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1 Constraints and consequences in medusan evolution. 2 3 J.H. Costello1 4 S.P. Colin2 5 J.O. Dabiri3 6 7 1 Biology Department 8 Providence College 9 Providence, RI 02819 10 Email: [email protected] 11 2 Environmental Sciences 12 Roger Williams University 13 One Old Ferry Rd. 14 Bristol, RI 02809 USA 15 Email: [email protected] 16 17 3 John O. Dabiri 18 Mail Code 138-78 19 California Institute of Technology 20 Pasadena, CA 91125 21 Email: [email protected] 22 23 24 25 = Corresponding Author 26 27 2 1 Abstract 2 Medusae were the earliest animals to evolve muscle-powered swimming in the seas. 3 Although they have achieved diverse and prominent ecological roles throughout the 4 world’s oceans, the limited cellular inheritance of the Medusozoa has constrained its 5 ecology and evolution. We argue that the primitive organization of cnidarian muscle 6 tissue limits force production and, hence, the mechanical alternatives for swimming bell 7 function. We present a model comparing the potential force production with the 8 hydrodynamic requirements of jet propulsion and conclude that jet production is possible 9 only at relatively small bell diameters. In contrast, production of a more complex wake 10 via what we term rowing propulsion permits much larger size but requires a different 11 suite of morphological features. Analysis of morphometric data from all medusan taxa 12 independently confirms size-dependent patterns of bell forms that correspond with model 13 predictions. Further, morphospace analysis indicates that various lineages within the 14 Medusozoa have proceeded along either of two evolutionary trajectories. The first 15 alternative involved restriction of jet propelled medusan bell diameters to small 16 dimensions. These medusae may either be solitary individuals (characteristic of 17 Anthomedusae and Trachymedusae), or aggregates of small individual medusan units 18 into larger colonial forms (characteristic of the nectophores of many members of the 19 Siphonophorae). The second trajectory involved use of rowing propulsion (characteristic 20 of Scyphozoa and some hydromedusan lineages such as the Leptomedusae and 21 Narcomedusae) that allows much larger bell sizes. Convergence on either of the differing 22 propulsive alternatives within the Medusozoa has emerged via parallel evolution among 23 different medusan lineages. For example, rowing propulsion has evolved independently 24 within the Scyphozoa, Leptomedusae and Narcomedusae. The variety of developmental 25 pathways and morphological structures employed among medusan lineages to achieve 26 either propulsive mode suggests that strong selective pressures underlie the highly 27 polarized medusan morphospace. The distinctions between propulsive modes have 28 important ecological ramifications because swimming and foraging are interdependent 29 activities for medusae. Prey selection is therefore dependent upon foraging mode. 30 Rowing swimmers are characteristically cruising predators that select different prey types 31 than jet-propelled medusae that are predominantly ambush predators. These relationships 32 indicate that the different biomechanical solutions to constraints on bell function have 33 entailed ecological consequences that are evident in the prey selection patterns and 34 trophic impacts of contemporary medusan lineages. 3 1 I. Introduction 2 Medusae are a diverse array of planktonic cnidarians occupying all of the world’s 3 oceans and some freshwater habitats. The Cnidaria is an ancient clade with origins in an 4 early radiation within the basal lineage giving rise to the rest of the animal kingdom 5 (Valentine 2004). Although the exact relationship between the ancient Cnidaria and the 6 rest of the Metazoa remain unresolved, it is clear that the cellular inheritance of medusae 7 rivals even the sponges in the restricted number of cell types available for body 8 construction (Bonner 1965, Valentine et al. 1994). Yet, unlike sponges, medusae are 9 characterized by the evolutionary innovation of muscle-powered motility. Diversification 10 of this muscular body plan allowed medusae to radiate into a variety of ecological niches 11 within planktonic and some benthic marine environments. However, the limited cellular 12 repertoire of the medusae also provides the opportunity to examine the means by which a 13 major animal lineage resolved constraints dictated by its phylogeny. By examining both 14 constraints and evolutionary solutions, we seek to define basic principles that organize 15 the structure and function of medusae. 16 Medusan diversity 17 Medusae are members of the subphylum Medusozoa that is characterized by 18 possession of a medusan stage during the life cycle of many members of the constituent 19 classes. The extant medusa-producing taxa within the Medusozoa include the classes 20 Hydrozoa, Scyphozoa and the Cubozoa. A fourth class, the Staurozoa, is an early 21 medusozoan taxon (Collins et al. 2006, van Iten et al. 2006) but produces no medusae. 22 Although possession of a medusa stage characterizes many members of the 23 Medusozoa, the form and organization of medusae vary substantially between and even 4 1 within the major medusozoan lineages. Among the extant medusozoans, the Cubozoa 2 and Scyphozoa bear a number of shared characters (Marques and Collins 2004, Collins et 3 al. 2006) and appear to form an early medusozoan clade (Collins et al. 2006). The 4 Cubozoa may represent the oldest class (Fig. 1) and it contains medusae noted for their 5 box-like shape (often known as "box-jellies"). The Cubozoa is not as species rich as the 6 other medusozoan classes and are generally thought to move via jet propulsion 7 (Gladfelter 1973, Shorten et al. 2005) and capture prey on extended tentacles (Larson 8 1976). The largest medusae are found in the Scyphozoa, which includes three orders: 9 Coronatae, Semaestomae and Rhizostomae. Among these, the latter two orders are the 10 most diverse. Members of these orders possess developed oral arms that often extend 11 well below the margin of the swimming bell. Among the Rhizostomae, these oral arms 12 are fused into complex oral arm cylinders containing hundreds to thousands of small 13 mouthlets used to consume prey. The most diverse medusozoan class, the Hydrozoa, is 14 comprised of two major clades, the Trachylina and the Hydroidolina, that have each 15 radiated into several medusa-producing lineages (Collins et al. 2006, Fig. 1). The 16 lineages within Trachylina appear to be well differentiated as the Limnomedusae, 17 Trachymedusae and the Narcomedusae. The second hydrozoan clade, the Hydroidolina, 18 has produced the most species rich lineages and the phylogenetic relationships between 19 some of these groups remain incompletely resolved at present (Collins et al. 2006). We 20 have chosen to use nomenclature that refers to the medusan component of the life history 21 and is therefore congruent with the medusan literature, rather than more recent and 22 systematically appropriate nomenclature that is less readily connected to the functional 23 ecology literature. Hcnce, our use of the terms Anthomedusae and Leptomedusae refer to 5 1 the taxa Anthoathecata and Leptothecata (Marques and Collins 2004, Collins et al. 2006) 2 respectively (as in Fig. 1). The Hydroidolina additionally contains a taxon that possesses 3 clonal aggregations of medusae as components of larger colonies – the Siphonophorae 4 (Fig. 1). 5 Life history organization within the Medusozoa varies substantially with some 6 species maintaining holoplanktonic life histories while a large number alternate between 7 benthic, asexually reproducing forms and sexually reproducing medusae (for examples, 8 see Boero et al. 1992). Although medusae are frequently independent, sexually mature, 9 feeding individuals, their function may be limited to brief periods of free swimming prior 10 to reproduction. In some forms, termed medusoids, the medusa form may remain 11 attached to the colony and is functionally reduced solely to reproduction. 12 Paralleling the diverse shapes and life history variations, medusae extend through 13 a spectrum of sizes spanning three orders of magnitude for mature individuals. Sexually 14 mature hydromedusae include species as small as 2.0 mm diameter while some adult 15 scyphomedusae may exceed 2.0 m in diameter (Omori and Kitamura 2004). 16 Siphonophoran colonies consisting of hundreds of individuals members may extend tens 17 of meters in length (Tregouboff and Rose 1957). 18 The taxonomic diversity of the Medusozoa, combined with the array of sizes, 19 shapes, and clonal organizations of its members has produced a diverse collection of 20 extant medusae. Our goal is identification of unifying patterns that underlie this 21 variation. 6 1 II. Patterns of swimming bell design within the Medusozoa 2 One of the chief defining characters of a medusa is the possession of a swimming 3 bell. Planktonic motility alone does not distinguish the medusozoans because many non- 4 medusan cnidarians possess planular larval stages which swim via cilia. However, 5 possession of a muscular swimming bell capable of propulsion is unique to the 6 Medusozoa. For many medusae, it is also the largest portion of the body and houses 7 most, if not all, of the digestive, reproductive and neural systems. Its dominance as an 8 essential medusan structure makes the swimming bell an appropriate first character for 9 describing medusan morphological patterns. 10 Is there an appropriate single variable that can be used to describe patterns

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