The relationship between dissolved oxygen concentration and maximum size in deep-sea turrid gastropods: an application of quantile regression

Bathymetric gradients in body size are the most well-known patterns of geographic variation in deep-sea organisms. The causes of size-depth relationships remain uncertain, but most have been attributed to rates of nutrient input. Chapelle and Peck (1999, Nature 399:114-115) recently hypothesized that body size in marine invertebrates is a function of dissolved oxygen concentration. We tested this hypothesis by using quantile regression techniques to assess the relationship of dissolved oxygen levels to maximum size in deep-sea turrid gastropods collected from the North Atlantic. Relationships were examined for a group of nine turrid species and within the abundant lower bathyal species Benthomangelia antonia (Dall, 1881). We controlled the analysis for depth because size in deep-sea gastropods varies bathymetrically. When the effects of depth are accounted for statistically, maximum size in B. antonia increases with increasing levels of dissolved oxygen. In turrids as a group, both depth and oxygen appear to explain significant proportions of the variance in maximum size. These findings suggest that a suite of factors, including dissolved oxygen concentration, may influence maximum size in deep-sea organisms.     

Genetic variability in the cosmopolitan deep-water ophiuran Ophiomusium lymani

A population of the cosmopolitan deep-sea ophiuran Ophiomusium lymani was studied by gel electrophoresis, and proved to be highly variable genetically; about 53% of the 15 loci studied are polymorphic, and the average individual is heterozygous at about 17% of the loci. This is approximately the same genetic variability displayed by other species, belonging to other phyla or classes, from the same deep-sea trawl. A similarly high level of genetic variation occurs in deep-sea organisms in general, and in a shallow-water tropical species. Both the deep-sea and the tropics are trophically stable environments. On the other hand, low genetic variabilities have been found in marine species from trophically unstable environments. These data suggest that any phylogenetic effects on genetic variability are secondary, and that the trophic regime may be of major importance in determining genetic strategies of adaptation.This study is no. 5 of a series of reports on the results of Expedition Quagmire.     

Genetic structure of dictyoceratid sponge populations on the western Coral Sea reefs

Allozyme variation at six polymorphic loci was examined in foliose dictyoceratid sponges from isolated reefs in the western Coral Sea. Four major genetic groups corresponding to the species Phyllospongia lamellosa, P. alcicornis, Carterospongia flabellifera and Collospongia auris were examined. A further two rare morphotypes from individual reefs formed genetic outliers to the P. lamellosa group, and may represent further taxa related to P. lamellosa. Gene frequencies in individual reef populations were largely in Hardy-Weinberg equilibrium, suggesting that random mating occurred in local populations of all four common species. Genetic variability was high and observed heterozygosities within populations ranged from 0.13 to 0.40. All four taxa showed significant genetic differentiation among populations (F _ST=0.05 to 0.36). Genetic distances (Nei's D) among populations within species ranged from 0 to 0.723 and increased with increasing geographical separation. There was evidence that genetic differentiation between populations to the north and to the south of the southern limit of the South Equatorial Current (SEC) divergence was greater than expected on the basis of their geographical separation. The SEC divergence may form a partial barrier to gene flow among populations of these ecologically important sponges on the submerged Queensland Plateau. Levels of migration among populations of three of the species was less than those required to prevent divergence of the populations through genetic drift (Nm<1). Restricted migration among populations may provide a mechanism to explain the occurrence of highly divergent populations of dictyoceratid sponges whose specific identity is not clear, and may allow them additionally to develop partial reproduction isolation from other populations.     

Genetic population structure in the black-spot sea bream (<Emphasis Type="Italic">Pagellus bogaraveo</Emphasis> Brünnich, 1768) from the NE Atlantic

The depletion of shallow-water fish stocks through overexploitation has led to increasing fishing pressure on deep-sea species. Poor knowledge of the biology of commercially valuable deep-water fish has led to the serial depletion of stocks of several species across the world. Data regarding the genetic structure of deep-sea fish populations is important in determining the impact of overfishing on the overall genetic variability of species and can be used to estimate the likelihood of recolonisation of damaged populations through immigration of individuals from distant localities. Here the genetic structure of the commercially fished deep-water species the blackspot sea bream, Pagellus bogaraveo is investigated in the northeastern Atlantic using partial DNA sequencing of mitochondrial cytochrome b (cyt-b) and D-loop regions and genotyping of microsatellite loci. An absence of variation in cyt-b and low genetic variation in D-loop sequences potentially indicate that P. bogaraveo may have undergone a severe bottleneck in the past. Similar bottlenecks have been detected in other Atlantic species of fish and have possibly originated from the last glaciation. P. bogaraveo may have been particularly vulnerable to the effects of low temperature and a fall in sea level because stages of its life history occur in shallow water and coastal sites. However, there are other explanations of low genetic variability in populations of P. bogaraveo, such as a low population size and the impacts of fishing on population structure. Analysis of population structure using both D-loop and microsatellite analysis indicates low to moderate, but significant, genetic differentiation between populations at a regional level. This study supports studies on other deep-sea fish species that indicate that hydrographic or topographic barriers prevent dispersal of adults and/or larvae between populations at regional and oceanographic scales. The implications for the management and conservation of deep-sea fish populations are discussed.Communicated by J.P. Thorpe, Port Erin     

Diets of deep-sea brachyuran crabs in the Western Mediterranean Sea

This study examines the feeding habits of Paromola cuvieri (Risso, 1816) and Geryon longipes A. Milne Edwards, 1881, the only two common deep-sea brachyuran crabs inhabiting the bathyal mud assemblages in the Catalan Sea (Western Mediterranean). Samples were obtained by bottom trawls at depths between 360 and 1871 m during 1983 to 1992. Both species had highly diverse diets, but very low feeding activity, as reflected by the high proportion of empty stomachs. Both characteristics may be important factors enabling deepsea crabs to adapt to bathyal zones, where trophic resources are scarce. The most important food items found in P. cuvieri were fish remains (teleost, sharks) and benthic decapods (Monodaeus couchii, Munida tenuimana). Scavenging activity plays an important role in this species. The diet of G. longipes included a broad range of benthic invertebrates. In the upper middle slope, the bivalve Abra longicallus, decapods (Calocaris macandreae and Monodaeus couchii), echinoderms and polychaetes were the dominant prey, with epibenthic peracarids as a secondary resource. On the lower middle slope, the incidence of decapod crustaceans (C. macandreae, Pontiphilus norvegicus) and peracarids in the diet declined. Small macrobenthic prey (glycerids, cumaceans or amphipods) were rare in the diet of both species, in accordance with the large size of the crab specimens studied. The absence of preferred prey items and the lack of food items of an optimum size on the lower slope may contribute to the progressive decline in abundance of P. cuvieri and G. longipes with increasing depth.     

Population genetics of the family ostreidae. I. Intraspecific studies of Crassostrea gigas and Saccostrea commercialis

The levels of genetic variation and estimates of genetic similarity and distance were determined for populations of Crassostrea gigas (Thunberg) and Saccostrea commercialis (Iredale and Roughley). The proportion of polymorphic loci in Japanese populations of C. gigas ranged from 0.58 to 0.63, while the individual heterozygosities ranged from 0.20 to 0.22. The proportion of polymorphic loci in Australian populations of S. commercialis ranged from 0.43 to 0.46, the individual heterozygosities from 0.17 to 0.19. The genetic similarity between different geographical populations of both species was approximately 99%. The genetic distance and similarity data derived from this investigation has resulted in some provisional reclassifications. The Portuguese oyster C. angulata (Lamarck) appears to be more appropriately regarded as a recent colonized isolate of C. gigas. The New Zealand oyster S. glomerata (Gould) is considered a subspecies of the eastern Australian rock oyster S. commercialis. The Japanese Kumamoto population of C. gigas warrants reclassification as the non-sibling species C. sikamea.     

Extreme mitochondrial DNA divergence within populations of the deep-sea gastropod Frigidoalvania brychia

The deep sea supports a diverse and highly endemic invertebrate fauna, the origin of which remains obscure. Little is known about geographic variation in deep-sea organisms or the evolutionary processes that promote population-level differentiation and eventual speciation. Sequence variation at the 16 S rDNA locus was examined in formalin-preserved specimens of the common upper bathyal rissoid Frigidoalvania brychia (Verrill, 1884) to examine its population genetic structure. The specimens came from trawl samples taken over 30 years ago at depths of 457-1,102 m at stations in the Northwest Atlantic south of Woods Hole, Massachusetts, USA. Near the upper boundary of its bathymetric range (500 m), extremely divergent haplotypes comprising three phylogenetically distinct clades (average uncorrected sequence divergence among clades ~23%, ~3% within clades) were found at stations separated by a maximum distance of ~80 km, suggesting the presence of high levels of intraspecific divergence or the possibility of morphologically cryptic species. Only one of these clades was found at two stations in the mid- to lower part of F. brychia's depth distribution (800-1,100 m), suggesting lower clade diversity with increasing depth, although among-sample divergence, with a single exception, was minimal. One station was genetically divergent from all others sampled, containing a unique suite of haplotypes including two found only at this site. Steep vertical selective gradients, major oceanographic changes during the late Cenozoic, and habitat fragmentation by submarine canyons might have contributed to an upper bathyal region that is highly conducive to evolutionary change.     

Genetic variance in Ophiomusium lymani (Ophiuroidea: Echinodermata) from lower bathyal depths in the Rocklall Trough (northeast Atlantic)

Specimens of the deep-sea brittle-star Ophiomusium lymani were collected from six sites in the Rockall Trough (northeast Atlantic_. Four monomorphic and four polymorphic loci were detected, with up to 75 individuals screened at any one locus. The results showed little difference in allele frequencies between sites and, consequently, estimates of genetic identity indicated no significant genetic differentiation between the populations sampled. Deficits of heterozygotes were observed at all polymorphic loci, but the deficiencies were only significant at the phosphoglucose isomerase locus from two locations. The deficit of heterozygotes was not the same across loci, suggesting that inbreeding is not the cause of the excess homozygosity. No relationship between heterozygosity and depth was observed.     

Genetic variation in marine teleosts: High variability in habitat specialists and low variability in habitat generalists

Genetic variation was reviewed in 106 species of marine teleosts. Two heterozygosity estimates were used, one including all protein and enzyme loci and a second excluding the non-enzymatic protein loci. Mean heterozygosities are 0.055±0.036 based on all loci in 106 species and 0.060+0.038 based on enzymatic loci in 89 species. A significant negative correlation was noted between heterozygosity and the proportion of general protein loci included in the estimate. A comparison was made of heterozygosities among taxonomic orders and families, life zones, reproductive mode, geographical range and size. High levels of genetic variation are found in Clupeiformes, Atheriniformes, Pleuronectiformes, temperate pelagic, tropical, intertidal-sublittoral and wide-range species. Low levels of genetic variation are found in Gadiformes, Scorpaeniformes, temperate demersal, polar, and narrowrange species. The most striking differences in heterozygosities are between temperate demersal flatfishes and temperate demersal round fishes. It is suggested that much of the data can be explained by a habitat specialist-generalist model, with high heterozygosities in specialists and low heterozygosities in generalists, but that this is only one of a mosaic of factors which influence genetic variation.     

Evaluation of hermit crab shell indices

A study on the alimentary ethology of conger eels was carried out over a period of four years. Individuals were captured at a depth ranging from 10 to 800 m. The parameters analysed lead to the following observations: (a) in the Central Mediterranean basin the feeding of Conger conger (L.) populations was mainly based on Osteichthyes, Crustacea and Cephalopoda; (b) the neritic population fed on a higher number of species than the epimesobathyal. The high percentage of empty stomachs in the bathyal population was due to the fact that the neritic females, at the end of trophic phase, set out on a reproductive migration towards the bathyal level.     

Bathymetric patterns of genetic variation in a deep-sea protobranch bivalve, Deminucula atacellana

The origin of the deep-sea benthic fauna is poorly understood and represents an enormous gap in our understanding of basic evolutionary phenomena. One obstacle to studying evolutionary patterns in the deep sea has been the technical difficulty of measuring genetic variation in species that are typically minute, rare, and must be recovered from extreme depths. We used molecular genetic techniques to quantify variation in the 16S rRNA mitochondrial gene within and among populations of the common protobranch bivalve Deminucula atacellana (Schenck, 1939). We analyzed 89 individuals from nine samples collected in the 1960s along a depth gradient from 1100 to 3800 m in the western North Atlantic. Genetic variability within populations is much lower than between populations, and peak haplotype numbers occur near the center of its depth distribution. Continental slope (<2500 m) and rise (>2500 m) populations were genetically distinct despite the lack of any obvious topographic or oceanographic features that would impede gene flow. These findings indicate that the deep-sea macrofauna can have strong population structure over small (134 km) spatial scales, similar to that observed in shallow-water and terrestrial organisms. This surprisingly high biodiversity at the genetic level affords the potential for adaptation and evolutionary diversification, the ultimate historical causes of high species diversity in the deep-sea benthos. Received: 24 July 1997 / Accepted: 26 January 1998     

Genetic differentiation in two sibling species of the brackish-water polychaete Hediste japonica complex (Nereididae)

Genetic divergence among ten populations of small- and large-egg forms of the brackish-water polychaete Hediste japonica complex was investigated on 14 isozyme loci by electrophoretic analysis. The two forms were distinguishable by complete allele substitutions at five loci, resulting in high genetic differentiation (Nei's D: 0.533 to 0.662). No genetic evidence of hybridization between the two forms was detected in sympatric populations in three rivers. These results indicate that the two forms are reproductively isolated, clearly showing that the two forms are distinct species. The genetic differentiation among populations was higher in the large-egg form (D: 0.005 to 0.111, G _ST: 0.435) than that in the small-egg form (D: 0.000 to 0.001, G _ST: 0.020). This genetic difference between the two forms seems to be attributable to a difference in their life histories. The average expected heterozygosity was low in populations of both the large-egg form (0.005 to 0.068) and the small-egg form (0.014 to 0.038) in comparison with other marine invertebrates. Received: 11 April 1997 / Accepted: 8 September 1997     

Population structure of the giant tiger prawn Penaeus monodon in Australian waters, determined using microsatellite markers

 We describe three highly polymorphic microsatellite loci which have been isolated from the giant tiger prawn Penaeus monodon. The number of alleles present among 312 samples at the loci Pmo9, Pmo25 and Pmo27 were 84, 34 and 35, respectively, with heterozygosities all >90%. Analyses of the distribution of length variation at three microsatellite loci among five Australian P. monodon populations revealed strong differentiation between populations from the west and those from the northern and eastern coasts. Tests for population differentiation (F st) values and an analogous measure for microsatellite loci (R st) all demonstrated that Western Australian P. monodon are a separate genetic stock which exhibits reduced genetic variation relative to the other populations. Reduced variability is consistent with a recent population bottleneck or colonization by a small founding population from the east when sea links between Indonesia, New Guinea and Australia were re-established following the last ice age. The results of this study are in agreement with previous surveys of P. monodon conducted with allozymes and mtDNA. Received: 18 December 1998 / Accepted: 27 August 1999     

Is Syllis gracilis (Polychaeta: Syllidae) a species complex? An allozyme perspective

The genetic relationships between morphologically indistinguishable marine and brackish populations of Syllis gracilis Grube, 1840 (Polychaeta: Syllidae) were studied by means of allozyme electrophoresis. Samples of S. gracilis from marine coastal and brackish-water habitats were examined for variation at 13 presumptive loci. In addition, a sample of the closely related species S. prolifera (Krohn, 1852) was analysed. Five loci were multiallelic in at least one population of S. gracilis and eight loci in S. prolifera. Low to moderate levels of within-population genetic variability were found, with average expected heterozygosity values ranging from H = 0.068 (±0.043 SE) to 0.187 (±0.069 SE) in the populations of S. gracilis; higher values were found in S. prolifera (H = 0.325 ± 0.076). The presence of various private alleles indicated a marked genetic divergence among populations of S. gracilis, with Nei's genetic distances ranging from D = 0.000 to 0.833 and a highly significant F _ST value. Furthermore, evidence for strong genetic heterogeneity between two sympatric marine populations was found. UPGMA cluster analysis and multidimensional scaling pointed out a clear genetic divergence between brackish and marine populations. At least two genetically divergent entities occurred in marine and brackish habitats. This could be due to local adaptation of individuals coming from marine populations to brackish habitats, but more presumably to the occurrence of a species complex within S. gracilis. Received: 6 June 1999 / Accepted: 7 February 2000     

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.     

Sibling species in interstitial flatworms: a case study using<Emphasis Type="Italic"> Monocelis lineata</Emphasis> (Proseriata: Monocelididae)

The genetic relationships between morphologically indistinguishable marine and brackish-water populations of Monocelis lineata (O.F. Müller, 1774) (Proseriata: Monocelididae) were analysed by means of allozyme electrophoresis. Fifteen samples of M. lineata (13 from the Mediterranean and two from the Atlantic) from coastal marine and brackish-water habitats were examined for variation at 18 loci. Eleven loci were polymorphic in at least one population of M. lineata. Low levels of within-population genetic variability were found, with average observed and expected heterozygosity values ranging from H_o=0.015±0.015 to 0.113±0.044, and from H_e=0.028±0.028 to 0.138±0.054, respectively. The occurrence of a number of private alleles indicated a marked genetic divergence among populations of M. lineata, with Rogers genetic distances ranging from D_R=0.003 to 0.676 and a highly significant F_ST value (0.918±0.012, P<0.001). UPGMA (unweighted pair-group method using arithmetic average) cluster analysis and multidimensional scaling showed a clear genetic divergence between marine and brackish-water populations. Moreover, Atlantic and Mediterranean populations were sharply separated. Our results suggest that M. lineata is a complex of sibling species.Communicated by R. Cattaneo-Vietti, Genova     

Influence of depth and season on the diet of the deep-water aristeid Aristeus antennatus along the continental slope (400 to 2300 m) in the Catalan Sea (western Mediterranean)

The composition of the diet of the deep-sea aristeid shrimp Aristeus antennatus (Risso, 1816) was determined based on the analysis of 1578 stomach contents. Samples were collected using bottom trawls during 1984 to 1989 along the deep continental slope (380 to 2266 m) in the Catalan Sea (Western Mediterranea). A. antennatus displayed a high feeding activity on a large variety of endobenthic and epibenthic invertebrates, whereas benthopelagic prey were supplementary to its diet. The shrimp's diet varied mainly as a function of depth. Various preferred prey items on the middle slope (Calocaris macandreae, Cirolana borealis, Abra longicallus) disappeared from its diet below 1300 m, coinciding with the transtion boundary between different taxocenoses in the Catalan Sea. Less mobile prey and inert remains (mainly pteropods) contributed a progressively larger share of the diet of Aristeus antennatus with increasing depth. The importance of seasonality in the changes in diet decreased with increasing depth, and was relatively high only in the upper middle slope (down to 1000 m depth), where two seasonal dietary groups were detected. The most distinct seasonal changes in diet were among benthopelagic prey. The diet of A. antennatus in the submarine canyons mainly consisted of endobenthic prey (large polychaetes, ophiuroids). The higher stomach-fullness values and less diversified diet in this area were probably related to high productivity in the submarine canyons.     

Reproductive isolation with little genetic divergence between Urticina (=Tealia) felina and U. eques (Anthozoa: Actiniaria)

There has long been doubt as to whether there are one or two British species of the sea anemone genus Urticina. In the present study, populations of both putative species, which occur sympatrically in the Isle of Man, have been compared by electrophoresis of isozymes and nematocyst analysis. The analysis of fourteen isozyme loci exhibited a high genetic identity between the two taxa (I=0.907), but four loci showed significant differences in gene frequencies; thus indicating reproductive isolation. The populations displayed highly significant differences in the sizes of the various nematocyst types. The individual analysis of data for each type of nematocyst revealed that the basitrics from the actinopharynx and from the tentacles contribute most to the observed difference. Consequently, U. felina (L.) and U. eques (Gosse) are assumed to be valid species, as suggested by Manuel (1981). The mean heterozygosities for each species (0.410 and 0.436, respectively) are the highest reported for cnidarians.     

Founding Lineages and Genic Variability in Plains Bison (Bison bison) from Badlands National Park, South Dakota

Abstract: Starch-gel electrophoresis was used to screen 101 bison from Badlands National Park, South Dakota, for variation at 24 genetic loci. The population was descended from founder groups of about 6 and 3 individuals, separated geographically for a minimum of 64 years. The purpose of this study was (1) to estimate levels of genic variability in this bison population, (2) to assess the extent to which descendents of the two founder groups differ genetically, and (3) to compare the genetic characteristics of the Badlands population with other bison populations. The Badlands herd was found to be polymorphic for only a single locus (MDH–1). Descendents of the founder groups were homogeneous with respect to allelic and genotypic frequencies at this locus. The MDH–1 polymorphism has not been observed in other bison populations, while several polymorphism reported in other bison populations were not detected in the Badlands herd. A mean heterozygosity of 0.012 was observed in the Badlands herd; this value is lower than that typically reported for mammals, though not as low as heterozygosities seen in other populations that have passed through severe bottlenecks in size. These results underscore the need for genetic data in planning breeding programs for species in captivity or managed in isolate reserves.     

Allozyme variation in global populations of striped mullet, Mugil cephalus (Pisces: Mugilidae)

The striped mullet, Mugil cephalus Linnaeus, 1758, is one of the few species of marine shore fish with a worldwide circumtropical distribution. Because of this distribution and the dependency of M. cephalus on coastal waters during various phases of its life cycle, as well as nearshore living habits, questions have been raised regarding levels of genetic divergence and gene flow among transoceanic populations. To cast more light on this, allozyme variation at 27 presumptive gene loci was investigated in ten globally diverse populations. The observed heterozygosity ranged from 0.018 (Hawaii) to 0.081 (Florida), averaging 0.050. The proportion of polymorphic loci showed a similar trend. Several populations were characterised by fixed allelic differences. Estimated gene diversities were very high, the allele frequency variation among populations was found to be 68%; genetic distances reached 0.242, with an average of 0.117. Estimated rates of gene flow were high among Mediterranean populations (Nm = 7.26), and between Mediterranean and East Atlantic populations (Nm= 2.86), but extremely low between non-contiguous populations within the Indian, Pacific and Atlantic Oceans, where Nm ranged from 0.03 to 0.05. Received: 7 April 1997 / Accepted: 4 February 1998