Heterochrony and the evolution of poecilogony: generating larval diversity

Poecilogony is the production of more than one type of young within a single species of marine invertebrate. We chose a poecilogonous polychaete to investigate potential differences in morphogenesis among offspring that are polymorphic in dispersal potentials (planktonic, benthic) and trophic modes (planktotrophy, adelphophagy). Differences in morphogenesis occur and are strongly influenced by maternal type. Females that provide extra-embryonic nutrition (as nurse eggs; type III females) also produce offspring with an accelerated onset of juvenile traits, relative to planktotrophic offspring of females that do not provide extra-embryonic nutrition (type I females). Thus, progeny of some females appear morphologically preadapted for a benthic lifestyle. Surprisingly, differences in phenotype among offspring do not parallel offspring ecotype, as offspring with early onset of juvenile traits (III) are ecologically bimodal. Some Type III offspring eat the nurse eggs (adelphophagy), have accelerated development, and hatch as benthic juveniles. In contrast, their siblings hatch as small, planktotrophic, dispersive larvae that are morphologically similar to their type III siblings, but ecologically similar to Type I planktotrophic larvae. We propose that poecilogony evolved through sequence heterochrony in morphogenesis with accelerated onset of juvenile traits in type III offspring. In addition, we suggest that heterochrony in life-history events (hatching, metamorphosis) also occurs, thereby generating offspring that are dimorphic in both phenotype and ecotype. Over time, selection acting on different levels of ontogeny (morphogenesis vs. dispersal) may balance this polymorphism and allow poecilogony to persist.     

Observations of serotonin and FMRFamide-like immunoreactivity in palp sensory structures and the anterior nervous system of spionid polychaetes

Evidence suggests that ciliated sensory structures on the feeding palps of spionid polychaetes may function as chemoreceptors to modulate deposit-feeding activity. To investigate the probable sensory nature of these ciliated cells, we used immunohistochemistry, epi-fluorescence, and confocal laser scanning microscopy to label and image sensory cells, nerves, and their organization relative to the anterior central nervous system in several spionid polychaete species. Antibodies directed against acetylated alphatubulin were used to label the nervous system and detail the innervation of palp sensory cells in all species. In addition, the distribution of serotonin (5-HT) and FMRFamide-like immunoreactivity was compared in the spionid polychaetes Dipolydora quadrilobata and Pygospio elegans. The distribution of serotonin immunoreactivity was also examined in the palps of Polydora cornuta and Streblospio benedicti. Serotonin immunoreactivity was concentrated in cells underlying the food groove of the palps, in the palp nerves, and in the cerebral ganglion. FMRFamide-like immunoreactivity was associated with the cerebral ganglia, nuchal organs and palp nerves, and also with the perikarya of ciliated sensory cells on the palps.     

Ultrastructural studies of dorsal ciliated organs in Spionidae (Annelida: Polychaeta)

The distribution and structural components of dorsal ciliated organs (dco) in 15 species of the Spionidae were studied by scanning- and transmission electron microscopy. Based on the distribution patterns of dco, the investigated species are divided into four non-systematic groups: (I) paired anterior dco, (II) paired dco extending posteriorly for several chaetigers, (III) paired anterior dco in combination with unpaired, sexually dimorphic, metameric dco, and (IV) paired anterior dco in combination with paired, metameric dco. Previous ultrastructural studies have only included species possessing organs of groups I and III. In the present investigation the ultrastructure of dco found in Laonice bahusiensis and Spio cf. filicornis (species with dco of groups II and IV) is studied in an attempt to consider their homology. Apart from the metameric dco of group III, similarities of the cellular components of the dco indicate a homology to nuchal organs.     

Chaetal arrangement and chaetogenesis of hooded hooks in Lumbrineris (Scoletoma) fragilis and Lumbrineris tetraura (Eunicida,Annelida)

As the structure and arrangement of chaetae are highly specific for annelid species and higher taxonomic entities, we assume that rather conservative information guarantees formation of specific chaetae. Each chaeta of an annelid is formed within an ectodermal invagination, and the modulation of the apical microvilli pattern of the basalmost cell of this invagination determines the structure of the chaeta. Any hypothesis of the homology of chaetae could thus be tested by examining the process of chaetal formation. Investigations into the ultrastructure and formation of hooded hooks in different capitellids and spionids revealed that these chaetae can be homologized. The hood of each of their hooded hooks is formed by elongation of two rings of microvilli peripheral to the chaetal anlage, which give rise to the inner and outer layers of the hood. The hood layers are well separated and surround an empty space. Superficially similar hooded hooks are described for certain Eunicida. Presently available cladistic analyses suggest that the hooded hooks of eunicidans evolved independently of those in Capitellidae and Spionidae. Compared with the latter two families, we therefore expected to find differences in chaetogenesis of the hooded hooks in the eunicids Lumbrineris (Scoletoma) fragilis and Lumbrineris tetraura (Lumbrineridae). This was the case. In these eunicidans, the hood was formed by the bisected apical wall of the chaetoblast right after the mid‐apical section of the chaeta had been sunk deeply into the chaetoblast during its formation. The apical wall generated a brush of microvilli that preformed the hood. Because the microvilli of the hood showed some accelerated differentiation, they soon merged with those of the slowly growing setal shaft to form the broad manubrium of the hooded hook in lumbrinerids. Our study confirms the predicted differences in chaetogenesis of the superficially similar hooded hooks of capitellids and spionids compared with those of eunicids.     

Atherospio guillei (Laubier and Ramos, 1974) comb. nov. (Polychaeta: Spionidae) and closest relatives

Atherospio guillei (Laubier and Ramos, 1974) comb. nov. is redescribed based on new material collected during a benthic survey in the German Bight, North Sea. Main characteristics of this species are a deeply incised prostomium, modified neurochaetae on chaetiger 5 superior to a small bundle of capillaries, branchiae fully fused to notopodial lamellae with digitiform distal process from chaetiger 7 over a limited number of succeeding chaetigers, predominately unidentate curved hooks with closely applied sheath from chaetiger 13-15 and a pygidium surrounded by several pairs of lateral cirri. Atherospio is closely related to Pygospiopsis and Pseudatherospio. Interrelationships of these genera are discussed.     

Feeding responses to particle-bound cues by a deposit-feeding spionid polychaete, Dipolydora quadrilobata (Jacobi 1883)

In marine soft-sediment habitats, chemical sensing by deposit-feeding organisms most likely plays a critical role in feeding behavior, yet, few specifics about this role and its ecological implications are known. We show that several particle-bound chemical cues stimulate feeding activity of a spionid polychaete Dipolydora quadrilobata (Jacobi 1883). Using glass beads as a proxy for sediment, we tested for feeding responses to a selected number of potential cues that might be used to indicate food availability or quality. We presented two sets of beads to individual intact worms: one with and one without covalently bound compounds such as single amino acids, mixtures of amino acids, and single simple sugars. Worms were exposed to the beads under slow flowing seawater so that any dissolved cues were flushed from the test chamber. Each worm was videotaped for 15 min immediately following the addition of beads, and these records were scored for the time the worm spent in a variety of behaviors. Responses to beads with and without cues were compared to identify compounds as stimulatory, inhibitory, or inactive. Five of the seven particle-bound cues tested significantly increased feeding activity, and none of those tested were found to be inhibitory.     

Morphological variation in Polydora ciliata complex (Polychaeta: Annelida)

Intraspecific variation in Polydora ciliata (Johnston) was assessed on the basis of evidence from morphological characters, which were studied by scanning electron microscopy. Differences were observed between populations of P. ciliata with respect to the setae of the fifth modified segment and in the caruncle. Two other species, namely P. ligni Webster and P. limicola (Annenkova), were also studied in order to assess interspecific variation. The two forms of P. ciliata , that is boring and non-boring, were found to be different morphologically.     

Ultrastructure of spermiogenesis and synthesis of enigmatic cytoplasmic inclusions in the spirally shaped spermatozoon of the polychaete Spio setosa (Annelida: Spionidae)

The sperm of Spio setosa (Polychaeta, Spionidae) are known to be very unusual in form; here, spermiogenesis and the structure of the spermatozoon in this species are described by transmission electron microscopy. While spermiogenesis is similar to that described for many other polychaetes, two notable exceptions to this process include the synthesis of abundant ring‐shaped and tubular, membrane‐bounded cytoplasmic inclusions in the midpiece, and the differentiation of a spirally shaped sperm head. Spermatids develop as free‐floating tetrads in the male's coelom. A microtubular manchette does not develop during chromatin condensation and nuclear elongation, and the spiral acrosome forms as a single Golgi‐derived vesicle that migrates anteriorly to become housed in a deep anterior nuclear fossa. Early in spermiogenesis, numerous Golgi‐derived, membrane‐bounded cytoplasmic inclusions appear in the cytoplasm; these ultimately occupy the sperm midpiece only. The mature spermatozoon in the male has a 15‐μm‐long head consisting of a nucleus coiled like a spring and a spiral acrosome with differentiated substructure, the posterior two thirds of which sits in an anterior nuclear fossa. The midpiece is wider than the rest of the spermatozoon and contains 9–10 spherical mitochondria surrounding the two centrioles, as well as numerous membrane‐bounded conoid and tubular cytoplasmic inclusions. The axoneme has a 9 + 2 arrangement of microtubules. By contrast, stored sperm in the female's seminal receptacles have lost the midpiece inclusions but contain an abundance of glycogen. The function of the midpiece inclusions remains unresolved, and the significance of their absence in stored sperm within the seminal receptacle and the appearance of midpiece glycogen stores remains unclear and requires additional investigation.