Evolution of Direct-Developing Larvae: Selection Vs Loss Margaret Snoke Smith,1 Kirk S
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Hypotheses Evolution of direct-developing larvae: selection vs loss Margaret Snoke Smith,1 Kirk S. Zigler,2 and Rudolf A. Raff1,3* Summary echinoderms, sea urchins, reveal that a majority of sea urchin Observations of a sea urchin larvae show that most species exhibit one of two life history strategies (Fig. 1).(10) species adopt one of two life history strategies. One strategy is to make numerous small eggs, which develop One strategy is to make many small eggs that develop into a into a larva with a required feeding period in the water larva that must feed and grow for weeks or months in the water column before metamorphosis. In contrast, the second column before metamorphosis. In the water column, these strategy is to make fewer large eggs with a larva that does larvae are dependent on plankton abundance for food and are not feed, which reduces the time to metamorphosis and subject to high levels of predation.(11) The other strategy thus the time spent in the water column. The larvae associated with each strategy have distinct morpholo- involves increasing egg size and maternal provisioning, which gies and developmental processes that reflect their decreases the reliance on planktonic food sources and the feeding requirements, so that those that feed exhibit time to metamorphosis, thus minimizing larval mortality. indirect development with a complex larva, and those that However, assuming finite resources for egg production, do not feed form a morphologically simplified larva and increasing egg size also reduces the total number of eggs exhibit direct development. Phylogenetic studies show that, in sea urchins, a feeding larva, the pluteus, is the produced. ancestral form and the morphologically simplified direct- Both of these life history strategies are associated with developing larva is derived. The current hypothesis for developmental differences resulting in distinct larval forms. evolution of the direct-developing larval form in sea Generally the strategy of producing many small eggs and a urchins suggests that major developmental changes feeding larva is characteristic of indirect development. In sea occur by neutral loss of larval features after the crucial transition to a nonfeeding life history strategy. We urchins, indirect developers produce a complex pluteus larva, present evidence from Clypeaster rosaceus, a sea urchin which has arms bearing a ciliary band, in which nest a mouth with a life history intermediate to the two strategies, and a gut—all structures associated with feeding and survival which indicates that major developmental changes for in the water column. In contrast, the strategy of producing accelerated development have been selected for in a larva fewer larger eggs and nonfeeding larva is characteristic of that can still feed and maintains an outward, pluteus morphology. We suggest that transformation of larval direct developers. These organisms produce a barrel-shaped form has resulted from strong selection on early initiation larva that has reduced or no arms, an incomplete or no ciliary and acceleration of adult development. BioEssays band, no mouth and no functional gut. One of the striking 29:566–571, 2007. ß 2007 Wiley Periodicals, Inc. differences between direct- and indirect-developing larvae is the timing of the formation of the large left coelom—the tissue Evolution of marine larvae that gives rise to much of the adult rudiment. Indirect Marine larval forms can evolve rapidly and dramatically, but the developers form a large left coelom and initiate adult selection pressures involved in the evolution of development development in advanced larvae, weeks after fertilization, are poorly understood. There is much debate among theories whereas direct developers form a large left coelom before the about what the important selective pressures are and how end of gastrulation and initiate adult development hours after these forces shape the evolution of life histories of marine fertilization. Phylogenetic studies show that indirect develop- (1–9) organisms. Observations in one prominent group of ment is the ancestral form of sea urchin development, but direct development has evolved independently multiple times.(2,12,13) 1Department of Biology, Indiana University, Bloomington, IN. 2Department of Biology, The University of the South, Sewanee, TN. Although much is known about the differences between 3School of Biological Sciences, University of Sydney, Sydney, Australia. direct and indirect developers, the evolutionary transition Funding agency: NSF. between the two modes is poorly understood because there is *Correspondence to: Rudolf A. Raff, Department of Biology, Indiana no fossil record of echinoid larvae. The current hypothesis for University, Myers Hall 150, 915 East Third Street, Bloomington, IN the evolution of direct-developing larvae is based on living, 47405. E-mail: [email protected] (13) DOI 10.1002/bies.20579 apparently intermediate larval forms and suggests that Published online in Wiley InterScience (www.interscience.wiley.com). major developmental changes happen relatively late in the process. Wray(13) has proposed, albeit recognizing that there 566 BioEssays 29.6 BioEssays 29:566–571, ß 2007 Wiley Periodicals, Inc. Hypotheses Figure 1. Larval development of a large number of sea-urchin species have been examined and can be sorted into one of three categories: small eggs with obligately feeding larvae, larger eggs with facultative feeding larvae, and still larger eggs with nonfeeding larvae. The distrubutions of sea urchin species into these catagories are listed here. This figure is based on Emlet 1990.(10) is selection for new features such as rapid metamorphosis, ment of these species allows us to test basic premises of the that the barrel-shaped morphology of many direct developers current model. The developmental shift to early formation of a is largely a result of relaxed selection on structures associated large left coelom, as seen in nonfeeding direct-developing with feeding.(14) According to this scenario, there is first an larvae, should occur relatively late in the evolution of direct- increase in egg size and provisioning that allows for the loss of development if features that speed development evolve after feeding ability (Fig. 2, steps 1 and 2). After this trophic change, feeding is lost and larval features are reduced. the selective pressures for maintenance of feeding structures We examined a potential intermediate, the larvae of the are relaxed and there is selection to reduce the time to facultative feeder, Clypeaster rosaceus, a sea biscuit urchin metamorphosis. It is not until the third step, after the ability to found in the Caribbean and southern US. Its larvae have an feed has been lost, that Wray suggests that major develop- exterior pluteus morphology and may feed, but they are not mental changes occur, indicating that the trophic switch is required to do so in order to metamorphose. The egg diameter crucial for the transition to direct development and that the of C. rosaceus, 275 microns(15,16) and time to metamorpho- developmental changes are secondary and potentially by- sis, 5–7 days(15) are also intermediate between direct and products of relaxed selection. indirect developers. C. subdepressus, a relative of C. rosaceus, is a typical obligate feeding, indirect developer. Intermediates and ancestors Internally, the pluteus of C. rosaceus presents a surprise. To evaluate Wray’s model and the idea that major develop- Although C. rosaceus maintains an outward pluteus morpho- mental changes occurred neutrally due to the change in logy there has been a heterochronic acceleration in the feeding ability near the end of the transition to direct formation of a large left coelom reminiscent in form, size and development, we can examine, against the predictions of the timing of direct-developing larvae (Fig. 3). Early onset and model, one of the few species that represents a transitional acceleration of the formation of a large left coelom in C. state, facultative feeding. Although such intermediate forms rosaceus suggests two major changes in the current thinking are only proxies for the fossil record, examining the develop- on how the direct development evolved (Fig. 2). First, major BioEssays 29.6 567 Hypotheses C. subdepressus eggs and plutei are clear as usual with indirect developers. Second, the transition to a barrel-shaped larva may be driven by selection for streamlined development of the adult and rapid metamorphosis. Subsequent loss of some feeding structures may be due to selection for allocation of the embryo resources to rapid development of adult structures, which suggests a different course of evolution than expected, and that adaptive selection may play a much stronger role than previously thought in shaping the evolution of the direct-developing larval form. Is Clypeaster rosaceus anomalous? As direct development has arisen independently in several echinoid lineages, it is possible that each species takes a different developmental path. However, early formation of a large left coelom is common in nonfeeding echinoids. For example, the taxonomically distant direct developers, Per- onella japonica,(17) H. erythrogramma,(18) Asthenosoma ijimai(19) and Phyllacanthus parvispinus(20) all form large left coeloms just following gastrulation. Without fossil larval intermediates, we may never know exactly how direct development evolved in each lineage of echinoids, but C. rosaceus and other species suggest that the heterochrony in large left coelom formation could be a general and early step of the transition of developmental mode. Selection on rapid development of adult features We suggest a new hypothesis of how direct development evolved in sea urchins (Figs. 3,4). First, following the transition to larger eggs, the observation from C. rosaceus suggests that the next step is to accelerate the timing of left coelom formation, not loss of the ability to feed. C. rosaceus can still feed, yet it vastly accelerates the development of a large left coelom before the end or just after gastrulation is complete. Secondly, we suggest that reducing the time to metamorphosis is not a passive step happening only after the ability to feed has been lost.