Molecular phylogenetics of the siphonophora (Cnidaria), with implications for the evolution of functional specialization

Siphonophores are a group of pelagic colonial hydrozoans (Cnidaria) that have long been of general interest because of the division of labor between the polyps and medusae that make up these "superorganisms." These polyps and medusae are each homologous to free living animals but are generated by an incomplete asexual budding process that leaves them physiologically integrated. They are functionally specialized for different tasks and are precisely organized within each colony. The number of functional types of polyps and medusae varies across taxa, and different authors have used this character to construct phylogenies polarized in opposite directions, depending on whether they thought siphonophore evolution proceeded by a reduction or an increase in functional specialization. We have collected taxa across all major groups of siphonophores, many of which are found exclusively in the deep sea, using remotely operated underwater vehicles (ROVs) and by SCUBA diving from ships in the open ocean. We have used 52 siphonophores and four outgroup taxa to estimate the siphonophore phylogeny with molecular data from the nuclear small subunit ribosomal RNA gene (18S) and the mitochondrial large subunit ribosomal RNA gene (16S). Parsimony reconstructions indicate that functionally specialized polyps and medusae have been gained and lost across the phylogeny. Maximum likelihood and Bayesian analyses of morphological data suggest that the transition rate for decreased functional specialization is greater than the transition rate for increased functional specialization for three out of the four investigated categories of polyps and medusae. The present analysis also bears on several long-standing questions about siphonophore systematics. It indicates that the cystonects are sister to all other siphonophores, a group that we call the Codonophora. We also find that the Calycophorae are nested within the Physonectae, and that the Brachystelia, a historically recognized grouping of short-stemmed taxa, are polyphyletic. [Cnidaria; colonial animals; deep sea; division of labor; functional specialization; Hydrozoa; phylogenetics; Siphonophores.].     

The distribution of siphonophores in a transect across the North Atlantic Ocean at 32°N

A study has been made of the distribution of siphonophores in a series of twelve oblique (0–1000 m) hauls made in a transect across the North Atlantic at 32°N, from 16°W to 60°W. A total of 66 species was identified, of which twelve were physonect siphonophores and the remainder calycophorans. In order to assess the changes in the population of the nineteen most abundant species, the species correlation coefficient matrix was calculated and six factors were extracted and rotated to simple structure. The first two factors indicated a clear east-west trend in the distributional pattern for thirteen of these siphonophore species. The coefficient of proportional similarity between stations was also calculated using the data for all of the species present.From this it was possible to divide the stations into two clear zones, namely the first three and the last eight, while the fourth station was intermediate. A comparison of these results with the TSD data for these stations showed that the fourth station was in the transitional zone between the eastern North Atlantic water and that characteristic of the Sargasso Sea, and that these two major water masses were distinguishable at all the depths where siphonophores would be expected to be found. It is concluded that there was some interrelationship between the physical features of the separate water masses and the composition of the siphonophore populations found in each. The problems involved in deciding on a sampling programme for such a study as this are also discussed.     

Siphonophores of upwelling areas of the Campeche Bank and the Mexican Caribbean Sea

The siphonophore fauna off the Yucatan Peninsula and in the Mexican Caribbean Sea remains practically unknown. This communication describes the composition, abundance and distribution of Siphonophora during summer 1984 and spring 1985. The local distribution and abundance of siphonophores were found to be strongly influenced by upwellings, especially during the spring survey. Community analysis suggests that siphonophore populations around the upwellings are relatively homogeneous.     

Siphonophores off a riverine system in the southern Gulf of Mexico: factors affecting their distribution and spatial niche breadth and overlap

Environmental factors determining the spatial pattern of the whole siphonophore community, as well as the hydrological occurrence ranges, small-scale vertical distribution, and spatial niche breadth and overlap of 23 siphonophore species collected off a riverine system in the southern Gulf of Mexico were analysed. A total of 149 zooplankton samples were collected in different strata of the water column (from 0 to 100 m) over a grid of 23 oceanographic stations during low (April) and high (October) rainy periods. Temperature and salinity measurements were taken with a CTD probe. Considering both seasons, salinity fluctuated between 30.7 and 37.0, and temperature between 18.2 and 29.0°C. Under these conditions, the hydrological occurrence ranges of species were analysed. Data on siphonophore biovolumes in the upper 30-m layer were subjected to a regression tree (RT) analysis taking the zooplankton biomass, the distance to the shore, the temperature, and the salinity as predictable variables. Results of the RT analysis showed that the distance from the shore, food availability, and temperature were among the most important factors affecting siphonophore spatial distribution. Food availability had a positive influence on the siphonophores distribution, whereas temperatures higher than 28.1°C seemed to depress most siphonophore populations. Diphyes dispar moderately dominated the community and represented 30% of the total biovolume. The calycophorans Abylopsis tetragona, A. eschscholtzi, Diphyes bojani, and Chelophyes appendiculata were the most generalist species as revealed by their niche breadth values, and Enneagonum hyalinum endured the widest salinity conditions (30.7–37.0) and was mainly distributed in coastal waters. The second most abundant species, the physonect Agalma okeni, exhibited a low mean niche overlap value with the calycophoran species. We hypothesise that differences in diet composition between physonects and calycophorans are the main cause of those low niche overlap values.     

Co-occurrence of hippopodiid siphonophores and their potential prey

It is a truism that the distribution of a predator should reflect that of its potential prey, but this is not well established for marine plankton communities. Purcell (1981) found that many siphonophore species were selective feeders and that one, Hippopodius hippopus, fed exclusively on ostracods. Pugh (1986) speculated that if such a dietary specificity also applied to other hippopodiid species, then a distributional relation between them and ostracods might be expected. This premise is examined using data from Discovery stations in the N.E. Atlantic Ocean. A clear relation is found between the abundance of ostracods and hippopodiids, while copepods have a better relation with other calycophoran siphonophores.     

Seasonal abundance and vertical distribution of mesopelagic calycophoran siphonophores in Monterey Bay, CA

The seasonal abundance and vertical distribution patterns ofa group of small calycophoran siphonophores (principally Chuniphyesmultidentata and Lensia conoidea) were investigated using aremotely operated vehicle (ROV) deployed in Monterey Bay, California.Abundance was assessed along 295 horizontal transects coveringa depth range of 100–1000 m over a three and a half yearperiod. The vertical distribution of the study animals changedseasonally, coupled to the onset and cessation of upwellingin the bay. While numerical abundance peaked after upwelling,there was no significant difference between seasons. The siphonophoreswere more broadly distributed over the depth range sampled duringthe upwelling or Shallow Mixed Layer (SML) period, than duringthe non-upwelling or Deep Mixed Layer (DML) period. There wereno significant differences in abundance or distribution patternsbetween years except in 1993, when there were significantlymore siphonophores observed during the SML period than duringthe DML period. This may reflect effects resulting from the1992–1993 El Niño event. The abundance of thesesiphonophores was negatively correlated with that of Nanomiabijuga, a physonect siphonophore of similar size and feedingbehavior found in the bay. The siphonophores studied here appearfrom preliminary data to migrate vertically, possibly with twoseparately migrating groups.     

Strategies for sperm chemotaxis in the siphonophores and ascidians: a numerical simulation study

Chemotactic swimming behaviors of spermatozoa toward an egg have been reported in various species. The strategies underlying these behaviors, however, are poorly understood. We focused on two types of chemotaxis, one in the siphonophores and the second in the ascidians, and then proposed two models based on experimental data. Both models assumed that the radius of the path curvature of a swimming spermatozoon depends on [Ca(2+)](i), the intracellular calcium concentration. The chemotaxis in the siphonophores could be simulated in a model that assumes that [Ca(2+)](i) depends on the local concentration of the attractant in the vicinity of the spermatozoon and that a substantial time period is required for the clearance of transient high [Ca(2+)](i). In the case of ascidians, trajectories similar to those in experiments could be adequately simulated by a variant of this model that assumes that [Ca(2+)](i) depends on the time derivative of the attractant concentration. The properties of these strategies and future problems are discussed in relation to these models.     

Honey bee colonies are group-level adaptive units

It is not widely recognized that natural selection has produced adaptive units at the level of groups. Multilevel selection theory shows that groups can evolve a high level of functional organization when between-group selection predominates over within-group selection. Strong empirical evidence that natural selection has produced adaptive units at the group level comes from studies of social insects in which we find colonies in certain species functioning as highly integrated units. The functional organization of a social insect colony is best understood for honey bees. Recent experimental analyses of honey bee colonies have revealed striking group-level adaptations that improve the foraging efficiency of colonies, including special systems of communication and feedback control. These findings are reviewed with the aim of showing that evolution has produced adaptively organized entities at the group level.     

Changes in the population structure,growth and mortality of striped weakfish <Emphasis Type="Italic">Cynoscion guatucupa</Emphasis> (Sciaenidae,Teleostei) of southern Brazil between 1976 and 2002

Siphonophores are exclusively marine cnidaria and their predatory role in plankton food-webs is well recognised. In this study, we analyse the structure and the spatial extent of siphonophore assemblages in relation to changes in freshwater outflows and food availability in the southern Gulf of Mexico during a high (October) and a low (April) outflow periods. A total of 149 samples were collected using a 505 μm multiple closing net at 1–6 levels (0–100 m) of the water column, depending on the bathymetry. Data on siphonophore species biovolumes (ml 100 m⁻³) were treated by means of the Bray-Curtis Dissimilarity Index, and two distinctive assemblages were identified: the ‘inner’ and the ‘outer’ assemblages, located over the inner and outer shelves. Temperature, salinity, zooplankton biomass, and siphonophore species were included in a Principal Component Analysis (PCA) to identify the factors associated with each assemblage. Geographical distribution of the assemblages practically remained the same during both seasons and its cross-shelf variability was stronger than the vertical one. Seasonally, diversity values were higher in October, when the highest river discharges occur. Spatially, the lowest diversity and mean siphonophore biovolumes values were registered in the ‘inner assemblage’, where the highest and lowest salinity values were recorded. We suggest that even when extreme salinity values (>36.5 or <34) might depress siphonophore populations in the coastal area, enough food availability in the concerned areas might mitigate the negative effect of salinity, since a positive and significant (p < 0.05) relationship was found between siphonophores biovolume and zooplankton biomass. Bassia bassensis, Diphyes dispar and Enneanogum hyalinum, present in both assemblages during both seasons, were able to survive in a wide range of salinity values, following perhaps, their prey. All the 23 species here registered were found in the ‘outer assemblage’; however, Abylopsis eschscholtzi, Chelophyes appendiculata and Diphyes bojani were more associated with the ‘outer’ group according to the PCA results. Enneagonum hyalinum was the only species frequently encountered and abundant in the ‘inner assemblage’ during both seasons and, supporting previous observations, this species might be considered as an indicator of nearshore waters. Handling editor: K. Martens     

Societies to genes: can we get there from here?

Understanding the organization and evolution of social complexity is a major task because it requires building an understanding of mechanisms operating at different levels of biological organization from genes to social interactions. I discuss here, a unique forward genetic approach spanning more than 30 years beginning with human-assisted colony-level selection for a single social trait, the amount of pollen honey bees (Apis mellifera L.) store. The goal was to understand a complex social trait from the social phenotype to genes responsible for observed trait variation. The approach combined the results of colony-level selection with detailed studies of individual behavior and physiology resulting in a mapped, integrated phenotypic architecture composed of correlative relationships between traits spanning anatomy, physiology, sensory response systems, and individual behavior that affect individual foraging decisions. Colony-level selection reverse engineered the architecture of an integrated phenotype of individuals resulting in changes in the social trait. Quantitative trait locus (QTL) studies combined with an exceptionally high recombination rate (60 kb/cM), and a phenotypic map, provided a genotype–phenotype map of high complexity demonstrating broad QTL pleiotropy, epistasis, and epistatic pleiotropy suggesting that gene pleiotropy or tight linkage of genes within QTL integrated the phenotype. Gene expression and knockdown of identified positional candidates revealed genes affecting foraging behavior and confirmed one pleiotropic gene, a tyramine receptor, as a target for colony-level selection that was under selection in two different tissues in two different life stages. The approach presented here has resulted in a comprehensive understanding of the structure and evolution of honey bee social organization.     

Morphology and phylogeny of the pseudocolonial dinoflagellates Polykrikos lebourae and Polykrikos herdmanae n. sp

Both the photosynthetic and heterotrophic forms of the only known marine benthic (sand-dwelling) species of Polykrikos, namely P. lebourae, were investigated using light and electron microscopy and molecular phylogenetic analyses. The pseudocolonies usually contained eight integrated zooids and two nuclei. Pseudocolonies consisting of four or five zooids and one nucleus were observed for the first time for this species; some of these reduced pseudocolonies contained plastids, while others were heterotrophic and contained taeniocyst-nematocyst complexes. The ultrastructure of the plastids in P. lebourae did not conform to the organization of thylakoids and enveloping membranes present in the peridinin-containing plastids of other photosynthetic dinoflagellates (i.e. stacks of 3 thylakoids and 3 outer membranes). Instead, the plastids in P. lebourae had thylakoids arranged in pairs and appeared to be enveloped by only two membranes. Molecular phylogenetic data using small subunit rDNA demonstrated that the photosynthetic and heterotrophic forms of P. lebourae represent two distinct clades. The more inclusive clade containing both forms of P. lebourae was most closely related to heterotrophic polykrikoids, namely P. kofoidii. These results led us to conclude that the photosynthetic and heterotrophic forms of P. lebourae are in fact two distinct lineages, and the heterotrophic form is described here as Polykrikos herdmanae n. sp.     

Genetic regulation of colony social organization in fire ants: an integrative overview

Expression of colony social organization in fire ants appears to be under the control of a single Mendelian factor of large effect. Variation in colony queen number in Solenopsis invicta and its relatives is associated with allelic variation at the gene Gp-9, but not with variation at other unlinked genes; workers regulate queen identity and number on the basis of Gp-9 genotypic compatibility. Nongenetic factors, such as prior social experience, queen reproductive status, and local environment, have negligible effects on queen numbers which illustrates the nearly complete penetrance of Gp-9. As predicted, queen number can be manipulated experimentally by altering worker Gp-9 genotype frequencies. The Gp-9 allele lineage associated with polygyny in South American fire ants has been retained across multiple speciation events, which may signal the action of balancing selection to maintain social polymorphism in these species. Moreover, positive selection is implicated in driving the molecular evolution of Gp-9 in association with the origin of polygyny. The identity of the product of Gp-9 as an odorant-binding protein suggests plausible scenarios for its direct involvement in the regulation of queen number via a role in chemical communication. While these and other lines of evidence show that Gp-9 represents a legitimate candidate gene of major effect, studies aimed at determining (i) the biochemical pathways in which GP-9 functions; (ii) the phenotypic effects of molecular variation at Gp-9 and other pathway genes; and (iii) the potential involvement of genes in linkage disequilibrium with Gp-9 are needed to elucidate the genetic architecture underlying social organization in fire ants. Information that reveals the links between molecular variation, individual phenotype, and colony-level behaviors, combined with behavioral models that incorporate details of the chemical communication involved in regulating queen number, will yield a novel integrated view of the evolutionary changes underlying a key social adaptation.     

Coelenterate organs

Cnidaria and ctenophores, though of the ‘tissue grade of construction’, can form organs of considerable complexity, for example the prehensile tentilla of Euplokamis, the erupting nematocyst batteries of the siphonophores Stephanophyes and Nanomia and the complex eyes of cubomedu‐sae such as Carybdea and Tripedalia. The polypoid and medusoid members of siphonophore colonies are functionally equivalent to organs and may be considered as ‘zooid‐derived organs’. There is no reason to regard the lack of a single, dominant nerve centre as a factor constraining organ development in coelenterates.     

Coordination in physonectid siphonophores

Intracellular and extracellular recordings from the stem, gastrozooids, palpons, tentacles and nectophores of physonectid siphonophores are presented. The stem organization previously described for Nanomia applies with only minor differences to Forskalia and Agalma. The endodermal epithelium of the stem is shown to be the pathway for slow potentials.

Pumping cycles and feeding activities are organized locally in gastrozooids and palpons. Protective retractions are coordinated, probably through a direct nervous link with the stem. This is also true of tentacles. The ectoderm of bracts is a conducting epithelium; excitation in it can induce nervous activity in the stem, but the mechanism is unknown.

Impulse traffic between stem and zooids is erratic and breaks down rapidly with repeated stimulation. The motor centres of the nectophores are connected to the stem by a labile nervous link, but an alternative epithelial pathway exists.     

Complete nucleotide sequence and gene rearrangement of the mitochondrial genome of the Japanese pond frog Rana nigromaculata

In this study, we determined the complete nucleotide sequence of the mitochondrial genome of the Japanese pond frog Rana nigromaculata. The length of the sequence of the frog was 17,804 bp, though this was not absolute due to length variation caused by differing numbers of repetitive units in the control regions of individual frogs. The gene content, base composition, and codon usage of the Japanese pond frog conformed to those of typical vertebrate patterns. However, the comparison of gene organization between three amphibian species (Rana, Xenopus and caecilian) provided evidence that the gene arrangement of Rana differs by four tRNA gene positions from that of Xenopus or caecilian, a common gene arrangement in vertebrates. These gene rearrangements are presumed to have occurred by the tandem duplication of a gene region followed by multiple deletions of redundant genes. It is probable that the rearrangements start and end at tRNA genes involved in the initial production of a tandemly duplicated gene region. Putative secondary structures for the 22 tRNAs and the origin of the L-strand replication (OL) are described. Evolutionary relationships were estimated from the concatenated sequences of the 12 proteins encoded in the H-strand of mtDNA among 37 vertebrate species. A quartet-puzzling tree showed that three amphibian species form a monophyletic clade and that the caecilian is a sister group of the monophyletic Anura.     

Quantitative observations on asexual reproduction of Aeolosoma viride (Annelida,Aphanoneura)

Agametic reproductive activity (via paratomy) of Aeolosoma viride was analyzed throughout the life cycle in individually reared specimens. Aeolosoma viride is organized in linear chains of 3–4 zooids; the main zooid is anterior, and the secondary zooids are positioned posterior to the main zooid in inverse order with respect to their degree of growth, the most advanced being at the posterior end, and those less advanced nearer the main zooid. On average, worms lived 66±10 d and produced 57±6 offspring. A budding area located in the sub‐terminal part of the main zooid produced chaetigers that formed the origin of the secondary zooids. A growth zone was located in the posterior end of each secondary zooids. Fission occurred between the penultimate and the last zooid of the chain. Just before fission, the growth zone of each secondary zooid became a budding area. Agametic reproduction was via multiple paratomy with linear succession of the secondary zooid and terminal fission. The structure of the chain was therefore modulated by the interaction of the processes of budding, growth, cephalic differentiation, and fission, which occurred continuously and on different timescales. Values of parameters describing paratomic activity (interval between origin of the zooids, time to produce a chaetiger, growth time of the zooids, and interval between the fission of the filial chains) are low early in an individual's life, but increase during senescence. Due to its relatively rapid lifecycle and high reproductive activity, A. viride is a convenient experimental organism for the study of agametic reproduction.     

Effect of zooid spacing on bryozoan feeding success: is competition or facilitation more important?

Most Recent bryozoan species are encrusting sheets, and many of these colonies have densely packed feeding zooids. In this study, I tested whether tight packing of feeding zooids affects food capture. Colonies of a bryozoan with an encrusting sheet form (Membranipora membranacea) were dissected to produce individuals whose feeding zooids were (1) closely packed, (2) more widely spaced, or (3) isolated. For each type, rates of particle ingestion were measured in still water and in a freestream velocity of 2.7 cm s(-1). Ingestion rate increased when zooids were closest together, probably because of reduced refiltration and increased feeding current strength farther from the lophophores. The mean incurrent velocity within 0.02 cm above the center of the lophophore was 0.28 cm s(-1) regardless of zooid spacing; however, when the incurrent velocity was measured more than 0.1 cm from the lophophores, zooids that were close together or spaced one zooid's width apart had significantly faster incurrent velocities than single zooids. Flow visualization suggests that isolated zooids and those spaced far apart refilter more water than zooids that are close together. These results along with the observed trend of increased zooid integration over evolutionary time suggest that the benefits of increasing coordination outweigh the consequences of intrazooid competition.