Symbiotic interactions in the Silurian of Baltica

Thirteen symbiotic associations occur in the Silurian of Baltica. Symbiosis was especially prominent among colonial animals, most commonly with stromatoporoids. These sponges hosted the most diverse fauna of endobiotic symbionts (including rugosans, Syringopora, ‘polychaetes’, cornulitids and lingulids). This pattern can be explained by the abundance of stromatoporoids in the Silurian of Baltica and their large skeletal volume, making them attractive hosts for smaller invertebrates. There is an evolutionary trend of an increasing number of different pairs of symbiotic taxa from the Llandovery to the Ludlow, with a remarkable increase in the Ludlow. This is likely related to an increase in the number of mutualistic taxa that could have had evolutionary advantages over organisms less amenable to symbiosis. The number of different pairs of symbiotic taxa also increased in the Wenlock, which may be linked to delayed recovery from the end‐Ordovician mass extinction.     

Symbiotic interactions in the Silurian of North America

There are at least 47 different symbiotic pairs of taxa and 16 symbiotic associations in the Silurian of North America. Crinoids are most common host species and they hosted variety of epibiotic and endobiotic symbionts, including Tremichnus, platyceratid gastropods, brachiopods, microconchids, cornulitids, cyclostome bryozoans and favositid tabulates. Eighteen symbiotic pairs contain at least one colonial partner. Stromatoporoids hosted the most diverse fauna of endobiotic symbionts, including cornulitids, lingulids, Chaetosalpinx, Heliocosalpinx and rugosans. Among 16 symbiotic associations of Silurian of North America, 8 are common between North America and Baltica. North American symbiotic associations involving stromatoporoid hosts are the most similar to their Baltic equivalents.     

Cryptostomid Bryozoans From The Sassito Formation,Upper Ordovician Cool‐Water Carbonates of the Argentinean Precordillera

Abstract: Two new bryozoan species are described from the Upper Ordovician Sassito Formation of the Argentinean Precordillera: Moyerella  spinata sp. nov. and Phylloporina  sassitoensis sp. nov. The bryozoans are found in cool‐water carbonates. The Silurian genus Moyerella is reported the first time in the Ordovician, showing palaeobiogeographic connections with Estonia and Siberia.     

Systematics, shell structure and affinities of the Palaeozoic Problematicum Cornulites

The genus Cornulites, with the type species C. serpularius Schlotheim, 1820, from the Silurian of Gotland, comprises annulated, conical or tubular calcite shells, often found attached to the hard parts of other organisms. No consensus has ever been reached over the zoological affinities of the taxon, and no examples of soft‐part preservation are known: detailed examination of shell structures and growth patterns provide the only means of assessing its systematic position. Using transverse and longitudinal thin sections of C. serpularius Vine, 1882, and C. cellulosus sp. nov. , from the Much Wenlock Limestone Formation of England, the shell structure of Cornulites is shown to be lamellar, but with conspicuous internal chambers (camerae) at the apical end of the shell and, particularly in C. cellulosus, numerous smaller vacuities (cellulae) between the lamellae in the apertural shell region. Growth of the shell was by the secretion of low‐magnesian calcite increments within one another, giving a cone‐in‐cone structure, with the prominent development of cellulae in C. cellulosus probably a constructional feature relating to an upright life position. By comparison of morphology and shell structure with other taxa, the zoological affinities of Cornulites are re‐examined; previously suggested affinities with annelids, foraminifers, molluscs and poriferans can be ruled out. Specific shell structures, most notably pseudopuncta similar to those of bryozoans and brachiopods, have led some recent workers to interpret cornulitids as lophophorates. However, it is shown that they can be interpreted alternatively as solitary, aseptate members of the stem‐Zoantharia (Cnidaria: Anthozoa). Four cornulitid species are recognized in the Much Wenlock Limestone Formation: C. cellulosus sp. nov. , C. gremialis sp. nov. , C. scalariformis and C. serpularius. In the absence of the type material, C. serpularius is here restricted to cornulitids closely resembling the specimens originally figured by Schlotheim. © 2007 The Linnean Society of London, Zoological Journal of the Linnean Society, 2007, 150 , 681–699.     

UPPER ORDOVICIAN BRYOZOANS OF THE PIN FORMATION (SPITI VALLEY, NORTHERN INDIA)

Abstract: Twenty‐nine species of bryozoans from the Upper Ordovician–Lower Silurian Pin Formation (Spiti, India) have been identified. Eight of these are new: Trematopora minima, Ulrichostylus bhargavai, Ptilodictya exiliformis, Phaenopora ordinarius, Oanduellina himalayaica, Pesnastylus? vesiculosum, Ralfina? originalis and Pinocladia triangulata. The fossil record and facies analyses of the area investigated indicate shallow‐water conditions within the subtropical–tropical realm. The distribution pattern of fossils among the Ordovician/Silurian succession on the Northern Gondwana shelf and the influence of the Late Ordovician cooling phases on marine organisms are distinctive owing to a dramatic reduction in diversity globally. As far as the bryozoan taxa of Spiti are concerned, only one (Helopora fragilis) of the 29 species was recorded above the Ordovician/Silurian boundary. Observed bryozoan communities are very similar to faunas of Laurentia, the Baltic, Siberia and southern China of early–late Ordovician age.     

New crinoids from the Baltic region (Estonia): fossil tip‐dating phylogenetics constrains the origin and Ordovician–Silurian diversification of the Flexibilia (Echinodermata)

This study documents previously unknown taxonomic and morphological diversity among early Palaeozoic crinoids. Based on highly complete, well preserved crown material, we describe two new genera from the Ordovician and Silurian of the Baltic region (Estonia) that provide insight into two major features of the geological history of crinoids: the early evolution of the flexible clade during the Great Ordovician Biodiversification Event (GOBE), and their diversification history surrounding the end‐Ordovician mass extinction. The unexpected occurrence of a highly derived sagenocrinid, Tintinnabulicrinus estoniensis gen. et. sp. nov., from Upper Ordovician (lower Katian) rocks of the Baltic palaeocontinent provides high‐resolution temporal, taxonomic and palaeobiogeographical constraints on the origin and early evolution of the Flexibilia. The Silurian (lower Rhuddanian, Llandovery) Paerticrinus arvosus gen. et sp. nov. is the oldest known Silurian crinoid from Baltica and thus provides the earliest Baltic record of crinoids following the aftermath of the end‐Ordovician mass extinction. A Bayesian ‘fossil tip‐dating’ analysis implementing the fossilized birth–death process and a relaxed morphological clock model suggests that flexibles evolved c. 3 million years prior to their oldest fossil record, potentially involving an ancestor–descendant relationship (via ‘budding’ cladogenesis or anagenesis) with the paraphyletic cladid Cupulocrinus. The sagenocrinid subclade rapidly diverged from ‘taxocrinid’ grade crinoids during the final stages of the GOBE, culminating in maximal diversity among Ordovician crinoid faunas on a global scale. Remarkably, diversification patterns indicate little taxonomic turnover among flexibles across the Late Ordovician mass extinction. However, the elimination of closely related clades may have helped pave the way for their subsequent Silurian diversification and increased ecological role in post‐Ordovician Palaeozoic marine communities. This study highlights the significance of studies reporting faunas from undersampled palaeogeographical regions for clade‐based phylogenetic studies and improving estimates of global biodiversity through geological time.     

A novel reef coral symbiosis

Reef building corals form close associations with unicellular microalgae, fungi, bacteria and archaea, some of which are symbiotic and which together form the coral holobiont. Associations with multicellular eukaryotes such as polychaete worms, bivalves and sponges are not generally considered to be symbiotic as the host responds to their presence by forming physical barriers with an active growth edge in the exoskeleton isolating the invader and, at a subcellular level, activating innate immune responses such as melanin deposition. This study describes a novel symbiosis between a newly described hydrozoan (Zanclea margaritae sp. nov.) and the reef building coral Acropora muricata (=A. formosa), with the hydrozoan hydrorhiza ramifying throughout the coral tissues with no evidence of isolation or activation of the immune systems of the host. The hydrorhiza lacks a perisarc, which is typical of symbiotic species of this and related genera, including species that associate with other cnidarians such as octocorals. The symbiosis was observed at all sites investigated from two distant locations on the Great Barrier Reef, Australia, and appears to be host species specific, being found only in A. muricata and in none of 30 other species investigated at these sites. Not all colonies of A. muricata host the hydrozoans and both the prevalence within the coral population (mean = 66%) and density of emergent hydrozoan hydranths on the surface of the coral (mean = 4.3 cm⁻², but up to 52 cm⁻²) vary between sites. The form of the symbiosis in terms of the mutualism–parasitism continuum is not known, although the hydrozoan possesses large stenotele nematocysts, which may be important for defence from predators and protozoan pathogens. This finding expands the known A. muricata holobiont and the association must be taken into account in future when determining the corals’ abilities to defend against predators and withstand stress.     

Frasnian bryozoans (Late Devonian) from the Khoshyeilagh Section,Alborz Mountains (northern Iran)

A bryozoan fauna containing seven species is described from the Upper Frasnian (Upper Devonian) rocks in the Khoshyeilagh Section, Alborz Mountains (northern Iran). The studied bryozoan assemblage includes one new trepostome species, Eridotrypella alborzensis sp. nov., an additional four species identified at species level: two trepostomes, Minussina akkayaensis Volkova, 1974 and Leptotrypella inaudita Morozova, 1961, and two rhabdomesine cryptostomes, Bigeyella mariae (Morozova, 1961) and Saffordotaxis multispinata (Morozova, 1955). Furthermore, two species are described in open nomenclature: the trepostome Schulgina sp. and the rhabdomesine cryptostome Nicklesopora sp. The studied fauna shows a close similarity at the species level between northern Iran and the Altai-Sayan Folded Belt (Russia), south China, and Transcaucasia.     

The oldest bryozoan reefs: a unique Early Ordovician skeletal framework construction

Adachi, N., Ezaki, Y. & Liu, J. 2011: The oldest bryozoan reefs: a unique Early Ordovician skeletal framework construction. Lethaia, Vol. 45, pp. 14–23. The oldest bryozoan reefs occur in the Lower Ordovician (late Tremadocian) Fenhsiang Formation of the Three Gorges area, South China. These reefs show a unique type of bryozoan (Nekhorosheviella) framework, and were constructed as follows: the first stage involved colonization by lithistid sponges, which acted as a baffler to trap sediments, providing bryozoans with a stable substrate for attachment. The bryozoans then grew as an encruser on the surfaces of sponges, showing a preferential downwards and lateral growth within the sponge scaffolding to avoid biological and physical disturbance. Finally, these biotic combinations among skeletal organisms formed a rigid, three‐dimensional skeletal framework. This mode of bryozoan growth in association with lithistid sponges is remarkable and unique in its growth direction, and the appearance of such reefs, just prior to the widespread development of skeletal‐dominated reefs as part of the Great Ordovician Biodiversification Event, provides an excellent example of the earliest attempts by skeletal organisms to form frameworks by themselves. This find significantly enhances our understanding of the initial stages of skeletal‐dominated reef evolution and the ensuing development of reefs during the Middle–Late Ordovician. □Bryozoa, Early Ordovician, lithistid sponge, Ordovician radiation, reef.     

Upper Ordovician bryozoans from the Xiazhen Formation of Yushan,northeastern Jiangxi,East China

The bryozoan fauna from the Xiazhen Formation (Katian, Upper Ordovician) of northeast Jiangxi Province, southeast China is reported here. Seventeen species of bryozoans belonging to fifteen genera and four orders are identified: Homotrypa yushanensis, Homotrypa sp., Prasopora yushanensis, Trematopora sp., Monotrypella sp., Rhombotrypa sp., Orbignyella sp., Constellaria jiangxiensis, Constellaria sp., Stictopora nicholsoni, Trigonodictya parvula, Ptilodictya ensiformis, Stictoporella sp., Pseudopachydictya sp., Nematopora sp., Arthrostylidae sp. indet., and Chasmatoporidae sp. indet. Four of these genera have been reported previously but nine genera (Trematopora, Monotrypella, Rhombotrypa, Orbignyella, Trigonodictya, Ptilodictya, Stictoporella, Pseudopachydictya, and Nematopora), one rhabdomesine and one fenestrate are found for the first time in the Late Ordovician strata of South China. Our palaeogeographical analysis suggests that the bryozoan association is typical for the Katian, which is mostly widespread in Laurentia, Siberia, Baltica and Mediterranean, and displays palaeobiogeographical relationships to the Laurentia–Siberia Province.     

Expression patterns of sterol transporters NPC1 and NPC2 in the cnidarian–dinoflagellate symbiosis

The symbiotic interaction between cnidarians (e.g., corals and sea anemones) and photosynthetic dinoflagellates of the genus Symbiodinium is triggered by both host–symbiont recognition processes and metabolic exchange between the 2 partners. The molecular communication is crucial for homeostatic regulation of the symbiosis, both under normal conditions and during stresses that further lead to symbiosis collapse. It is therefore important to identify and fully characterise the key players of this intimate interaction at the symbiotic interface. In this study, we determined the cellular and subcellular localization and expression of the sterol‐trafficking Niemann–Pick type C proteins (NPC1 and NPC2) in the symbiotic sea anemones Anemonia viridis and Aiptasia sp. We first established that NPC1 is localised within vesicles in host tissues and to the symbiosome membranes in several anthozoan species. We demonstrated that the canonical NPC2‐a protein is mainly expressed in the epidermis, whereas the NPC2‐d protein is closely associated with symbiosome membranes. Furthermore, we showed that the expression of the NPC2‐d protein is correlated with symbiont presence in healthy symbiotic specimens. As npc2‐d is a cnidarian‐specific duplicated gene, we hypothesised that it probably arose from a subfunctionalisation process that might result in a gain of function and symbiosis adaptation in anthozoans. Niemann–Pick type C proteins may be key players in a functional symbiosis and be useful tools to study host–symbiont interactions in the anthozoan–dinoflagellate association.     

An exotic invader drives the evolution of plant traits that determine mycorrhizal fungal diversity in a native competitor

The symbiosis between land plants and arbuscular mycorrhizal fungi (AMF) is one of the most widespread and ancient mutualisms on the planet. However, relatively little is known about the evolution of these symbiotic plant–fungal interactions in natural communities. In this study, we investigated the symbiotic AMF communities of populations of the native plant species Pilea pumila (Urticaceae) with varying histories of coexistence with a nonmycorrhizal invasive species, Alliaria petiolata (Brassicaceae), known to affect mycorrhizal communities. We found that native populations of P. pumila with a long history of coexistence with the invasive species developed more diverse symbiotic AMF communities. This effect was strongest when A. petiolata plants were actively growing with the natives, and in soils with the longest history of A. petiolata growth. These results suggest that despite the ancient and widespread nature of the plant–AMF symbiosis, the plant traits responsible for symbiotic preferences can, nevertheless, evolve rapidly in response to environmental changes.     

Bryozoa from the Surmaq Formation (Permian) of the Hambast Mountains,south of Abadeh,central Iran

The Permian bryozoan fauna of the Surmaq Formation exposed in a section near Kuh-e Hambast (Hambast Mountains, central Iran) includes ten species. Four species (Fistulipora sawatai Sakagami 1999, Fistulipora takauchiensis Sakagami 1961, Fistulipora monticulosa Nikiforova 1933, and Eridopora parasitica, Waagen and Wentzel 1886) indicate a Middle Permian (Murgabian) age of the formation. Six additional taxa, three cystoporates Fistulipora sp. 1, Fistulipora sp. 2, and Fistuliporidae gen. et sp. indet., as well as three trepostomes Dyscritella sp., Trepostomata gen. et sp. indet. 1 and Trepostomata gen. et sp. indet. 2 could not be identified at the genus and species level. The investigated fauna refers to the Middle Permian of Thailand, Pakistan, Indonesia, and Japan.     

Heritability of symbiont density reveals distinct regulatory mechanisms in a tripartite symbiosis

Beneficial eukaryotic–bacterial partnerships are integral to animal and plant evolution. Understanding the density regulation mechanisms behind bacterial symbiosis is essential to elucidating the functional balance between hosts and symbionts. Citrus mealybugs, Planococcus citri (Risso), present an excellent model system for investigating the mechanisms of symbiont density regulation. They contain two obligate nutritional symbionts, Moranella endobia, which resides inside Tremblaya princeps, which has been maternally transmitted for 100–200 million years. We investigate whether host genotype may influence symbiont density by crossing mealybugs from two inbred laboratory‐reared populations that differ substantially in their symbiont density to create hybrids. The density of the M. endobia symbiont in the hybrid hosts matched that of the maternal parent population, in keeping with density being determined either by the symbiont or the maternal genotype. However, the density of the T. princeps symbiont was influenced by the paternal host genotype. The greater dependency of T. princeps on its host may be due to its highly reduced genome. The decoupling of T. princeps and M. endobia densities, in spite of their intimate association, suggests that distinct regulatory mechanisms can be at work in symbiotic partnerships, even when they are obligate and mutualistic.     

Evolution,palaeoecology, and palaeobiogeography of the Late Ordovician–Early Silurian brachiopod Epitomyonia

Epitomyonia is characterized by various types of dorsal ridges, which may be transverse, longitudinal, or highly convoluted and probably served as skeletal supports for lophophores of various complexity. Multivariate analyses suggest that the Epitomyonia-bearing brachiopod associations lived in relatively shallow-water environment in the Late Ordovician, and inhabited mainly deep-water environments in the early Wenlock. The temporal and spatial change in the faunal distribution may be explained by three alternative scenarios: (1) Epitomyonia followed the broad evolutionary trend of the Palaeozoic Evolutionary Fauna to shift from shallow- to deeper-water settings over time; (2) the dicoelosiid communities could not compete with the large-shelled pentameride communities in continental shelf settings during the Early Silurian; or (3) only the shallow-water Epitomyonia died out in the Late Ordovician mass extinction event, whereas some poorly known deep-water Late Ordovician forms survived into the Early Silurian. Epitomyonia paucitropida n. sp. from the lower Whittaker Formation (late Katian) of the Mackenzie Mountains, northwestern Canada, is reported as the first known Ordovician species of Epitomyonia from the palaeocontinent of Laurentia, characterized by a small shell with weak, transverse dorsal ridges that are most primitive for the genus.     

The specificity of Burkholderia symbionts in the social amoeba farming symbiosis: Prevalence,species, genetic and phenotypic diversity

The establishment of symbioses between eukaryotic hosts and bacterial symbionts in nature is a dynamic process. The formation of such relationships depends on the life history of both partners. Bacterial symbionts of amoebae may have unique evolutionary trajectories to the symbiont lifestyle, because bacteria are typically ingested as prey. To persist after ingestion, bacteria must first survive phagocytosis. In the social amoeba Dictyostelium discoideum, certain strains of Burkholderia bacteria are able to resist amoebal digestion and maintain a persistent relationship that includes carriage throughout the amoeba's social cycle that culminates in spore formation. Some Burkholderia strains allow their host to carry other bacteria, as food. This carried food is released in new environments in a trait called farming. To better understand the diversity and prevalence of Burkholderia symbionts and the traits they impart to their amoebae hosts, we first screened 700 natural isolates of D. discoideum and found 25% infected with Burkholderia. We next used a multilocus phylogenetic analysis and identified two independent transitions by Burkholderia to the symbiotic lifestyle. Finally, we tested the ability of 38 strains of Burkholderia from D. discoideum, as well as strains isolated from other sources, for traits relevant to symbiosis in D. discoideum. Only D. discoideum native isolates belonging to the Burkholderia agricolaris, B. hayleyella, and B. bonniea species were able to form persistent symbiotic associations with D. discoideum. The Burkholderia–Dictyostelium relationship provides a promising arena for further studies of the pathway to symbiosis in a unique system.     

Genetics of the relationship between the ciliate Paramecium bursaria and its symbiotic algae

Abstract. Paramecium bursaria , a freshwater protozoan, typically harbors hundreds of symbiotic algae ( Chlorella sp.) in its cytoplasm. The relationship between host paramecia and symbiotic algae is stable and mutually beneficial in natural environments. We recently collected an aposymbiotic strain of P. bursaria . Infection experiments revealed that the natural aposymbiotic strain (Ysa2) showed unstable symbiosis with Chlorella sp. The algae aggregated at the posterior region of the host, resulting in aposymbiotic cell production after cell division. Cross-breeding analyses were performed to determine the heritability of the aposymbiotic condition. In crosses of Ysa2 with symbiotic strains of P. bursaria , F1 progeny were able to form stable symbioses with Chlorella sp. However, unstable symbiosis, resembling Ysa2 infection, occurred in some F2 progeny of sibling crosses between symbiotic F1 clones. Infection experiments using aposymbiotic F2 cells showed that these F2 subclones have limited ability to reestablish the symbiosis. These results indicate that the maintenance of stable symbiosis is genetically controlled and heritable, and that Ysa2 is a mutant lacking the mechanisms to establish stable symbiosis with Chlorella sp.     

Host-symbiont co-speciation and reductive genome evolution in gut symbiotic bacteria of acanthosomatid stinkbugs

Background  

Host-symbiont co-speciation and reductive genome evolution have been commonly observed among obligate endocellular insect symbionts, while such examples have rarely been identified among extracellular ones, the only case reported being from gut symbiotic bacteria of stinkbugs of the family Plataspidae. Considering that gut symbiotic communities are vulnerable to invasion of foreign microbes, gut symbiotic associations have been thought to be evolutionarily not stable. Stinkbugs of the family Acanthosomatidae harbor a bacterial symbiont in the midgut crypts, the lumen of which is completely sealed off from the midgut main tract, thereby retaining the symbiont in the isolated cryptic cavities. We investigated histological, ecological, phylogenetic, and genomic aspects of the unique gut symbiosis of the acanthosomatid stinkbugs.     

Evidence of photosymbiosis in Palaeozoic tabulate corals

Coral reefs form the most diverse of all marine ecosystems on the Earth. Corals are among their main components and owe their bioconstructing abilities to a symbiosis with algae (Symbiodinium). The coral–algae symbiosis had been traced back to the Triassic (ca 240 Ma). Modern reef-building corals (Scleractinia) appeared after the Permian–Triassic crisis; in the Palaeozoic, some of the main reef constructors were extinct tabulate corals. The calcium carbonate secreted by extant photosymbiotic corals bears characteristic isotope (C and O) signatures. The analysis of tabulate corals belonging to four orders (Favositida, Heliolitida, Syringoporida and Auloporida) from Silurian to Permian strata of Europe and Africa shows these characteristic carbon and oxygen stable isotope signatures. The δ¹⁸O to δ¹³C ratios in recent photosymbiotic scleractinians are very similar to those of Palaeozoic tabulates, thus providing strong evidence of such symbioses as early as the Middle Silurian (ca 430 Ma). Corals in Palaeozoic reefs used the same cellular mechanisms for carbonate secretion as recent reefs, and thus contributed to reef formation.     

Furrows and firmgrounds: evidence for predation and implications for Palaeozoic substrate evolution in Rusophycus burrows from the Silurian of New York

Tarhan, L.G., Jensen, S. & Droser, M.L. 2011: Furrows and firmgrounds: evidence for predation and implications for Palaeozoic substrate evolution in Rusophycus burrows from the Silurian of New York. Lethaia, Vol. 45, pp. 329–341. The Silurian Herkimer Formation of east‐central New York contains abundant, exceptionally preserved composite Rusophycus‐Teichichnus burrows. We suggest that the most likely interpretation of these composite trace fossils is as structures formed by trilobites entering the sediment in search of prey. Parallel alignment of the paired traces, asymmetrical configuration of the Teichichnus along the longitudinal axis of the associated Rusophycus, depth correlation and deformation of the Teichichnus all suggest that this relationship was predatory. In addition, sectioned material indicates that these Rusophycus may have been open at the sediment‐water interface, while the crisp preservation of both Rusophycus and Teichichnus, along with the preservation of such delicate morphological details as scratch marks, suggests that the sediment must have been relatively firm at the time the traces were formed. The formation and preservation of Rusophycus in cohesive sediments located very close to the sediment‐water interface hold important implications for the manner in which we consider Palaeozoic substrates and their temporal and spatial evolution. Moreover, these findings demonstrate that the morphology and taphonomy of ichnological associations may, in the context of sedimentological relationships, prove a powerful proxy for tracking substrate conditions through both space and time. □firmgrounds, New York, predation, Rusophycus, substrate, taphonomy.