Reference: Biol. Bull. 203: 58-69. (AimuM 2002) Evolution of Fast Development of Planktonic Embryos to Early Swimming JENNIFER M. STAYER AND RICHARD R. STRATHMANN* Fridav Harbor Laboratories and Department of Zoology, University of Washington, 620 University Road, Friday Harbor. Washington 98250 Abstract. Planktonic embryos of marine animals swim at an early stage and age. Although natural selection has apparently favored rapid development of structures for swimming, taxa have not converged on the same, minimal time from first cell division to first swimming. Comparisons of 34 species with planktonic embryos in 10 phyla revealed factors that account for variation in time to swimming. Time to first swimming correlated significantly with time from first to second cleavage (first cell cycle) in analyses of all embryos sampled and separately within the Spiralia and Echinodermata. Time to first swimming also correlated sig-nificantly with egg diameter in some clades, but not in all. Correlations between egg diameter and cell cycle duration were low except for the three species of Urochordata. De-velopment to a feeding or nonfeeding larva did not affect time to first swimming beyond effects attributable to egg size. Time to first swimming did not correlate with type of locomotion developed (uniciliated cells, multiciliated cells, or muscle). Nonetheless, differences in locomotion are as-sociated with changes in cell cycle durations prior to swim-ming. The ratios of time to first swimming and time for first cell cycle suggests that allocation of time to multiplication of cells versus differentiation of cells is resolved differently in species with different types of locomotion. Introduction Many marine invertebrates release their eggs individually into the plankton, where each embryo develops with little protection. A common feature of such embryos is rapid development of locomotion. We expect that the factors influencing ace and stace at first swimminc have influenced Received 3 December 2001: accepted 25 April 2002. * To whom correspondence should he addressed. E-mail: rrstrath u. washington.edu the evolution of most animal embryos. Multicellular ani-mals originated and diverged into most major existing clades in the sea. and development via small, solitary em-bryos is inferred to be an ancient and persisting mode of development. We also expect that planktonic development of more recent origin has converged to some extent on similar early swimming. Here we examine the degree of convergence and divergence in rates of development and time to first swimming by comparing diverse planktonic embryos. Solitary embryos are at risk. Embryos contain rich nutri-ent stores for predators but are more limited than larvae in means of defense or flight. Although planktonic embryos have extra-embryonic envelopes or coats (Strathmann, 1987), some contain toxins (Lindquist, 1996; McClintock and Baker, 1997), and the plankton may be a safer environ-ment than the bottom, planktonic embryos lack the parental care, protective gel. or tough envelope that shields most benthic embryos. Planktonic embryos are therefore among the least protected and most vulnerable embryos of marine animals. Sources of mortality for planktonic embryos include pre-dation (Pennington and Chia, 1984); ultraviolet radiation (Morgan and Christy, 1996; Epel et ai, 1999); advection from suitable adult habitat (Jackson and Strathmann. 1981): and deposition on the bottom, where risks may be even greater for single embryos. Although mortality rates for planktonic embryos have not been estimated, they are pre-sumably at least as great as those of small larvae (Penning-ton ct ul., 1986). Estimates of instantaneous mortality rates for small planktonic larvae are high, ranging from 0.04 to 1.0 per day (Strathmann. 1985; Rumrill. 1990). There are no obvious benefits from prolonging planktonic embryonic development. Planktonic embryos have limited opportunities for growth or reproduction. Active transport 58
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