Heteroplasmy in a deep-sea protobranch bivalve suggests an ancient origin of doubly uniparental inheritance of mitochondria in Bivalvia

Most metazoan species have strict maternal inheritance of the mitochondrial genome. In bivalves, a unique inheritance pattern called doubly uniparental inheritance (DUI) occurs in at least seven bivalve families. In this system of mitochondrial inheritance, males inherit and carry mtDNA from both parents, while females only carry mtDNA from the mother. Here, we present evidence of mitochondrial heteroplasmy in deep-sea protobranch bivalves. Divergent 16S rRNA and cytochrome b sequences were obtained within individuals of Ledella ultima. Ledella sublevis also exhibited divergent 16S sequences. Levels of divergence between 16S sequences within individuals were 27 and 15 % for each species, respectively. Ratios of homoplasmic to heteroplasmic individuals were not significantly different from 1:1, in agreement with sex ratios in protobranchs. The results provide the first evidence for mitochondrial heteroplasmy in the protobranchs and suggest DUI might have evolved much earlier in the evolution of the Bivalvia than previously thought.     

Larval and post-larval morphogenesis in the gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae)

Structural changes occurring in the alimentary tract, perivisceral cavity, foot, hypobranchial gland, and gills of larval and post-larval Solemya reidi, a gutless protobranch bivalve, were examined using both light and electron microscopy at 1, 3, 5, 18, 34 and 42 d after fertilization. A fully developed mouth, esophagus, and anus, together with the rudiments of a stomach and rectum are present before metamorphosis. At metamorphosis, the cells making up the dorsal and lateral walls of the stomach dissociate, and by 18 d the mouth and anus are the only remaining portions of the alimentary tract. The larval test is ingested into the perivisceral cavity at metamorphosis and its autolysis continues through at least the 42nd day after fertilization. The foot, gills, and hypobranchial gland, poorly developed at metamorphosis, develop slowly and are still undergoing extensive morphogenesis at 42 d.Harbor Branch Oceanographic Institution Contribution No. 601.     

Association of bacteria with larvae of the gutless protobranch bivalve Solemya reidi (Cryptodonta: Solemyidae)

Rod-shaped bacteria were consistently observed by transmission electron microscopy in the locomotory test of larvae and in the perivisceral cavity of post-larvae of Solemya reidi, a gutless protobranch bivalve known to possess intracellular chemoautotrophic bacterial symbionts in the adult gill. Bacteria develop within granular vesicles in the larval test, where they either remain to be ingested at metamorphosis, or are released into the space separating the test and embryo, to be subsequently ingested through the larval mouth. In either case, bacteria lie within the perivisceral cavity following metamorphosis. Bacteria were not seen either in or on gametes or in gills of juveniles. It is hypothesized that these bacteria represent a transmission stage of the gill symbionts present in adult S. reidi and are not evident in gametes or gills of juveniles due to cryptic packaging within granular vesicles. Perpetuation of this symbiosis would therefore be assured through vertical transmission, as is typical of other marine invertebrate-bacteria endosymbioses.Harbor Branch Oceanographic Institution Contribution No. 602     

Larval dispersal of a deep-sea hydrothermal vent bivalve from the Galápagos Rift

The prodissoconch morphology of an unclassified mytilid from a hydrothermal vent on the Galápagos Rift indicates the presence of a planktotrophic larval stage with longrange dispersal capabilities. Recorded abyssal currents are probably sufficient to transport such larvae hundreds of kilometers. It is suggested that one or more aspects of the unusual biological or physico-chemical conditions (such as high microbial densities, elevated water temperatures, and hydrogen sulfide concentrations) encountered at vents, provide a stimulus to larval settlement. Such a behavioral response, perhaps coupled with a gregarious settling response, would provide a means of concentrating relatively sedentary organisms in and around these restricted, geographically isolated regions.     

Genome-size variation in bivalve molluscs determined by flow cytometry

Six of the nine described species of the mole crab genus Emerita are distributed in the Americas, two [E. analoga (Stimpson, 1857) and E. rathbunae Schmitt, 1935] on the west coast, and four [E. benedicti Schmitt, 1935, E. brasiliensis Schmitt, 1935, E. portoricensis Schmitt, 1935 and E. talpoida (Say, 1817)] on the east. The presence of an extended planktonic larval stage in all Emerita species suggests high dispersal potential and the possibility of extensive gene flow among conspecific populations. Two taxa were sampled to study the extent of gene flow between widely separated conspecific populations: E. analoga (California and Chile) and E. talpoida (Massachusetts, South Carolina, and the west coast of Florida), while all other taxa were characterized from a single location. Portions of two mitochondrial genes, cytochrome oxidase I (COI) and 16S ribosomal RNA (16S rRNA) were sequenced. For data analysis, approximately 500 bp (COI) and 400 bp (16S rRNA) were examined. Estimated genetic divergence of 5.41% in COI between E. talpoida populations sampled from the Gulf of Mexico and the Atlantic coast, and 3.47% between E. analoga sampled in Chile and California, indicates that in both cases there has been no recent gene flow between disjunct populations. Additional molecular and morphological studies are necessary to decide whether disjunct populations should be accorded specific status. We predict that many marine invertebrates with antitropical distributions similar to E. analoga may consist of sibling species. In contrast to relationships inferred earlier from distribution patterns, parsimony analyses of both COI and 16S rRNA data yield similar phylogenetic trees in which E. analoga is separated from a clade composed of other species in the Americas; a bootstrap value (67%) in the COI inferred tree marginally supports the separation, but the same tree topology with a higher bootstrap value (84%) is obtained with 16S rRNA sequence data. Genetic divergence among the taxa indicates that the Emerita species constitute an old group and that distribution of species has been modified by past climatic and geological events.     

Electrophoretic identification and genetic analysis of bivalve larvae

Taxonomic identification and genetic analysis of larval marine invertebrates have been vexing problems. We describe a polyacrylamide mini-gel electrophoresis technique for resolving proteins from individual larval bivalves (shell length 250 to 350 m) and apply this technique to three species of laboratory-cultured larval oysters [Ostrea edulis L., 1758, Crassostrea gigas (Thunberg, 1793) and c. virginica (Gmelin, 1791)] reared during summer 1989. Electrophoretic patterns of proteins clearly discriminate among the three species and allow genetic analysis of a polymorphic allozyme locus (Pgi) in field-collected larvae and juveniles of C. virginica. This technique provides an economical tool for largescale taxonomic, ecologic, and genetic studies of meroplanktonic stages of various species.     

Leucine aminopeptidase variation and fitness parameters in the estuarine bivalve Geukensia demissa

Investigations into several potential fitness parameters in collections of the estuarine bivalve Geukensia demissa (Dillwyn), (from Newport Bay and Alamitos Bay in southern California, conducted from 1981 to 1984) under both field and laboratory conditions, revealed differences in growth rate, tissue weight, and mortality which were correlated with leucine aminopeptidase-1 (LAP-1) genotype. The results of these fitness studies are consistent among themselves and with the results of previous population genetic studies on G. demissa. As a whole, these studies suggest that differential fitness among LAP-1 genotypes in conjunction with a variable environment act to maintain the LAP-1 polymorphism in natural populations of this species.     

Geographic variation in a predator-induced defense and its genetic basis

Predator-induced morphological defenses are a well-known form of phenotypic plasticity, but we continue to have a limited understanding of geographic variation in these responses and its genetic basis. Here we examine genetic variation and geographic differentiation in the inducible defenses of tadpoles (Rana pirica) in response to predatory salamander larvae (Hynobius retardatus). To do so, we crossed male and female frogs from a "mainland" Japanese island having predaceous salamanders and a more isolated island not having predaceous salamanders and raised resulting offspring in the presence and absence of H. retardatus. Mainland tadpoles exhibited a higher capacity to express the inducible morphology (a more bulgy body) than those from the predator-free island, and expression of the bulgy morph in mainland-island hybrids produced phenotypes that were intermediate to those produced by pure crosses. In addition, parental sex had no effect on expression of the bulgy morph. Our results support the hypothesis that geographic variation in inducible defenses is linked to the additive effects of autosomal alleles that are shaped by differences in historical exposure to the inducing predator.     

Genetic variation in deep-sea invertebrate populations: The bathyal gastropod Bathybembix bairdii

Five populations of the bathyal trochid gastropod Bathybembix bairdii (Dall) taken from depths of 579 to 1156 m in the Southern California Continental Borderland were surveyed for levels of genetic variability at 18 presumptive gene loci, using techniques of starch gel electrophoresis. All the populations were highly similar genetically; none of the populations possessed unique alleles. Four of 5 polymorphic loci scored in all the populations displayed statistically significant heterogeneity of allelic frequencies among stations. Only the diallelic fumarase (FUM) locus displayed a trend with depth. The geographic and depth patterns of the genetic variability in these populations do not support the hypothesis that the high levels of genetic variability observed in bathyal populations are an artifact of gene flow between populations differentiated with depth. The 16.2% of the loci heterozygous per individual of B. bairdii is of the same order as the average heterozygosities reported for other deep-sea invertebrate taxa. These reports of high genetic variability in a physically constant and seasonless environment are reviewed and discussed in the context of the trophic-stability hypothesis of Ayala and Valentine and the time, size and divergence hypothesis of Soulé. Evidence is presented that despite the observed correlation of average heterozygosities in benthic marine invertebrates with seasonality of the trophic regime, this is not apparent for an enzyme system (leucine amino peptidase) which might be expected to display this trend if it reflected a genetic strategy to cope with trophic seasonality. The time, size and divergence hypothesis, focusing on population size, accounts for the general features of levels of genetic variability in deep-sea invertebrates.     

Temporal patterns in diversity and species composition of deep-sea benthic copepods in bathyal Sagami Bay,central Japan

Little is known about temporal changes in the diversity and species composition of deep-sea metazoan meiofauna and their relationships with changes in the food supply. Those changes were studied for benthic copepod assemblages based on 2-year time-series data at a bathyal site in Sagami Bay (1430 m depth), central Japan, where annual fluctuation in the abundance of benthic foraminiferans was previously observed. Species diversity of benthic copepods at the site was as high as, or slightly higher than, that observed at other deep-sea sites, but did not fluctuate temporally through the study period. Multivariate analyses did not reveal any clear seasonal or directional change occurring over the longer term in their species composition, although there was some consistent pattern. These results indicate a lack of, or only weak, seasonality in the diversity and species structure of the deep-sea benthic copepod assemblages, even though the fresh organic food supply fluctuates seasonally. They also suggest that there are differences between copepods and foraminiferans in the response to changes in environmental factors, and that spatial differences in the composition of copepod communities are greater than temporal ones at this deep-sea site.Communicated by T. Ikeda, Hakodate     

Seasonal variation in the white muscle biochemical composition of deep-sea macrourids in the North-east Atlantic

The peculiar limpet-like morphology of the genus Colobocentrotus is unique among the regular echinoids. This shape has been interpreted as an adaptation to life in areas of extreme wave exposure. In this study the attachment strength of C. atratus is compared with that of three sympatric species, Echinometra mathaei, Heterocentrotus trigonarius and Stomopneustes variolaris, which have more typical echinoid morphology and live in different microhabitats. For each species, the adhesion of individual sea urchins was measured as well as the tenacity of single tube foot and the mechanical properties of the tube foot stems. Colobocentrotus always presented the highest measured values, although not always significantly different from those of the other species. Of the mechanical properties of the stem measured, the stem extensibility was the only property that was significantly different among species. In general the stems of all the species studied became more extensible and more difficult to break with increasing strain rate, providing an adaptative advantage to the sea urchin when subjected to rapid loads such as waves. In terms of single tube foot tenacity, C. atratus tube feet attached with a tenacity (0.54 MPa) two times higher than the one of E. mathaei, H. trigonarius and S. variolaris (0.21–0.25 MPa). Individual sea urchins of the four species, however, attached with a similar strength (0.2–0.26 MPa). The calculation of safety factors showed that it is the very high number of adoral tube feet of C. atratus and not the overall shape of the animal that allows this species to withstand very high water velocities. However, C. atratus streamlined morphology may be a functional adaptation to reduce the impact of other hydrodynamic forces (such as wave impingement forces) or to cope with other selective environmental stresses (such as dessication), and thus to inhabit extremely exposed areas of the intertidal.     

Geographic and bathymetric patterns of mitochondrial 16S rRNA sequence divergence among deep-sea amphipods,Eurythenes gryllus

The physical uniformity of the deep sea suggests a lack of absolute barriers to faunal dispersal, and thus genetic homogeneity in broadly distributed species is expected. The deep-sea amphipod Eurythenes gryllus Lichtenstein (Crustacea: Lysianassoidea) is considered a panoceanic, cold-water stenotherm, with a vertical depth distribution from 184 to 6500 m. We surveyed mtDNA sequence diversity in E. gryllus to assess genetic diversity and population structure in different oceans and across traditionally defined bathyal and abyssal zones. DNA sequences (437 nucleotides length) from the mitochondrial large-subunit ribosomal RNA gene (16S rRNA) of 95 individuals, collected between 1982 and 1990 from 14 locations in the central North Pacific (including multiple samples on the slope of a seamount), castern and western North Atlantic, and the Arctic Ocean, were obtained. Our analysis of DNA sequence diversity indicates (1) genetic homogeneity among sites within the same depth zone at the scale of ocean basins; and (2) genetically divergent, cryptic taxa distributed at different depths, with the greatest diversity in the bathyal zone. These observations suggest that ecological and physical conditions are important isolating mechanisms that may lead to speciation in this group.     

Seasonal variation in reproduction and population structure of the bivalve Limopsis tajimae in the upper bathyal zone of Suruga Bay, Japan

Seasonal variation in reproduction and population size structure was investigated for the suspension-feeding bivalve Limopsis tajimae Sowerby inhabiting the upper bathyal zone (300 m deep) of Suruga Bay, central Japan. The bivalve was collected at 1- to 4-month intervals for a period of 22 months, and bottom environment was monitored concurrently to detect factors affecting seasonality in the bivalve. Bottom water temperature, organic carbon and nitrogen contents in the sediments did not exhibit seasonal variation. Size-adjusted soft-tissue weight varied slightly, but statistically significantly between stations and months. However, its seasonal pattern was not obvious, and the pattern of temporal variation was totally different between stations. The sex ratio did not deviate from 1:1, and there was no significant difference between shell lengths of females and males. Females possess both immature small oocytes and large developed oocytes in their ovaries throughout the year, suggesting that they can potentially undergo year-round continuous reproduction. The proportion of developed oocytes in each female varied greatly from month to month, although no seasonal cycle was obvious. Population size structure of L. tajimae was polymodal. A mode of the smallest size class occurred in most months, suggesting long periods of bivalve recruitment. These findings indicate that seasonal variation in reproduction of the bivalve was negligible, probably reflecting constant physical and nutritive conditions of the bottom environment. Received: 6 January 1998 / Accepted: 19 May 1998     

Population structure and reproductive patterns of the NW Mediterranean deep-sea macrourid Trachyrincus scabrus (Rafinesque, 1810)

Macrourid fish are one of the most abundant marine species on continental margins worldwide. Although they play an important role in the ecosystem, little is known about their overall biology. We report here a large data set of the most abundant macrourid in Mediterranean waters, Trachyrincus scabrus, showing the main population and reproductive characteristics. The study was based on 3,239 specimens collected between 300 and 1,500 m depth on the northwestern Mediterranean in 2003–2004 and 2008–2009. The population showed a depth-related structure with the largest individuals at 1,100 m depth and the smallest (i.e., immature) at shallower depths. Macroscopic and microscopic analyses of the gonads showed that T. scabrus has a highly seasonal reproductive pattern. Spawning females were found during winter when the organic matter fluxes were highest on the continental slope. T. scabrus is a batch spawner with group-synchronous oocyte development and present low average fecundity of 14,191 oocytes.     

Relatedness and microgeographic genetic variation in Rhytidoponera mayri,an Australian arid-zone ant

Summary We use a multiallelic regression and jack-knife technique to estimate relatedness and its confidence limits in a sample of 117 nests of the Australian arid zone ant Rhytidoponera mayri, using the genotypes at a prolifically-polymorphic amylase locus. Relatedness between workers from the same nest is low, whether calculated with respect to the complete sample of nests (b=0.121<0.158<0.195), or by restricting the analysis to those nests bordering a cell in a Gabriel-connectedness graph (b=0.101<0.126<0.151). Relatedness between workers of neighboring nests was determined for nearest-neighbors (b=0.021<0.054<0.087), and for nests connected in the Gabriel network (b=0.018<0.036<0.054). Relatedness is thus low but significant at both within- and between-nest levels, as is consistent with a life history involving multiple egg-layers and colony foundation via fission. Estimating relatedness for the different alleles separately yields some significant differences between alleles. We also tested for geographic substructuring using autocorrelation analysis of nine alleles separately and the factor scores for the first two principal components of all the allele frequencies: six of the eleven patterns tested differed significantly from randomness at the 95% level.     

Local variation of within-host clonal diversity coupled with genetic homogeneity in a marine trematode

Despite their ubiquity and importance to intertidal ecosystems, information is currently lacking regarding the genetic diversity of trematode parasites within coastal organisms and the distribution of their genetic variation among intertidal habitats. In this study, we quantified the clonal diversity of the coastal marine trematode Maritrema novaezealandensis within Zeacumantus subcarinatus snail hosts from three coastal bays in Otago Harbour, New Zealand, using five microsatellite loci to determine if differences exist in the frequency of occurrence of multi-clone infections. In addition, we examined gene flow among M. novaezealandensis collected from the three bays. The frequency of mixed-clone infections varied fourfold among bays and no genetic differentiation was detected among intertidal bays. Across the coastal bays studied, M. novaezealandensis comprises a single population that is potentially infecting multiple Z. subcarinatus populations with varying life history traits.     

The community effects of phenotypic and genetic variation within a predator population

Natural populations are heterogeneous mixtures of individuals differing in physiology, morphology, and behavior. Despite the ubiquity of phenotypic variation within natural populations, its effects on the dynamics of ecological communities are not well understood. Here, we use a quantitative genetics framework to examine how phenotypic variation in a predator affects the outcome of apparent competition between its two prey species. Classical apparent competition theory predicts that prey have reciprocally negative effects on each other. The addition of phenotypic trait variation in predation can marginalize these negative effects, mediate coexistence, or generate positive indirect effects between the prey species. Long-term coexistence or facilitation, however, can be preceded by long transients of extinction risk whenever the heritability of phenotypic variation is low. Greater heritability can circumvent these ecological transients but also can generate oscillatory and chaotic dynamics. These dramatic changes in ecological outcomes, in the sign of indirect effects, and in stability suggest that studies which ignore intraspecific trait variation may reach fundamentally incorrect conclusions regarding ecological dynamics.