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seminars in CELL & DEVELOPMENTAL BIOLOGY, Vol. 11, 2000: pp. 395–402 doi: 10.1006/scdb.2000.0192, available online at http://www.idealibrary.com on Functional design in the evolution of embryos and larvae Richard R. Strathmann contain most or all of the cell types of an adult. Animals in at least eight phyla divide longitudinally or transversely or separate from marginal fragments, with the pieces regenerating missing parts.2–4 Colonial animals, such as sponges, cnidarians, bryozoans, pterobranchs, and ascidians, produce multicellular buds with initially few cell types but many cells, and many also divide into large fragments. Starting life with more cells can result in more rapid development. Starting with numerous differentiated cells confers capacity for diverse functions. Why should multicellular organisms, with all the advantages of numerous and differentiated cells, so regularly reduce themselves to a single cell? Suggested hypotheses fall into two overlapping categories. (1) A unicellular stage exposes offspring that are each uniformly of one genotype to selection, thereby purging deleterious mutations (and more rarely fixing beneficial ones). (2) A unicellular stage reduces conflicts of interest among genetically different replicators within an organism.5–10 For the first hypothesis, Kondrashov10 modelled mutation load with asexual propagation at the equilibrium between mutation rate and selection. If all cells are recent descendants of one cell, the mutation load does not increase with the number of cells in the propagule, but if distantly related initiating cells form the propagule, then the mutation load approaches one as the number of cells in the propagule increases. In multicellular animals, cells from lineages separated by a large number of mitotic divisions can be included in one propagule. Thus the equilibrium mutation load is expected to be larger for animals with multicellular propagules than for plants, whose cells grow and change shape but do not move to distant parts of the body. Conflicts among genetically distinct replicators are of varied sorts. Some conflicts arise from mutation, as in cancer. By inclusion in multicellular propagules, cancers could persist through several generations. Pathogens are also genetically distinct replicators whose interests conflict with their host’s. A function of development is to put the right kind of cells in the right place at the right time. Other functional analyses help define what is right. As examples, functional analyses offer explanations for the unicellular bottleneck in life histories that necessitates embryos, evolutionary divergences in embryonic cell cycles, conditions permissive of loss of larval structures and consequent change in embryonic development, and the decoupled development of larval bodies and juvenile rudiments. Functional analyses also reveal the specifications required of morphogenesis, hence defining developmental phenomena to be explained. Key words: ascidian / cell cycle / echinoid / plasticity / stasis c 2000 Academic Press Most studies of the evolution of development describe change or stasis in developmental processes. The studies seldom explain why a change occurred or why stasis has been so prolonged. Analysis of the functional requirements for embryos and larvae is a necessary part of such an explanation. Such analyses are rare in developmental biology.1 The following examples illustrate several ways that functional requirements shape development. In these examples, it should become apparent that developmental processes have also shaped functional requirements. Why are there embryos? Developmental biologists ask how embryos develop. Life history theorists ask why embryos exist. Many organisms produce multicellular propagules that From the Friday Harbor Laboratories and the Department of Zoology, University of Washington, 620 University Road, Friday Harbor, WA 98250, USA. E-mail: [email protected] c 2000 Academic Press 1084–9521 / 00 / 060395+ 08 / $35.00/0 395 R. R. Strathmann in the right types of cells in the right numbers in the right places in the organism. Another functional requirement is that multicellular function be restored rapidly. The urgency depends on the vulnerability of the embryo. Planktonic embryos receive less protection than brooded or encapsulated embryos. Comparisons of mortality rates of planktonic larvae and protected aggregations of embryos indicate higher mortality rates for planktonic larvae.16 For embryos at risk from predators or other external causes of mortality, one would expect selection for rapid development. Rapid development reduces the period of vulnerability. Selection for rapid development includes selection for rapid cell cycles in embryos. Selection should decrease cell cycle duration until the costs of an even shorter cell cycle balance the advantages of a further reduction in the period of vulnerability. Differences in rates of early development could arise from trade-offs between risks from external sources of mortality and the costs associated with fast cell cycles. Jennifer Staver and I tested the hypothesis that early embryonic cell cycles are more rapid for planktonic embryos than for embryos in protected aggregations (unpublished observations). In six out of eight independent evolutionary divergences in protection, the time from first to second cleavage was shorter for the planktonic embryos. The evolutionary divergences in protection included examples from five phyla (molluscs, phoronids, brachiopods, echinoderms, ascidians). In most of the paired comparisons, the protected embryos had longer cell cycles. In no paired comparison did the protected embryos have a shorter cell cycle. Other comparisons from other phyla confirm this pattern. In the familiar mouse and frog, the interval from first to second cleavage is longer in the more protected embryos of the mammal than in those of the amphibian. The differences in cell cycle duration in these comparisons is not the result of temperature, nor are the more slowly developing protected embryos consistently from larger eggs. In some cases, as in mouse versus frog, the protected embryos are smaller, warmer, and slower. To my knowledge, the trade-offs governing the evolution of cell cycle durations are unknown. Hypotheses include (but are not limited to) costs with short cell cycles in less protection against molecular damage or less effective repair, greater quantities of rate-limiting materials that are maternally supplied to eggs, or less early transcription. Differences in risk to embryos and the differing environments for protected and planktonic embryos Unicellular propagules restrict opportunities for vertical transmission, as compared to multicellular propagules, especially when embryos are not closely associated with a parent. Fusion chimaeras occur in several phyla of animals, including the sponges, cnidarians, bryozoans, and even chordates.11 Fusion chimaeras open the possibility of competition among cells for inclusion in the germ line, with cells of some genotypes shirking their somatic responsibilities but contributing disproportionately to the next generation.12 Such differential reproductive success of cell lineages in chimaeras has been demonstrated for ascidians.13 A unicellular stage in the life history is one of the ways of reducing parasitism of germ line cells of one genotype on the soma of another.7 The disadvantages of multicellular propagules apply to asexual multicellular propagules, but are especially evident for sexual reproduction. Processes of recombination produce genetically distinct cells. Combining numbers of these cells into a multicellular organism would result in a highly chimaeric offspring. Syngamy that involved multiple pairs of cells and that followed meiosis or involved multiple partners in a mating would also produce genetic diversity within offspring. Although the disadvantages of multicellular propagules are acute and more obvious for sexual reproduction, a unicellular stage nevertheless persists with amictic parthenogenesis. Asexual production of embryos has even persisted in animals that can also produce larger multicellular propagules by fission or fragmentation,14, 15 although the number and lineages of parental cells in these embryos remains to be demonstrated. The relative importance of pathogens or deleterious mutations as agents of selection for persistence of unicellular stages has not been demonstrated. Fusion chimaeras should be important where they occur, but they appear to be rare in non-colonial animals. Analyses of the costs and benefits of multicellular and unicellular propagules depend on combined studies of functional morphology, population genetics, and developmental processes. Key phenomena that affect the costs and benefits of unicellular and multicellular propagules include cell–cell recognition, defenses against pathogens, effectiveness of apoptosis in eliminating mutant cells, and cell motility. Evolution of embryonic cell cycles A function of an embryo is to restore a multicellular organism that gains the advantages of differentiated cells, specialized for different functions. Studies of development have emphasized the processes that result 396 Function of development Evolutionary loss of tails of ascidian tadpoles contrasts with the conservatism of the vertebrate ‘pharyngula’ stage. Similarities among vertebrate pharyngulas was an inspiration for von Baer’s and Haeckel’s laws on evolutionary conservatism of early stages in development. The conservatism of the pharyngula has been questioned20 and HeLa cells (of human origin) have been described as new species (without vertebrate anatomy),21 but it is nevertheless true that all animals classified as vertebrates retain a notochord, dorsal nerve cord, and axial body muscles at some stage in their development. How is it that ascidian species have ‘unchordated’ in their evolution while vertebrates have not, despite the immense diversification of vertebrate species? Differences in function of these structures are an essential part of the explanation, although developmental differences enter as well. It is instructive to compare the tailless ascidians to the floating head and no tail mutants in zebra fish. These unfortunate zebra fish demonstate that mutations interfering with differentiation of the notochord are possible, with consequent drastic reduction of dorsal nerve cord and axial muscles.22 Mutations that go part way in removing vertebrate traits occur, but they are lethal for functional reasons. These mutant fish demonstrate that the conservatism in the vertebrate body plan is not purely developmental. It is the result of functional constraints associated with vertebrate ways of life. This example illustrates the importance of functional burden in evolutionary stasis and change in development. The functional burden on notochorddependent structures in the ascidian is low because these structures appear only in the tadpole stage. These structures are lost at metamorphosis, and their absence in the tadpole makes little difference to the postmetamorphic juvenile. It makes little difference because the tadpole does not feed or grow (a functional reason) and because development of the pharynx does not depend on the notochord (a developmental reason). The functional burden on notochord-dependent structures is high in vertebrates because these structures are necessary for feeding and escape at nearly all postembryonic stages. Burden can increase or decrease during evolution.23 If the ancestral chordate was like an ascidian,24 then the functional burden on structures dependent on the notochord has increased in the vertebrates. If the ancestral chordate was like a larvacean or cephalochordate (requiring the may combine to affect synchrony or asynchrony in cleavages. Van den Biggelaar and Haszprunar17 compared the number of cells in gastropod embryos at the time when the mesentoblast is formed. Snails with planktonic embryos form the mesentoblast when there are 63 cells. Although snails with encapsulated embryos form the mesentoblast when there are fewer cells, their formation of the mesentoblast is not accelerated. The authors do not give developmental schedules, but the snails with protected embryos have longer embryonic cell cycles than the snails with planktonic embryos. In protected embryos, the mesentoblast is formed when there are fewer cells because the lineages of animal pole micromeres (fated to become ectoderm) are retarded even more than the vegetal pole macromeres (one of which eventually produces the mesentoblast). The overall retardation has occurred in association with protection. A functional hypothesis for the greater retardation of the presumptive ectoderm is that the encapsulated embryos have no immediate need for ciliated bands for swimming or apical sense organs (which are ectodermal), whereas the planktonic embryos begin swimming much earlier in their development, using locomotory cilia at an early stage. Burden and loss of function: transitions in modes of larval development Evolutionary loss of function is often accompanied by reduction or loss of structures. The first structures formed in larvae are those used in swimming or feeding. It is therefore no surprise that the loss or reduction of these structures is often accompanied by changes in cell fates and morphogenetic processes. Loss of the larval tail in ascidians is a spectacular example that involves a profound change in the chordate body.18 Tailless ascidians have lost the notochord, dorsal nerve cord, and axial body muscles characteristic of chordates. Tails have been lost multiple times and such losses have been concentrated within the family Molgulidae.19 Thus molgulids have ‘unchordated’ several times in their evolution. Retention of pharyngeal openings hardly qualifies them as chordates. The hemichordates have pharyngeal openings but lack of other chordate features put them in another phylum. Tailless ascidians are still classified as chordates. They have not even changed genus. The taxonomic conservatism is due to respect for ancestors and perhaps due to adults being more conspicuous than larvae. 397 R. R. Strathmann between two different cell lineages.28 The ciliary band forms a continuous loop that encloses the oral field and mouth. The form of this ciliary band is a compromise between requirements of feeding and swimming.29, 30 Feeding requires an effective stroke of cilia perpendicular to the band and away from the oral field. This brings food particles toward the ciliary band, and the particles induce local reversals of ciliary beat that retain the food on the oral field and aid transport toward the mouth. Swimming requires that the direction of the effective stroke of cilia have a component toward the posterior so that the larva moves forward. In sea urchin larvae, this requirement is met by loops of the band on arms that are directed anteriorly with a slight outward tilt and by transverse sections of the band between the arms. The larval arms are supported by skeletal rods. Interactions of mesenchyme and ectoderm are responsible for the form and position of these skeletal rods. The form of the pluteus arms and ciliary bands depends in part on the skeleton. In contrast, larval seastars and sea cucumbers (some other echinoderms) have no skeletal rods or anteriorly directed arms. Instead the loops of the band are everywhere slightly tilted so that there is a posterior component to the ciliary currents. These tilts of the band are easily overlooked but are necessary for its function and require a more precise positioning of cells than one would first suppose.1 The morphogenetic processes that produce these subtle tilts of the bands of seastar and sea cucumber larvae are as yet unknown. Evolution of larger eggs is associated with loss of the necessity for feeding,31 and eventually the larval ciliation evolves into transverse bands or ciliary fields as arrangements more suited for the sole requirement of swimming.32 Extreme reduction of the ciliary band has occurred in the sea urchin Heliocidaris erythrogramma (with a non-feeding larva) which has diverged from its sister species Heliocidaris tuberculata (which has retained a feeding larva). H. erythrogramma provides an extensively studied example of changes in cell fates and morphogenetic processes associated with loss of function.33, 34 Maternal H. e. × paternal H. t. hybridization is possible and offers an opportunity to explore the genetic basis of profound evolutionary changes in morphogenesis.33 A remarkable result of the maternal H. e. × H. t. cross is restoration of a continuously looping ciliary band, but the skeletal rods do not develop normally in the hybrid.33 The hybrid’s superficial resemblance notochord and notochord-dependent structures for feeding and growth), then the functional burden on structures dependent on the notochord decreased in the ascidians when they evolved a sessile habit during the feeding stages, with consequent loss of the tail at metamorphosis. If a population of fishes had evolved a sessile habit, so that at an early stage they became attached to the bottom and fed with a pharyngeal filter, then the functional burden on notochorddependent structures would have decreased for these vertebrates, and we might see viable fish in which a mutation for taillessness had spread to become characteristic of the species. Loss of tails also illustrates a deficiency in many claims of developmental constraint. In cases where mutations producing the phenotype occur but the phenotype is disadvantageous, there is a functional constraint. Developmental processes might or might not be combining with such a functional constraint to restrict evolutionary change, but the environment affects what enhances survival and reproduction and what does not. With appropriate culture conditions, vertebrates evolved into protists, with HeLa cells an especially successful example.25 Before leaving tailless ascidians, it is worth noting the multiple evolutionary loss of tails in molgulids and very rare loss in other families of ascidians. Berrill suggested a functional hypothesis: taillessness evolved frequently in molgulids because they live in sandy habitats where larval habitat selection has little advantage. This is inconsistent, however, with a tailless molgulid on a rocky shore26 and with selective settlement by swimming larvae of other animals in sandy habitats. Sandy habitats are by no means uniform for settling larvae.27 The traits that have facilitated tail loss in molgulids are as yet undemonstrated. Setting specifications for a developmental process Functional analyses show the degree of developmental specification that is required of a structure, thus revealing aspects of morphogenesis that are otherwise overlooked. An example is the orientation of ciliary bands of echinoderm larvae. Overlooking the necessary specification for larval forms has misled interpretation of an otherwise extraordinarily informative hybridization experiment. The ciliary bands of echinodem larvae consist of columnar ciliated cells that differentiate at the border 398 Function of development proceed with little effect on the juvenile sea urchin. Modularity in development confers flexibility in evolution and accounts for numerous violations of von Baer’s law. Evolutionary divergence among animals is not consistently greater at later developmental stages. What accounts for this modularity? One suggested origin of modularity is sequential evolution of the modules. The separate and different development of larval body and echinus rudiment in sea urchins suggested the hypothesis that ancestral bilaterian animals resembled the present day larvae, and the juvenile and adult stages evolved via the origin of cells set aside from development of the larval body.36, 37 This hypothesis identified important differences among animals’ embryos and larvae, but as originally stated, it did not account for patterns of evolutionary divergence in what juvenile structures develop from separate rudiments and what larval structures are retained through metamorphosis. For example, in the sea cucumbers (relatives of the sea urchins), the ‘set-aside’ cells with no apparent function in the larval stage are simply parts of the coelom and mesenchyme, and the body axes and site of the mouth are retained through metamorphosis. In the cidaroid sea urchins, which are the sister group of euechinoids (other living sea urchins), the juvenile mouth forms at the larva’s lower left side, but the juvenile rudiment is not internalized.38 Thus the extensive setting aside of cells for postlarval structures in euechinoids appears to be a derived condition, and much less setting aside of cells the ancestral condition. Moreover, numbers of cell divisions in the larval tissues are not constrained as originally proposed.36 Echinoderm larval bodies vary greatly in size and thus cell number, both among species and as a developmental response to food supply. Explicit analyses of the functional consequences of juvenile rudiments can improve hypotheses on modularity and set-aside cells. Functional advantages of modularity appear to be diverse. For bottom-living marine animals with planktonic larvae, structures suited to life at the sea bed can be unsuited to life in the plankton and vice versa. Hence metamorphosis occurs at about the time the animals change habitat. One advantage of internalized or localized rudiments of juvenile structures is to keep them out of the way while they are functionless.39, 40 Formation of the juvenile mouth at a new site on the lower left side of the sea urchin larva permits continued larval feeding during development of the juvenile, right up to the time of settlement and to a larval seastar or sea cucumber suggested the hypothesis that the early hybrid larva resembled ‘the dipleurula-type larva typical of other classes of echinoderms and is considered to represent the ancestral echinoderm larval form’. In the photos, however, there is no indication of the tilts of the ciliary band required by larval seastars or sea cucumbers. The H. e. × H. t. hybrid is more simply interpreted as a larva that has formed the ciliary band but without development of the skeletal rods that would produce the form of a sea urchin pluteus.35 The resemblance to larval seastars or sea cucumbers is explicable by subtraction of the skeletal rods rather than resurrection of the ontogenetic pathway that produces the larval ciliary bands of sea cucumbers or seastars. The feeding larvae of echinoderms (pluteus, bipinnaria, and auricularia) are, at early stages, sufficiently similar, that a diagram of their common features (drawn 30 years ago) resembles the H. e. × H. t. hybrid, but with a stronger ventral flexure.30 The form of the hybrid’s ciliary band can be interpreted in relation to divergence in its immediate parents’ development (as other features of the hybrid were interpreted by the authors). From the evidence presented thus far, there is no apparent need to suppose a ‘surprisingly long term retention of an ancient pattern of larval development’. There was a long term retention of an ancient pattern in H. tuberculata because it retained a feeding larva, but the retention is not surprising because the ciliated band developed each generation and mutations were eliminated by selection during its entire evolutionary history. This story should in no way diminish interest in what is a remarkable evolutionary divergence in embryos and larvae, and the potential of the hybrids for probing the developmental processes involved.33 The moral is that attention to functional morphology can help developmental biologists interpret evolutionary divergence of developmental processes. Evolution of modularity, along with some set-aside cells Development of body parts in separate, largely independent modules permits evolutionary divergence in one part with little divergence in another. Evolutionary loss of the ascidian tail can proceed with little effect on the pharynx. Evolutionary loss of larval ciliary bands, skeletal rods, and mouth can 399 R. R. Strathmann completion of metamorphosis.30 Secondly, if developing juvenile structures are tucked away, they can be kept longer in a less differentiated state, with advantages for growth41 as they are nourished by the larva. Thirdly, development of juvenile structures to an advanced state before metamorphosis permits a rapid transition to a new form and habitat. Setting some cells aside as they develop into postlarval structures is a means of preparing the sea urchin for a rapid change in form and habitat. Functional requirements of larvae, juveniles, and transitions in form and habitat help explain which cells are ‘set aside’. Endoderm forming midgut becomes functional in feeding larvae and continues to be midgut through and past metamorphosis. These cells also store nutritional reserves that are carried through metamorphosis. Continuity of midgut is common to most marine invertebrate larvae, whereas the extent to which mesodermal and ectodermal cells are ‘set aside’ varies greatly. In echinoderms and hemichordates, some mesodermal cells (some mesenchyme and parts of the coelom) lack apparent function in the larva and contribute to the postlarval juvenile, but the hydrocoel (a premier example of presumed set-aside cells) functions as a larval excretory organ42 and mesenchyme contributes to larval muscles. A plausible hypothesis is that metamorphoses evolved many times in the marine bilateria and that the setting aside of cells that form juvenile structures accompanied divergence of larval and juvenile forms and the elaboration of metamorphic transitions. An additional advantage of modularity can be developmental plasticity, in which developmental timing, size of structures, or form of structures are altered in response to environmental cues. Developmental plasticity in sea urchin larvae is an example that involves the cells set aside in the echinus rudiment. The echinus rudiment develops within the pluteus larva and becomes most of the sea urchin’s body wall at metamorphosis. Timing of development of the rudiment relative to the larval body depends on the supply of food for the larva.43, 44 At low concentrations of food (algal cells), the formation of the echinus rudiment is delayed. Even the invagination of ectoderm towards the hydrocoel is delayed. Instead, the larva grows longer arms and a longer ciliated band. A hungry pluteus develops eight long arms but almost no rudiment. A satiated larva develops stubby arms, but accelerated development of the rudiment is already apparent by the six-armed stage. These changes in both timing and size appear to be adaptive. The longer arms mean a longer ciliary band and thus faster processing of water for food when food is limiting.45 The larva first increases its ability to catch food and then allocates growth to the rudiment. When food is abundant, however, higher rates of capture do not increase growth rates. The larva begins forming the juvenile structures immediately, reducing the time for its development. The plasticity appears suited to minimizing the development times over a range of food concentrations. Rapid development is presumably advantageous because mortality rates of these tiny larvae are high.46 A shorter larval period should yield higher survival. Decoupling of the development of the rudiment from structures for larval feeding permits this developmental plasticity. Conversely, selection for this developmental plasticity may have contributed to this decoupling in development. A cautionary tale: stasis and change in a seemingly simple and much studied trait Tests of functional hypotheses can be based on the consequences of experimental change in a trait, comparisons of performance of different organisms, or both.47 Unsurprisingly, tests often reveal unsuspected complications and raise new questions. Comparison of 3 million years of evolutionary divergence of eggs of echinoderms on the two sides of the Isthmus of Panama revealed the predicted trend of larger eggs in the ocean with a lower concentration of food.48 Eggs were predicted to be larger where there was slower larval growth or greater larval death rates. Production of smaller eggs permits production of more eggs, but the smaller eggs are at greater risk because more growth and hence a longer development is required in early life. The predicted optimum size is a compromise between fecundity of the mother and mortality of the offspring. Confirmation of a prediction by replicated evolutionary events is gratifying, but the comparison also revealed that the genus was a better predictor of egg size than the ocean. The importance of ancestry in the evolution of egg size suggests that selection on egg size depends on other traits of these animals, not just their environment, and that the traits differ among genera. At present, these generic differences are anyone’s guess. Experimentally decreasing sea urchin egg volume by half is not directly lethal.47 The generic differences could involve the habitats occupied by the adults (despite interocean differences), 400 Function of development differences in larval forms, or other consequences of coadapted gene complexes or pleiotropic effects that involve egg size. The interocean comparison suggests that in each genus there is a well integrated phenotype that results in stabilizing selection on egg size in a wide range of habitats. Evolutionary divergence and stasis in development is not simple. Analyses of the functional demands met by embryos and larvae are an essential part of explanations but do not tell the whole story. 4. 5. 6. 7. 8. Discussion 9. 10. A function of developmental processes is putting the right kinds of cells in the right places at the right times. The criterion for ‘right’ is survival and reproduction. For this essay, I gave some examples of functional hypotheses that predict what is right. These were qualitative statements, due to the limits of a short essay and my abilities. Quantitative predictions are more vulnerable to tests than qualitative predictions. Mathematical skills are useful and, for many of us, a reason for collaboration. Converting ‘evodevo’ from descriptions of evolutionary change to explanations of evolutionary change will require a connection to survival and reproduction. Functional analyses are necessary for making this connection. 11. 12. 13. 14. 15. 16. 17. 18. 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