Evolution, 58(6), 2004, pp. 1209–1224
THE EVOLUTION OF LARVAL MORPHOLOGY AND SWIMMING PERFORMANCE
IN ASCIDIANS
MATTHEW J. MCHENRY1,2
AND
SHEILA N. PATEK3,4
1 The
Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138
2 E-mail: [email protected]
3 The Department of Integrative Biology, University of California, Berkeley, California 94720
4 E-mail: [email protected]
Abstract. The complexity of organismal function challenges our ability to understand the evolution of animal locomotion. To meet this challenge, we used a combination of biomechanics, phylogenetic comparative analyses, and
theoretical morphology to examine evolutionary changes in body shape and how those changes affected swimming
performance in ascidian larvae. Results of phylogenetic comparative analyses suggest that coloniality evolved at least
three times among ascidians and that colonial species have a convergent larval morphology characterized by a large
trunk volume and shorter tail length in proportion to the trunk. To explore the functional significance of this evolutionary
change, we first verified the accuracy of a mathematical model of swimming biomechanics in a solitary (C. intestinalis)
and a colonial (D. occidentalis) species and then ran numerous simulations of the model that varied in tail length and
trunk volume. The results of these simulations were used to construct landscapes of speed and cost of transport
predictions within a trunk volume/tail length morphospace. Our results suggest that the reduction of proportionate
tail length in colonial species resulted in improved energetic economy of swimming. The increase in the size of larvae
with the origin of coloniality facilitated faster swimming with negligible energetic cost, but may have required a
reduction in adult fecundity. Therefore, the evolution of ascidians appears to be influenced by a trade-off between
the fecundity of the adult stage and the swimming performance of larvae.
Key words.
Ciona intestinalis, Distaplia occidentalis, kinematics, larvae, morphology, morphospace, urochordata.
Received September 11, 2003.
The biomechanical complexity of animal motion presents
challenges for understanding broad patterns of locomotor
evolution. Measures of locomotor performance typically have
a nonlinear dependency on numerous aspects of the morphology and motion of an animal’s body (McMahon 1984;
Alexander 2003; Biewener 2003) and interspecific variation
in these traits may be substantial. Ascidians (Chordata: Urochordata) present an interesting case study of locomotor evolution because the larvae of colonial species are similar in
size and shape despite having evolved independently at least
three times among urochordates (Swalla et al. 2000). Through
the integration of biomechanics, phylogenetic comparative
analyses, and theoretical morphology, we examined how evolutionarily convergent colonial life histories have influenced
the morphology and swimming performance of ascidian larvae.
Biomechanical, Comparative, and Theoretical Approaches
to the Evolution of Organismal Function
Research on the evolution of organismal function may use
extant species by either testing for correlations between traits
and performance or by investigating functional mechanisms
(reviews include Wake and Roth 1989; Bennett and Huey
1990; Garland and Carter 1994; Thomason 1995; Koehl 1996;
Lauder 2003). A correlative approach explores natural covariation between traits and performance (e.g., Arnold and
Bennett 1988; Jayne and Bennett 1990; Losos 1990; Patek
and Oakley 2003) to formulate mechanistic hypotheses (e.g.,
Bennett et al. 1989; Jayne and Bennett 1989; Friedman et al.
1992) and to consider the influence of shared ancestry on
functional relationships (e.g., Losos 1990; Bauwens et al.
1995). Form-function relationships established with a strictly
correlative approach (reviewed by Arnold 1983; Huey and
Accepted March 15, 2004.
Bennett 1986; Jayne and Bennett 1989) may be confounded
by variation in performance caused by traits other than those
examined (Koehl 1996). Many mechanistic investigations
have attempted to resolve the causal relationships between
traits and performance by developing mathematical models
of locomotion (e.g., Daniel 1983; Liu et al. 1996; Sane and
Dickinson 2002; McHenry et al. 2003). However, such idiographic studies have limited applicability to evolutionary
questions because they generally neglect the effects of intraand interspecific variation in favor of understanding general
functional principles. Mechanistic studies that examine the
extreme differences among species within a group (e.g.,
Kingsolver and Koehl 1985; Crompton 1989; Emerson and
Koehl 1990; Drucker and Lauder 2001) have proven valuable
for exploring the extremes of performance exhibited by a
group of species. However, general principles and knowledge
of performance extremes alone are limited in their ability to
inform our understanding of changes in function that result
from a sequence of historical transformations.
Theoretical morphology provides the tools to examine historical transformations with mechanistic models toward the
ultimate goal of testing evolutionary hypotheses. This analytical technique involves constructing a theoretical spectrum
of morphological parameters (a morphospace), the measurement of species distributions within that space, and using a
mathematical model to determine the functional significance
of morphologies that are both represented and absent among
species (Raup and Michelson 1965; Raup 1967; McGhee
1999). This model may be used to generate predictions of
performance for each position in the morphospace and thereby generate a performance landscape (also known as a performance surface: Arnold 2003; a fitness landscape: Gilchrist
and Kingsolver 2003; or a functional morphospace: Moore
1209
q 2004 The Society for the Study of Evolution. All rights reserved.
1210
M. J. MCHENRY AND S. N. PATEK
and Ellers 1993). Performance landscapes have been used to
test adaptive hypotheses that ammonite shell geometry generates high locomotor stability (Raup 1967) and strength
against hydrostatic pressure (Daniel et al. 1997), to determine
whether morphological disparity among labrid fishes facilitates disparity in function (Hulsey and Wainwright 2002), to
identify developmental constraints in the body shape of sea
urchins (Ellers 1993), and to investigate the effects of environmental change on the macroevolution of vascular plants
(Niklas 1997). The models used to generate performance
landscapes may come in the form of simple algebraic equations (e.g., Moore and Ellers 1993) or elaborate computational simulations (e.g., Daniel et al. 1997), depending on
the complexity of the functional system.
The present study tested the accuracy of a mathematical
model of swimming in ascidian larvae (McHenry et al. 2003)
and used this model to construct landscapes of swimming
performance. According to this model, the hydrodynamics of
swimming vary widely among ascidian species, which swim
at Reynolds numbers (Re 5 rUL/m, where U is mean swimming speed, L is body length, r and m are the density and
viscosity of water; Lamb 1945) from 5 in Ciona intestinalis
(Bone 1992) to 100 in Distaplia occidentalis (McHenry
2001). At any Re value, the magnitude and direction of propulsive forces depends on the shape of the larval body and
the undulatory motion of the tail.
Ascidian Larvae
Ascidians are a large and diverse group of marine invertebrates with a complex life history characterized by a sessile
adult and a pelagic larval stage. Comprised of more than 3000
species (Jeffery 1997), ascidians were included in the phylum
Chordata because their larvae possess a notochord (Kowalevsky 1866), an organ that plays a role in their undulatory
swimming (McHenry 2001). Recent phylogenetic studies
(e.g., Cameron et al. 2000; Swalla et al. 2000) support this
classification and find that the urochordata (which includes
ascidians and the less speciose pelagic larvaceans and thaliaceans) is a monophyletic group that includes ascidians as
a polyphyletic assemblage united by the presence of a sessile
adult stage (Swalla et al. 2000; Stach and Turbeville 2002).
The larval stage provides an ascidian with its only opportunity for dispersal by locomotion. Ascidian larvae have a
rigid globose trunk that is propelled through the water by its
flexible tail, thereby bearing a gross resemblance to an anuran
tadpole. These tadpole larvae (sensu Brusca and Brusca 1990)
do not feed and therefore rely on a fixed storage of energy
to survive through dispersal and metamorphosis (Burighel
and Cloney 1997). This suggests that larvae that swim with
a relatively low energetic cost of transport (McMahon 1984)
should have an improved chance of survival through the larval stage (as in bryozoans; Wendt 2000). Field observations
suggest that larvae may enter into and exit from fast horizontal currents with vertically oriented swimming. Therefore,
dispersal distance may be influenced by the speed with which
a larva traverses these currents (Young 1986; Bingham and
Young 1991; Stoner 1992). Fast swimming may also shorten
the duration of the dispersal phase and allow larvae greater
control over their selection of a microhabitat for settlement
(van Duyl et al. 1981; Durante 1991; Stoner 1994; Svane and
Dolmer 1995). Therefore, speed and cost of transport are two
measures of swimming performance that may have important
consequences for dispersal distance and duration, microhabitat selection, larval survivorship, and, ultimately, to fitness.
Although ascidians exhibit tremendous diversity in lifehistory traits (reviewed by Svane and Young 1989), solitary
and colonial species represent the two major types of ascidian
life-history strategies. Colonial (i.e., compound and social)
ascidians produce adult zooids by asexual reproduction and
they generally brood a relatively small number of large larvae
that spend a brief time in the plankton (less than a few hours;
Berrill 1935). Solitary species generally broadcast spawn
their gametes and their numerous small larvae develop rapidly in the plankton. Therefore, solitary species may provide
less material investment and protection for larvae than colonial species, but they have higher fecundity (Svane and
Young 1989). The larvae of colonial species are so much
larger than solitary species that their trunks may be more
than three orders of magnitude greater in volume (Cloney
1978).
It remains unclear to what degree patterns of life-history
traits and larval morphology are due to shared ancestry or
convergent evolution. It has long been appreciated that both
solitary and colonial species are distributed throughout ascidian families (Berrill 1950) and recent phylogenetic studies
suggest that coloniality has a number of independent origins
(Swalla et al. 2000). Finding the phylogenetic distribution of
life-history strategy is requisite for understanding whether
the observed patterns in larval morphology are correlated
with life history or due to shared ancestry. Using recent phylogenetic systematic studies (e.g., Swalla et al. 2000; Stach
and Turbeville 2002), we examined the phylogenetic distribution of larval morphology among solitary and colonial species.
The broad goals of the present study were to determine
the patterns of evolutionary change in larval morphology
among ascidians and to understand how this change affected
swimming performance. We pursued these goals by focusing
on four questions: (1) Can a mathematical model accurately
predict swimming performance across species? (2) How does
tail motion affect swimming performance? (3) Do colonial
ascidians have a convergent larval morphology? (4) How has
evolutionary change in larval morphology affected swimming
performance?
MATERIALS
AND
METHODS
Biomechanics
The peripheral shape of the body and the tail motion of
C. intestinalis and D. occidentalis were measured to model
the hydrodynamics of their swimming. These measurements
were previously reported for D. occidentalis (McHenry 2001),
and are newly presented for C. intestinalis. Adults of both
C. intestinalis and D. occidentalis were collected in northern
California, USA, and held in a recirculating seawater tank at
168C. Larvae of C. instestinalis were cultured from the gametes of adults using standard embryological techniques (see
Strathmann 1987). Colonies of D. occidentalis were exposed
to bright incandescent light after being kept in darkness over-
1211
EVOLUTION OF ASCIDIAN LARVAE
night to stimulate the release of brooded larvae (Cloney
1987).
Morphometrics of body shape
The peripheral shape of the bodies of larvae was measured
using digital still images and approximated with a series of
equations. Digital photographs (Coolpix 700, Nikon, Melville, NY) of larvae from dorsal and lateral views (N 5 5 for
C. intestinalis, N 5 11 for D. occidentalis) were imported
into Matlab (rel. 12 Mathworks, Natick, MA; on a Lifebook
E, Fujitsu, Tokyo), where a custom program found the coordinates describing the peripheral shape of the body. The
dorsal margin of the trunk was described by a half-ellipse
having a major axis equal to half the length, lmax, and a minor
axis equal to the radius, wmax, of the trunk. The trunk radius
was measured as half of the mean of the maximum thickness
of the trunk measured from lateral and dorsal views. The
distance between the trunk midline and the peripheral margin,
w, was defined relative to its position along the midline, l,
with the following equation for an ellipse (Thomas and Finney 1980):
w(l) 5
!
[
2
wmax
12
]
4(l 2 lmax /2) 2
,
2
lmax
(1)
where 0 , l , lmax. Half-ellipses were used in this way to
describe the dorsal, ventral, and lateral margins of the trunk.
The trunk was assumed to be circular in cross section with
a radius equal to w. The cellular region of the tail was also
assumed to be circular in cross-section (as in McHenry 2001;
McHenry and Strother 2003), with the radius tapering posteriorly, as described by the following equation:
r(s) 5 2
rmax s
1 rmax
0.85F
(2)
where rmax is the maximum measured radius, s is the position
along the midline of the tail and 0 , s , 0.85F, where F is
the tail length. The distance between the dorsal margin of
the tail fin and the tail midline, q, was described with the
following function:
qmax
q(s) 5 
1.25qmax (1 2 s/F )
at s , 0.2
at s $ 0.2,
(3)
where qmax is the maximum height of the tail fin and 0 , s
, F. Assuming dorsoventral symmetry, we used the same
function to describe the ventral margin of the tail fin. From
these measurements of peripheral shape, we calculated the
body mass, m, center of mass, and the moment of inertia
using a program written in Matlab (for details, see McHenry
et al. 2003). We tested for significant differences in morphological parameters between D. occidentalis and C. intestinalis using an unpaired Student’s t-test in Matlab (Sokal
and Rohlf 1995).
Kinematics of swimming
The three-dimensional tail kinematics of freely swimming
larvae of both species were recorded with two high-speed
video cameras (Motionscope PCI Mono/1000S, Redlake Im-
aging, San Diego, CA). Coordinates along the midline of the
body were found from video images of larvae and transformed with respect to the frontal plane of the body using a
custom computer program (for details see McHenry 2001).
Undulatory kinematics were described by fitting midline coordinates to equations (explained in McHenry 2001) that describe changes in the angle between the trunk and tail and
the curvature of the tail with time. Neglecting any asymmetry
in tail motion, these equations allowed the kinematics to be
described completely by the maximum curvature of the tail,
kmax, the maximum angle between the trunk and the tail, umax,
and the tail-beat frequency, f. The kinematics of species were
compared (N 5 5 in C. intestinalis and N 5 14 for D. occidentalis) by testing for significant differences in these parameters using an unpaired Student’s t-test (Sokal and Rohlf
1995).
Mathematical modeling of swimming
We used a mathematical model of the biomechanics of
swimming that was developed by McHenry et al. (2003). This
model approximates the quasi-steady fluid forces acting on
the trunk and tail of a larva given a description of the body’s
peripheral shape, tail kinematics, and mass. We solved the
equations describing these forces numerically using a variable order Adams-Bashforth-Moulton solver programmed in
Matlab (Shampine and Gordon 1975) to find how the velocity,
rate of rotation, position, and orientation of the body changed
with time in two dimensions during a swimming sequence.
The mean swimming speed and the hydrodynamic cost of
transport were calculated to assess the performance of each
mathematical simulation. Each simulation lasted for a duration of six tail beats and the results from unsteady swimming were discarded by removing calculations for the first
tail beat. The hydrodynamic cost of transport (COT) was
calculated with the following equation (McHenry and Jed
2003):
O U T Dt ,
COT 5
n
i51
i i
mx
(4)
where i is the index for each of the n instantaneous values
of speed, Ui, and thrust, Ti, and x is the net distance traversed
over the duration of a swimming sequence. This measure of
energetic economy neglects internal costs and therefore provides a minimum estimate of the metabolic cost of transport
(Schmidt-Nielsen 1972).
The accuracy of the model was tested by comparing predictions of speed for C. intestinalis and D. occidentalis with
measurements. In simulations and experiments, average
speed was calculated as the mean of instantaneous speed
values. This measure of speed is not equivalent to the net
speed of swimming (i.e., total distance divided by duration),
because of the meandrous path followed by models and larvae. For each larva that we measured tail kinematics and
speed, a mathematical simulation was run with the same kinematics, and the predicted and measured speeds were compared with a paired Student’s t-test for each species.
The relative contributions of differences in morphological
and kinematic parameters on the performance differences be-
1212
M. J. MCHENRY AND S. N. PATEK
TABLE 1.
Morphometric data for comparative analyses.
Trunk
length
(mm)
Trunk
radius
(mm)
Log10
trunk volume
(mm3)
Tail
length
(mm)
Body
length
(mm)
Solitary
Ascidia mentula
Ascidiella aspersas
Ascidiella scabra
Ciona intestinalis
Corella inflata
Dendrodoa grossularia
Halocynthia roretzi
Herdmania pallida
Molgula tubifera
Molgula citrina
Molgula oculata
Molgula complanata
Molgula manhattensis
Polycarpa fibrosa
Pyura pachydermatina
Styela partita
0.17
0.31
0.30
0.30
0.20
0.62
0.39
0.24
0.17
0.39
0.11
0.40
0.15
0.20
0.31
0.22
0.06
0.09
—
0.06
0.08
0.24
0.12
0.08
—
0.12
0.04
—
0.04
0.11
0.11
0.06
22.97
22.30
0.47
0.87
0.60
1.16
0.63
2.07
1.38
0.91
0.50
1.32
0.37
1.20
0.50
0.83
0.94
0.64
0.64
1.19
0.90
1.46
0.84
2.68
1.77
1.15
0.67
1.71
0.48
1.60
0.65
1.02
1.25
0.85
Berrill 1931, Berrill 1950
Berrill 1929
Berrill 1931
present study
Young 2002, present study
Berrill 1929
Satoh 1994
Sebastian 1953
Berrill 1931
Grave 1926
Jeffery and Swalla 1992
Berrill 1931
Berrill 1950
Berrill 1929
Anderson et al. 1976
Berrill 1950
Colonial
Aplidium constallatum
Aplidium punctum
Botrylloides leachii
Botrylloides sp.
Botrylloides simodensis
Botryllus gigas
Botryllus schlosseri
Clavelina picta
Didemnum pacificum
Distaplia occidentalis
Distomus variolosus
Morchellium argus
Perophora listeri
Polyandrocarpa gravei
0.79
0.53
0.56
1.08
0.47
0.85
0.52
1.08
0.53
1.29
0.83
0.50
0.32
0.38
0.19
0.19
0.18
0.28
0.18
0.28
0.18
0.32
0.19
0.18
0.27
—
0.12
0.12
21.24
21.41
21.44
20.75
21.48
20.86
21.43
20.64
21.40
21.04
20.90
1.46
0.98
1.04
1.89
1.27
2.08
1.15
2.52
1.18
2.27
1.72
1.30
0.58
1.45
2.25
1.51
1.60
2.97
1.73
2.93
1.67
3.60
1.71
3.55
2.55
1.80
0.90
1.83
Grave 1921
Berrill 1950
Berrill 1935
McHenry 2001, present study
Mukai et al. 1987
Berrill 1935
Berrill 1950
Berrill 1935
Tokioka 1953
present study
Berrill 1950
Berrill 1931
Berrill 1950
Grave 1932
Species
tween C. intestinalis and D. occidentalis were examined by
running a series of simulations. Simulations were run with
parameter values of both species for tail length, tail height,
trunk volume, trunk shape (the ratio of trunk radius to length),
and tail kinematic parameters (tail-beat frequency, maximum
curvature, and maximum trunk angle). For example, to examine the effect of tail length, we first ran a simulation using
all the parameter values of C. intestinalis, and then ran a
simulation of the same model except that it used the tail
length of D. occidentalis. The resulting differences in performance were used to indicate the effect of tail length.
Phylogenetic Comparative Analyses
The evolutionary patterns of life-history strategy and larval
morphology were examined by mapping traits onto phylogenies and applying phylogenetically independent contrast
analyses (Felsenstein 1985; Harvey and Pagel 1991). These
analyses were conducted using five published phylogenies
(figs. 2, 4 from Stach and Turbeville 2002) and were coded
into MacClade (ver. 4.05, Maddison and Maddison 2000).
We will refer to the phylogeny found by strict consensus of
18S rDNA sequences (fig. 2A in Stach and Turbeville 2002)
as tree A, by strict consensus of 18S rDNA and morphological
traits (fig. 2B in Stach and Turbeville 2002) as tree B, by
maximum likelihood of 18S rDNA sequences (fig. 2C in
Stach and Turbeville 2002) as tree C, by strict consensus of
22.60
22.59
21.12
21.90
22.48
21.92
23.41
23.33
22.34
22.07
22.81
22.01
21.93
Source
partial cox 1 mitochondrial DNA sequences (fig. 4A in Stach
and Turbeville 2002) as tree D, and by strict consensus of
amino acid sequences translated from partial cox 1 mitochondrial DNA sequences (fig. 4B in Stach and Turbeville
2002) as tree E.
Life-history data were obtained from published sources
(Berrill 1950; Burighel and Cloney 1997; Swalla et al. 2000;
Cloney et al. 2002; Morris et al. 2002) for all taxa included
in the Stach and Turbeville (2002) phylogenies. Analyses of
morphology were implemented using modified trees that only
included taxa with morphological data. For cases in which
genera were monophyletic in all trees, we exchanged species
data within genera such that we maximized the amount of
comparative data to be used in the analyses. Due to these
modifications of the tree structure, we were not able to incorporate branch lengths into the trees when conducting independent contrast tests.
We reconstructed the phylogenetic pattern of life-history
strategy using MacClade’s most parsimonious reconstruction
(Maddison and Maddison 2000) based on all five trees under
consideration. Phylogenetic comparative tests of correlations
between traits were conducted using CAIC (ver. 2.6.9, Purvis
and Rambaut 1995). Brunch algorithms were used for the
categorical tests examining colonial/solitary transitions and
Crunch algorithms were used for morphological traits. Morphological traits were log-transformed to reduce the depen-
1213
EVOLUTION OF ASCIDIAN LARVAE
FIG. 1. The body shape of larvae. The peripheral shape of the bodies of larvae of (A) Distaplia occidentalis (N 5 11) and (B) Ciona
intestinalis (N 5 5) is shown from dorsal and lateral views, with mean values (horizontal hatches, 61 SD) at 70 positions down the
length of the body. The black lines show the curves fit to these data (eq. 1–3). The mean values (11 SD) for (C) linear body dimensions
and (D) trunk volume for each species. Note that the error bars are too small to be visible in D.
dence of the variance on the mean (Sokal and Rohlf 1995)
and to examine scaling relationships (see below). Statistical
correlations of contrasts were calculated using a regression
line forced through the origin, as implemented by CAIC
(Purvis and Rambaut 1995).
Morphological traits were recorded from values reported
in the literature (sources listed in Table 1), measured from
scans of published camera lucida drawings, or measured from
digital photographs of larvae. The positions of morphological
landmarks were recorded from scans of drawings (Epson
3200 Photo, San Jose, CA) and digital photographs (Nikon
Coolpix 700) using a custom program in Matlab. We measured trunk length and radius and tail length and calculated
the volume of the trunk by assuming an ellipsoidal shape
(McHenry et al. 2003). Distaplia occidentalis was excluded
in these comparisons because this species was not included
in the phylogenetic analysis of Stach and Turbeville (2002).
The scaling of body shape was examined in colonial and
solitary species using both species and contrast values. The
exponential relationship between trunk volume and tail length
was described by a scaling constant, a, and scaling factor, b,
of an exponential equation (F 5 aVb; Huxley 1932). We
tested whether colonial and solitary species scaled isometrically (F 5 aV0.33) by calculating the profile likelihood confidence intervals for the regression slopes (JMP 5.0.1) and
observing whether the slope value of 0.33 fell within these
confidence intervals. We compared species and contrast values of colonial and solitary species regression slopes and
intercepts using a t-test modified for comparing linear regressions (Zar 1999, ch. 18).
Theoretical Morphology
Theoretical morphology was used to examine the distribution of colonial and solitary species in a morphospace and
performance landscape. We used a principal components
analysis to define areas of trunk volume/tail length morphospace occupied by colonial and solitary species. The
boundaries of these areas were defined by ellipses of 95%
confidence intervals for the major and minor axes of variation
in each of these groups (Sokal and Rohlf 1995). We found
the speed and cost of transport predicted for positions
1214
M. J. MCHENRY AND S. N. PATEK
FIG. 2. The undulatory motion of the tail. The lateral motion of the midline of the tail can be seen as a time series from a dorsal view
of a larva of (A) Distaplia occidentalis and (B) Ciona intestinalis. The mean values and standard deviations of the (C) maximum curvature
of the tail, (D) the maximum trunk angle, and (E) tail-beat frequency for both species (N 5 5 for C. intestinalis and N 5 14 for D.
occidentalis).
throughout the morphospace by running simulations of our
biomechanical model (see above) over a range of trunk volume and tail length values at 15 equal intervals, for a total
of 225 simulations, which spanned beyond the range of measured values in each parameter measured. Simulations were
run with the tail kinematics and body shape of C. intestinalis.
For example, trunk volume was varied by altering the trunk
width and trunk length, but the ratio of these parameters
remained equal to that of C. intestinalis throughout all simulations.
RESULTS
Morphology, Kinematics, and Performance of Ciona
intestinalis and Distaplia occidentalis
A comparison of morphology and kinematics between C.
intestinalis and D. occidentalis presents some of the differences and similarities between colonial and solitary species.
The peripheral shapes of the bodies of both species were well
approximated by the equations and parameter values describing body shape (eq. 1–3; Fig. 1A, B). Distaplia occidentalis
was significantly larger (unpaired t-test, P ,, 0.001) than
C. intestinalis in all linear dimensions measured (Fig. 1C).
Furthermore, the mean trunk volume of D. occidentalis larvae
(V̄ 5 3.35 3 1021 mm3) was more than 100 times greater
than that of C. intestinalis (V̄ 5 2.60 3 1023 mm3, Fig. 1D).
The undulatory motions of both species were qualitatively
similar (Fig. 2A, B) and the two species were indistinguishable in their maximum curvature (P 5 0.75, Fig. 2C) and
maximum trunk angle (P 5 0.74, Fig. 2D). However, D.
occidentalis swam with a significantly higher tail-beat frequency than C. intestinalis (P 5 0.04, Fig. 2E).
Mathematical simulations of the biomechanics of swimming predicted different trajectories and average swimming
speeds for the two species (Fig. 3). Distaplia occidentalis was
predicted to generate greater trunk rotation with each tail
beat and thereby followed a relatively meandrous trajectory
(Fig. 3A) compared to the swimming of C. intestinalis (Fig.
3B). The average speed of swimming (mean of instantaneous
values) in both species oscillated with time (Fig. 3C, D), but
the average speed of swimming was more than an order of
magnitude greater in D. occidentalis than in C. intestinalis
(Fig. 3E, F), a difference that was reflected in measurements
of freely swimming larvae. In both species, the mathematical
EVOLUTION OF ASCIDIAN LARVAE
1215
FIG. 3. Typical results from the mathematical model of swimming biomechanics. Points show examples of the movement predicted for
the center of mass over a duration of seven tail-beats at intervals of 2 msec, starting at the arrow, for (A) Distaplia occidentalis and (B)
Ciona intestinalis. The predicted average speed (mean of instantaneous values) for the (C) D. occidentalis model in A and (D) the C.
intestinalis model shown in B. The mean (11 SD) swimming speed predicted and measured for (E) D. occidentalis and (F) C. intestinalis
larvae.
model predicted speeds that were statistically indistinguishable from these measurements of speed (paired t-test, P 5
0.07 in D. occidentalis, Fig. 3E; P 5 0.28 in C. intestinalis,
Fig. 3F).
The effect of individual morphometric and kinematic differences on the performance differences between D. occidentalis and C. intestinalis were evaluated with the results of
a series of simulations (a–f in Fig. 4). Increasing the tail
length and height from the size of C. intestinalis (a in Fig.
4) to that of D. occidentalis (c in Fig. 4) resulted in an 18%
decrease in speed and a 27% increase in the cost of transport.
Increasing the trunk volume to the size of D. occidentalis (d
in Fig. 4) resulted in swimming that was nearly twice the
speed, but had a lower cost of transport. A further decrease
in the cost of transport was achieved by changing the trunk
shape (the ratio of trunk radius to length) from that of C.
intestinalis (d in Fig. 4) to that of D. occidentalis (e in Fig.
4). However, these effects of morphology were small relative
to the effect of tail kinematics. A model having the body
shape of D. occidentalis, but the tail kinematics of C. intestinalis (e in Fig. 4) moved with a speed that was just 14%
the speed and 3% the cost of transport of the same model
animated with the kinematics of D. occidentalis (f in Fig. 4).
Phylogeny and Independent Contrasts
Parsimony reconstructions of ascidian life history suggested that the common ancestor to the urochordates was
solitary, and that coloniality evolved independently at least
three times among urochordates (Fig. 5). The clade of Stye-
lidae 1 Pyuridae includes both solitary and colonial species
and suggests at least one origin of coloniality. All Aplousobranchiata species were colonial, which implies an origin
of coloniality prior to their most recent common ancestor.
Perophora japonica is a colonial member of the largely solitary Phlebobranchiata clade. Coloniality appears to have either evolved in the lineage leading to P. japonica (as in trees
A and C), or possibly prior to the common ancestor to the
Phlebobranchiata and Thaliacea (equivocal in tree B). The
origin of coloniality arising prior to the common ancestor of
the Thaliacea was not considered in our analysis of larval
morphology due to a lack of larval data for this group. As a
result of these patterns of life-history evolution, independent
contrast analyses based on each of these trees yielded either
three or four contrasts for comparison of larval morphology
between species of each life-history strategy (Table 2).
Phylogenetically independent contrast analyses were used
to examine whether the observed patterns of larval morphology in colonial species were the result of shared ancestry
or evolutionary convergence (Fig. 6). We found that colonial
ascidians have significantly greater trunk volume than the
larvae of solitary species (P̄ 5 0.035, Table 2) and that tail
length was significantly correlated with trunk volume (P̄ 5
0.004, Table 2, Fig. 7A, B). However, colonial species were
statistically indistinguishable from solitary species in tail
length (P̄ 5 0.515). Although the absolute values for tail
length were indistinguishable between colonial and solitary
species, the scaling of tail length relative to trunk volume
was different in these groups (see below).
1216
M. J. MCHENRY AND S. N. PATEK
and tail length morphospace occupied by ascidian larvae (Fig.
7C). The species values for Herdmania pallida approximated
the mean trunk volume and tail length of solitary species (V
5 8.2 3 1024 mm3, F 5 0.91 mm) and the mean values for
colonial species were approximated by Aplidium constellatum
(V 5 1.4 3 1022 mm3, F 5 1.46 mm). Therefore, we considered these species to be representative of larvae produced
by the species of their respective life history strategy.
The results of our mathematical simulations allowed us to
examine the effects of trunk volume and tail length on swimming performance given the same tail kinematics (Fig. 8).
The fastest swimming was predicted for larvae having relatively long tails (F . 2.5 mm) and either low (V , 1023
mm3) or intermediate (1022 mm3 , V , 1021 mm3) trunk
volume (Fig. 8A). However, the cost of transport was lowest
in larvae having relatively small tails (F , 1.6 mm) and large
trunks (V . 1023 mm3), and greatest in larvae with large tails
(F . 1.6 mm) and small trunks (V , 1023 mm3, Fig. 8B).
The morphospace occupied by colonial species was characterized by slightly slower speed, but a lower cost of transport than solitary species. For example, the solitary H. pallida
moved 69 % faster than colonial A. constellatum (12.3 mm
sec21 compared to 8.5 mm sec21), but with a 44% greater
cost of transport (2.5 J kg21 m21 compared to 1.1 J kg21 m21,
Fig. 8C). A model larva having the proportionate tail length
of H. pallida, but the trunk volume of A. constellatum moved
faster than both species, but with an intermediate cost of
transport (13.6 mm sec21, 2.2 J kg21 m21, Fig. 8C). Neither
group of species occupies regions of morphospace that result
in extremely fast or energetically costly swimming. Furthermore, the influence of morphological variation on swimming
performance is subtle compared to the effect of tail motion
(Fig. 4, described above).
DISCUSSION
FIG. 4. The effect of morphology and kinematics on swimming
performance. The parameter values and predicted performance are
aligned in columns for each of six simulations (a–f). Filled squares
denote which of the listed parameters have the value for Distaplia
occidentalis and open squares denote which have the value for Ciona
intestinalis. The resulting performance for each simulation is presented in the bar charts for the (A) speed and (B) cost of transport
predicted for larvae.
Both colonial and solitary species were found to scale isometrically. For all regressions of log-transformed values of
trunk volume and tail length, the slope of 0.33 fell within
the limits of the confidence intervals for both independent
contrast and species values (Table 3). Scaling factors did not
differ significantly between solitary and colonial species.
However the scaling constant (i.e., the intercept of the regression, Fig. 7C) was significantly different between colonial and solitary species values (Table 3). The lower intercept
of colonial ascidians (Table 3, Fig. 7C) means that these
species have a tail length that is smaller in proportion to
trunk volume than solitary species.
Morphospace and Performance Landscapes
The 95% confidence intervals of principal components for
solitary and colonial species defined areas of trunk volume
Can a mathematical model accurately predict swimming
performance across species?
The accuracy of a mathematical model of swimming was
tested by comparing predictions of speed with measurements
in C. intestinalis and D. occidentalis. These species are representative of many of the differences between solitary and
colonial species (Table 1, Fig. 6). For example, D. occidentalis has a trunk volume that is more than two orders of
magnitude greater than that of C. intestinalis (Fig. 1D). Therefore, our finding that the predicted speeds were indistinguishable from measurements in both species (Fig. 3) suggests that
the model accurately characterizes the dynamics of swimming in a diversity of ascidian larvae.
Although mathematical models of organismal function
may be based on extrapolations from first principles, complex
models are inevitably dependent on numerous simplifying
assumptions. A model’s predictions may vary tremendously
depending on the assumptions used by the investigator. For
example, both Daniel et al. (1997) and Hassan et al. (2002)
created sophisticated finite- element models of the shells of
extinct ammonites to test how septal complexity affects shell
strength. Daniel et al.’s finding that septal complexity reduces
shell strength was explicitly refuted by the model of Hassan
et al. Without a validation of either model with measurements
EVOLUTION OF ASCIDIAN LARVAE
1217
FIG. 5. The phylogenetic pattern of life-history strategy among urochordates. Colonial (filled circles), solitary (open circles), and
equivocal (half-filled circles) states are mapped onto the phylogenetic relationships proposed by Stach and Turbeville (2002) using
parsimony reconstruction (MacClade ver. 4.05, Maddison and Maddison 2000). The major urochordate clades are denoted with shaded
boxes with names given to the right and the full species names are given in only tree A. See Materials and Methods for details.
1218
TABLE 2.
Comparisons
M. J. MCHENRY AND S. N. PATEK
Phylogenetically independent contrast analyses.
Number of
contrasts
Slope
r2
P
Log trunk volume versus life history
3
0.43
Tree A
3
0.33
Tree B
3
0.34
Tree C
4
0.45
Tree D
3
0.59
Tree E
0.43
Mean
0.926
0.901
0.970
0.838
0.915
0.910
0.038
0.051
0.015
0.029
0.044
0.035
Log tail length versus life history
3
0.03
Tree A
3
0.03
Tree B
3
0.04
Tree C
4
0.04
Tree D
3
0.05
Tree E
0.04
Mean
0.156
0.205
0.156
0.310
0.261
0.217
0.606
0.547
0.605
0.330
0.489
0.515
Log trunk volume
Tree A
Tree B
Tree C
Tree D
Tree E
Mean
0.674
0.839
0.698
0.697
0.719
0.726
0.002
,0.001
,0.001
,0.001
0.016
0.004
versus log tail length
0.26
10
0.30
13
0.29
15
0.26
12
0.22
6
0.26
from related extant species, it is difficult to evaluate which
investigators more accurately replicated the biomechanics of
ammonoid shells. In the present study, model verification was
an essential first step toward applying the biomechanics of
ascidian larvae (McHenry et al. 2003) to tests of evolutionary
hypotheses of larval morphology and performance.
How does tail motion affect swimming performance?
Our results suggest that although the body shape of a larva
has important functional consequences (Fig. 8), interspecific
differences in swimming speed may largely be explained by
differences in tail-beat frequency (Figs. 2, 4). Our simulation
results found a sevenfold increase in swimming speed when
a model was run with the high-frequency kinematics of D.
occidentalis (f in Fig. 4) compared to the same model having
the low-frequency kinematics of C. intestinalis (e in Fig. 4),
whereas manipulations of morphology resulted in much
smaller changes in speed (Figs. 4, 8). This suggests that interspecific variation in speed may largely be explained by
differences in tail-beat frequency and that selection for increased speed could result in an evolutionary increase in tailbeat frequency.
Swimming with higher tail-beat frequency may allow a
larva to move faster, but this high performance comes at a
great energetic cost. The simulation moving at the rapid tailbeat frequency of D. occidentalis (f in Fig. 4) was over 32
times more energetically costly than swimming at the slow
frequency of C. occidentalis (e in Fig. 4). However, it is
possible that small increases in speed may be achieved without an energetic cost over the course of evolution from changes in larval morphology. For example, increasing the trunk
volume from that of C. intestinalis (c in Fig. 4) to that of D.
occidentalis (d in Fig. 4) resulted in swimming that was 2.2
times faster, but the cost of transport was reduced by 58%
(Fig. 4). This suggests that selection for faster swimming at
the same or reduced energetic cost may act on morphological
traits such as trunk volume.
Do colonial ascidians have a convergent larval
morphology?
Our phylogenetic analysis supports prior evidence that the
common ancestor to the urochordates was solitary and that
coloniality had multiple independent origins (Fig. 5). These
results are consistent with traditional taxonomy, which largely ignored coloniality as a trait for classification and considered both life-history strategies to be represented in many
ascidian families (Berrill 1950). Although urochordate phylogenetics remains a debated topic, there is no evidence (e.g.,
Cameron et al. 2000; Swalla 2001) that coloniality, evolved
in a single evolutionary event among ascidian species. All
trees considered presently agreed on at least three independent origins of coloniality, and this robust feature was the
most important to our comparative analysis because each
origin provided the opportunity to compare the larval traits
of one life-history strategy against another.
The results of our independent contrast analyses suggest
that colonial ascidians have a convergent larval morphology.
Although both species and contrast values scaled isometrically among both groups of species (Fig. 7), colonial ascidians had a significantly greater trunk volume (Table 2; Figs.
6, 7) and shorter tails in proportion to the trunk volume (as
shown by their lower scaling constant, Fig. 7, Table 3). These
morphological differences have implications for both the locomotion and life-history strategy of these groups of species.
For example, a larger material investment in the larvae of
colonial species (reflected by trunk volume) requires that
adults either have lower fecundity or higher total reproductive
investment than solitary species and a greater investment may
have an adverse effect on adult growth or survivorship
(Stearns 1992). In fact, colonial ascidians likely use a similar
total reproductive investment as solitary species because they
generally produce fewer of their relatively large larvae (Svane
and Young 1989). The large investment that colonial species
provide for each larva may be necessary to create a trunk
volume with the capacity to accommodate the differentiated
adult organs carried during dispersal that solitary larvae typically do not carry (Berrill 1975). Therefore, the large trunk
volume of colonial species affects not only the performance
of larval locomotion (see below), but may have a cost in
terms of adult fecundity and a benefit in allowing larvae to
carry adult organs.
How has evolutionary change in larval morphology affected
swimming performance?
Using a mathematical model of swimming biomechanics
allowed an examination of how morphology influences swimming performance in the absence of the potentially confounding effects of kinematic variation. We investigated the individual effects of trunk volume and tail length on swimming
performance by running a series of simulations with model
larva that differed only in these two parameters. Simulation
results suggest that the evolutionary convergence of colonial
species toward larger trunk volume and proportionately shorter tail length resulted in swimming that was slower, but with
EVOLUTION OF ASCIDIAN LARVAE
1219
FIG. 6. The phylogenetic distribution of larval morphology. The silhouettes illustrate the proportions of tail length, trunk radius, and
trunk length for representative solitary (open circles) and colonial (filled circles) species. The phylogenetic relationships in this case
were derived from tree C.
a lower cost of transport, than solitary species (e.g., a in Fig.
8) or larvae the size of colonial species with the proportionate
tail length of solitary species (e.g., c in Fig. 8).
The position of a larva in morphospace may affect both
locomotor performance and life-history traits that affect fitness. Among solitary ascidians, larger species are predicted
to swim faster (Fig. 8A) but have virtually the same cost of
transport as smaller species (Fig. 8B). More rapid swimming
may allow larvae to make their dispersal phase more brief
(which improves fitness in other marine invertebrates, e.g.,
bryozoans, Wendt 1996), and may enhance control over dispersal distance and habitat selection (van Duyl et al. 1981;
Durante 1991; Stoner 1994; Svane and Dolmer 1995). This
suggests that natural selection should favor larger, solitary
larvae. However, assuming a fixed total reproductive investment, larger larvae come at the cost of adult fecundity.
Similarly, Sinervo and Huey (1990) experimentally demonstrated that larger eggs in lizards create young capable of
faster running with the same stamina as young produced from
smaller eggs. However, larger lizard eggs come at the cost
of fecundity (Sinervo and Licht 1991).
The effects of larval morphology on multiple aspects of
performance may be considered with a multidimensional performance landscape. This landscape is distinct from Raup’s
concept of a multidimensional morphospace (see Raup and
Michelson 1965) because it is the performance variables, not
the morphometric parameters, that create deviation from a
three-dimensional surface. Figure 9 illustrates such a landscape in trunk volume/tail length morphospace using arrows
that point in the direction of increasing performance. Under
the assumption of a fixed total reproductive investment, increased fecundity is directed toward smaller body size along
the axis of isometric scaling (Fig. 9A). The results of our
mathematical simulations (Figs. 8A, 8B) indicate the directions of increasing speed and energetic economy (i.e., reduced cost of transport, Fig. 9A).
1220
M. J. MCHENRY AND S. N. PATEK
TABLE 3. Scaling of log-transformed trunk volume versus tail
length. b, scale factor; L1, lower 95% confidence interval, L2 upper
95% confidence interval; N, sample size.
b
L1
L2
N
Contrast values of colonial species
Tree B
0.42
0.22
Tree C
0.42
0.22
0.65
0.62
5
6
Contrast values of solitary species
Tree B
0.35
0.25
Tree C
0.34
0.17
0.46
0.51
4
4
Species values
Colonial
Solitary
0.49
0.39
13
13
0.34
0.31
Comparison
0.18
0.23
P
df
0.75
0.46
0.59
23
6
6
Colonial versus scaling constant
Species values
0.01
22
Colonial versus scaling factor
Species values
Tree B
Tree C
This multidimensional performance landscape may be used
to predict evolutionary change under selective conditions. For
example, if natural selection strongly favored increased fecundity regardless of the cost to locomotor performance, the
larvae of a solitary species would be predicted to isometrically decrease in tail length and trunk volume (a in Fig. 9B).
Under strong selection for faster swimming, tail length would
increase over the course of evolution at an allometric rate
outpacing increases in trunk volume (b in Fig. 9B). In contrast, selection for improved energetic economy would result
in an allometric reduction in tail length and an increase in
trunk volume (c in Fig. 9B). However, the observed pattern
of evolutionary change does not follow any of these patterns,
which suggests a more complex evolutionary scenario (Fig.
9C).
The evolutionary convergence of larval morphology in colonial ascidians may have resulted from trade-offs between
the swimming speed and energetic economy of larvae and
the fecundity of adults. The relatively low energetic cost of
swimming with a proportionately short tail supports the hypothesis that the tail length of colonial ascidians evolved as
an adaptation for high energetic economy. The relatively low
speed that accompanies this disproportionately short tail is
partially offset by the larger size of colonial species. The
←
FIG. 7. Trunk volume and tail length among ascidian larvae. (A,
B) These representative contrast values for trunk volume and tail
length were log-transformed. Open circles represent comparisons
between solitary species, closed circles are for comparisons between
colonial species, and the gray line shows the scaling predicted by
isometry. (A) Dark lines show linear regressions for contrasts between solitary and between colonial species based on tree C. (B)
The dark line illustrates the linear regression for all contrasts, including contrasts between solitary and colonial species (filled
squares) and ambiguous nodes (half-filled circles), based on tree
D. Tree D most closely represents the independent contrasts results
from the average across all trees. (C) Ellipses of 95% confidence
intervals for solitary (thin line) and colonial (heavy line) species
are drawn around species values in this log-transformed morphospace of trunk volume and tail length. The straight lines show the
least-squares scaling relationship for solitary (thin line) and colonial
(heavy line) species.
EVOLUTION OF ASCIDIAN LARVAE
1221
FIG. 8. Swimming performance predicted by mathematical simulations using the mean tail kinematic parameters of Ciona intestinalis.
The effects of trunk volume and tail length on the swimming speed (A) and cost of transport (B) are shown by contour lines and a
gradient of gray values. The 95% confidence intervals for the distribution of solitary (thin line) and colonial (thick line) species (as in
Fig. 7C) are overlaid on the contour map. Italicized letters denote the positions of individual species: (a) Herdmania pallida, (b) Aplidium
constellatum, and (c) a scaled-up model of larva H. pallida having the trunk volume of A. constellatum. (C) The speed (gray bars, left
axis) and cost of transport (white bars, right axis) predicted for larvae a–c.
1222
M. J. MCHENRY AND S. N. PATEK
evolutionary increase in larval size in colonial species may
have been favored by selection for faster swimming. However, further increases in size may have resulted in a penalty
to fecundity that exceeded the benefits of even faster swimming.
This consideration of evolutionary forces has necessarily
made simplifying assumptions, so it is important to consider
the potential for more complex dynamics in the evolution of
ascidian larvae. For example, ascidian larvae may be constrained from occupying regions of morphospace that are not
occupied by extant species. The size of larvae may influence
the dynamics of ascidian life-history evolution beyond the
fecundity of the adult stage (Roff 1992; Stearns 1992). Furthermore, the evolution of swimming performance is a function of changes in both tail motion and morphology. Our
finding that swimming performance is strongly affected by
tail-beat frequency (described above) suggests that evolutionary changes in performance my largely be attributed to
change in this kinematic trait. The present study conducted
an intensive three-dimensional kinematic analysis that would
be prohibitively labor intensive to conduct on the numerous
species necessarily for a broadly comparative study. However, we found that the only significant kinematic difference
between C. intestinalis and D. occidentalis was in their tailbeat frequency, a parameter that is relatively easy to measure
from video recordings of swimming. It would therefore be
tractable and interesting to examine how changes in tail-beat
frequency have influenced the evolution of swimming speed
in ascidian larvae in a future study.
In summary, the present study finds that colonial ascidians
have independently evolved a larval morphology with a larger
trunk volume and proportionately smaller tail length than
solitary species. Our mathematical modeling suggests that
this evolutionary convergence resulted in slower swimming
with improved energetic economy. However, the larger size
of colonial larvae may have required a reduction in adult
fecundity. These results were found through the use of biomechanical techniques that verified the accuracy of a mathematical model, phylogenetic comparative analyses that rigorously demonstrated the convergence of trunk volume, and
theoretical morphology to examine the functional significance of convergent morphology in the absence of the confounding effects of behavioral variation. This integration of
approaches holds potential for understanding the evolution
of organismal function in a diversity of complex organismal
systems.
ACKNOWLEDGMENTS
We thank M. Koehl, G. Lauder, and B. Swalla for their
advice. Two anonymous reviewers provided valuable sug-
←
FIG. 9. Multidimensional performance landscape. Arrows denote
the direction of increasing performance in speed (green), energetic
economy (orange), and fecundity (violet) for ascidian larvae. (A)
The direction of increasing speed was determined from the performance landscape shown in Figure 8A and the direction of higher
energetic economy (i.e., lower cost of transport) was found from
Figure 8B. Increased fecundity is directed along the axis of iso-
metric scaling. (B) Predicted evolutionary change from the position
of a typical solitary species (filled circle) is illustrated in the direction of heavy black arrows under different selective conditions:
(a) selection for increased fecundity, (b) selection for faster swimming, and (c) selection for improved energetic economy. (C) Ellipses of 95% confidence intervals approximate the distribution of
solitary (thin gray line) and colonial (heavy gray line) species.
EVOLUTION OF ASCIDIAN LARVAE
gestions for the manuscript. Larvae and adults of C. intestinalis were provided by the Levine lab at the University of
California at Berkeley. This work was supported with a National Science Foundation predoctoral fellowship and grantsin-aid of research from the American Society of Biomechanics, Sigma Xi, the Department of Integrative Biology
(University of California Berkeley) and the Society for Integrative and Comparative Biology to MJM, the Miller Institute for Basic Research in Science to SNP, and grants from
the National Science Foundation (OCE-9907120) and the Office of Naval Research (AASERT N00014-97-1-0726) to M.
Koehl.
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Corresponding Editor: P. Wainwright