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The Evolution of Larval Morphology and Swimming Performance in Ascidians

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The Evolution of Larval Morphology and Swimming Performance in Ascidians 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 1The Museum of Comparative Zoology, Harvard University, Cambridge, Massachusetts 02138 2E-mail: [email protected] 3The Department of Integrative Biology, University of California, Berkeley, California 94720 4E-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, 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 signi®cance of this evolutionary change, we ®rst veri®ed 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 in¯uenced 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. Accepted March 15, 2004. The biomechanical complexity of animal motion presents Bennett 1986; Jayne and Bennett 1989) may be confounded challenges for understanding broad patterns of locomotor by variation in performance caused by traits other than those evolution. Measures of locomotor performance typically have examined (Koehl 1996). Many mechanistic investigations a nonlinear dependency on numerous aspects of the mor- have attempted to resolve the causal relationships between phology and motion of an animal's body (McMahon 1984; traits and performance by developing mathematical models Alexander 2003; Biewener 2003) and interspeci®c variation of locomotion (e.g., Daniel 1983; Liu et al. 1996; Sane and in these traits may be substantial. Ascidians (Chordata: Uro- Dickinson 2002; McHenry et al. 2003). However, such idi- chordata) present an interesting case study of locomotor evo- ographic studies have limited applicability to evolutionary lution because the larvae of colonial species are similar in questions because they generally neglect the effects of intra- size and shape despite having evolved independently at least and interspeci®c variation in favor of understanding general three times among urochordates (Swalla et al. 2000). Through functional principles. Mechanistic studies that examine the the integration of biomechanics, phylogenetic comparative extreme differences among species within a group (e.g., analyses, and theoretical morphology, we examined how evo- Kingsolver and Koehl 1985; Crompton 1989; Emerson and lutionarily convergent colonial life histories have in¯uenced Koehl 1990; Drucker and Lauder 2001) have proven valuable the morphology and swimming performance of ascidian lar- for exploring the extremes of performance exhibited by a vae. group of species. However, general principles and knowledge of performance extremes alone are limited in their ability to Biomechanical, Comparative, and Theoretical Approaches inform our understanding of changes in function that result to the Evolution of Organismal Function from a sequence of historical transformations. Research on the evolution of organismal function may use Theoretical morphology provides the tools to examine his- extant species by either testing for correlations between traits torical transformations with mechanistic models toward the and performance or by investigating functional mechanisms ultimate goal of testing evolutionary hypotheses. This ana- (reviews include Wake and Roth 1989; Bennett and Huey lytical technique involves constructing a theoretical spectrum 1990; Garland and Carter 1994; Thomason 1995; Koehl 1996; of morphological parameters (a morphospace), the measure- Lauder 2003). A correlative approach explores natural co- ment of species distributions within that space, and using a variation between traits and performance (e.g., Arnold and mathematical model to determine the functional signi®cance Bennett 1988; Jayne and Bennett 1990; Losos 1990; Patek of morphologies that are both represented and absent among and Oakley 2003) to formulate mechanistic hypotheses (e.g., species (Raup and Michelson 1965; Raup 1967; McGhee Bennett et al. 1989; Jayne and Bennett 1989; Friedman et al. 1999). This model may be used to generate predictions of 1992) and to consider the in¯uence of shared ancestry on performance for each position in the morphospace and there- functional relationships (e.g., Losos 1990; Bauwens et al. by generate a performance landscape (also known as a per- 1995). Form-function relationships established with a strictly formance surface: Arnold 2003; a ®tness landscape: Gilchrist correlative approach (reviewed by Arnold 1983; Huey and 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 (van Duyl et al. 1981; Durante 1991; Stoner 1994; Svane and test adaptive hypotheses that ammonite shell geometry gen- Dolmer 1995). Therefore, speed and cost of transport are two erates high locomotor stability (Raup 1967) and strength measures of swimming performance that may have important against hydrostatic pressure (Daniel et al. 1997), to determine consequences for dispersal distance and duration, microhab- whether morphological disparity among labrid ®shes facili- itat selection, larval survivorship, and, ultimately, to ®tness. tates disparity in function (Hulsey and Wainwright 2002), to Although ascidians exhibit tremendous diversity in life- identify developmental constraints in the body shape of sea history traits (reviewed by Svane and Young 1989), solitary urchins (Ellers 1993), and to investigate the effects of en- and colonial species represent the two major types of ascidian vironmental change on the macroevolution of vascular plants life-history strategies. Colonial (i.e., compound and social) (Niklas 1997). The models used to generate performance ascidians produce adult zooids by asexual reproduction and landscapes may come in the form of simple algebraic equa- they generally brood a relatively small number of large larvae tions (e.g., Moore and Ellers 1993) or elaborate computa- that spend a brief time in the plankton (less than a few hours; tional simulations (e.g., Daniel et al. 1997), depending on Berrill 1935). Solitary species generally broadcast spawn the complexity of the functional system. their gametes and their numerous small larvae develop rap- The present study tested the accuracy of a mathematical idly in the plankton. Therefore, solitary species may provide model of swimming in ascidian larvae (McHenry et al. 2003) less material investment and protection for larvae than co- and used this model to construct landscapes of swimming lonial species, but they have higher fecundity (Svane and performance. According to this model, the hydrodynamics of Young 1989). The larvae of colonial species are so much swimming vary widely among ascidian species, which swim larger than solitary species that their trunks may be more at Reynolds numbers (Re 5rUL/m, where U is mean swim- than three orders of magnitude greater in volume (Cloney ming speed, L is body length, r and m are the density and 1978). viscosity of water; Lamb 1945) from 5 in Ciona intestinalis It remains unclear to what degree patterns of life-history (Bone 1992) to 100 in Distaplia occidentalis (McHenry traits and larval morphology are due to shared ancestry or 2001). At any Re value, the magnitude and direction of pro- convergent evolution. It has long been appreciated that both pulsive forces depends on the shape of the larval body and solitary and colonial species are distributed throughout as- the undulatory motion of the tail. cidian families (Berrill 1950) and recent phylogenetic studies suggest that coloniality has a number of independent origins Ascidian Larvae (Swalla et al. 2000). Finding the phylogenetic distribution of life-history strategy is requisite for understanding whether Ascidians are a large and diverse group of marine inver- the observed patterns in larval morphology are correlated tebrates with a complex life history characterized by a sessile with life history or due to shared ancestry. Using recent phy- adult and a pelagic larval stage. Comprised of more than 3000 logenetic systematic studies (e.g., Swalla et al. 2000; Stach species (Jeffery 1997), ascidians were included in the phylum
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