ca, Crocodylus acutus; Ccat, Crocodylus cataphractus; Cin, Crocodylus intermedius; Cj, Crocodylus johnstoni; Cm, Crocodylus mindorensis; Cmor, Crocodylus moreletii; Cnil, Crocodylus niloticus; Cnov, Crocodylus novaeguineae; Cpal, Crocodylus palustris; Cpor, Crocodylus porosus; Crho, Crocodylus rhombifer; Cs, Crocodylus siamensis; Ot, Osteolaemus tetraspis; Ts, Tomistoma schlegelii; Crob, Crocodylus robustus; Coss, Crocodylus ossifragus; Dollo, Dollosuchus dixoni.

P. Piras et al.

© 2008 The Authors36 Global Ecology and Biogeography, 18, 30–40, Journal compilation © 2008 Blackwell Publishing Ltd

positive values we find Tomistoma, in which nasals are extremely

short, while at the opposite lies Crocodylus acutus, which

possesses the longest nasals. PC2 is associated also with a

maxillary lengthening at negative values, so that two longirostral

forms (as Tomistoma and C. acutus) occupy (just along PC2)

opposite positions. Nevertheless they are visibly close along PC1.

Analysis of mechanical performance of the rostrum using beam theory

Log10(sigmas) coming from simulation 5 were correlated with

dominant dimensions of shape analysis of Alligatoroidea and

Crocodyloidea, respectively. Bivariate relationships between

log10(sigmas) and dominant dimensions of Alligatoroidea and

Crocodyloidea are shown in Fig. 5(b) and 5(d) respectively.

Obviously, longirostral forms present higher log10(sigmas)

values, but the correlation between performance and shape is

clearly different in the two groups, being visibly stronger in

Crocodyloidea. In fact, while in this group some species are

unequivocally longirostral, no such morphologies are present in

Alligatoroidea; only a minor variability is present, spanning from

Melanosuchus to Paleosuchus.

Analysis of rostrum shape, extent of occurrence and maximum size using variation partitioning

All variation partitioning analyses returned different quantitative

results for Alligatoroidea and Crocodyloidea. In the analysis of

rostrum shape, as shown in Fig. 6, both the functional fraction

and overlapping fraction are higher in Crocodyloidea than in

Alligatoroidea. Conversely, the phylogeny explains much more

variation in Alligatoroidea. All R2 are significant. Partition

variation applied to the extent of occurrence (as the dependent

variable), phylogeny, rostrum shape and maximum body size

(as independent variables) shows that Crocodyloidea possesses

a functional factor (expressed by rostrum shape) higher than

Alligatoroidea (Fig. 7). Analyses performed on maximal body

size (as the dependent variable) and phylogeny (as independent

variables) showed that the phylogenetic signal is higher in

Alligatoroidea (61.4% of size variation explained by phylogeny)

than in Crocodyloidea (54.3%).

DISCUSSION

Diniz-Filho & Bini (2008) suggested that the structure of the

variation of characters in clades may contain keys for predicting

their evolutionary fate. We are aware that a proper analysis of

fitness involves testing, at the level of populations, the effect of

morphological variation on functional performance, and the

effect of performance on fitness (Arnold, 1983; Kingsolver &

Huey, 2003). Thus comparative methods designed to deal with

Figure 6 Results from variation partitioning analyses involving significant principal coordinates of rostral shape analysis (as the dependent variable matrix), performance and phylogeny (as independent variable matrices). Fraction ‘a’ corresponds to the ‘pure’ functional component, fraction ‘c’ to the ‘pure’ phylogenetic component, fraction ‘b’ to the phylogenetically structured functional variation and fraction ‘d’ to the unexplained component.

Figure 7 Results from variation partitioning analyses involving extent of occurrence (as the dependent variable), phylogeny, rostrum shape principal coordinates and maximum species size (as independent variable matrices). Fraction ‘A’ corresponds to ‘pure’ shape, fraction ‘B’ to ‘pure’ species maximal size and fraction ‘C’ to pure phylogeny. For simplicity, fractions not discussed in the text (D, E, F and G) were omitted.


© 2008 The Authors Global Ecology and Biogeography, 18, 30–40, Journal compilation © 2008 Blackwell Publishing Ltd 37

variation at the level of species, such as those used in the present

study, cannot be used to analyse fitness (i.e. morphological disparity

cannot be used as a surrogate of fitness). Here we only tested the

first component of Arnold’s (1983) model: the relationship

between morphological disparity (quantified using geometric

morphometrics) and functional performance (assessed using the

biomechanical approach of beam theory). Following Diniz-Filho

& Bini (2008), the results of these tests were used to make the

following predictions on the evolutionary fate of clades. (1)

Confronted with climatic change, clades showing characters with

high ‘pure’ ecological (functional) components may quickly

respond through trait shift and adaptation to the new conditions.

(2) Characters showing a high fraction explained by ecology and

phylogeny may be tightly linked to environmental conditions

because this variation is the outcome of niche conservatism

(Desdevises et al., 2003). Thus, confronted with climatic change,

species showing this kind of character may track the favourable

ecological conditions by geographical range shifts, generating

phylogenetic signal by persistence of ancestral phenotypes

(Diniz-Filho & Bini, 2008). (3) Finally, characters showing a high

‘pure’ phylogenetic fraction are in a suboptimal condition. In the

past, these characters did not track environmental changes (this

was possible because they were not tightly linked to fitness).

Thus they do not reflect current conditions but past ecological

conditions. In this case, the response to climatic change will

depend upon whether characters are more or less linked to

fitness. When they are not tightly linked to fitness, characters will

persist out of their optimum (reflecting the past ecological

conditions in which they originated). On the contrary, when

they are tightly linked to fitness, organisms will either track

favourable ecological conditions by geographical range shifts

(when possible) or become extinct (Diniz-Filho & Bini, 2008).

This model can be used in two ways. First, it can be used to make

predictions about how a given clade may react faced with a given

environmental perturbation. Our study is an example of this

kind of approach: we have analysed skull shape, skull performance,

geographical extent of occurrence and body size of all extant

species of Crocodyloidea and Alligatoroidea in a phylogenetic

context, in order to make predictions about how these clades

may react when confronted with climatic change. Second, it can

be used retrospectively, by making predictions about how

different clades (e.g. crocodiles and dinosaurs) reacted to a given

environmental perturbation (e.g. the Cretaceous–Tertiary crisis).

Although in this second case predictions can be easily tested

(by analysing morphological disparity, species richness and

geographical distribution of crocodiles and dinosaurs before and

after the biological crisis), in the first case (and in our study),

unfortunately, predictions cannot be tested.

Global climatic change has an important effect on the

geographical range distribution of many animal species, e.g.

modifying the species composition of communities, and there-

fore the potential prey of alligators and crocodiles. Thus climatic

change may have an indirect effect on the diet of these animals,

and may affect both their performance in prey capture (which

depends on the geometry of the skull rostrum), and their fitness.

In Crocodyloidea, geometric variation of skull rostra shows a

‘pure’ functional (biomechanical) component (linked to

performance in prey capture) more than four times higher

than that of Alligatoroidea (Fig. 6). The fraction of geometric

variation of skull rostra explained by phylogeny and function is

also more than four times higher in Crocodyloidea than in

Alligatoroidea (Fig. 6). According to the hypothesis of Diniz-

Filho & Bini (2008), these results suggest that the geometry of

skull rostra is tightly linked to performance in prey capture (an

important component of fitness) in Crocodyloidea. Species of

this clade may quickly respond to climatic changes through

either (1) trait shift, adaptation to a new diet and speciation or

(2) geographical range shifts (tracking favourable ecological

conditions), as suggested, respectively, by the high ‘pure

functional’ component, and the high ‘phylogenetically

structured functional variation’ component of skull rostrum

variation (Fig. 6). In contrast, in Alligatoroidea, geometric

variation of skull rostra shows a high ‘pure’ historical (phylo-

genetic) component (more than four times higher than in

Crocodyloidea, Fig. 6). According to the hypothesis by Diniz-

Filho & Bini (2008), this result suggests that in Alligatoroidea,

geometric variation of skull rostra is not tightly linked to

fitness; therefore, this character will persist out of the optimum

and generate a phylogenetic signal.

Rostral shape in Alligatoroidea is associated with an overall

change in skull morphology along its evolutionary history.

A basal cladogenesis that can be traced back to the Palaeocene

gave rise to two major clades, Alligatorinae and Caimaninae;

the latter comprises the recent genera Paleosuchus, Caiman

and Melanosuchus. Rostral and skull shapes differ in both major

clades in the cranio-madibular articulation, maxillary festooning,

pattern dentition, palatine curvature, presence of rostral canthi,

presence of palpebral ossification, frontal ossification and

robustness of the cranial table (see also Brochu, 1999). On the

contrary, in Crocodyloidea rostral morphology (relative length

and shape) is extremely variable along their evolutionary history.

Longirostry has come out recurrently as a homoplasic feature

linked to dietary adaptation and fishing capabilities even within

the clade Crocodylinae (containing the recent genus Crocodylus)

since their origin near the Eocene–Oligocene boundary (Aoki,

1983; Tchernov, 1986; Brochu, 2003). Two extreme cases include

the longirostral Euthecodon (from the Mio-Pliocene of East

Africa) and the brevirostral extant genus Osteolaemus.

One of our predictions suggests that Crocodyloidea may

undergo geographical range shifts to track favourable ecological

conditions under climatic change (see above). Although we are

unable to test this prediction, we can check whether a relationship

exists between home range and the geometric variation of skull

rostra, controlling for phylogeny and body size (two factors

known to influence home range). The results do not contradict

our hypothesis. ‘Pure’ skull rostrum shape explains a significant

portion of home range variation in both Crocodyloidea and

Alligatoroidea, and the portion of variation explained in the first

group is higher than that explained in the second one (Fig. 7).

Therefore, we predict that global climatic change will have a

more important effect on Crocodyloidea (promoting trait

shift, adaptation to a new diet, and speciation, and modifying the

P. Piras et al.


geographical range distribution of species, which may track

favourable ecological conditions) than in Alligatoroidea.

The evolutionary history of the clade Alligatoroidea is marked

by its tightness to the ecosystems, as a steneotopic organism

adapted to a narrow range of environmental conditions,

associated with continental freshwater ecosystems. Lingual salt

glands capable of excreting hyperosmotic sodium chloride (salt

water) are absent from the alligatorids (A. mississippiensis and

C. crocodylus) (Taplin & Grigg, 1989). This imposes a physiological

constraint in the dispersal capabilities of Alligatoroidea, and thus

the disjoint distribution of A. sinensis and A. mississippiensis

could be better explained in terms of habitat fidelity theory

(Vrba, 1995) than by dispersal (see Brochu, 2003, for the dispersive

hypothesis), considering fragmentation and drift of their ecosystems

during the Oligocene–Miocene temperate climate at high

latitude in North America and Asia (see Markwick, 1998a). On

the contrary, Crocodylinae are better adapted through a suite of

morphological specializations for life in hyperosmotic environments

(Jackson et al., 1996). Salinity discrimination in Crocodylinae

has been used to explain the distribution of living crocodilians by

means of their dispersive capability. Furthermore, speciation

phenomena in Crocodylinae have also been associated with the

increase in variation of rostral shapes (see Tchernov, 1986, for

the area of Great Rudolf Basin where Crocodylus lloidi, Crocodylus

niloticus, Crocodylus cataphractus and Euthecodon coexisted

during the Pliocene–Pleistocene time interval).

The main effect of climatic change has been the increase

in mean annual temperatures registered in recent years. For

ectothermic animals like crocodiles and alligators, global

warming has important effects on metabolic rates. These effects

are mediated by body mass, because both the surface to volume

ratio and the caloric transmission per mass unit decrease as body

mass increases (in geometrically similar animals, while the surface

is proportional to length raised to the second power, volume and

mass are proportional to length raised to the third power). Thus

global warming may promote mass homeothermy in species of

large body size: although these animals generate little physiological

heat (compared with endotherms), high external temperatures

during daytime and the low surface to volume ratio (allowing

retention of much heat at night) promotes the conservation of a

roughly constant temperature. Mass homeothermy (linked to

large size) may increase fitness because it allows high growth

rates, which are energetically costly because of high protein turn-

over (Montes et al., 2007) and a shortening of the juvenile period

of growth (during which individuals undergo high predation

pressure). In conclusion, we expect that global warming may

promote an increase in species-specific body size because both

variables contribute to reaching mass homeothermy, which may

increase the fitness both by increasing growth rates and by

shortening the juvenile period of growth. However, what is the

evolutionary plasticity of maximal body size in the clades

studied? Variation partitioning analyses of maximum skull size

(as an indicator of maximum body mass), using the phylogenetic

PCs as a single set of independent variables, show that the

fraction of variance independent of phylogeny is higher in

Crocodyloidea than in Alligatoroidea. These results strongly

suggest that maximum body mass is evolutionarily more

plastic in the first clade than in the second one (in other words,

Crocodyloidea may appear more reactive to selection for changing

body mass than Alligatoroidea). These results agree with those

obtained in variation partitioning of rostrum shape, suggesting

that Crocodyloidea may track potential environmental changes.

Extant alligatoroid taxa exhibit rather similar rostral shape

and size; most retain a ‘generalist’ rostrum (Brochu, 2001). When

body size notably increased along the evolutionary history of

Alligatoroidea (which includes the giant genus Purrusaurus from

the Miocene of South America, a member of the alligatoroid clade

Nettosuchidae), selection favoured changes in the rostrum width

towards a duck-shaped form. This also occurs in the extant

Melanosuchus. However, the most conspicuous evolutionary

trend within the clade is dwarfism. Cenozoic North American and

European genera such as Allognathosuchus, Arambourgia, Baryphracta,

among others show miniaturized skulls, transforming their rostrum

to what has been denominated ‘blunt snouts’ (see also Brochu,

2001). None of the extant taxa bear such a skull configuration.

Considering that mostly extant species were analysed in this

study (only three fossil Crocodyloidea were included in the

sample), it could be argued that recent diversity of crocodilians

is relict in comparison to the past (Marcwick, 1994a,b, 1995,

1998a,b; Brochu, 2003; Kotsakis et al., 2004). However, as the

aim of the paper is to predict how two contemporaneously living

groups (Alligatoroidea and Crocodyloidea) may respond to an

environmental change, the use of a sample containing mainly

extant species is not a limit but a necessary condition. Moreover,

a greater taxonomic diversity does not necessarily imply a greater

morphological disparity. Nevertheless, looking at the fossil

record of Crocodyloidea and Alligatoroidea helps to understand

their past diversity and disparity (some qualitative considerations

have been made here, see above).

It should be kept in mind that our predictions about the

possible effects of global environmental changes on the biodiversity

(species richness and morphological disparity) of Alligatoridae

and Crocodylidae are macroevolutionary and more linked to

climatic change than to quick changes derived from human

activity such as habitat loss, illegal trade, etc. Data on life-history

traits of Alligatoridae and Crocodylidae, such as life span, age at

sexual maturity and offspring size, among others, may be necessary

to make predictions on how these animals may respond to

anthropic environmental changes.

ACKNOWLEDGEMENTS

Paolo Piras had access to the collections of the Natural History

Museum in London, to the Institut Royal des Sciences Naturelles

in Bruxelles and to the Museum d’Histoire Naturelle in Paris

thanks to the SINTHESYS program, and to the collection of the

Field Museum in Chicago thanks to the Visiting Scholarship Pro-

gram. Part of this research was conducted during a post-doctoral

stay of Paolo Piras, supervised by Jorge Cubo, at the Université

Pierre et Marie Curie. We thank Professor Diniz-Filho, two

anonymous referees and Michel Laurin for their comments.

Michel Laurin also improved the English of the manuscript.


© 2008 The Authors Global Ecology and Biogeography, 18, 30–40, Journal compilation © 2008 Blackwell Publishing Ltd 39

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SUPPORTING INFORMATION

Additional Supporting Information may be found in the online

version of this article:

Appendix S1 List of materials used in this study.

Appendix S2 Beam theory computation detail.

Please note: Wiley-Blackwell is not responsible for the content

or functionality of any supporting materials supplied by the

authors. Any queries (other than missing material) should be

directed to the corresponding author for the article.

Editor: José Alexandre F. Diniz-Filho

BIOSKETCHES

Paolo Piras is a post-doctoral researcher at Université

Pierre et Marie Curie, Paris. He is interested in

macroevolutianry process, and is involved in the study

of Eusuchian systematics and evolution, as well as the

evolution of Plio-Pleistoicene faunas of Europe.

Luciano Teresi earned a PhD in theoretical and applied

mechanics at Sapienza, Università di Roma (Italy) and

is now an assistant professor at the School of Engineering,

Università Roma Tre, Italy. Main researches include

finite element methods in nonlinear elasticity, biomechanics

of growth and electro-mechanical modeling of the heart.

Angela Delgado-Buscalioni is assistant professor at

the Universidad Autónoma de Madrid. She is interested

on skull geometry, integrating neontological and

palaeobiological data, as well as in early taphonomic

alterations in recent and fossil archosaurs.

Jorge Cubo is Maitre de Conferences at the Université Pierre

et Marie Curie, Paris. He is interested in the quantification

of phylogenetic, functional and structural components of

variation in morphological characters in tetrapods.

http://hyms.fme.googlepages.com/downloadmorphologica

http://www3.canisius.edu/~sheets/moremorph.html

http://hyms.fme.googlepages.com/downloadmorphologica

http://www3.canisius.edu/~sheets/moremorph.html

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