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Fossil Nematodes From Mexican Amber
Abstract
Fossil nematodes occur in amber found in the La Quinta Formation (Late Oligocene) of the southern Mexican state of Chiapas. This amber is around 25 million years old and was deposited in marine sediments during the late Oligocene epoch. Breeding populations of a member of Aphelenchoididae are described as Oligaphelenchoides atrebora n. gen., n. sp. Two specimens which appear to represent males in the family Diplogasteridae are described as Oligodiplogaster antiqua n. gen., n. sp. A third species which is considered microbivorous (free-living) is described as robustus n. sp. in the fossil genus Vetus Taylor.
... The Chiapas amber has been interpreted to be the result of resinous exudates of two species of the leguminose tree Hymenea. Based on paleontological evidence, Hymenea communities probably developed near the ancient coast, in estuarine environments, very similar to modern mangroves (e. g., Langenheim et al., 1967;Cobben, 1971;Frost and Langenheim, 1974;Poinar, 1992;Langenheim, 1995;Graham, 1993;Poinar and Brown, 2002;García-Villafuerte, 2008;Calvillo-Canadell et al., 2010;Sol orzano-Kraemer, 2010). ...
... Estimates for the age of the amber converge on the Late Oligocene to Early Miocene (Langenheim, 1966;Tomasini-Ortíz and Martínez-Hern andez, 1984;Poinar, 1992Poinar, , 2003Santiago-Blay and Poinar, 1993;Bousfield and Poinar, 1994;Poinar and Brown, 2002;Engel, 2004;Castañeda-Posadas and Cevallos-Ferriz, 2007). The results vary slightly depending on which amber-bearing unit in particular is considered. ...
... There are several reports on nematodes preserved in amber from Cretaceous Lebanese and Burmese pieces, as well as from Eocene Baltic and Miocene Dominican and Mexican amber (Poinar, 2011). Three species of nematodes were described by Poinar (1977) in amber pieces from the La Quinta Formation. Due to the poor preservation of our specimen, comparison with those species and others is difficult. ...
Amber from the Campo La Granja mine in Chiapas, Mexico, is distinct from other sources of amber in Chiapas. Campo La Granja amber has distinct layers created by successive flows of resin with thin layers of sand on most surfaces. Aquatic and semi-aquatic arthropods are commonly found. Together these pieces of evidence suggest an estuarine environment similar to modern mangrove communities. The aquatic crustaceans are the most intriguing aspect of the biota. A large number of ostracods have been found in the amber-many with their carapaces open, suggesting that they were alive and submerged in water at the time of entombment. The only known examples of brachyuran crabs preserved in amber are found in the Campo La Granja amber. Amphipods, copepods, isopods, and tanaids are also members of the crustacean fauna preserved in amber.
... A Bacillus sporangium inside of the body of the mycetophagous nematode, Oligaphelenchoides atrebora in Mexican amber ( Figure 19), could indicate the presence of an infectious disease in the entire nematode population [30]. Bacillus sp. are known to infect extant nematodes [31] as well as insects and humans. ...
... Evidence of pathogenic fungi attacking nematodes was found among a population of the mycetophagous nematode, Oligaphelenchoides atrebora, in Mexican amber [30]. The inner tissues of infected nematodes had been replaced by fungal mycelia (Figure 62), some of which were sporulating ( Figure 63) [115]. ...
The present work uses fossils and subfossils to decipher the origin and evolution of terrestrial pathogens and endoparasites. Fossils, as interpreted by morphology or specific features of their hosts, furnish minimum dates for the origin of infectious agents, coevolution with hosts, and geographical locations. Subfossils, those that can be C14 dated (roughly under 50,000 years) and are identified by morphology as well as molecular and immunological techniques, provide time periods when humans became infected with various diseases. The pathogen groups surveyed include viruses, bacteria, protozoa, fungi, and select multicellular endoparasites including nematodes, trematodes, cestodes, and insect parasitoids in the terrestrial environment.
... Nematoda eggs, as well as adult and juvenile individuals have been identified in amber samples dating from the Oligocene of Mexico and the Dominican Republic (Poinar, 1977;Jansson and Poinar, 1986;. However, based on bibliographic survey efforts, to date, no articles recording the presence of parasitic forms in Oligocene avian trace fossils from the Tremembé Formation were found. ...
... One is a Bacillus sporangium inside the pseudocoel of the fossil mycetophagous nematode, Oligaphelenchus atrebora ( Fig. 2.15) in Mexican amber. This bacterium was most likely a parasite that developed in the body cavity of the nematode (Poinar 1977). Members of Bacillus sp. are known to infect present day nematodes (Dollfus 1946). ...
Fossil evidence of ancient pathogens is rare and limited mostly to specimens associated with arthropod vectors in amber. In various fossil vectors is evidence of cytoplasmic and nuclear polyhedrosis viruses, pathogenic spirochetes, rickettsia, actinomycetes and protozoa. Also present in amber are examples of fossil virus-like tumors and indirect evidence of iridoviruses, polydnaviruses, pathogenic bacteria and protozoans. Many of these pathogens resemble those being transmitted today to a range of vertebrate hosts by arthropod vectors. Based on these findings, it is clear that invertebrate and vertebrate viruses, as well as a range of pathogenic bacteria and protozoa, were well established by the mid-Cretaceous.
... Following a few authors who have described and figured microorganisms contained in amber (e.g. Poinar, 1977;Waggoner, 1993;Poinar et al., 1993a,b ;Poinar, 1994;Dörfelt and Schäfer, 1998 ;Schönborn et al., 1999), he was the first to tackle the difficult exercise of identifying these micro-inclusions in French ambers. In a first work, he thus mentioned the microflora contained in amber of Sparnacian age in the South of France (Breton et al., 1999). ...
... Furthermore, the ontogeny and ultrastructure of nematodes is poorly understood and there is a lack of an informative fossil record (e.g. Poinar, 1977Poinar, , 1983Poinar, , 2003. Such diYculties have led to the erection of multiple, at least partially conXicting classiWcations that can be grouped into two overall hypotheses. ...
... Furthermore, the ontogeny and ultrastructure of nematodes is poorly understood and there is a lack of an informative fossil record (e.g. Poinar, 1977Poinar, , 1983Poinar, , 2003. Such diYculties have led to the erection of multiple, at least partially conXicting classiWcations that can be grouped into two overall hypotheses. ...
Phylogenetic reconstructions of relations within the phylum Nematoda are inherently difficult but have been advanced with the introduction of large-scale molecular-based techniques. However, the most recent revisions were heavily biased towards terrestrial and parasitic species and greater representation of clades containing marine species (e.g. Araeolaimida, Chromadorida, Desmodorida, Desmoscolecida, Enoplida, and Monhysterida) is needed for accurate coverage of known taxonomic diversity. We now add small subunit ribosomal DNA (SSU rDNA) sequences for 100 previously un-sequenced species of nematodes, including 46 marine taxa. SSU rDNA sequences for >200 taxa have been analysed based on Bayesian inference and LogDet-transformed distances. The resulting phylogenies provide support for (i) the re-classification of the Secernentea as the order Rhabditida that derived from a common ancestor of chromadorean orders Araeolaimida, Chromadorida, Desmodorida, Desmoscolecida, and Monhysterida and (ii) the position of Bunonema close to the Diplogasteroidea in the Rhabditina. Other, previously controversial relationships can now be resolved more clearly: (a) Alaimus, Campydora, and Trischistoma belong in the Enoplida, (b) Isolaimium is placed basally to a big clade containing the Axonolaimidae, Plectidae, and Rhabditida, (c) Xyzzors belongs in the Desmodoridae, (d) Comesomatidae and Cyartonema belongs in the Monhysterida, (e) Globodera belongs in the Hoplolaimidae and (f) Paratylenchus dianeae belongs in the Criconematoidea. However, the SSU gene did not provide significant support for the class Chromadoria or clear evidence for the relationship between the three classes, Enoplia, Dorylaimia, and Chromadoria. Furthermore, across the whole phylum, the phylogenetically informative characters of the SSU gene are not informative in a parsimony analysis, highlighting the short-comings of the parsimony method for large-scale phylogenetic modelling.
... Little is known of the origins of the aphelenchoidids. Fossil remains, ca 25 mya old, of a putative aphelenchoidid were found in Mexican amber together with hyphae (Poinar, 1977(Poinar, , 2011, suggesting that these nematodes were fungal feeders. ...
The purposes of this paper are to clarify the taxonomic status of the fig-pollinating wasp associate Schistonchus sensu lato(Nematoda: Aphelenchoididae) and to suggest directions for future research on the systematics, life history and ecology of the group. Molecular phylogenetic analyses suggest that Schistonchus s.l.is polyphyletic, and the composition of the three major clades is outlined, together with information on nematode morphology, plant host species, associated pollinating wasp species, and distribution. Biological information and collection data is presented for Schistonchus s.l.from Ficussycones (Moracea) in Africa, Australia, Asia and Central America, and its putative phylogeny is discussed based on molecular and morphological evidence. Both wasps and figs are millions of years old and have worldwide distribution in tropical areas, i.e., opportunities for Schistonchus s.l.-like nematodes to have evolved could have occurred more than once. In addition, figs and their pollinating wasps have variable life histories, which could have provided opportunities for Schistonchus s.l.to also develop different life histories. However, these histories occur inside fig sycones and in association with wasps, which has apparently led to evolutionary convergence and extreme morphological conservatism. Diagnostic characters and their states, derived from examination of described species and morphospecies of Schistonchus s.l.and informed by molecular phylogenetic inferences, are discussed and illustrated. Schistonchus sensu strictois redefined, and Ficophagusn. gen. and Martinineman. gen. are proposed. Schistonchus s.s.is morphologically characterised by having the excretory pore opening in the region of, or posterior to, the metacorpus; Ficophagusn. gen. by having the excretory pore opening very near the cephalic region; and Martinineman. gen. by having it opening at the anterior end of the metacorpus. Several species of Schistonchus s.s.have a labial disc, but there is no evidence of this in either Ficophagusn. gen. or Martinineman. gen.
... Little is known of the origins of the aphelenchoidids. Fossil remains, ca 25 mya old, of a putative aphelenchoidid were found in Mexican amber together with hyphae (Poinar, 1977(Poinar, , 2011, suggesting that these nematodes were fungal feeders. ...
The purposes of this paper are to clarify the taxonomic status of the fig-pollinating wasp associate Schistonchus sensu
lato (Nematoda: Aphelenchoididae) and to suggest directions for future research on the systematics, life history and ecology of the
group. Molecular phylogenetic analyses suggest that Schistonchus s.l. is polyphyletic, and the composition of the three major clades is
outlined, together with information on nematode morphology, plant host species, associated pollinating wasp species, and distribution.
Biological information and collection data is presented for Schistonchus s.l. from Ficus sycones (Moracea) in Africa, Australia, Asia
and Central America, and its putative phylogeny is discussed based on molecular and morphological evidence. Both wasps and figs are
millions of years old and have worldwide distribution in tropical areas, i.e., opportunities for Schistonchus s.l.-like nematodes to have
evolved could have occurred more than once. In addition, figs and their pollinating wasps have variable life histories, which could have
provided opportunities for Schistonchus s.l. to also develop different life histories. However, these histories occur inside fig sycones and
in association with wasps, which has apparently led to evolutionary convergence and extreme morphological conservatism. Diagnostic
characters and their states, derived from examination of described species and morphospecies of Schistonchus s.l. and informed by
molecular phylogenetic inferences, are discussed and illustrated. Schistonchus sensu stricto is redefined, and Ficophagus n. gen. and
Martininema n. gen. are proposed. Schistonchus s.s. is morphologically characterised by having the excretory pore opening in the
region of, or posterior to, the metacorpus; Ficophagus n. gen. by having the excretory pore opening very near the cephalic region; and
Martininema n. gen. by having it opening at the anterior end of the metacorpus. Several species of Schistonchus s.s. have a labial disc,
but there is no evidence of this in either Ficophagus n. gen. or Martininema n. gen.
Keywords – diagnosis, Ficus, fig tree, fig wasp, molecular, morphology, mutualism, new combination, new genus, phoresy, syconia.
... Even where the whole of the phylum has been investigated authors often shoe-horned those groups together for which they did not have much detailed knowledge . Furthermore, the ontogeny and ultrastructure of nematodes is poorly understood and there is a lack of an informative fossil record (e.g. Poinar, 1977 Poinar, , 1983 Poinar, , 2003). Such diYculties have led to the erection of multiple, at least partially conXicting classiWcations (De) that can be grouped into two overall hypotheses. ...
Phylogenetic reconstructions of relations within the phylum Nematoda are inherently difficult but have been advanced with the introduction of large-scale molecular-based techniques. However, the most recent revisions were heavily biased towards terrestrial and parasitic species and greater representation of clades containing marine species (e.g. Araeolaimida, Chromadorida, Desmodorida, Desmoscolecida, Enoplida, and Monhysterida) is needed for accurate coverage of known taxonomic diversity. We now add small subunit ribosomal DNA (SSU rDNA) sequences for 100 previously un-sequenced species of nematodes, including 46 marine taxa. SSU rDNA sequences for >200 taxa have been analysed based on Bayesian inference and LogDet-transformed distances. The resulting phylogenies provide support for (i) the re-classification of the Secernentea as the order Rhabditida that derived from a common ancestor of chromadorean orders Araeolaimida, Chromadorida, Desmodorida, Desmoscolecida, and Monhysterida and (ii) the position of Bunonema close to the Diplogasteroidea in the Rhabditina. Other, previously controversial relationships can now be resolved more clearly: (a) Alaimus, Campydora, and Trischistoma belong in the Enoplida, (b) Isolaimium is placed basally to a big clade containing the Axonolaimidae, Plectidae, and Rhabditida, (c) Xyzzors belongs in the Desmodoridae, (d) Comesomatidae and Cyartonema belongs in the Monhysterida, (e) Globodera belongs in the Hoplolaimidae and (f) Paratylenchus dianeae belongs in the Criconematoidea. However, the SSU gene did not provide significant support for the class Chromadoria or clear evidence for the relationship between the three classes, Enoplia, Dorylaimia, and Chromadoria. Furthermore, across the whole phylum, the phylogenetically informative characters of the SSU gene are not informative in a parsimony analysis, highlighting the short-comings of the parsimony method for large-scale phylogenetic modelling.
This chapter discusses the evolutionary history of nematode parasites of invertebrates, vertebrates and plants based on fossil remains in amber, stone and coprolites dating from the Palaeozoic to the Holocene. The earliest parasitic nematode is a primitive plant parasite from the Devonian. Fossil invertebrate-parasitic nematodes first appeared in the Early Cretaceous, while the earliest fossil vertebrate-parasitic nematodes are from Upper Triassic coprolites. Specific examples of fossil nematode parasites over time are presented, along with views on the origin and evolution of nematodes and their hosts.
A fossil worm-like organism, ca. 0.5 mm long, showing cuticle, gut and setae. is contained in the solid part of the wall of a clitellate cocoon from the Early Cretaceous (Barremian). It is interpreted as having been entrapped and embedded in the intitially viscous cocoon secretion which solidified and thus prevented decay. Size, shape, posture, and an unsegmented but annulated cuticle with irregularly distributed setae have led to the identification of the fossil as a nematode. described as Captivonema cretacea gen. et sp. n., of uncertain family and order affinity. Fossil association end mode of preservation indicate a free-living life habit in damp plant litter.
Cell-free extracts of 93 strains from 23 species and biotypes ofPhotobacterium, Beneckea, andVibrio were electrophoresed on polyacrylamide gels and then stained for superoxide dismutase (SOD) activity. All strains exhibited
a single activity band with the exception ofPhotobacterium leiognathi, which had one major and two minor bands. Strains representative of all three genera were found to have SOD activities that
were sensitive to treatment with H2O2, suggesting that they were iron-containing enzymes. Examination of the effect of gel concentration on relative mobility (Rm)
suggested that all the iron-containing SODs had very similar molecular weight. Most species could be distinguished on the
basis of differences in the Rm values of their SODs.Vibrio was readily separable fromBeneckea andPhotobacterium. A limited electrophoretic analysis of the SODs fromAeromonas, Serratia, Proteus, Erwinia, and other species of terrestrial enterobacteria indicated groupings that were in agreement with previous studies.
Carnivory is the consumption of one animal by another animal; among invertebrates in terrestrial and freshwater ecosystems this type of feeding can take three forms: prédation, parasitoidism, and parasitism. Differences among these three functional modes involve (i) whether the duration of feeding on the prey item is quick or there is an accommodation, coevolutionary or otherwise, between the carnivore and the host prey; (ii) whether the prey or host is killed; (Hi) whether single or multiple prey or host items are consumed during the carnivore's lifespan, and (iv) the relative sizes of the carnivore and its prey or host. Uniformitarian and nonuniformitarian evidence directly relating to the history of carnivory can be found in exceptionally preserved deposits from the mid-Paleozoic to the Recent, but such evidence is relatively rare because carnivores are the least represented trophic group in ecosystems. Six types ofpaleobiological data provide evidence for carnivory: taxonomic affiliation, fossil structural andfunctional attributes, organismic damage, gut contents, coprolites, and indications ofmechanisms for predator avoidance. Only 12 invertebrate phyla have become carnivorous in the continental realm. Six are lophotrochozoans (Acanthocephala, Rotifera, Platyhelminthes, Nemertinea, Mollusca, and Annelida) and six are ecdysozoans (Nematoda, Nematomorpha, Tardigrada, Onychophora, Pentastoma, and Arthropoda). Most of these groups have poor continental fossil records, but the two most diversenematodes and arthropodshave comparatively good representation. The record of arthropods documents (i) the presence of predator s among primary producers, herbivores, and decomposers in early terrestrial ecosystems; (ii) the addition later in the fossil record of the more accommodationist strategies of parasitoids and parasites interacting with animal hosts; (Hi) the occurrence of simpler food-web structures in terrestrial ecosystems prior toparasitoid and parasite diversification; and (iv) a role for mass extinction in the degradation of food-web structure that ultimately affected carnivory. Future research should explore how different modes of carnivory have brought about changes in ecosystem structure through time. Despite numerous caveats and uncertainties, trace fossils left by predators on skeletons of their prey remain one of the most promising research directions in paleoecology and evolutionary paleobiology.
Parasitologists are fond of alluding to the possible antiquity of their chosen group. They may even place the origin in a specific period of geological time and trace its co-evolution, or lack thereof, with the hosts. These speculations usually make only passing comments on the actual fossil record, but a critical examination suggests that this area can throw much light on both the origins and evolution of parasitism. This review is concerned primarily with the fossil record and its immediate implications. It does not appraise parasite evolution in the light of evidence from sources, often of excellent quality, such as comparative anatomy and physiology or ecology. As some parasitologists may not be entirely familiar with the geological column and time scale, Table 1 depicts these and indicates some records of parasitism mentioned here, together with the major events in this history of life.(Accepted October 29 1980)
Fossil nematodes in pieces of Mexican amber, approximately 25 million years old, appeared to have been parasitized by fungi showing a striking resemblance to present-day nematophagous species.
IntroductionThe genera Photorhabdus and Xenorhabdus are members of the family Enterobacteriaceae that encompass the intestinal bacterial symbionts living in commensalism with entomopathogenic nematodes (EPNs) of the genera Heterorhabditis and Steinernema, respectively (Akhurst and Boemare, 1990; Forst et al., 1997). Most of them are pathogenic for insects when injected into the hemocoel. In addition, some nonsymbiotic strains of Photorhabdus have been identified as opportunistic pathogens for humans (Farmer et al., 1989; Peel et al., 1999). Various insect and vertebrate symbionts are members of the γ-subclass of Proteobacteria, which contains a wide spectrum of animal and human pathogens, such as members of the families Enterobacteriaceae, Legionellaceae, Pasteurellaceae, Vibrionaceae, and the genera Pseudomonas (sensu stricto) and Acinetobacter (Stackebrandt, 1999). Symbionts of EPNs are phylogenetic neighbors of an important group of endosymbionts of insects (the RDP tree of the [{ht ...
The genome of the insect pathogenPhotorhabdus luminescens TT01 strain contains multiple genes predicted to encode toxins. One of these,plu0840, has 55% sequence identity with an enterotoxin fromAeromonas hydrophila. In order to further investigate this gene, we successfully cloned the completeplu0840 fromPhotorhabdus sp. HB78 and expressed it as a GST-Plu0840 fusion protein inEscherichia coli BL21 (DE3) using pGEX-4T-1 as a vector. Most of GST-Plu0840 was insoluble and sequestered into inclusion bodies. The inclusion
bodies were harvested and dissolved. The resultant protein was cleaved and purified from the GST-tag. Oral bioassay showed
that Plu0840 inhibited growth ofSpodoptera litura andSpodoptera exigua larvae.
Photorhabdus luminescens, a Gram-negative bacterium, secretes a protein toxin (PL toxin) that is toxic to insects. In this study, the effects of the PL toxin on large receptor-free unilamellar phospholipid vesicles (LUVs) of Manduca sexta and on brush border membrane vesicles (BBMVs) of M. sexta and Tenebrio molitor were examined. Cry1Ac served as a positive control in our experiments due to its known channel-forming activity on M. sexta. Voltage clamping assays with dissected midguts of M. sexta and T. molitor clearly showed that both Cry1Ac and PL toxin caused channel formation in the midguts, although channel formation was not detected for T. molitor midguts under Cry1Ac and it was less sensitive to PL toxin than to Cry1Ac for M. sexta midguts. Calcein release experiments showed that both toxins made LUVs (unilamellar lipid vesicles) permeable, and at some concentrations of the toxins such permeabilizing effects were pH-dependent. The lowest concentrations of PL toxin were more than 600-fold and 24-fold lower to induce BBMV permeability of T. molitor and M. sexta than those to induce calcein release from LUVs of M. sexta. These further support that PL toxin is responsible for channel formation in the larvae midguts. The lower concentration to induce permeability in BBMV than in LUV is, probably, attributable to that BBMV has PL toxin receptors that facilitate the toxin to induce permeabilization. Furthermore, our results indicate that the effects of PL toxin on BBMV permeability of M. sexta were not significantly influenced by Gal Nac, but those of Cry1Ac were. This implies that PL toxin and Cry1Ac might use different molecular binding sites in BBMV to cause channel formation.
As an insect pathogen, Photorhabdus luminescens possesses an arsenal of toxins. Here we cloned and expressed a probable toxin from P. luminescens subsp. akhurstii YNd185, designated as Photorhabdus insecticidal toxin (Pit). The pit gene shares 94% nucleotide and 98% predicted amino acid sequence identity with plu1537, a predicted ORF from P. luminescens subsp. laumondii TT01 and 30% predicted amino acid sequence similarity to a fragment of a 13.6 kDa insecticidal crystal protein gene of Bacillus thuringiensis (Bt). The pit was expressed as a GST-Pit fusion protein in E. coli, most of which was insoluble and sequestered into inclusion bodies. The inclusion bodies were harvested and dissolved. The resultant protein was purified and the Pit was cleaved from the fusion protein by thrombin and purified from GST then used for bioassay. Pit killed Galleria mellonella (LD(50), 30 ng/larva) and Spodoptera litura (LD(50), 191 ng/larva) via hemocoel injection. Relative to a control that lacked toxin, Pit did not significantly increase mortality of S. litura and Helicoverpa armigera when introduced orally, but the treatment did inhibit growth of the insects. The present study demonstrated that Pit possessed insecticidal activity.
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