(2004). The evolution of body shape and swimming performance in ...

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q 2004 The Society for the Study of Evolution. All rights reserved.

Evolution, 58(6), 2004, pp. 1209–1224

THE EVOLUTION OF LARVAL MORPHOLOGY AND SWIMMING PERFORMANCEIN ASCIDIANS

MATTHEW J. MCHENRY1,2 AND SHEILA N. PATEK3,4

1The Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 021382E-mail: [email protected]

3The Department of Integrative Biology, University of California, Berkeley, California 947204E-mail: [email protected]

Abstract. The complexity of organismal function challenges our ability to understand the evolution of animal lo-comotion. To meet this challenge, we used a combination of biomechanics, phylogenetic comparative analyses, andtheoretical morphology to examine evolutionary changes in body shape and how those changes affected swimmingperformance in ascidian larvae. Results of phylogenetic comparative analyses suggest that coloniality evolved at leastthree times among ascidians and that colonial species have a convergent larval morphology characterized by a largetrunk volume and shorter tail length in proportion to the trunk. To explore the functional significance of this evolutionarychange, 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 andtrunk volume. The results of these simulations were used to construct landscapes of speed and cost of transportpredictions within a trunk volume/tail length morphospace. Our results suggest that the reduction of proportionatetail length in colonial species resulted in improved energetic economy of swimming. The increase in the size of larvaewith the origin of coloniality facilitated faster swimming with negligible energetic cost, but may have required areduction in adult fecundity. Therefore, the evolution of ascidians appears to be influenced by a trade-off betweenthe 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. Accepted March 15, 2004.

The biomechanical complexity of animal motion presentschallenges for understanding broad patterns of locomotorevolution. Measures of locomotor performance typically havea nonlinear dependency on numerous aspects of the mor-phology and motion of an animal’s body (McMahon 1984;Alexander 2003; Biewener 2003) and interspecific variationin these traits may be substantial. Ascidians (Chordata: Uro-chordata) present an interesting case study of locomotor evo-lution because the larvae of colonial species are similar insize and shape despite having evolved independently at leastthree times among urochordates (Swalla et al. 2000). Throughthe integration of biomechanics, phylogenetic comparativeanalyses, and theoretical morphology, we examined how evo-lutionarily convergent colonial life histories have influencedthe morphology and swimming performance of ascidian lar-vae.

Biomechanical, Comparative, and Theoretical Approachesto the Evolution of Organismal Function

Research on the evolution of organismal function may useextant species by either testing for correlations between traitsand performance or by investigating functional mechanisms(reviews include Wake and Roth 1989; Bennett and Huey1990; Garland and Carter 1994; Thomason 1995; Koehl 1996;Lauder 2003). A correlative approach explores natural co-variation between traits and performance (e.g., Arnold andBennett 1988; Jayne and Bennett 1990; Losos 1990; Patekand 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 onfunctional relationships (e.g., Losos 1990; Bauwens et al.1995). Form-function relationships established with a strictlycorrelative approach (reviewed by Arnold 1983; Huey and

Bennett 1986; Jayne and Bennett 1989) may be confoundedby variation in performance caused by traits other than thoseexamined (Koehl 1996). Many mechanistic investigationshave attempted to resolve the causal relationships betweentraits and performance by developing mathematical modelsof locomotion (e.g., Daniel 1983; Liu et al. 1996; Sane andDickinson 2002; McHenry et al. 2003). However, such idi-ographic studies have limited applicability to evolutionaryquestions because they generally neglect the effects of intra-and interspecific variation in favor of understanding generalfunctional principles. Mechanistic studies that examine theextreme differences among species within a group (e.g.,Kingsolver and Koehl 1985; Crompton 1989; Emerson andKoehl 1990; Drucker and Lauder 2001) have proven valuablefor exploring the extremes of performance exhibited by agroup of species. However, general principles and knowledgeof performance extremes alone are limited in their ability toinform our understanding of changes in function that resultfrom a sequence of historical transformations.

Theoretical morphology provides the tools to examine his-torical transformations with mechanistic models toward theultimate goal of testing evolutionary hypotheses. This ana-lytical technique involves constructing a theoretical spectrumof morphological parameters (a morphospace), the measure-ment of species distributions within that space, and using amathematical model to determine the functional significanceof morphologies that are both represented and absent amongspecies (Raup and Michelson 1965; Raup 1967; McGhee1999). This model may be used to generate predictions ofperformance for each position in the morphospace and there-by generate a performance landscape (also known as a per-formance surface: Arnold 2003; a fitness landscape: Gilchristand Kingsolver 2003; or a functional morphospace: Moore

1210 M. J. MCHENRY AND S. N. PATEK

and Ellers 1993). Performance landscapes have been used totest adaptive hypotheses that ammonite shell geometry gen-erates high locomotor stability (Raup 1967) and strengthagainst hydrostatic pressure (Daniel et al. 1997), to determinewhether morphological disparity among labrid fishes facili-tates disparity in function (Hulsey and Wainwright 2002), toidentify developmental constraints in the body shape of seaurchins (Ellers 1993), and to investigate the effects of en-vironmental change on the macroevolution of vascular plants(Niklas 1997). The models used to generate performancelandscapes may come in the form of simple algebraic equa-tions (e.g., Moore and Ellers 1993) or elaborate computa-tional simulations (e.g., Daniel et al. 1997), depending onthe complexity of the functional system.

The present study tested the accuracy of a mathematicalmodel of swimming in ascidian larvae (McHenry et al. 2003)and used this model to construct landscapes of swimmingperformance. According to this model, the hydrodynamics ofswimming vary widely among ascidian species, which swimat Reynolds numbers (Re 5 rUL/m, where U is mean swim-ming speed, L is body length, r and m are the density andviscosity of water; Lamb 1945) from 5 in Ciona intestinalis(Bone 1992) to 100 in Distaplia occidentalis (McHenry2001). At any Re value, the magnitude and direction of pro-pulsive forces depends on the shape of the larval body andthe undulatory motion of the tail.

Ascidian Larvae

Ascidians are a large and diverse group of marine inver-tebrates with a complex life history characterized by a sessileadult and a pelagic larval stage. Comprised of more than 3000species (Jeffery 1997), ascidians were included in the phylumChordata because their larvae possess a notochord (Kowa-levsky 1866), an organ that plays a role in their undulatoryswimming (McHenry 2001). Recent phylogenetic studies(e.g., Cameron et al. 2000; Swalla et al. 2000) support thisclassification and find that the urochordata (which includesascidians and the less speciose pelagic larvaceans and thal-iaceans) is a monophyletic group that includes ascidians asa polyphyletic assemblage united by the presence of a sessileadult stage (Swalla et al. 2000; Stach and Turbeville 2002).

The larval stage provides an ascidian with its only oppor-tunity for dispersal by locomotion. Ascidian larvae have arigid globose trunk that is propelled through the water by itsflexible tail, thereby bearing a gross resemblance to an anurantadpole. These tadpole larvae (sensu Brusca and Brusca 1990)do not feed and therefore rely on a fixed storage of energyto survive through dispersal and metamorphosis (Burigheland Cloney 1997). This suggests that larvae that swim witha relatively low energetic cost of transport (McMahon 1984)should have an improved chance of survival through the lar-val stage (as in bryozoans; Wendt 2000). Field observationssuggest that larvae may enter into and exit from fast hori-zontal currents with vertically oriented swimming. Therefore,dispersal distance may be influenced by the speed with whicha larva traverses these currents (Young 1986; Bingham andYoung 1991; Stoner 1992). Fast swimming may also shortenthe duration of the dispersal phase and allow larvae greatercontrol over their selection of a microhabitat for settlement

(van Duyl et al. 1981; Durante 1991; Stoner 1994; Svane andDolmer 1995). Therefore, speed and cost of transport are twomeasures of swimming performance that may have importantconsequences for dispersal distance and duration, microhab-itat selection, larval survivorship, and, ultimately, to fitness.

Although ascidians exhibit tremendous diversity in life-history traits (reviewed by Svane and Young 1989), solitaryand colonial species represent the two major types of ascidianlife-history strategies. Colonial (i.e., compound and social)ascidians produce adult zooids by asexual reproduction andthey generally brood a relatively small number of large larvaethat spend a brief time in the plankton (less than a few hours;Berrill 1935). Solitary species generally broadcast spawntheir gametes and their numerous small larvae develop rap-idly in the plankton. Therefore, solitary species may provideless material investment and protection for larvae than co-lonial species, but they have higher fecundity (Svane andYoung 1989). The larvae of colonial species are so muchlarger than solitary species that their trunks may be morethan three orders of magnitude greater in volume (Cloney1978).

It remains unclear to what degree patterns of life-historytraits and larval morphology are due to shared ancestry orconvergent evolution. It has long been appreciated that bothsolitary and colonial species are distributed throughout as-cidian families (Berrill 1950) and recent phylogenetic studiessuggest that coloniality has a number of independent origins(Swalla et al. 2000). Finding the phylogenetic distribution oflife-history strategy is requisite for understanding whetherthe observed patterns in larval morphology are correlatedwith life history or due to shared ancestry. Using recent phy-logenetic systematic studies (e.g., Swalla et al. 2000; Stachand Turbeville 2002), we examined the phylogenetic distri-bution of larval morphology among solitary and colonial spe-cies.

The broad goals of the present study were to determinethe patterns of evolutionary change in larval morphologyamong ascidians and to understand how this change affectedswimming performance. We pursued these goals by focusingon four questions: (1) Can a mathematical model accuratelypredict swimming performance across species? (2) How doestail motion affect swimming performance? (3) Do colonialascidians have a convergent larval morphology? (4) How hasevolutionary change in larval morphology affected swimmingperformance?

MATERIALS AND METHODS

Biomechanics

The peripheral shape of the body and the tail motion ofC. intestinalis and D. occidentalis were measured to modelthe hydrodynamics of their swimming. These measurementswere previously reported for D. occidentalis (McHenry 2001),and are newly presented for C. intestinalis. Adults of bothC. intestinalis and D. occidentalis were collected in northernCalifornia, USA, and held in a recirculating seawater tank at168C. Larvae of C. instestinalis were cultured from the gam-etes of adults using standard embryological techniques (seeStrathmann 1987). Colonies of D. occidentalis were exposedto bright incandescent light after being kept in darkness over-

1211EVOLUTION OF ASCIDIAN LARVAE

night to stimulate the release of brooded larvae (Cloney1987).

Morphometrics of body shape

The peripheral shape of the bodies of larvae was measuredusing digital still images and approximated with a series ofequations. Digital photographs (Coolpix 700, Nikon, Mel-ville, NY) of larvae from dorsal and lateral views (N 5 5 forC. intestinalis, N 5 11 for D. occidentalis) were importedinto Matlab (rel. 12 Mathworks, Natick, MA; on a LifebookE, Fujitsu, Tokyo), where a custom program found the co-ordinates describing the peripheral shape of the body. Thedorsal margin of the trunk was described by a half-ellipsehaving a major axis equal to half the length, lmax, and a minoraxis equal to the radius, wmax, of the trunk. The trunk radiuswas measured as half of the mean of the maximum thicknessof the trunk measured from lateral and dorsal views. Thedistance 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 Fin-ney 1980):

24(l 2 l /2)max2w(l) 5 w 1 2 , (1)max 2[ ]! lmax

where 0 , l , lmax. Half-ellipses were used in this way todescribe the dorsal, ventral, and lateral margins of the trunk.The trunk was assumed to be circular in cross section witha radius equal to w. The cellular region of the tail was alsoassumed to be circular in cross-section (as in McHenry 2001;McHenry and Strother 2003), with the radius tapering pos-teriorly, as described by the following equation:

r smaxr(s) 5 2 1 r (2)max0.85F

where rmax is the maximum measured radius, s is the positionalong the midline of the tail and 0 , s , 0.85F, where F isthe tail length. The distance between the dorsal margin ofthe tail fin and the tail midline, q, was described with thefollowing function:

q at s , 0.2maxq(s) 5 (3)1.25q (1 2 s /F ) at s $ 0.2, max

where qmax is the maximum height of the tail fin and 0 , s, F. Assuming dorsoventral symmetry, we used the samefunction to describe the ventral margin of the tail fin. Fromthese measurements of peripheral shape, we calculated thebody mass, m, center of mass, and the moment of inertiausing a program written in Matlab (for details, see McHenryet al. 2003). We tested for significant differences in mor-phological parameters between D. occidentalis and C. intes-tinalis using an unpaired Student’s t-test in Matlab (Sokaland Rohlf 1995).

Kinematics of swimming

The three-dimensional tail kinematics of freely swimminglarvae of both species were recorded with two high-speedvideo cameras (Motionscope PCI Mono/1000S, Redlake Im-

aging, San Diego, CA). Coordinates along the midline of thebody were found from video images of larvae and trans-formed with respect to the frontal plane of the body using acustom computer program (for details see McHenry 2001).Undulatory kinematics were described by fitting midline co-ordinates to equations (explained in McHenry 2001) that de-scribe changes in the angle between the trunk and tail andthe curvature of the tail with time. Neglecting any asymmetryin tail motion, these equations allowed the kinematics to bedescribed 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 werecompared (N 5 5 in C. intestinalis and N 5 14 for D. oc-cidentalis) by testing for significant differences in these pa-rameters using an unpaired Student’s t-test (Sokal and Rohlf1995).

Mathematical modeling of swimming

We used a mathematical model of the biomechanics ofswimming that was developed by McHenry et al. (2003). Thismodel approximates the quasi-steady fluid forces acting onthe trunk and tail of a larva given a description of the body’speripheral shape, tail kinematics, and mass. We solved theequations describing these forces numerically using a vari-able order Adams-Bashforth-Moulton solver programmed inMatlab (Shampine and Gordon 1975) to find how the velocity,rate of rotation, position, and orientation of the body changedwith time in two dimensions during a swimming sequence.

The mean swimming speed and the hydrodynamic cost oftransport were calculated to assess the performance of eachmathematical simulation. Each simulation lasted for a du-ration of six tail beats and the results from unsteady swim-ming were discarded by removing calculations for the firsttail beat. The hydrodynamic cost of transport (COT) wascalculated with the following equation (McHenry and Jed2003):

n

U T DtO i ii51COT 5 , (4)

mx

where i is the index for each of the n instantaneous valuesof speed, Ui, and thrust, Ti, and x is the net distance traversedover the duration of a swimming sequence. This measure ofenergetic economy neglects internal costs and therefore pro-vides a minimum estimate of the metabolic cost of transport(Schmidt-Nielsen 1972).

The accuracy of the model was tested by comparing pre-dictions of speed for C. intestinalis and D. occidentalis withmeasurements. In simulations and experiments, averagespeed was calculated as the mean of instantaneous speedvalues. This measure of speed is not equivalent to the netspeed of swimming (i.e., total distance divided by duration),because of the meandrous path followed by models and lar-vae. For each larva that we measured tail kinematics andspeed, a mathematical simulation was run with the same ki-nematics, and the predicted and measured speeds were com-pared with a paired Student’s t-test for each species.

The relative contributions of differences in morphologicaland kinematic parameters on the performance differences be-


TABLE 1. Morphometric data for comparative analyses.

Species

Trunklength(mm)

Trunkradius(mm)

Log10trunk volume

(mm3)

Taillength(mm)

Bodylength(mm) Source

SolitaryAscidia mentulaAscidiella aspersasAscidiella scabraCiona intestinalis

0.170.310.300.30

0.060.09—

0.06

22.9722.30

22.60

0.470.870.601.16

0.641.190.901.46

Berrill 1931, Berrill 1950Berrill 1929Berrill 1931present study

Corella inflataDendrodoa grossulariaHalocynthia roretziHerdmania pallidaMolgula tubifera

0.200.620.390.240.17

0.080.240.120.08—

22.5921.1221.9022.48

0.632.071.380.910.50

0.842.681.771.150.67

Young 2002, present studyBerrill 1929Satoh 1994Sebastian 1953Berrill 1931

Molgula citrinaMolgula oculataMolgula complanataMolgula manhattensisPolycarpa fibrosaPyura pachydermatinaStyela partita

0.390.110.400.150.200.310.22

0.120.04—

0.040.110.110.06

21.9223.41

23.3322.3422.0722.81

1.320.371.200.500.830.940.64

1.710.481.600.651.021.250.85

Grave 1926Jeffery and Swalla 1992Berrill 1931Berrill 1950Berrill 1929Anderson et al. 1976Berrill 1950

ColonialAplidium constallatumAplidium punctumBotrylloides leachiiBotrylloides sp.Botrylloides simodensisBotryllus gigasBotryllus schlosseriClavelina picta

0.790.530.561.080.470.850.521.08

0.190.190.180.280.180.280.180.32

21.2421.4121.4420.7521.4820.8621.4320.64

1.460.981.041.891.272.081.152.52

2.251.511.602.971.732.931.673.60

Grave 1921Berrill 1950Berrill 1935McHenry 2001, present studyMukai et al. 1987Berrill 1935Berrill 1950Berrill 1935

Didemnum pacificumDistaplia occidentalisDistomus variolosusMorchellium argusPerophora listeriPolyandrocarpa gravei

0.531.290.830.500.320.38

0.190.180.27—

0.120.12

21.4021.0420.90

22.0121.93

1.182.271.721.300.581.45

1.713.552.551.800.901.83

Tokioka 1953present studyBerrill 1950Berrill 1931Berrill 1950Grave 1932

tween C. intestinalis and D. occidentalis were examined byrunning a series of simulations. Simulations were run withparameter 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, maximumcurvature, and maximum trunk angle). For example, to ex-amine the effect of tail length, we first ran a simulation usingall the parameter values of C. intestinalis, and then ran asimulation of the same model except that it used the taillength of D. occidentalis. The resulting differences in per-formance were used to indicate the effect of tail length.

Phylogenetic Comparative Analyses

The evolutionary patterns of life-history strategy and larvalmorphology were examined by mapping traits onto phylog-enies and applying phylogenetically independent contrastanalyses (Felsenstein 1985; Harvey and Pagel 1991). Theseanalyses were conducted using five published phylogenies(figs. 2, 4 from Stach and Turbeville 2002) and were codedinto MacClade (ver. 4.05, Maddison and Maddison 2000).We will refer to the phylogeny found by strict consensus of18S rDNA sequences (fig. 2A in Stach and Turbeville 2002)as tree A, by strict consensus of 18S rDNA and morphologicaltraits (fig. 2B in Stach and Turbeville 2002) as tree B, bymaximum likelihood of 18S rDNA sequences (fig. 2C inStach and Turbeville 2002) as tree C, by strict consensus of

partial cox 1 mitochondrial DNA sequences (fig. 4A in Stachand Turbeville 2002) as tree D, and by strict consensus ofamino acid sequences translated from partial cox 1 mito-chondrial DNA sequences (fig. 4B in Stach and Turbeville2002) 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 includedin the Stach and Turbeville (2002) phylogenies. Analyses ofmorphology were implemented using modified trees that onlyincluded taxa with morphological data. For cases in whichgenera were monophyletic in all trees, we exchanged speciesdata within genera such that we maximized the amount ofcomparative data to be used in the analyses. Due to thesemodifications of the tree structure, we were not able to in-corporate branch lengths into the trees when conducting in-dependent contrast tests.

We reconstructed the phylogenetic pattern of life-historystrategy using MacClade’s most parsimonious reconstruction(Maddison and Maddison 2000) based on all five trees underconsideration. Phylogenetic comparative tests of correlationsbetween traits were conducted using CAIC (ver. 2.6.9, Purvisand Rambaut 1995). Brunch algorithms were used for thecategorical tests examining colonial/solitary transitions andCrunch algorithms were used for morphological traits. Mor-phological traits were log-transformed to reduce the depen-


FIG. 1. The body shape of larvae. The peripheral shape of the bodies of larvae of (A) Distaplia occidentalis (N 5 11) and (B) Cionaintestinalis (N 5 5) is shown from dorsal and lateral views, with mean values (horizontal hatches, 61 SD) at 70 positions down thelength 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 dimensionsand (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). Statisticalcorrelations of contrasts were calculated using a regressionline forced through the origin, as implemented by CAIC(Purvis and Rambaut 1995).

Morphological traits were recorded from values reportedin the literature (sources listed in Table 1), measured fromscans of published camera lucida drawings, or measured fromdigital photographs of larvae. The positions of morphologicallandmarks were recorded from scans of drawings (Epson3200 Photo, San Jose, CA) and digital photographs (NikonCoolpix 700) using a custom program in Matlab. We mea-sured trunk length and radius and tail length and calculatedthe volume of the trunk by assuming an ellipsoidal shape(McHenry et al. 2003). Distaplia occidentalis was excludedin these comparisons because this species was not includedin the phylogenetic analysis of Stach and Turbeville (2002).

The scaling of body shape was examined in colonial andsolitary species using both species and contrast values. Theexponential relationship between trunk volume and tail lengthwas described by a scaling constant, a, and scaling factor, b,

of an exponential equation (F 5 aVb; Huxley 1932). Wetested whether colonial and solitary species scaled isomet-rically (F 5 aV0.33) by calculating the profile likelihood con-fidence intervals for the regression slopes (JMP 5.0.1) andobserving whether the slope value of 0.33 fell within theseconfidence intervals. We compared species and contrast val-ues of colonial and solitary species regression slopes andintercepts using a t-test modified for comparing linear re-gressions (Zar 1999, ch. 18).

Theoretical Morphology

Theoretical morphology was used to examine the distri-bution of colonial and solitary species in a morphospace andperformance landscape. We used a principal componentsanalysis to define areas of trunk volume/tail length mor-phospace occupied by colonial and solitary species. Theboundaries of these areas were defined by ellipses of 95%confidence intervals for the major and minor axes of variationin each of these groups (Sokal and Rohlf 1995). We foundthe speed and cost of transport predicted for positions


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 viewof a larva of (A) Distaplia occidentalis and (B) Ciona intestinalis. The mean values and standard deviations of the (C) maximum curvatureof 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 ourbiomechanical model (see above) over a range of trunk vol-ume and tail length values at 15 equal intervals, for a totalof 225 simulations, which spanned beyond the range of mea-sured values in each parameter measured. Simulations wererun with the tail kinematics and body shape of C. intestinalis.For example, trunk volume was varied by altering the trunkwidth and trunk length, but the ratio of these parametersremained equal to that of C. intestinalis throughout all sim-ulations.

RESULTS

Morphology, Kinematics, and Performance of Cionaintestinalis and Distaplia occidentalis

A comparison of morphology and kinematics between C.intestinalis and D. occidentalis presents some of the differ-ences and similarities between colonial and solitary species.The peripheral shapes of the bodies of both species were wellapproximated by the equations and parameter values describ-ing body shape (eq. 1–3; Fig. 1A, B). Distaplia occidentaliswas 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 greaterthan that of C. intestinalis (V̄ 5 2.60 3 1023 mm3, Fig. 1D).The undulatory motions of both species were qualitativelysimilar (Fig. 2A, B) and the two species were indistinguish-able in their maximum curvature (P 5 0.75, Fig. 2C) andmaximum trunk angle (P 5 0.74, Fig. 2D). However, D.occidentalis swam with a significantly higher tail-beat fre-quency than C. intestinalis (P 5 0.04, Fig. 2E).

Mathematical simulations of the biomechanics of swim-ming predicted different trajectories and average swimmingspeeds for the two species (Fig. 3). Distaplia occidentalis waspredicted to generate greater trunk rotation with each tailbeat 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 instantaneousvalues) in both species oscillated with time (Fig. 3C, D), butthe average speed of swimming was more than an order ofmagnitude greater in D. occidentalis than in C. intestinalis(Fig. 3E, F), a difference that was reflected in measurementsof freely swimming larvae. In both species, the mathematical


FIG. 3. Typical results from the mathematical model of swimming biomechanics. Points show examples of the movement predicted forthe 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. intestinalislarvae.

model predicted speeds that were statistically indistinguish-able from these measurements of speed (paired t-test, P 50.07 in D. occidentalis, Fig. 3E; P 5 0.28 in C. intestinalis,Fig. 3F).

The effect of individual morphometric and kinematic dif-ferences on the performance differences between D. occi-dentalis and C. intestinalis were evaluated with the results ofa series of simulations (a–f in Fig. 4). Increasing the taillength 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 (din Fig. 4) resulted in swimming that was nearly twice thespeed, but had a lower cost of transport. A further decreasein the cost of transport was achieved by changing the trunkshape (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 relativeto the effect of tail kinematics. A model having the bodyshape of D. occidentalis, but the tail kinematics of C. intes-tinalis (e in Fig. 4) moved with a speed that was just 14%the speed and 3% the cost of transport of the same modelanimated with the kinematics of D. occidentalis (f in Fig. 4).

Phylogeny and Independent Contrasts

Parsimony reconstructions of ascidian life history sug-gested that the common ancestor to the urochordates wassolitary, and that coloniality evolved independently at leastthree times among urochordates (Fig. 5). The clade of Stye-

lidae 1 Pyuridae includes both solitary and colonial speciesand suggests at least one origin of coloniality. All Aplou-sobranchiata species were colonial, which implies an originof coloniality prior to their most recent common ancestor.Perophora japonica is a colonial member of the largely sol-itary Phlebobranchiata clade. Coloniality appears to have ei-ther evolved in the lineage leading to P. japonica (as in treesA and C), or possibly prior to the common ancestor to thePhlebobranchiata and Thaliacea (equivocal in tree B). Theorigin of coloniality arising prior to the common ancestor ofthe Thaliacea was not considered in our analysis of larvalmorphology due to a lack of larval data for this group. As aresult of these patterns of life-history evolution, independentcontrast analyses based on each of these trees yielded eitherthree or four contrasts for comparison of larval morphologybetween species of each life-history strategy (Table 2).

Phylogenetically independent contrast analyses were usedto examine whether the observed patterns of larval mor-phology in colonial species were the result of shared ancestryor evolutionary convergence (Fig. 6). We found that colonialascidians have significantly greater trunk volume than thelarvae of solitary species (P̄ 5 0.035, Table 2) and that taillength was significantly correlated with trunk volume (P̄ 50.004, Table 2, Fig. 7A, B). However, colonial species werestatistically indistinguishable from solitary species in taillength (P̄ 5 0.515). Although the absolute values for taillength were indistinguishable between colonial and solitaryspecies, the scaling of tail length relative to trunk volumewas different in these groups (see below).


FIG. 4. The effect of morphology and kinematics on swimmingperformance. The parameter values and predicted performance arealigned in columns for each of six simulations (a–f). Filled squaresdenote which of the listed parameters have the value for Distapliaoccidentalis and open squares denote which have the value for Cionaintestinalis. The resulting performance for each simulation is pre-sented in the bar charts for the (A) speed and (B) cost of transportpredicted for larvae.

Both colonial and solitary species were found to scale iso-metrically. For all regressions of log-transformed values oftrunk volume and tail length, the slope of 0.33 fell withinthe limits of the confidence intervals for both independentcontrast and species values (Table 3). Scaling factors did notdiffer significantly between solitary and colonial species.However the scaling constant (i.e., the intercept of the re-gression, Fig. 7C) was significantly different between colo-nial and solitary species values (Table 3). The lower interceptof colonial ascidians (Table 3, Fig. 7C) means that thesespecies have a tail length that is smaller in proportion totrunk volume than solitary species.

Morphospace and Performance Landscapes

The 95% confidence intervals of principal components forsolitary and colonial species defined areas of trunk volume

and tail length morphospace occupied by ascidian larvae (Fig.7C). The species values for Herdmania pallida approximatedthe mean trunk volume and tail length of solitary species (V5 8.2 3 1024 mm3, F 5 0.91 mm) and the mean values forcolonial species were approximated by Aplidium constellatum(V 5 1.4 3 1022 mm3, F 5 1.46 mm). Therefore, we con-sidered these species to be representative of larvae producedby the species of their respective life history strategy.

The results of our mathematical simulations allowed us toexamine the effects of trunk volume and tail length on swim-ming performance given the same tail kinematics (Fig. 8).The fastest swimming was predicted for larvae having rel-atively long tails (F . 2.5 mm) and either low (V , 1023

mm3) or intermediate (1022 mm3 , V , 1021 mm3) trunkvolume (Fig. 8A). However, the cost of transport was lowestin larvae having relatively small tails (F , 1.6 mm) and largetrunks (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 char-acterized by slightly slower speed, but a lower cost of trans-port than solitary species. For example, the solitary H. pallidamoved 69 % faster than colonial A. constellatum (12.3 mmsec21 compared to 8.5 mm sec21), but with a 44% greatercost of transport (2.5 J kg21 m21 compared to 1.1 J kg21 m21,Fig. 8C). A model larva having the proportionate tail lengthof H. pallida, but the trunk volume of A. constellatum movedfaster than both species, but with an intermediate cost oftransport (13.6 mm sec21, 2.2 J kg21 m21, Fig. 8C). Neithergroup of species occupies regions of morphospace that resultin extremely fast or energetically costly swimming. Further-more, the influence of morphological variation on swimmingperformance is subtle compared to the effect of tail motion(Fig. 4, described above).

DISCUSSION

Can a mathematical model accurately predict swimmingperformance across species?

The accuracy of a mathematical model of swimming wastested by comparing predictions of speed with measurementsin C. intestinalis and D. occidentalis. These species are rep-resentative of many of the differences between solitary andcolonial species (Table 1, Fig. 6). For example, D. occiden-talis has a trunk volume that is more than two orders ofmagnitude greater than that of C. intestinalis (Fig. 1D). There-fore, our finding that the predicted speeds were indistinguish-able from measurements in both species (Fig. 3) suggests thatthe model accurately characterizes the dynamics of swim-ming in a diversity of ascidian larvae.

Although mathematical models of organismal functionmay be based on extrapolations from first principles, complexmodels are inevitably dependent on numerous simplifyingassumptions. A model’s predictions may vary tremendouslydepending on the assumptions used by the investigator. Forexample, both Daniel et al. (1997) and Hassan et al. (2002)created sophisticated finite- element models of the shells ofextinct ammonites to test how septal complexity affects shellstrength. Daniel et al.’s finding that septal complexity reducesshell strength was explicitly refuted by the model of Hassanet al. Without a validation of either model with measurements


FIG. 5. The phylogenetic pattern of life-history strategy among urochordates. Colonial (filled circles), solitary (open circles), andequivocal (half-filled circles) states are mapped onto the phylogenetic relationships proposed by Stach and Turbeville (2002) usingparsimony reconstruction (MacClade ver. 4.05, Maddison and Maddison 2000). The major urochordate clades are denoted with shadedboxes with names given to the right and the full species names are given in only tree A. See Materials and Methods for details.


TABLE 2. Phylogenetically independent contrast analyses.

ComparisonsNumber ofcontrasts Slope r2 P

Log trunk volume versus life historyTree ATree BTree CTree DTree E

Mean

33343

0.430.330.340.450.590.43

0.9260.9010.9700.8380.9150.910

0.0380.0510.0150.0290.0440.035

Log tail length versus life historyTree ATree BTree CTree DTree E

Mean

33343

0.030.030.040.040.050.04

0.1560.2050.1560.3100.2610.217

0.6060.5470.6050.3300.4890.515

Log trunk volume versus log tail lengthTree ATree BTree CTree DTree E

Mean

10131512

6

0.260.300.290.260.220.26

0.6740.8390.6980.6970.7190.726

0.002,0.001,0.001,0.001

0.0160.004

from related extant species, it is difficult to evaluate whichinvestigators more accurately replicated the biomechanics ofammonoid shells. In the present study, model verification wasan essential first step toward applying the biomechanics ofascidian larvae (McHenry et al. 2003) to tests of evolutionaryhypotheses of larval morphology and performance.

How does tail motion affect swimming performance?

Our results suggest that although the body shape of a larvahas important functional consequences (Fig. 8), interspecificdifferences in swimming speed may largely be explained bydifferences in tail-beat frequency (Figs. 2, 4). Our simulationresults found a sevenfold increase in swimming speed whena model was run with the high-frequency kinematics of D.occidentalis (f in Fig. 4) compared to the same model havingthe low-frequency kinematics of C. intestinalis (e in Fig. 4),whereas manipulations of morphology resulted in muchsmaller changes in speed (Figs. 4, 8). This suggests that in-terspecific variation in speed may largely be explained bydifferences in tail-beat frequency and that selection for in-creased speed could result in an evolutionary increase in tail-beat frequency.

Swimming with higher tail-beat frequency may allow alarva to move faster, but this high performance comes at agreat energetic cost. The simulation moving at the rapid tail-beat frequency of D. occidentalis (f in Fig. 4) was over 32times more energetically costly than swimming at the slowfrequency of C. occidentalis (e in Fig. 4). However, it ispossible that small increases in speed may be achieved with-out an energetic cost over the course of evolution from chang-es in larval morphology. For example, increasing the trunkvolume from that of C. intestinalis (c in Fig. 4) to that of D.occidentalis (d in Fig. 4) resulted in swimming that was 2.2times 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 morphologicaltraits such as trunk volume.

Do colonial ascidians have a convergent larvalmorphology?

Our phylogenetic analysis supports prior evidence that thecommon ancestor to the urochordates was solitary and thatcoloniality had multiple independent origins (Fig. 5). Theseresults are consistent with traditional taxonomy, which large-ly ignored coloniality as a trait for classification and consid-ered both life-history strategies to be represented in manyascidian families (Berrill 1950). Although urochordate phy-logenetics remains a debated topic, there is no evidence (e.g.,Cameron et al. 2000; Swalla 2001) that coloniality, evolvedin a single evolutionary event among ascidian species. Alltrees considered presently agreed on at least three indepen-dent origins of coloniality, and this robust feature was themost important to our comparative analysis because eachorigin provided the opportunity to compare the larval traitsof one life-history strategy against another.

The results of our independent contrast analyses suggestthat colonial ascidians have a convergent larval morphology.Although both species and contrast values scaled isometri-cally among both groups of species (Fig. 7), colonial ascid-ians had a significantly greater trunk volume (Table 2; Figs.6, 7) and shorter tails in proportion to the trunk volume (asshown by their lower scaling constant, Fig. 7, Table 3). Thesemorphological differences have implications for both the lo-comotion and life-history strategy of these groups of species.For example, a larger material investment in the larvae ofcolonial species (reflected by trunk volume) requires thatadults either have lower fecundity or higher total reproductiveinvestment than solitary species and a greater investment mayhave an adverse effect on adult growth or survivorship(Stearns 1992). In fact, colonial ascidians likely use a similartotal reproductive investment as solitary species because theygenerally produce fewer of their relatively large larvae (Svaneand Young 1989). The large investment that colonial speciesprovide for each larva may be necessary to create a trunkvolume with the capacity to accommodate the differentiatedadult organs carried during dispersal that solitary larvae typ-ically do not carry (Berrill 1975). Therefore, the large trunkvolume of colonial species affects not only the performanceof larval locomotion (see below), but may have a cost interms of adult fecundity and a benefit in allowing larvae tocarry adult organs.

How has evolutionary change in larval morphology affectedswimming performance?

Using a mathematical model of swimming biomechanicsallowed an examination of how morphology influences swim-ming performance in the absence of the potentially confound-ing effects of kinematic variation. We investigated the in-dividual effects of trunk volume and tail length on swimmingperformance by running a series of simulations with modellarva that differed only in these two parameters. Simulationresults suggest that the evolutionary convergence of colonialspecies toward larger trunk volume and proportionately short-er tail length resulted in swimming that was slower, but with


FIG. 6. The phylogenetic distribution of larval morphology. The silhouettes illustrate the proportions of tail length, trunk radius, andtrunk length for representative solitary (open circles) and colonial (filled circles) species. The phylogenetic relationships in this casewere 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 proportionatetail length of solitary species (e.g., c in Fig. 8).

The position of a larva in morphospace may affect bothlocomotor performance and life-history traits that affect fit-ness. Among solitary ascidians, larger species are predictedto swim faster (Fig. 8A) but have virtually the same cost oftransport as smaller species (Fig. 8B). More rapid swimmingmay 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 dis-persal distance and habitat selection (van Duyl et al. 1981;Durante 1991; Stoner 1994; Svane and Dolmer 1995). Thissuggests that natural selection should favor larger, solitarylarvae. However, assuming a fixed total reproductive in-vestment, larger larvae come at the cost of adult fecundity.Similarly, Sinervo and Huey (1990) experimentally demon-strated that larger eggs in lizards create young capable of

faster running with the same stamina as young produced fromsmaller eggs. However, larger lizard eggs come at the costof fecundity (Sinervo and Licht 1991).

The effects of larval morphology on multiple aspects ofperformance may be considered with a multidimensional per-formance landscape. This landscape is distinct from Raup’sconcept of a multidimensional morphospace (see Raup andMichelson 1965) because it is the performance variables, notthe morphometric parameters, that create deviation from athree-dimensional surface. Figure 9 illustrates such a land-scape in trunk volume/tail length morphospace using arrowsthat point in the direction of increasing performance. Underthe assumption of a fixed total reproductive investment, in-creased fecundity is directed toward smaller body size alongthe axis of isometric scaling (Fig. 9A). The results of ourmathematical simulations (Figs. 8A, 8B) indicate the direc-tions of increasing speed and energetic economy (i.e., re-duced cost of transport, Fig. 9A).


FIG. 7. Trunk volume and tail length among ascidian larvae. (A,B) These representative contrast values for trunk volume and taillength were log-transformed. Open circles represent comparisonsbetween solitary species, closed circles are for comparisons betweencolonial species, and the gray line shows the scaling predicted by

TABLE 3. Scaling of log-transformed trunk volume versus taillength. b, scale factor; L1, lower 95% confidence interval, L2 upper95% confidence interval; N, sample size.

b L1 L2 N

Contrast values of colonial speciesTree BTree C

0.420.42

0.220.22

0.650.62

56

Contrast values of solitary speciesTree BTree C

0.350.34

0.250.17

0.460.51

44

Species valuesColonialSolitary

0.340.31

0.180.23

0.490.39

1313

Comparison P df

Colonial versus scaling factorSpecies valuesTree BTree C

0.750.460.59

2366

Colonial versus scaling constantSpecies values 0.01 22

←

isometry. (A) Dark lines show linear regressions for contrasts be-tween solitary and between colonial species based on tree C. (B)The dark line illustrates the linear regression for all contrasts, in-cluding contrasts between solitary and colonial species (filledsquares) and ambiguous nodes (half-filled circles), based on treeD. Tree D most closely represents the independent contrasts resultsfrom the average across all trees. (C) Ellipses of 95% confidenceintervals for solitary (thin line) and colonial (heavy line) speciesare drawn around species values in this log-transformed morphos-pace of trunk volume and tail length. The straight lines show theleast-squares scaling relationship for solitary (thin line) and colonial(heavy line) species.

This multidimensional performance landscape may be usedto predict evolutionary change under selective conditions. Forexample, if natural selection strongly favored increased fe-cundity regardless of the cost to locomotor performance, thelarvae of a solitary species would be predicted to isometri-cally decrease in tail length and trunk volume (a in Fig. 9B).Under strong selection for faster swimming, tail length wouldincrease over the course of evolution at an allometric rateoutpacing increases in trunk volume (b in Fig. 9B). In con-trast, selection for improved energetic economy would resultin an allometric reduction in tail length and an increase intrunk volume (c in Fig. 9B). However, the observed patternof 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 co-lonial ascidians may have resulted from trade-offs betweenthe swimming speed and energetic economy of larvae andthe fecundity of adults. The relatively low energetic cost ofswimming with a proportionately short tail supports the hy-pothesis that the tail length of colonial ascidians evolved asan adaptation for high energetic economy. The relatively lowspeed that accompanies this disproportionately short tail ispartially offset by the larger size of colonial species. The


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 agradient of gray values. The 95% confidence intervals for the distribution of solitary (thin line) and colonial (thick line) species (as inFig. 7C) are overlaid on the contour map. Italicized letters denote the positions of individual species: (a) Herdmania pallida, (b) Aplidiumconstellatum, and (c) a scaled-up model of larva H. pallida having the trunk volume of A. constellatum. (C) The speed (gray bars, leftaxis) and cost of transport (white bars, right axis) predicted for larvae a–c.


FIG. 9. Multidimensional performance landscape. Arrows denotethe direction of increasing performance in speed (green), energeticeconomy (orange), and fecundity (violet) for ascidian larvae. (A)The direction of increasing speed was determined from the perfor-mance landscape shown in Figure 8A and the direction of higherenergetic economy (i.e., lower cost of transport) was found fromFigure 8B. Increased fecundity is directed along the axis of iso-

←

metric scaling. (B) Predicted evolutionary change from the positionof a typical solitary species (filled circle) is illustrated in the di-rection of heavy black arrows under different selective conditions:(a) selection for increased fecundity, (b) selection for faster swim-ming, and (c) selection for improved energetic economy. (C) El-lipses of 95% confidence intervals approximate the distribution ofsolitary (thin gray line) and colonial (heavy gray line) species.

evolutionary increase in larval size in colonial species mayhave been favored by selection for faster swimming. How-ever, further increases in size may have resulted in a penaltyto fecundity that exceeded the benefits of even faster swim-ming.

This consideration of evolutionary forces has necessarilymade simplifying assumptions, so it is important to considerthe potential for more complex dynamics in the evolution ofascidian larvae. For example, ascidian larvae may be con-strained from occupying regions of morphospace that are notoccupied by extant species. The size of larvae may influencethe dynamics of ascidian life-history evolution beyond thefecundity of the adult stage (Roff 1992; Stearns 1992). Fur-thermore, the evolution of swimming performance is a func-tion of changes in both tail motion and morphology. Ourfinding that swimming performance is strongly affected bytail-beat frequency (described above) suggests that evolu-tionary changes in performance my largely be attributed tochange in this kinematic trait. The present study conductedan intensive three-dimensional kinematic analysis that wouldbe prohibitively labor intensive to conduct on the numerousspecies necessarily for a broadly comparative study. How-ever, we found that the only significant kinematic differencebetween C. intestinalis and D. occidentalis was in their tail-beat frequency, a parameter that is relatively easy to measurefrom video recordings of swimming. It would therefore betractable and interesting to examine how changes in tail-beatfrequency have influenced the evolution of swimming speedin ascidian larvae in a future study.

In summary, the present study finds that colonial ascidianshave independently evolved a larval morphology with a largertrunk volume and proportionately smaller tail length thansolitary species. Our mathematical modeling suggests thatthis evolutionary convergence resulted in slower swimmingwith improved energetic economy. However, the larger sizeof colonial larvae may have required a reduction in adultfecundity. These results were found through the use of bio-mechanical techniques that verified the accuracy of a math-ematical model, phylogenetic comparative analyses that rig-orously demonstrated the convergence of trunk volume, andtheoretical morphology to examine the functional signifi-cance of convergent morphology in the absence of the con-founding effects of behavioral variation. This integration ofapproaches holds potential for understanding the evolutionof organismal function in a diversity of complex organismalsystems.

ACKNOWLEDGMENTS

We thank M. Koehl, G. Lauder, and B. Swalla for theiradvice. Two anonymous reviewers provided valuable sug-


gestions for the manuscript. Larvae and adults of C. intes-tinalis were provided by the Levine lab at the University ofCalifornia at Berkeley. This work was supported with a Na-tional Science Foundation predoctoral fellowship and grants-in-aid of research from the American Society of Biome-chanics, Sigma Xi, the Department of Integrative Biology(University of California Berkeley) and the Society for In-tegrative and Comparative Biology to MJM, the Miller In-stitute for Basic Research in Science to SNP, and grants fromthe National Science Foundation (OCE-9907120) and the Of-fice of Naval Research (AASERT N00014-97-1-0726) to M.Koehl.

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