Developmental dimorphism: consequences for larval behavior and dispersal potential in a marine gastropod

Specific effects of alternative developmental programs on swimming and settlement behavior for marine larvae have not been identified experimentally. A major impediment to this research has been the rarity of species with variable development. Here, we compared traits related to movement and habitat selection for different ontogenetic stages of long-lived, feeding larvae (planktotrophic) and short-lived, nonfeeding larvae (lecithotrophic) of the herbivorous gastropod Alderia modesta. Newly hatched planktotrophic larvae swam in meandering paths with equal rates of upward and downward movement. As planktotrophic larvae developed towards competence (physiological ability to metamorphose), their swimming paths became straighter, faster, and increasingly directed towards the bottom, traits shared by newly hatched lecithotrophic larvae. Despite differing in developmental history, competent planktotrophic (32-d-old) and lecithotrophic larvae (competent upon hatching) exhibited qualitatively similar swimming behaviors and substrate specificity. However, lecithotrophic larvae moved downward at twice the speed of competent planktotrophic larvae, potentially producing a 5-fold higher rate of contact with the bottom in natural flows. Competent larvae swam downwards rather than passively sinking, even though sinking rates were faster than swimming speeds; active swimming may allow larvae to keep the velum extended, permitting rapid response to chemical settlement cues and promoting successful habitat colonization. Differences between larvae of the two development modes may reflect fine-tuning by selection of traits important for dispersal and settlement into patchy adult habitats.     

Changes in the timing of mantle formation and larval life history traits in linguliform and craniiform brachiopods

The distribution of embryonic and larval mantles is documented in linguliform and craniiform brachiopods. Criteria are presented for identifying these mantle types. The mantle type is related to planktotrophic and lecithotrophic larval life history patterns. In the Linguliformea and Craniiformea, all Lower Palaeozoic families with adequate preservation had larval mantles, indicating the presence of a planktotrophic larva. Heterochronic changes in the time of mantle origin, from the larval to the embryonic stage of development, has occurred several times. In the Lingulidae this change appears to have taken place at about the time the family originated in the Devonian and has been retained in extant genera. The family Discinidae has also retained a planktotrophic larval stage from the Lower Palaeozic to the present. The extant genus Crania in the Craniidae has a short-lived lecithotrophic larva that lacks a mantle. Through the Lower Jurassic, this family had planktotrophic larvae with a larval shell. During the Upper Jurassic, genera with a lecithotrophic larva that lacked a larval shell began to appear; however, the last genera in this family with a planktotrophic larva and a larval shell did not become extinct until the Tertiary.     

Poecilogony and population genetic structure in Elysia pusilla (Heterobranchia: Sacoglossa), and reproductive data for five sacoglossans that express dimorphisms in larval development

Credible cases of poecilogony, the production of two distinct larval morphs within a species, are extremely rare in marine invertebrates, yet peculiarly common in a clade of herbivorous sea slugs, the Sacoglossa. Only five animal species have been reported to express dimorphic egg sizes that result in planktotrophic and lecithotrophic larvae: the spionid polychaete Streblospio benedicti and four sacoglossans distributed in temperate estuaries or the Caribbean. Here, we present developmental and genetic evidence for a fifth case of poecilogony via egg-size dimorphism in the Sacoglossa and the first example from the tropical Indo-Pacific. The sea slug Elysia pusilla produced both planktotrophic and lecithotrophic larvae in Guam and Japan. Levels of genetic divergence within populations were markedly low and rule out cryptic species. However, divergence among populations was exceptionally high (10-12% at the mitochondrial cytochrome c oxidase I locus), illustrating that extensive phylogeographic structure can persist in spite of the dispersal potential of planktotrophic larvae. We review reproductive, developmental, and ecological data for the five known cases of poecilogony in the Sacoglossa, including new data for Costasiella ocellifera from the Caribbean. We hypothesize that sacoglossans achieve lecithotrophy at smaller egg sizes than do related clades of marine heterobranchs, which may facilitate developmental plasticity that is otherwise vanishingly rare among animals. Insight into the environmental drivers and evolutionary results of shifts in larval type will continue to be gleaned from population-level studies of poecilogonous taxa like E. pusilla, and should inform life-history theory about the causes and consequences of alternative development modes in marine animals.     

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.     

Notes on the reproduction of high-Antarctic molluscs from the Weddell Sea

Summary The reproductive modes of 66 molluscan species from the Weddell Sea, Antarctica were investigated either by rearing of specimens in aquaria (Neomeniomorpha [Solenogastres], Polyplacophora and Gastropoda) or by studies of the larval shell (Bivalvia). The results show that not all marine invertebrates living in cold water environments produce large eggs, provide postspawning parental care or lack planktonic larvae (Thorson's rule), nor that brooding behaviour is always associated with small adult size. Several lecithotrophic (Solenogastres, Polyplacophora) and meroplanktonic, planktotrophic larvae (Gastropoda) were observed in aquaria. Investigations of the larval shell morphology indicate a planktotrophic or lecithotrophic larval stage in 27 Bivalvia species. With exception of two species of meroplanktonic gastropod larvae no developmental stages of benthic molluscs were ever found in plankton hauls in the Weddell Sea. This indicates that most larvae may live demersally. Brooding occurred in 1 Monoplacophora and 17 Bivalvia species. Intracapsular metamorphosis with very long embryonic development was observed in 15 Gastropoda species.     

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.     

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.     

Live history evolution in Serpulimorph polychaetes: a phylogenetic analysis

The widely accepted hypothesis of plesiomorphy of planktotrophic, and apomorphy of lecithotrophic, larval development in marine invertebrates has been recently challenged as a result of phylogenetic analyses of various taxa. Here the evolution of planktotrophy and lecithotrophy in Serpulimorph polychaetes (families Serpulidae and Spirorbidae) was studied using a hypothesis of phylogenetic relationships in this group. A phylogenetic (parsimony) analysis of 36 characters (34 morphological, 2 developmental) was performed for 12 selected serpulid and 6 spirorbid species with known reproductive/developmental strategies. Four species of Sabellidae were used in the outgroup. The analysis yielded 4 equally parsimonious trees of 78 steps, with a consistency index (CI) of 0.654 (CI excluding uninformative characters is 0.625). Under the assumption of unweighted parsimony analysis, planktotrophic larvae are apomorphic and non-feeding brooded embryos are plesiomorphic in serpulimorph polychaetes. The estimated polarity of life history transitions may be strengthened by further studies demonstrating an absence of a unidirectional bias in planktotrophy-lecithotrophy transition in polychaetes.     

Anti-tubulin labeling reveals ampullary neuron ciliary bundles in opisthobranch larvae and a new putative neural structure associated with the apical ganglion

This investigation examines tubulin labeling associated with the apical ganglion in a variety of planktotrophic and lecithotrophic opisthobranch larvae. Emphasis is on the ampullary neurons, in which ciliary bundles within the ampulla are strongly labeled. The larvae of all but one species have five ampullary neurons and their associated ciliary bundles. The anaspid Phyllaplysia taylori, a species with direct development and an encapsulated veliger stage, has only four ampullary neurons. The cilia-containing ampulla extends to the pretrochal surface via a long, narrow canal that opens to the external environment through a very small pore (0.1 microm diameter). Cilia within the canal were never observed to project beyond the opening of the apical pore. The ampullary canals extend toward and are grouped with the ciliary tuft cells and remain in this location as planktotrophic larvae feed and grow. If, as has been reported, the ciliary tuft is motile, the pores may be continually bathed in fresh seawater. Such an arrangement would increase sensitivity to environmental chemical stimuli if the suggested chemosensory function of these neurons is correct. In general, ciliary bundles of newly hatched veligers are smaller in planktotrophic larvae than in lecithotrophic larvae. In planktotrophic larvae of Melibe leonina, the ciliary bundles increase in length and width as the veligers feed and grow. This may be related to an increase in sensitivity for whatever sensory function these neurons fulfill. An unexpected tubulin-labeled structure, tentatively called the apical nerve, was also found to be associated with the apical ganglion. This putative nerve extends from the region of the visceral organs to a position either within or adjacent to the apical ganglion. One function of the apical nerve might be to convey the stimulus resulting from metamorphic induction to the visceral organs.     

Introduction to symposium: Poecilogony--a window on larval evolutionary transitions in marine invertebrates

Poecilogony is the intraspecific variation in developmental mode that has been described in some marine invertebrates. Poecilogonous species produce different larval forms (e.g., free-swimming planktotrophic larvae as well as brooded lecithotrophic or adelphophagic larvae). Poecilogony can be a controversial topic, since it is difficult to identify and characterize the phenomenon with certainty. It has been challenging to determine whether poecilogony represents developmental polymorphism with a genetic basis or developmental polyphenism reflecting plastic responses to environmental cues. Other outstanding questions include whether common mechanisms underlie the developmental variation we observe in poecilogonous species, and whether poecilogony is maintained in different taxa through similar mechanisms or selective pressures. Poecilogonous species provide a unique opportunity to elucidate the cellular, developmental, and genetic mechanisms underlying evolutionary transitions in developmental mode, as well as to help clarify the selective pressures and possible ecological circumstances that might be involved. Here, we describe an integrative approach to the study of poecilogony and its role in larval evolutionary transitions highlighted during a symposium held at the 2012 annual meeting of the Society for Integrative and Comparative Biology.     

The transition from planktotrophy to lecithotrophy in larvae of Lower Palaeozoic Rhynchonelliform brachiopods

Criteria are established for defining the presence of protegula formed on embryonic or larval mantle in representative genera of Lower Palaeozoic Obolellata, Strophomenata and Rhynchonellata. Width was used to define protegular type. Taxa with only an embryonic protegulum are inferred to have had lecithotrophic larvae while taxa with a larval protegulum or an embryonic protegulum surrounded by a larval protegulum are inferred to have had planktotrophic larvae. All or most of the taxa examined in the Obolellata, the Strophomenata and the orders Protorothida and Orthida in the Rhynchonellata had planktotrophic larvae. In the Pentamerida a minority of genera had only a larval, or an embryonic and a larval protegulum while a majority had protegular widths indicating lecithotrophy. In the orders Rhynchonellida, Atrypida, Athyrida and Spiriferida derived from the Pentamerida (with the exception of one species in the Atrypida) a number of the genera had protegular widths indicating lecithotrophy. It is suggested that the onset of lecithotrophy in the Pentamerida was associated with a developmental innovation in which the mantle lobe of the larva was reflected over the apical lobe during the process of metamorphosis. This evolutionary innovation probably occurred during the late Cambrian or early Ordovician and was subsequently inherited during the process of cladogenesis.     

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.     

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.     

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 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.     

Structure of the first-formed shell of the Middle Ordovician orthid-like brachiopods from the Leningrad Region

Shell structure of the first-formed shell of the Middle Ordovician orthid-like brachiopods from the Leningrad Region is described. The 190-μm-wide first-formed shell is composed of finely granular layer while 700-μm-wide first-formed shell is fibrous. Thus the order Orthida in the Early Paleozoic included brachiopods with both planktotrophic and lecithotrophic larvae in the ontogeny.