Phagocytosis of algal chloroplasts by digestive gland cells in the photosynthesis-capable slug Elysia timida (Mollusca, Opisthobranchia, Sacoglossa)

Parapodia of the sacoglossan slug Elysia timida were preserved by high-pressure cryofixation during feeding experiments and investigated with transmission electron microscopy. This slug has been known for its long-term retention of active chloroplasts and photosynthesis. We observed different stages of phagocytosis of chloroplast components from ingested algal food by slug digestive gland cells. Thylakoid stacks and stroma of chloroplasts were engulfed by the slug cells. In the slug cells thylakoids were surrounded by one membrane only. This membrane is interpreted as having been generated by the mollusk during phagocytosis. It is inferred to be eukaryotic in origin and unlikely, therefore, to be endowed with the translocons system ordinarily regulating import of algal gene-encoded plastid preproteins. Our structural findings suggest that chloroplast components in the slug cells are thylakoid stacks with chloroplast stroma only.     

Systematics and phylogeny of the Aglajidae (Opisthobranchia: Mollusca)

The generic limits within the Aglajidae are reviewed and modified, based on the study of 21 species. Navanax Pilsbry, 1895 is reinstated as a genus distinct from Aglaja. The generic placement of several species is altered from previous works. An evaluation of morphological characters suggests that each of six genera has distinctive external morphology. The systematic value of twelve characters is critically reviewed. The evolutionary relationships of the Aglajidae and its genera to other philinacean familes are discussed.     

Mating behaviour in the sea slug Elysia timida (Opisthobranchia, Sacoglossa): hypodermic injection, sperm transfer and balanced reciprocity

Background

Unisexuality, or all female reproduction, is rare among vertebrates. Studying these exceptional organisms may give useful information with respect to the evolution and maintenance of sexual reproduction. Poecilia formosa was the first unisexual vertebrate species to be detected and since then has served as a paradigmatic organism for unisexuality and studies on the evolution of sex. It reproduces through gynogenesis, using sperm of males from related species to trigger parthenogenetic development of the unreduced diploid eggs. Like in other unisexual vertebrates, triploids occur in a certain range of P. formosa. It has been suggested that the addition of the host species derived third chromosome set is evolutionary important. Clonal organisms lack sufficient genotypic diversity for adaptive changes to variable environments. Also non-recombining genomes cannot purge deleterious mutations and therefore unisexual organisms should suffer from a genomic decay. Thus, polyploidization leading to triploidy should bring "fresh" genetic material into the asexual lineage. To evaluate the importance of triploidy for maintaining the asexual species, it is important to know whether such an introgression event happens at a reasonable frequency.

Results

In an earlier study it was found that all triploid P. formosa in the Rio Purificación river system are of monophyletic origin. Here we have analyzed fish from a different river system. Using microsatellite analysis we can show that the triploids from this new location are genetically divergent and most probably of an independent origin.

Conclusion

Our data support the hypothesis that triploidy was not a single chance event in the evolutionary history of P. formosa and hence might be a relevant mechanism to increase genotypic divergence and at least partially counteract the genetic degeneration connected to asexuality. It is, however, much rarer than in other asexual vertebrates analyzed so far and thus probably only of moderate evolutionary importance for the maintenance of the asexual breeding complex.     

Towards a phylogeny and evolution of Acochlidia (Mollusca: Gastropoda: Opisthobranchia)

The Acochlidia are unique among opisthobranch gastropods in combining extremely high morphological and ecological diversity with modest species diversity. The phylogeny of acochlidians has never been addressed by cladistic means, as their evolution has remained unknown. This study gives a first overview on more than 150 biological and morphological characters that are potentially useful for phylogenetic analysis. Based on 107 characters, a parsimony analysis (PAUP) was performed for all 27 valid acochlidian species together with 11 (plus two) outgroup taxa. The resulting strict consensus tree shows a moderate overall resolution, with at least some bootstrap support for most resolved nodes. The Acochlidia are clearly monophyletic, and originate from an unresolved basal opisthobranch level. The Acochlidia split into the Hedylopsacea (Tantulum (Hedylopsis (Pseudunela (Strubellia (‘Acochlidium’, ‘Palliohedyle’))))) and Microhedylacea (Asperspina (Pontohedyle, ‘Parhedyle’, ‘Microhedyle’, (Ganitus, Paraganitus))). The formerly enigmatic Ganitidae, resembling sacoglossan opisthobranchs by having dagger‐like rachidian radular teeth, are likely to be highly derived microhedylids. The paraphyly of some of the traditionally recognized family level taxa induced a preliminary reclassification. From the phylogenetic hypothesis obtained, we conclude that the acochlidian ancestor was marine mesopsammic. The colonization of limnic systems occurred twice, independently: first in the Caribbean (with the development of the small interstitial Tantulum elegans), and second in the Indo‐Pacific, with a radiation of large‐sized benthic acochlidian species. The evolution of extraordinary reproductive features, such as hypodermic impregnation by a complex copulative aparatus in hedylopsaceans, cutaneous insemination via spermatophores in microhedylaceans, and gonochorism in Microhedylidae s.l. (including Ganitidae), is discussed. © 2010 The Linnean Society of London, Zoological Journal of the Linnean Society, 2010, 158 , 124–154.     

Population genetics and phylogeography of freshwater mussels in North America, Elliptio dilatata and Actinonaias ligamentina (Bivalvia: Unionidae)

Extrinsic and intrinsic forces combined shape the population structure of every species differently. Freshwater mussels are obligate parasites to a host fish during a juvenile stage (glochidia). Elliptio dilatata (ED) and Actinonaias ligamentina (AL) are co-occurring freshwater mussel taxa with similar North American distribution and share some potential host fish. Using mitochondrial DNA, we determined the genotypes of 190 + individuals from collection sites in at least two tributaries in the Lake Erie and Ohio River watersheds, along with the Ouachita and Strawberry rivers in the southeast. Both species had followed a stepping-stone model of dispersal, with greater pairwise genetic structure among collection sites of ED. Also, phylogeographical analysis for ED found significant geographical structuring of haplotype diversity. Overall, within-population variation increased significantly from north to south, with low genetic diversity in the Strawberry River. We calculated significant among-population structure for both species (ED: Phi(ST) = 0.62, P < 0.001; AL: Phi(ST) = 0.16, P < 0.001). Genetic analysis identified the Ouachita River as an area of significant reproductive isolation for both species. Results for AL indicated dispersal into northern areas from two genetically distinct glacial refugia, where results for ED indicated dispersal followed by low gene flow in northern areas. The conservation strategies for mussels that co-occur in the same 'bed' could be species specific. Species such as ED have management units on the population scale, where AL has a more homogeneous genetic structure across its range.     

Stomach of Aplysia depilans (Mollusca,Opisthobranchia): a histochemical,ultrastructural, and cytochemical study

We report the results of a morphological, histochemical, and cytochemical characterization of the Aplysia depilans stomach, an organ little studied in opisthobranchs. Very thin ciliated cells with microvilli on their apical surfaces are predominant in the epithelium lining the lumen of the stomach. Many lysosomes with a strong arylsulphatase activity were present in the apical regions of these cells that could also contain some lipid droplets and glycogen. Small peroxisomes were observed, usually around lipid droplets or mitochondria. Bottle-shaped secretory cells are very common in this epithelium and produce a secretion rich in proteins and acidic mucopolysaccharides. Most of the cytoplasm of these mucus-producing cells was filled with a very high number of granules and the nucleus is dislocated to the basal region. Cisternae of rough endoplasmic reticulum were abundant around the nucleus and several Golgi stacks were also present in this area. In spite of the variation in the electron density of the granules, only one type of secretory cell seems to be present in the stomach epithelium, since granules with very different electron densities were frequently found in the same cell. A few neurons were also found in the stomach epithelium of this species. Fibrocytes, muscle cells, nerves, and amebocytes were observed in the connective tissue of the stomach wall.     

Quantifying temporal variation in heterobranch (Mollusca: Gastropoda) sea slug assemblages: tests of alternate models

Assemblages of heterobranch sea slugs are notoriously variable in space and time which has sometimes led to their exclusion from broader studies of patterns of biodiversity. This variability may also result in a failure to detect underlying spatial and temporal patterns. Assemblage data (species abundances) from three intertidal sites over a period of 13 months, were used to compare the conclusions drawn from three different analytical approaches—a non-specific test for differences among months, and tests of cyclicity, and seriation, using specific model matrices. While no significant difference was detected for the non-specific test (i.e. concluding no significant temporal variation), the data were significantly correlated to both model matrices with the cyclicity model outperforming the seriation model at two of the three sites. The study also highlighted the spatial variability of assemblages over a scale of just a few kilometres. Wider testing using previously published datasets confirmed the utility of these models for exploring specific hypotheses about patterns of temporal change.     

Comparison of Alimentary Systems in Shelled and Non-shelled Sacoglossa (Mollusca,Opisthobranchia)

The Sacoglossa (= Ascoglossa) comprise a ‘complete’ evolutionary series from species with a large shell into which the animal can withdraw completely, through species with a reduced shell covering only the visceral mass, to shell-less (‘nudibranchiate’) forms some of which have lateral wing-like extensions, parapodia, others bearing leaf-like or cylindrical dorsal appendages, cerata. The Sacoglossa are all specialized suctorial feeders, and almost all are stenophagous herbivores. Hence many anatomical adaptations to a particular food occur in the alimentary system. However, a number of characters seem to reflect phylogenetic relationships as well. Among these are presence/absence, shape, and position of pharyngeal pouches, basic shape of radular teeth, branching pattern of digestive gland, and position of anus. The classificatory significance of these characters is discussed.     

Ultrastructure and Phylogenetic Significance of Notaspidean Spermatozoa (Mollusca, Gastropoda, Opisthobranchia)

Spermatozoa of five notaspidean opisthobranchs [Berthellina citrina, Berthella ornata, Pleuro-branchus peroni, Pleurobranchaea maculata, Umbruculum sinicum] were examined using TEM. In all five species, the acrosome (sensu lato) consists of an apical vesicle (the acrosomal vesicle) and acrosomal pedestal. The acrosomal pedestal overlaps the nuclear apex, and in P. peroni (and possibly B. ornata) is periodically banded—-the first reported incidence of this type of substructure in any euthyneuran acrosome. Although sperm nuclei of P. peroni, B. ornata and B. citrina differ in length and also the number of keels present (nucleus 7 μm long with four/five keels present in Pleurobranchus; 17 μm long with one keel in Berthella; 15 μm long with a very weak keel in Berthellina), the basal invagination to which the centriolar derivative, axoneme and coarse fibres are attached is always poorly developed, and very little overlap between nucleus and midpiece occurs. In P. maculata and U. sinicum, the nucleus forms a helical cord around the axoneme and mitochondrial derivative such that it is not possible to recognize exclusively ‘nuclear’ and ‘midpiece’ regions of the spermatozoon. In all notaspideans investigated, (1) the axoneme, coarse fibres and glycogen helix are enclosed by the paracrystalline and matrix components of the mitochondrial derivative and (2) a dense ring structure (attached to the plasma membrane) and glycogen piece are observed. While the glycogen piece is very short (0.85–1.43 μm) with a very degenerate axoneme in B. citrina, B. ornata and P. peroni, this region of the spermatozoan is well developed (30–35 μm long) in U. sinicum and exhibits a fully intact 9 + 2 axoneme. The ‘glycogen piece’(or its presumed homologue) in P. maculata spermatozoa is very short (0.65 μm), devoid of any axonemal remnant and constructed of a hollow, internal cylinder attached to an outer (incomplete) shell, and contains scattered (glycogen) granules. Spermatozoal structure supports a close relationship between the genera Berthellina, Berthella and Pleurobranchus. These three genera have more distant links with Pleurobranchaea, while Umbraculum maintains an isolated, specialized position within the Notaspidea.     

Population genetics of geographically restricted and widespread species of Myrica (Myricaceae)

Allozyme variation of 11 putative loci in five populations of the rare Myrica adenophora Hance, and four populations of its widespread congeneric species, M. rubra (Lour.) Sieb. & Zucc. was studied. Among the 21 alleles studied, no unique allele was detected for M. adenophora, whereas M. rubra had 3 alleles not found in the former species. In terms of genetic diversity, populations of the rare species contained fewer alleles per locus (1.5 versus 1.7), fewer effective number of alleles per locus (1.12 versus 1.20), fewer number of alleles per polymorphic locus (2.14 versus 2.46), lower percentage of polymorphic loci (30.9 versus 40.9), and lower expected heterozygosity (0.106 versus 0.163) than populations of the widespread species. Genetic distances within species average 0.043 for M. adenophora and 0.045 for M. rubra, and between species ranged from 0.052 to 0.177, with a mean of 0.103, which agrees with the very similar gross morphologies of these two species. Intrapopulation differentiation was similar in both species: G(ST) = 0.152 for M. adenophora, and 0.146 for M. rubra, whereas estimated gene flow based on G(ST) values were moderate in these two species (Nm = 1.39 versus 1.46). We inferred that M. rubra and M. adenophora are a progenitor-derivative species pair that emerged before migrating into Taiwan during the last glacial period. We consider the Hengchun population (Chiupeng, Hsuhai, and Chufengpi) and Taitung population (Tienkuan and Lanshan) of M. adenophora which probably arose from two subsets of the genome of M. rubra. Genetic drift was inferred to be one of the forces shaping the observed genetic structure in M. adenophora and M. rubra.     

Comparative immunohistochemistry of the cephalic sensory organs in Opisthobranchia (Mollusca,Gastropoda)

The structure and function of the central nervous systems of opisthobranch gastropods have been studied extensively. However, the organisation and function of the peripheral nervous system are poorly understood. The cephalic sensory organs (CSOs) are known to be chemosensory structures in the head region of opisthobranchs. In the present study, we used immunohistochemical methods and confocal laserscanning microscopy to comparatively examine the CSOs of different opisthobranchs, namely Acteon tornatilis, Aplysia punctata, Archidoris pseudoargus and Haminoea hydatis. We wanted to characterise sensory epithelia in order to infer the function of sensory structures and the organs they constitute. Immunoreactivity against the three antigens tyrosine hydroxylase, FMRFamide and serotonin was very similar in the CSOs of all investigated species. Tyrosine hydroxylase-like immunoreactivity was detected primarily in subepidermal sensory cell bodies, which were much more abundant in the anteriorly situated CSOs. This observation indicates that these cells and the respective organs may be involved in contact chemoreception and mechanoreception. The dominant features of FMRFamide-like immunoreactivity, especially in the posterior CSOs, were tightly knotted fibres which reveal glomerulus-like structures. This suggests an olfactory role for these organs. Serotonin-like immunoreactivity was detected in an extensive network of efferent fibres, but was not found within any peripheral cell bodies. Serotonin-like immunoreactivity was found in the same glomerulus-like structures as FMRFamide-like immunoreactivity, indicating a function of serotonin in the efferent control of olfactory inputs. Besides this functional implication, this study could also add some knowledge on the doubtful homology of the CSOs in opisthobranch gastropods.     

Histology and ultrastructure of the salivary glands in Bulla striata (Mollusca, Opisthobranchia)

Abstract. The ribbon‐shaped salivary glands in Bulla striata were studied with light microscopy and transmission electron microscopy (TEM). Secretion is produced in tubules formed by two types of secretory cells, namely granular mucocytes and vacuolated cells, intercalated with ciliated cells. A central longitudinal duct lined by the same cell types collects the secretion and conducts it to the buccal cavity. In granular mucocytes, the nucleus is usually central and the secretory vesicles contain oval‐shaped granular masses attached to the vesicle membrane. Glycogen granules can be very abundant, filling the space around the secretory vesicles. These cells are strongly stained by PAS reaction for polysaccharides. Their secretory vesicles are also stained by Alcian blue, revealing acidic mucopolysaccharides, and the tetrazonium reaction detects proteins in minute spots at the edge of the vesicles, corresponding to the granular masses observed in TEM. Colloidal iron staining for acidic mucopolysaccharides in TEM reveals iron particles in the electron‐lucent region of the vesicles, while the granular masses are free of particles. In vacuolated cells, which are thinner and less abundant than the granular mucocytes, the nucleus is basal and the cytoplasm contains large electron‐lucent vesicles. These vesicles are very weakly colored by light microscopy techniques, but colloidal iron particles could be observed within them. The golf tee‐shaped ciliated cells contain some electron‐dense lysosomes in the apical region. In these cells, the elongated nucleus is subapically located, and bundles of microfibrils are common in the slender cytoplasmic stalk that reaches the basal lamina. The morphological, histochemical, and cytochemical data showed some similarities between salivary glands in B. striata and Aplysia depilans. These similarities could reflect the phylogenetic relationship between cephalaspidean and anaspidean opisthobranchs or result from a convergent adaptation to an identical herbivorous diet.     

A new poecilogonous species of sea slug (Opisthobranchia: Sacoglossa) from California: comparison with the planktotrophic congener Alderia modesta (Loven, 1844)

Cryptic species are increasingly recognized as commonplace amongmarine gastropods, especially in taxa such as shell-less opisthobranchsthat lack many discrete taxonomic characters. Most cases ofpoecilogony, the presence of variable larval development withina single species, have historically turned out to representcryptic species, with each possessing a single canalized typeof development. One well-characterized example of poecilogonywas attributed to the sacoglossan opisthobranch Alderia modesta;in southern California, slugs resembling this member of a monotypicgenus produce both long-lived, planktotrophic and short-lived,lecithotrophic larvae. Paradoxically, however, A. modesta isexclusively planktotrophic everywhere else in the northern Pacificand Atlantic Oceans. A recently completed molecular study foundthat slugs from poecilogonous populations south of Bodega Harbor,California, comprise an evolutionarily distinct lineage separatefrom northern, strictly planktotrophic slugs. We now describethe southern species as A. willowi n. sp., based on differencesin morphology of the dorsum and radula, characteristics of theegg mass, larval development mode and nuclear and mitochondrialgenetic markers. A DNA barcode is provided, based on 27 fixeddifferences in the cytochrome c oxidase subunit I gene thatcan reliably differentiate Pacific specimens of Alderia species.Genetic and morphological data are concordant with developmentalevidence, confirming that A. willowi is a true case of poecilogony.An improved understanding of the ecological differences betweenthese sister taxa may shed light on the selective pressuresthat drove the evolution of lecithotrophy in the southern species. (Received 1 November 2005; accepted 20 September 2006)     

Origins and relationships of primitive members of the Opisthobranchia (Mollusca: Gastropoda)

An examination of possible prosobranch precursors of opisthobranchs and pulmonates suggests that archaeogastropods are poor candidates, as they lack the complex female glands which characterize all higher gastropods. Similarities between members of the Rissoacea and Cerithiacea with the Opisthobranchia and Pulmonata are here considered to be a result of parallel evolution. Much of the basis for suggesting phylogenetic aRinities between members of these taxa hinges on the supposition that pyramidellids are opisthobranchs. This contention is questioned, as the euthyneurous nervous system and hermaphroditic reproductive system share weak structural and positional homologies with opisthobranchs. The range of morphological variation within the Pyramidellidae should be more thoroughly investigated, as this taxon is poorly known. The reproductive system of members of the Littorinacea is largely homologous with that found in the least derived opisthobranchs and pulmonates. This, when considered in conjunction with other morphological and palaeontological evidence, suggests that the least derived mesogastropods, the Littorinacea, provide a more precise model of the opisthobranch-pulmonate ancestor among living prosobranchs. The specialization of the digestive system in littorinaceans suggests that morphological divergence has taken place following the cladogenesis of these taxa, and that a direct ancestor/descendent relationship cannot be implied from extant littorinaceans. The status of Acteon and other acteonids as archetypal opisthobranchs is questioned. Moditication 01 all morphological systems, with the exception of the shell and mantle complex, diminish the position of the Acteonidae as ancestral opisthobranchs. Members of the Ringiculidae more closely approach the ancestral form, but have undergone modification, as well. No extant opisthobranch retains all plesiomorphic character states. For this reason, in addition to the fact that contusion exists as to the plesiomorphic conditions of some characters within the Opisthobranchia, a hypothetical ancestral opisthobranch is characterized. It appears that parallel evolution, which confounds the relationships of certain prosobranchs and opisthobranchs, is also evident within the Opisthobranchia. Much of the confusion that has surrounded the determination of phylogenetic relationships within the Opisthobranchia relates directly to the high incidence of parallelism throughout the subclass.     

Population genetics of a tropical sea cucumber species (Stichopus monotuberculatus) in China

Stichopus monotuberculatus is a valuable tropical sea cucumber that is distributed throughout the Indo-Pacific Ocean, including Guangxi, Hainan Land and Xisha Islands of China. Increasing demand and over-fishing, however, have seriously depleted the wild populations of this species in China. In this study, we applied both mitochondrial and nuclear DNA markers to characterize the population genetic subdivisions and phylogeographic histories of S. monotuberculatus sampled from Southern China. Based on both classes of molecular markers, our results demonstrated significant genetic structure among S. monotuberculatus populations, and revealed that the three populations (Q, S and B) experienced demographic expansion during the late Pleistocene (50,000–190,000 years BP). This study provides the basic information on natural population structure of S. monotuberculatus that may help to preserve and manage tropical sea cucumbers in China.     

The Chromodorididae (Opisthobranchia: Mollusca) of the Indo-West Pacific: a review of the genera

The full anatomy of over fifty species of the Chromodorididae is described including the type species of all but one of the nominal genera. The holotype material of the type species of Ehrenberg's problematic genera Glossodoris, Actinodoris and Pterodoris is described. Sixteen genera are recognized within the family Chromodorididae including four new monotypic genera. Glossodoris is shown to be a senior synonym of Casella , not Chromodoris , and Ceratosoma and Verconia are shown to be members of the Chromodorididae. The separation of Cadlina, Tyrinna and Cadinella into a separate sub-family Cadlininae is considered unnecessary.
A large suite of characters including features of the external shape, mantle glands, gills, foregut, jaw-plates, radula and reproductive system are used to define the genera. A tentative phylogeny of the family is proposed.     

Redescription of Potamolithus paranensis (Pilsbry, 1911) and Potamolithus simplex (Pilsbry, 1911) (Gastropoda: Tateidae)

Potamolithus Pilsbry &; Rush, 1896 is a species-rich genus, endemic to South America, with many of its species considered Vulnerable due to a restricted distribution; half of them are called into question, since they are known only from their shells. The purpose of this article is to describe the anatomy of P. paranensis (Pilsbry, 1911 Pilsbry, H.A. (1911) Non-marine Mollusca of Patagonia. In: Scott, W.B. (Ed.), Reports of the Princeton University Expeditions to Patagonia, 1896–1899, Vol 3, Zoology, Part V. The University, USA, Princeton, NJ, pp. 513–633. [Google Scholar]) and P. simplex (Pilsbry, 1911 Pilsbry, H.A. (1911) Non-marine Mollusca of Patagonia. In: Scott, W.B. (Ed.), Reports of the Princeton University Expeditions to Patagonia, 1896–1899, Vol 3, Zoology, Part V. The University, USA, Princeton, NJ, pp. 513–633. [Google Scholar]) from the Argentinean Misiones province, and to evaluate the value of anatomical features in this genus. These two species differ in penis morphology and pigmentation, ctenidium length, and relative position of the opening of the pallial oviduct, seminal receptacle and bursa copulatrix. Consequently, it appears that anatomical data could help solve taxonomic conflicts that are currently unresolved by shell morphology alone.     

Ocean barriers and glaciation: evidence for explosive radiation of mitochondrial lineages in the Antarctic sea slug Doris kerguelenensis (Mollusca, Nudibranchia)

Strong currents and deep passages of water can be barriers for larval dispersal of continental marine animals, but potential effects on direct developers are under-investigated. We examined the genetic structure of Doris kerguelenensis , a directly developing sea slug that occurs across the Drake Passage, the body of water separating Antarctica from South America. We found deep mitochondrial divergences within populations on both sides of the Drake Passage, and South American animals formed multiple sister-group relationships with Antarctic animals. A generalised molecular clock suggested these trans-Drake pairs diverged during the Pliocene–Pleistocene, after the formation of the Drake Passage. Statistical parsimony methods recovered 29 separate haplotype networks (many sympatric) that likely correlate with allopatric events caused by repeated glacial cycles. Data from 16S were congruent but more conserved than COI, and the estimated ancestral 16S haplotype was widespread. The marked difference in the substitution rates between these two mitochondrial genes results in different estimates of connectivity. Demographic analyses on networks revealed some evidence for selection and expanding populations. Contrasting with the Northern Hemisphere, glaciation in Antarctica appears to have increased rather than reduced genetic diversity. This suggests orbitally forced range dynamics based on Northern Hemisphere phylogeography do not hold for Antarctica. The diverse lineages found in D. kerguelenensis point towards a recent, explosive radiation, likely reflecting multiple refuges during glaciation events, combined with limited subsequent dispersal. Whether recognised as cryptic species or not, genetic diversity in Antarctic marine invertebrates appears higher than expected from morphological analyses, and supports the Antarctic biodiversity pump phenomenon.