Effects of embryo energy,egg size,and larval food supply on the development of asteroid echinoderms

Organisms have limited resources available to invest in reproduction, causing a trade‐off between the number and size of offspring. One consequence of this trade‐off is the evolution of disparate egg sizes and, by extension, developmental modes. In particular, echinoid echinoderms (sea urchins and sand dollars) have been widely used to experimentally manipulate how changes in egg size affect development. Here, we test the generality of the echinoid results by (a) using laser ablations of blastomeres to experimentally reduce embryo energy in the asteroid echinoderms (sea stars), Pisaster ochraceus and Asterias forbesi and (b) comparing naturally produced, variably sized eggs (1.7‐fold volume difference between large and small eggs) in A. forbesi. In P. ochraceus and A. forbesi, there were no significant differences between juveniles from both experimentally reduced embryos and naturally produced eggs of variable size. However, in both embryo reduction and egg size variation experiments, simultaneous reductions in larval food had a significant and large effect on larval and juvenile development. These results indicate that (a) food levels are more important than embryo energy or egg size in determining larval and juvenile quality in sea stars and (b) the relative importance of embryo energy or egg size to fundamental life history parameters (time to and size at metamorphosis) does not appear to be consistent within echinoderms.     

How do changes in parental investment influence development in echinoid echinoderms?

SUMMARY Understanding the relationship between egg size, development time, and juvenile size is critical to explaining patterns of life-history evolution in marine invertebrates. Currently there is conflicting information about the effects of changes in egg size on the life histories of echinoid echinoderms. We sought to resolve this conflict by manipulating egg size and food level during the development of two planktotrophic echinoid echinoderms: the green sea urchin, Strongylocentrotus droebachiensis and the sand dollar, Echinarachnius parma . Based on comparative datasets, we predicted that decreasing food availability and egg size would increase development time and reduce juvenile size. To test our prediction, blastomere separations were performed in both species at the two-cell stage to reduce egg volume by 50%, producing whole- and half-size larvae that were reared to metamorphosis under high or low food levels. Upon settlement, age at metamorphosis, juvenile size, spine number, and spine length were measured. As predicted, reducing egg size and food availability significantly increased age at metamorphosis and reduced juvenile quality. Along with previous egg size manipulations in other echinoids, this study suggests that the relationship between egg size, development time, and juvenile size is strongly dependent upon the initial size of the egg.     

Effects of egg size on the development time of non-feeding larvae

The evolution of egg size in marine invertebrates remains a topic of central importance for life-history biologists, and the pioneering work of Vance has strongly influenced our current views. Vance's model and most models developed since have assumed that increases in egg size result in an increase in the prefeeding period of marine invertebrate larvae. For lecithotrophic species, this means that the entire development period should be correlated with egg size. Despite the importance of this assumption, it has not been tested at the appropriate scale-within species. We investigated the effects of egg size on development time for three lecithotrophic species from two phyla: the ascidians Phallusia obesa and Ciona intestinalis, and the echinoid Heliocidaris erythrogramma. We found that within individual broods of eggs, larger eggs took longer than smaller eggs to develop or become metamorphically competent larvae. It has long been recognized that producing larger eggs decreases fecundity, but our results show that increasing egg size also carries the extra cost of an extended planktonic period during which mortality can occur. The substantial variation in egg sizes observed within broods may represent a bet-hedging strategy by which offspring with variable dispersal potentials are produced.     

Effects of egg size reduction and larval feeding on juvenile quality for a species with facultative-feeding development

In free-spawning marine invertebrates, larval development typically proceeds by one of two modes: planktotrophy (obligate larval feeding) from small eggs or lecithotrophy (obligate non-feeding) from relatively large eggs. In a rare third developmental mode, facultative planktotrophy, larvae can feed, but do not require particulate food to complete metamorphosis. Facultative planktotrophy is thought to be an intermediate condition that results from an evolutionary increase in energy content in the small eggs of a planktotrophic ancestor. We tested whether an experimental reduction in egg size is sufficient to restore obligate planktotrophy from facultative planktotrophy and whether the two sources of larval nutrition (feeding and energy in the egg) differentially influence larval survival and juvenile quality. We predicted, based on its large egg size, that a reduction in egg size in the echinoid echinoderm Clypeaster rosaceus would affect juvenile size but not time to metamorphosis. We reduced the effective size of whole (W) zygotes by separating blastomeres at the two- or four-cell stages to create half- (H) or quarter-size (Q) “zygotes” and reared larvae to metamorphosis, both with and without particulate food. Larvae metamorphosed at approximately the same time regardless of food or egg size treatment. In contrast, juveniles that developed from W zygotes were significantly larger, had higher organic content and had longer and more numerous spines than juveniles from H or Q zygotes. Larvae from W, H and Q zygotes were able to reach metamorphosis without feeding, suggesting that the evolution of facultative planktotrophy in C. rosaceus was accompanied by more than a simple increase in egg size. In addition, our results suggest that resources lost by halving egg size have a larger effect on larval survival and juvenile quality than those lost by withholding particulate food.     

Relationships among Egg Size, Composition, and Energy: A Comparative Study of Geminate Sea Urchins

Egg size is one of the fundamental parameters in the life histories of marine organisms. However, few studies have examined the relationships among egg size, composition, and energetic content in a phylogenetically controlled context. We investigated the associations among egg size, composition, and energy using a comparative system, geminate species formed by the closure of the Central American Seaway. We examined western Atlantic (WA) and eastern Pacific (EP) species in three echinoid genera, Echinometra, Eucidaris, and Diadema. In the genus with the largest difference in egg size between geminates (Echinometra), the eggs of WA species were larger, lipid rich and protein poor compared to the smaller eggs of their EP geminate. In addition, the larger WA eggs had significantly greater total egg energy and summed biochemical constituents yet significantly lower egg energy density (energy-per-unit-volume). However, the genera with smaller (Eucidaris) or no (Diadema) differences in egg size were not significantly different in summed biochemical constituents, total egg energy, or energy density. Theoretical models generally assume a strong tradeoff between egg size and fecundity that limits energetic investment and constrains life history evolution. We show that even among closely-related taxa, large eggs cannot be assumed to be scaled-up small eggs either in terms of energy or composition. Although our data comes exclusively from echinoid echinoderms, this pattern may be generalizable to other marine invertebrate taxa. Because egg composition and egg size do not necessarily evolve in lockstep, selective factors such as sperm limitation could act on egg volume without necessarily affecting maternal or larval energetics.     

Morphogenesis and phenotypic divergence in two developmental morphs of Streblospio benedicti (Annelida,Spionidae)

Abstract. The morphology of marine invertebrate larvae is strongly correlated with egg size and larval feeding mode. Planktotrophic larvae typically have suites of morphological traits that support a planktonic, feeding life style, while lecithotrophic larvae often have larger, yolkier bodies, and in some cases, a reduced expression of larval traits. Poecilogonous species provide interesting cases for the analysis of early morphogenesis, as two morphs of larvae are produced by a single species. We compared morphogenesis in planktotrophic and lecithotrophic morphs of the poecilogonous annelid Streblospio benedicti from the trochophore stage through metamorphosis, using observations of individuals that were observed alive, with scanning electron microscopy, or in serial sections. Offspring of alternate developmental morphs of this species are well known to have divergent morphologies in terms of size, yolk content, and the presence of larval bristles. We found that some phenotypic differences between morphs occur as traits that are present in only one morph (e.g., larval bristles, bacillary cells on the prostomium and pygidium), but that much of the phenotypic divergence is based on heterochronic changes in the differentiation of shared traits (e.g., gut and coelom). Tissue and organ development are compared in both morphs in terms of their structure and ontogenetic change throughout early development and metamorphosis.     

Evolution of marine invertebrate reproductive patterns

A simple model of the evolution of reproductive patterns in marine benthic invertebrates is presented. The aim is to discuss the dichotomous distribution of forms into those which produce a large number of small eggs with planktotrophic development, and those which produce a small number of large eggs with direct or lecithotrophic development. The fecundity of adult individuals is assumed to be inversely proportional to egg size, and the mortality of planktonic larvae is assumed to be density independent and size dependent. The growth of planktonic larvae is assumed to be sigmoid with metamorphosis occurring at a given size. The model concludes that there are at most two evolutionarily stable egg sizes. Depending on larval growth rate and death rate, the metamorphosis size, a smaller egg size, or both may be evolutionarily stable. The predictions of the model are compared to patterns observed in nature. Illustrative data are supplied mainly from prosobranch molluscs.     

EFFECTS OF EGG SIZE ON POSTLARVAL PERFORMANCE: EXPERIMENTAL EVIDENCE FROM A SEA URCHIN

Many life-history and developmental studies of marine invertebrates assume that eggs of species with nonfeeding larvae are large because they provide materials for rapid development. Using the sea urchin Heliocidaris erythrogramma which has 400 μm eggs and nonfeeding larvae, we removed an acellular, lipid-rich component from the blastula equivalent to ca. 40% of the egg volume and ca. 50% of the organic mass. Experimentally manipulated, reduced-lipid larvae survived well, developed in the usual time (3.5 d), and high percentages of the original numbers metamorphosed into anatomically normal juveniles. Control juveniles were larger at metamorphosis, grew more, and survived longer than siblings that lacked this lipid-rich material. Moderate increases in egg size in species with nonfeeding larvae may enhance postlarval performance significantly and therefore may reflect selection on early juvenile traits. The contrasts of our results and comparable experiments with feeding larvae suggests that egg size may play fundamentally different roles in species with feeding and nonfeeding larvae. The accommodation of materials reserved for the juvenile stage should be considered among hypotheses on evolutionary modification of developmental patterns.     

Inferring larval type in fossil bryozoans

Pachut, J.F. & Fisherkeller, P. 2010: Inferring larval type in fossil bryozoans. Lethaia, Vol. 43, pp. 396–410. Larval type in extinct organisms might be recognizable because larvae of living marine invertebrates are approximately of the same size as the initial post‐larval organism. Two larval types typically occur. Planktotrophic larvae feed on other members of the plankton, potentially prolonging their larval existence and producing broad geographic distributions. Conversely, lecithotrophic larvae feed on yolk supplied by the fertilized egg, often settle quickly after release, and display more restricted distributions. However, some lecithotrophic bryozoans undergo embryonic fission forming multiple, small, polyembryonic larvae. The relationship between post‐larval size and larval type was evaluated in bryozoans by comparing the size of the ancestrula, the founding individual of a colony, to the sizes of extant planktotrophic, lecithotrophic and polyembryonic lecithotrophic larvae and ancestrulae. The sizes of larvae and ancestrulae in extant lecithotrophic and planktotrophic cheilostome (gymnolaemate) species are statistically the same. They are, however, statistically larger than the polyembryonic larvae of extant cyclostomes (stenolaemates). In turn, the sizes of cyclostome larvae are indistinguishable from the ancestrulae of extant and fossil cyclostomes, the ancestrulae of other fossil stenolaemate species measured from the literature, and the ancestrulae of three of four genera from North American Cincinnatian strata. Ancestrulae of a fourth genus, Dekayia, are the same size as cyclostome ancestrulae but are statistically smaller than the ancestrulae of other stenolaemates. With few exceptions, stenolaemates have statistically smaller larvae and ancestrulae than both lecithotrophic and planktotrophic cheilostomes. We infer that the sizes of fossil ancestrulae permit the discrimination of taxa that had polyembryonic lecithotrophic larvae from those possessing other larval types. This inference is strengthened, in several cases, by the co‐occurrence of brood chambers (gynozooecia) and restricted palaeobiogeographic distributions. The presence of cyclostomes in Early Ordovician strata suggests that polyembryony may have been acquired during the initial radiation of Class Stenolaemata. Polyembryony appears to be a monophyletic trait, but confirmation requires the demonstration that species of several stenolaemate suborders lacking skeletally expressed brood chambers possessed polyembryonic larvae. □Ancestrulae, evolution, fossil bryozoans, gynozooecia, larvae.     

Marine algal symbionts benefit benthic invertebrate embryos deposited in gelatinous egg masses

Algae colonize the gelatinous egg masses of marine invertebrates. This study demonstrates a symbiotic relationship between marine algae and the invertebrate embryos in gelatinous egg masses found in Indian River Lagoon, FL, USA. The benefits to the embryos in this association differ among host species investigated. The embryos of the polychaete Axiothella mucosa graze on the diatom assemblage in their egg masses and the fitness of the crawl-away juveniles is improved by this food source. The tenuous egg masses of the polychaete Arenicola cristata and the mollusk Haminoea succinea are negatively buoyant when spawned and become buoyant when symbiotic algae are present. In addition to increased dispersal of their lecithotrophic larvae, the potential of the egg masses of A. cristata and H. succinea to float may reduce predation on the embryos by benthic predators such as the gastropod Nassarius vibex. Photosynthetically derived oxygen from the algae may benefit the embryos of the opisthobranch Haminoea elegans by increasing oxygen supply when crawl-away juveniles emerge from the egg mass. However, when mostly earlier stage larvae are hatched from egg masses of H. elegans, the additional oxygen supplied by the algae does not provide a substantial advantage. Algae were absent in the gelatinous egg mass core of only one of the five species examined, Haminoea antillarum. H. antillarum has both a short embryonic development time and denser egg mass gel than the other four species tested. What is not understood is whether invertebrate egg masses are an opportunistic space for algae to colonize or whether only a few microalgal species can exploit the gelatinous substrate.     

Brood care among basommatophorans: a unique reproductive strategy in the freshwater limpet snail Protancylus (Heterobranchia: Protancylidae), endemic to ancient lakes on Sulawesi, Indonesia

In molluscan taxa inhabiting marine environments oviparity and reproduction via planktonic larvae is predominant while incubation and viviparity is most frequently found in taxa inhabiting brackish or freshwater aquatic habitats. Brooding has evolved repeatedly and independently in several limnic taxa among Bivalvia and Gastropoda. However, among basommatophoran gastropods no such cases were yet known. We here report on a unique reproductive strategy involving brood care in the lacustrine freshwater limpet genus Protancylus, endemic to the ancient lakes on central Sulawesi (former Celebes), Indonesia, namely the Lake Poso and the Malili lake system, because this constitutes the first known case of this behaviour among the Basommatophora. Protancylus live exclusively as epizoans on those pachychilid gastropods of the viviparous genus Tylomelania, also a Sulawesi endemic species, that inhabit mostly soft substrates. We found that the two known species Protancylus pileolus from Lake Poso and P. adhaerens from the Malili lake system both retain gelatinous egg strings underneath their outer mantle, where up to 15 (mostly eight or nine) shelled juveniles are brooded. Nourishment is provided within the egg capsule only. Thus, brood care in Protancylus resembles the reproductive strategy found recently among pachychilid gastropods Jagora from the Philippines, but differs from euviviparous (i.e. matrotrophic) incubation among thiarid gastropods possessing a brood pouch with juveniles being nourished via a ‘pseudoplacenta’ in several taxa.     

Lipid dynamics in the embryos of Patiriella species (Asteroidea) with divergent modes of development

Evolution of lecithotrophic development in sea stars involved a modification in maternal provisioning from the production of yolk-dominated to lipid-dominated eggs. The dynamics of lipid reserves in the embryos of four Patiriella species differing in their lipid provisions were examined. Patiriella regularis had small yolk protein-dominated eggs (150 microm in diameter) and an ancestral mode of development through planktotrophic larvae. Patiriella calcar, Patiriella exigua and Patiriella pseudoexigua had large eggs (390-440 microm in diameter) and lecithotrophic planktonic, benthic and intragonadal larvae, respectively. Patiriella exigua deposited negatively buoyant eggs containing substantial yolk protein and lipid reserves onto the substratum. In contrast, the planktonic eggs of P. calcar and the intragonadal eggs of P. pseudoexigua were dominated by lipid and were neutrally and positively buoyant, respectively. By the blastula stage there was little trace of lipid in P. regularis embryos. Blastulae of the lecithotrophic developers, by contrast, had conspicuous lipid droplets distributed through their cells. In parallel with the change from cuboidal to columnar epithelium during the blastula to gastrula transition, lipid reserves became redistributed into the basal cytoplasm. The extent of lipid transport reflected the amount of lipid reserves. In P. pseudoexigua embryos with the greatest lipid load, basal shunting was followed by secretion of lipid into the blastocoele where it was stored for the perimetamorphic period. Evolution of lecithotrophy in Patiriella appears to reflect selection to provide metamorphic stages with nutrients normally accrued by feeding larvae with the consequence that early development is burdened by voluminous, potentially inert nutritive stores. Lipid redistribution coincident with a major developmental stage transition may be required to facilitate unimpeded morphogenesis. This phenomenon may be characteristic of lecithotrophic development in echinoderms and appears pre-adaptive for extrusion of lipid in species like P. pseudoexigua with particularly extensive lipid reserves.     

The importance of larval eyes in the polychaete Capitella teleta: effects of larval eye deletion on formation of the adult eye

In many marine invertebrates with biphasic life cycles, juvenile/adult traits begin to develop before metamorphosis. For structures that are present at multiple developmental stages, but have distinct larval and adult forms, it is unclear whether larval and adult structures have shared or distinct developmental origins. In this study, we examine the relationship between the larval and adult eyes in the polychaete Capitella teleta. In addition, we describe a novel marker for larval and juvenile photoreceptor cells. Infrared laser deletion of individual micromeres in early embryos suggests that the same micromeres at the eight‐cell stage that are specified to generate the larval eyes also form the adult eyes. Direct deletion of the larval eye, including the pigment cell and the corresponding photoreceptor cell, resulted in a lack of shading pigment cells in juveniles and adults, demonstrating that this structure does not regenerate. However, a sensory photoreceptor cell was present in juveniles following direct larval eye deletions, indicating that larval and adult photoreceptors are separate cells. We propose that the formation of the adult eye in juveniles of C. teleta requires the presence of the pigment cell of the larval eye, but the adult photoreceptor is either recruited from adjacent neural tissue or arises de novo after metamorphosis. These results are different from the development and spatial orientation of larval and adult eyes found in other polychaetes, in which two scenarios have been proposed: larval eyes persist and function as adult eyes; or, distinct pigmented adult eyes begin developing separately from larval eyes prior to metamorphosis.     

Investigating the developmental onset of regenerative potential in the annelid Capitella teleta

An animal's ability to regrow lost tissues or structures can vary greatly during its life cycle. The annelid Capitella teleta exhibits posterior, but not anterior, regeneration as juveniles and adults. In contrast, embryos display only limited replacement of specific tissues. To investigate when during development individuals of C. teleta become capable of regeneration, we assessed the extent to which larvae can regenerate. We hypothesized that larvae exhibit intermediate regeneration potential and demonstrate some features of juvenile regeneration, but do not successfully replace all lost structures. Both anterior and posterior regeneration potential of larvae were evaluated following amputation. We used several methods to analyze wound sites: EdU incorporation to assess cell proliferation; in situ hybridization to assess stem cell and differentiation marker expression; immunohistochemistry and phalloidin staining to determine presence of neurites and muscle fibers, respectively; and observation to assess re-epithelialization and determine regrowth of structures. Wound healing occurred within 6 h of amputation for both anterior and posterior amputations. Cell proliferation at both wound sites was observed for up to 7 days following amputation. In addition, the stem cell marker vasa was expressed at anterior and posterior wound sites. However, growth of new tissue was observed only in posterior amputations. Neurites from the ventral nerve cord were also observed at posterior wound sites. De novo ash expression in the ectoderm of anterior wound sites indicated neuronal cell specification, although the absence of elav expression indicated an inability to progress to neuronal differentiation. In rare instances, cilia and eyes re-formed. Both amputations induced expanded expression of the myogenesis gene MyoD in preexisting tissues. Our results indicate that amputated larvae complete early, but not late, stages of regeneration, which indicates a gradual acquisition of regenerative ability in C. teleta. Furthermore, amputated larvae can metamorphose into burrowing juveniles, including those missing brain and anterior sensory structures. To our knowledge, this is the first study to assess regenerative potential of annelid larvae.     

Reproduction and larval morphology of broadcasting and viviparous species in the Cryptasterina species complex

The Cryptasterina group of asterinid sea stars in Australasia comprises cryptic species with derived life histories. C. pentagona and C. hystera have planktonic and intragonadal larvae, respectively. C. pentagona has the gonochoric, free-spawning mode of reproduction with a planktonic lecithotrophic brachiolaria larva. C. hystera is hermaphroditic with an intragonadal lecithotrophic brachiolaria, and the juveniles emerge through the gonopore. Both species have large lipid-rich buoyant eggs and well-developed brachiolariae. Early juveniles are sustained by maternal nutrients for several weeks while the digestive tract develops. C. hystera was reared in vitro through metamorphosis. Its brachiolariae exhibited the benthic exploration and settlement behavior typical of planktonic larvae, and they attached to the substratum with their brachiolar complex. These behaviors are unlikely to be used in the intragonadal environment. The presence of a buoyant egg and functional brachiolaria larva would not be expected in an intragonadal brooder and indicate the potential for life-history reversal to a planktonic existence. Life-history traits of species in the Cryptasterina group are compared with those of other asterinids in the genus Patiriella with viviparous development. Modifications of life-history traits and pathways associated with evolution of viviparity in the Asterinidae are assessed, and the presence of convergent adaptations and clade-specific features associated with this unusual mode of parental care are examined.     

THE GENETIC BASIS OF LIFE-HISTORY CHARACTERS IN A POLYCHAETE EXHIBITING PLANKTOTROPHY AND LECITHOTROPHY

The polychaete Streblospio benedicti is unusual in that several field populations consist of individuals that exhibit either planktotrophic or lecithotrophic larval development. Planktotrophy in this species involves production of many small ova that develop into feeding larvae with a two- to three-week planktonic period. Lecithotrophy involves production of fewer, larger ova that develop into nonfeeding larvae that are brooded longer and have a brief planktonic stage. Reciprocal matings were performed to investigate genetic variance components and the correlation structure of life-history traits associated with planktotrophy and lecithotrophy. Our objective was to better understand persistence of this developmental dichotomy in Streblospio benedicti, and among marine invertebrates in general. Substantial additive genetic variation (75–98% of total) was detected for the following characters at first reproduction: female length; position of the first gametogenic setiger and first brood pouch; ovum diameter; three traits related to fecundity (numbers of ova per ovary, larvae per brood pouch, and larvae per brood); median larval planktonic period and the presence of larval swimming setae; but not for total number of brood pouches; larval length; larval feeding; and larval survivorship. Based on the unusual geographic distribution of development modes in this species, we hypothesize that the developmental traits have evolved in allopatry and have only recently come into contact in North Carolina. The high additive contribution to variance observed for many traits may be inflated due to (a) nonrandom breeding in nature, and (b) examination of only one component of an age-structured population at one time. Nuclear interaction variance and maternal variance accounted for 84% of the total variation in larval survivorship. This observation supports other empirical studies and theoretical predictions that nonadditive components of variance will increase in importance in individual traits that are most closely tied to fitness. A network of life-history trait correlations was observed that defines distinct planktotrophic and lecithotrophic trait complexes. Negative genetic correlations were present between fecundity and egg size, between fecundity and position of the first gametes, and between larval survivorship and median planktonic period. Positive genetic correlations were detected between fecundity and female size at first reproduction and between planktonic period and the presence of swimming setae. Intergenerational product-moment correlations were negative for larval length and fecundity, planktonic period and egg size, female size and larval survivorship, and fecundity and larval survivorship. If the genetic correlation structure observed in the laboratory persists in the field, it may constrain responses of individual characters to directional selection, and indirectly perpetuate the dichotomies associated with planktotrophy and lecithotrophy.     

Poecilogony in the caenogastropod Calyptraea lichen (Mollusca: Gastropoda)

In marine invertebrates, polymorphism and polyphenism in mode of development are known as “poecilogony.” Understanding the environmental correlates of poecilogony and the developmental mechanisms that produce it could contribute to a better understanding of evolutionary transitions in mode of development. However, poecilogony is rare in marine invertebrates, with only ten recognized, well‐documented cases. Five examples occur in sacoglossan gastropods, and five occur in spionid polychaetes. Here, we document the eleventh case, and the first in a caenogastropod mollusc. Females of Calyptraea lichen collected in the field or reared in the laboratory often produce broods of planktotrophic larvae. They can also be collected with mixed broods, in which each capsule contains planktotrophic larvae, nurse embryos, and adelphophagic embryos. Adelphophages eat the nurse embryos and hatch as short‐lived lecithotrophic larvae, or even as juveniles. Mitochondrial COI and 16S DNA sequences for females with different types of broods differ by less than 0.5%, supporting conspecific status. Some females collected in the field with mixed broods subsequently produced planktotrophic broods, demonstrating that females can produce two different kinds of broods. Calyptraea lichen is therefore polyphenic in two ways: mode of development can vary among embryos within a capsule, and females can change the types of broods they produce.     

Convergent maternal provisioning and life-history evolution in echinoderms

In marine invertebrates, the frequent evolution of lecithotrophic nonfeeding development from a planktotrophic feeding ancestral developmental mode has involved the repeated, independent acquisition of a large, lipid-rich, usually buoyant egg. To investigate the mechanistic basis of egg-size evolution and the role of maternally provisioned lipids in lecithotrophic development, we identified and quantified the egg lipids in six sea urchin species and five sea star species encompassing four independent evolutionary transformations to lecithotrophy. The small eggs of species with planktotrophic development were dominated by triglycerides with low levels of wax esters, whereas the larger eggs of lecithotrophs contain measurable triglycerides but were dominated by wax ester lipids, a relatively minor egg component of planktotrophs. Comparative analysis by independent contrasts confirmed that after removing the influence of phylogeny, the evolution of a large egg by lecithotrophs was correlated with the conspicuous deposition of wax esters. Increases in wax ester abundance exceeded expectations based solely on changes in egg volume. Wax esters may have roles in providing buoyancy to the egg and for postmetamorphic provisioning. Experimentally reducing the amount of wax esters in blastula stage embryos of the lecithotroph Heliocidaris erythrogramma resulted in a viable but nonbuoyant larvae. During normal development for H. erythrogramma, wax ester biomass remained constant during development to metamorphosis (five days postfertilization), but decreased during juvenile development before complete mouth formation (12 days postfertilization) and was further reduced at 18 days postfertilization. The function of wax esters may be specific to the lecithotrophic developmental mode because there were negligible wax esters present in competent pluteus larvae of Strongylocentrotus drobachiensis, a planktotrophic species. These data suggest that this seminal evolutionary modification, the production of a large egg, has been accomplished in part by the elaboration of a preexisting oogenic component, wax esters. The modification of preexisting oogenic processes may facilitate the observed high frequency of transformations in larval mode in marine invertebrates.     

The ploys of sex: relationships among the mode of reproduction,body size and habitats of coral-reef brittlestars

Observations were made of 33 species of brittlestars (3980 specimens) from specific substrata collected in four zones on the Belize Barrier Reef, Caribbean Sea. The body size of most species of brittlestars with planktonic larvae differs significantly among different substrata. Generally, individuals from the calcareous alga Halimeda opuntia are smallest, those found in corals (Porites porites, Madracis mirabilis, and Agaricia tenuifolia) are larger, and those from coral rubble are the largest. This suggests that brittlestars with planktonic larvae move to new microhabitats as they grow. In contrast, most brooding and fissiparous species are relatively small and their size-distributions are similar among all substrata. Halimeda harbours denser concentrations of brittlestars and more small and juvenile individuals than the other substrata. Juveniles of the brooding and fissiparous species are most common in Halimeda on the Back Reef whereas juveniles developing from planktonic larvae are most common in Halimeda patches in deeper water. Fissiparity and brooding may be means for individuals (genomes) of small, apomictic species to reach large size (and correspondingly high fecundities) in patchy microhabitats that select for small body sizes. Small brittlestar species and juveniles are most numerous in the microhabitats called refuge-substrata, such as Halimeda, which may repel predators and reduce environmental stress. Whether young brittlestars are concentrated in refuge-substrata through settlement behavior, migration, or differential survival remains unknown. Experiments revealed that coral polyps kill small brittlestars, perhaps accounting for the rarity of small and juvenile brittlestars in coral substrata.