Bruno Pernet

Intermediate Modes of Larval Development: Bridging the Gap between Planktotrophy and Lecithotrophy

SUMMARY The extraordinary diversity of larval form and function in marine invertebrates has motivated many studies of development, ecology, and evolution. Among organisms with pelagic development via a larval stage, this diversity is often reduced to a dichotomy between two broad nutritional categories: planktotrophy and lecithotrophy. Despite the clear utility of the planktotrophy–lecithotrophy dichotomy to those interested in the history or consequences of life history patterns, it is also clear that a number of larval forms do not fit neatly into either of these general categories. Here we review studies of these intermediate larval forms, focusing on descriptions of larvae known as facultative feeders. Recent descriptions of larval development suggest that facultative feeders and other intermediate larval forms are not as rare as commonly assumed. We assess the importance of these forms for models of life‐history evolution and call for a more‐detailed and nuanced view of larval biology to account for their existence. Clearer knowledge of the phylogenetic distribution and frequency of occurrence of larvae that exhibit intermediate nutritional requirements is also essential for evaluating current ideas on evolutionary transitions between planktotrophy and lecithotrophy. Finally, intermediate larval types provide valuable and underutilized opportunities for testing hypotheses in the fields of larval ecology and the evolution of development.

Persistent Ancestral Feeding Structures in Nonfeeding Annelid Larvae

Evolutionary loss of the requirement for feeding in larvae of marine invertebrates is often followed by loss of structures involved in capturing and digesting food. Studies of echinoderms suggest that larval form evolves rapidly in response to loss of the requirement for feeding, but a lack of data from other taxa makes it difficult to assess the generality of this result. I show that many members of a large clade of annelids, the Sabellidae, retain ancestral systems for particle capture despite loss of the need and ability to feed. In at least one species, Schizobranchia insignis, an opposed-band system of prototrochal, food-groove, and metatrochal ciliary bands can concentrate suspended particles and transport them to the mouth, but captured particles are invariably rejected because larvae lack a functional gut. The persistence of particle capture systems in larvae of sabellids suggests that they have lost larval feeding very recently, that opposed bands are inexpensive to construct and operate, or that opposed bands have some alternative function. These observations also suggest a hypothesis on how the ability to feed is lost in larvae of annelids and other spiralians following increases in egg size.

Gamete interactions and genetic differentiation among three sympatric polychaetes

The evolution of gamete incompatibility between free‐spawning marine invertebrate species has been explained by three hypotheses: (1) independent divergence at gamete recognition loci; (2) selection against hybrids; and (3) a process of sexual selection involving polymorphic gamete recognition loci (Metz and Palumbi 1996). The first two hypotheses predict that gamete incompatibility appears only after gene flow has been halted for other reasons and the third that gamete incompatibility appears simultanously with blocks to gene flow. Here I show that gametes of three sympatric polychaetes in the genus Arctonoe are compatible in all crosses, over a broad range of gamete concentrations and contact times. Although at least some hybrid crosses produce fertile adults, allozyme and mitochondrial DNA sequence data indicate that the three species do not regularly exchange genes. These data are consistent with predictions of the first two hypotheses for the evolution of gamete incompatibility, but allow rejection of the third hypothesis. Gametes of the three species are compatible despite estimated divergence times of 1–3 M.Y.B.P.; in several other marine invertebrates, divergence times of the same magnitude are associated with asymmetric or complete gamete incompatibility. It appears likely that segregation of symbiotic adults on their respective host species restricts mating opportunities, and thus gene flow, among Arctonoe species.

Capture of Large Particles by Suspension-Feeding Scaleworm Larvae (Polychaeta: Polynoidae)

Most of the polychaete larvae in which feeding mechanisms have been studied feed using an opposed-band mechanism, capturing particles with prototrochal and metatrochal ciliary bands and transporting them to the mouth via a food groove. However, many other planktotrophic polychaete larvae lack a metatroch and food groove and thus must feed in a different way. In this latter group are the larvae of polynoid polychaetes, which not only lack a metatroch and food groove but also bear a bundle of long cilia (the oral brush) attached near the left side of the mouth. In feeding experiments with polystyrene beads and plankton, larvae of the polynoid Arctonoe vittata ingested larger particles (up to 60 {mu}m in diameter) than those ingested by the opposed-band feeding larvae of the serpulid Serpula vermicularis (up to 12 μm in diameter). Videotaped images of feeding A. vittata larvae showed that capture behavior was elicited as particles in a feeding current driven by the prototroch approached or contacted the larval episphere. Particles on or very near the episphere were disengaged by a recoiling motion of the larva and were then moved to the mouth, probably by the oral brush. This feeding mechanism may be widespread in the polychaete superfamily Aphroditacea, which includes about 10% of extant polychaete species.

Size and Organic Content of Eggs of Marine Annelids, and the Underestimation of Egg Energy Content by Dichromate Oxidation

Dichromate oxidation is a simple technique that is often used to estimate the energy content of eggs in studies of marine invertebrate life histories (1). We used this method to measure the energy contents of the eggs of 12 species of marine annelids. In combination with measures of egg ashfree dry weight (AFDW), these data yielded estimates of AFDW-specific energy density that were mostly lower than the average weight-specific energy density of carbohydrates. This seemed unlikely to be correct, as invertebrate eggs typically contain little carbohydrate and instead are composed primarily of energy-dense protein and lipid (1, 2). After validating our methods (by using them to estimate energy content and AFDW of the eggs of a previously studied echinoderm) and reexamining published data on the energy contents of echinoderm eggs, we conclude that dichromate oxidation often underestimates the energy contents of small eggs of marine invertebrates. This systematic error, which is likely related to the tendency of the assay to incompletely oxidize proteins, can only be corrected with substantial independent data on egg biochemical composition. We thus suggest that dichromate oxidation should not be used for routine measurement of the total energy content of marine invertebrate eggs. Maternal investment of energy per offspring is a variable of fundamental importance in models of the evolution of life histories (3, 4). It is relatively easy to quantify in freespawning marine invertebrates, where maternal investment is primarily limited to the organic material provided in the egg. Among echinoderms, egg energy and organic content

Functional and Evolutionary Implications of Opposed Bands, Big Mouths, and Extensive Oral Ciliation in Larval Opheliids and Echiurids (Annelida)

Larvae of two annelids, the opheliid Armandia brevis and the echiurid Urechis caupo, captured small particles between opposed prototrochal and metatrochal ciliary bands and also captured large particles with wide ciliated mouths. The body volume of larval A. brevis increased more rapidly than the estimated maximum clearance rate as segments were added. Capture of larger particles by late-stage larvae may compensate for this potentially unfavorable allometry. The existence of larvae that use two feeding mechanisms at once, not previously known in annelids, suggests possible evolutionary routes between larval forms that feed only with opposed bands (e.g., serpulids and oweniids) and those that use complex oral ciliature to feed primarily on large particles (e.g., polynoids and nephtyids). In particular, the metatroch and food groove of opposed-band feeders may have arisen as expansions of oral ciliation in ancestral large-particle feeders; alternatively, extensive oral ciliation in large-particle feeders may have originated as a modification of metatroch and food-groove cilia in ancestral opposed-band feeders.

Escape Hatches for the Clonal Offspring of Serpulid Polychaetes

Serpulid polychaetes in the genera Filograna and Salmacina reproduce asexually by releasing a single bud at a time from their posterior ends into their calcareous tubes. Here I show that buds of Salmacina amphidentata gain access to the exterior of these tubes via escape hatches built into the tubes by the parent worms. Each escape hatch consists of a hole in the tube blocked by a calcareous disc that is supported in place by an organic membrane. After buds detach from their parents, the calcareous discs are dislodged, and buds begin to form their own tubes from the resulting openings. Repeated bouts of asexual reproduction result in the formation of aggregations of branched tubes. A survey of Filograna and Salmacina spp. from the Atlantic, Indian, and Pacific oceans suggests that the formation of escape hatches for clonal offspring is common to many members of these genera.

Evolutionary changes in the timing of gut morphogenesis in larvae of the marine annelid Streblospio benedicti

SUMMARY The planktonic larvae of marine invertebrates are diverse in their nutritional modes, suggesting that evolutionary transitions in larval nutritional mode have been frequent. One approach to identifying the developmental changes that play important roles in such transitions is to compare “intermediate” larval forms to closely related larvae representative of their common ancestor. Here we make such a comparison between obligately planktotrophic and facultatively feeding larvae of the poecilogonous polychaete annelid Streblospio benedicti. We used feeding experiments to show that the derived, facultatively feeding larvae of this species develop the ability to feed at a later developmental stage (five muscle bands) than planktotrophic larvae (two to three muscle bands). This delay in the onset of feeding ability does not appear to be caused by delay in the formation of particle capture structures, but instead by delay in the development of a continuous, functional gut. These observations are consistent with the hypothesis that evolutionary increases in egg size in annelids lead predictably to heterochronic delays in gut development, and hence to transitions in larval nutritional mode.

Opposed Ciliary Bands in the Feeding Larvae of Sabellariid Annelids

The larvae of marine annelids capture food using an unusual diversity of suspension-feeding mechanisms. Many of the feeding mechanisms of larval annelids are poorly known despite the abundance and ecological significance of both larvae and adults of some annelid taxa. Here we show that larvae of two species of sabellariid annelids, Sabellaria cementarium and Phragmatopoma californica, bear prototrochal and metatrochal cilia that beat in opposition to each other. For larvae of S. cementarium, we provide evidence that these opposed bands of cilia are used to capture suspended particles. In video recordings, captured particles were overtaken by a prototrochal cilium and then moved with the cilium to the food groove, a band of cilia between the prototroch and metatroch. They were then transported by cilia of the food groove to the mouth. Lengths of the prototrochal cilia, lengths of the prototrochal ciliary band, size range of the particles captured, and estimated rates of clearance increased with larval age and body size. Confirmation of the presence of opposed bands in larvae of sabellariids extends their known occurrence in the annelids to members of 10 families. Opposed bands in these different taxa differ in the arrangements and spacing of prototrochal and metatrochal cilia, and in whether they are used in combination with other feeding mechanisms. Opposed bands appear to be particularly widespread among the larvae of sabellidan annelids (a clade that includes sabellariids, sabellids, and serpulids), even in some species whose larvae do not feed. A parsimony analysis suggests that opposed bands are ancestral in this clade of annelids.

Kilometer-scale Spatial Variation in Prevalence of the Rhizocephalan Lernaeodiscus porcellanae on the Porcelain Crab Petrolisthes cabrilloi

Abstract We studied spatial variation in the prevalence of the rhizocephalan barnacle Lernaeodiscus porcellanae on its porcelain crab host, Petrolisthes cabrilloi, at four southern California intertidal sites separated by only a few km. The prevalence of rhizocephalan externae varied significantly among sites in 2008-2009, with the southernmost site, White Point, consistently showing higher prevalence than the others. Externa prevalence was a good proxy of estimated true prevalence, i.e., the prevalence of rhizocephalans as a whole, not just those that had formed externae. We examined several hypotheses that might explain the observed spatial variation in prevalence. Host susceptibility to infection (indicated by the proxy of damage to host limbs, some of which are used to remove parasite infective stages), did not differ among sites. At all sites, prevalence was slightly higher in female crabs than in males, and the sex ratio at White Point was slightly female-biased while that at the other sites was male-biased; thus, among-site differences in sex ratio did contribute to observed variation in prevalence. However, most spatial variation in prevalence appeared to be due to the effect of host size. At all sites the probability of infection increased with increasing host size, and White Point crabs were on average much larger than crabs at other sites. Overall, the size-class distribution of host crabs explained 80.4% of the variation in prevalence of L. porcellanae. Larger P. cabrilloi have likely had greater opportunity to be infected by rhizocephalans, either because they are older, or because they have undergone more molts, during which they are especially vulnerable to infection. A deeper understanding of small-scale spatial variation in prevalence in L. porcellanae will require information on the causes of among-site variation in host population size structure.