Jon Mallatt

Nearly complete rRNA genes assembled from across the metazoan animals: effects of more taxa, a structure-based alignment, and paired-sites evolutionary models on phylogeny reconstruction.

This study (1) uses nearly complete rRNA-gene sequences from across Metazoa (197 taxa) to reconstruct animal phylogeny; (2) presents a highly annotated, manual alignment of these sequences with special reference to rRNA features including paired sites (http://purl.oclc.org/NET/rRNA/Metazoan_alignment) and (3) tests, after eliminating as few disruptive, rogue sequences as possible, if a likelihood framework can recover the main metazoan clades. We found that systematic elimination of approximately 6% of the sequences, including the divergent or unstably placed sequences of cephalopods, arrowworm, symphylan and pauropod myriapods, and of myzostomid and nemertodermatid worms, led to a tree that supported Ecdysozoa, Lophotrochozoa, Protostomia, and Bilateria. Deuterostomia, however, was never recovered, because the rRNA of urochordates goes (nonsignificantly) near the base of the Bilateria. Counterintuitively, when we modeled the evolution of the paired sites, phylogenetic resolution was not increased over traditional tree-building models that assume all sites in rRNA evolve independently. The rRNA genes of non-bilaterians contain a higher % AT than do those of most bilaterians. The rRNA genes of Acoela and Myzostomida were found to be secondarily shortened, AT-enriched, and highly modified, throwing some doubt on the location of these worms at the base of Bilateria in the rRNA tree--especially myzostomids, which other evidence suggests are annelids instead. Other findings are marsupial-with-placental mammals, arrowworms in Ecdysozoa (well supported here but contradicted by morphology), and Placozoa as sister to Cnidaria. Finally, despite the difficulties, the rRNA-gene trees are in strong concordance with trees derived from multiple protein-coding genes in supporting the new animal phylogeny.

The evolutionary and genetic origins of consciousness in the Cambrian Period over 500 million years ago

Vertebrates evolved in the Cambrian Period before 520 million years ago, but we do not know when or how consciousness arose in the history of the vertebrate brain. Here we propose multiple levels of isomorphic or somatotopic neural representations as an objective marker for sensory consciousness. All extant vertebrates have these, so we deduce that consciousness extends back to the groups origin. The first conscious sense may have been vision. Then vision, coupled with additional sensory systems derived from ectodermal placodes and neural crest, transformed primitive reflexive systems into image forming brains that map and perceive the external world and the bodys interior. We posit that the minimum requirement for sensory consciousness and qualia is a brain including a forebrain (but not necessarily a developed cerebral cortex/pallium), midbrain, and hindbrain. This brain must also have (1) hierarchical systems of intercommunicating, isomorphically organized, processing nuclei that extensively integrate the different senses into representations that emerge in upper levels of the neural hierarchy; and (2) a widespread reticular formation that integrates the sensory inputs and contributes to attention, awareness, and neural synchronization. We propose a two-step evolutionary history, in which the optic tectum was the original center of multi-sensory conscious perception (as in fish and amphibians: step 1), followed by a gradual shift of this center to the dorsal pallium or its cerebral cortex (in mammals, reptiles, birds: step 2). We address objections to the hypothesis and call for more studies of fish and amphibians. In our view, the lamprey has all the neural requisites and is likely the simplest extant vertebrate with sensory consciousness and qualia. Genes that pattern the proposed elements of consciousness (isomorphism, neural crest, placodes) have been identified in all vertebrates. Thus, consciousness is in the genes, some of which are already known.

The Origin of the Vertebrate Jaw: Neoclassical Ideas Versus Newer, Development-Based Ideas

Abstract Here I consider ways to test two hypotheses of the origin of jawed vertebrates: my neoclassical hypothesis, which derived from comparative morphology; and the heterotopic hypothesis, which derives from modern developmental findings. The heterotopic hypothesis, unlike the neoclassical hypothesis, says that major developmental changes had to occur before the upper jaws could evolve: a caudal shift in the expression domains of genes that pattern oral structures; and the loss of ancestral, lamprey-like upper lips. To test whether these did occur, I propose studies on the development of chondrichthyans (sharks and chimaeroid ratfishes), an understudied group that is likely to retain primitive features of the jaw region. The heterotopic hypothesis says no gnathostome retains the upper lip that is so prominent in larval lampreys, yet the neoclassical hypothesis identified such lips in sharks and ratfishes, and it predicts that their lip-skeleton likewise develops from premandibular neural crest. The development and innervation of upper-lip muscles in lampreys and chimaeroids can also be compared. The proposed studies can determine if the upper lips of chondrichthyans and lampreys are homologous (which would support the neoclassical hypothesis), or homoplasious (which would support the heterotopic hypothesis). Also, I argue that the evolution of the upper jaws (as lateral structures) was not linked to a nasohypophyseal complex (which is a median structure), although such a link is claimed by the heterotopic hypothesis. Finally, I update the neoclassical hypothesis to address recent evidence that the trabeculae of the lamprey skull are not homologous to the trabeculae cranii of gnathostomes.

PUMPING RATES AND PARTICLE RETENTION EFFICIENCIES OF THE LARVAL LAMPREY, AN UNUSUAL SUSPENSION FEEDER

The suspension feeding larvae of lampreys (ammocoetes) inhabit fine-grained sediments where particulate organic matter is concentrated, but whose low permeability limits the rate at which ammocoetes can pump water (flow rate). This study determined: 1) flow rates through the pharynges of ammocoetes, both within and out of the sediment, and 2) the ability of ammocoetes to filter particles from suspension (retention efficiency) over a wide range of algal cell concentrations (Chlorella pyrenoidosa, 1-75 mg/l).For most suspension feeders, flow rate and retention efficiency must be measured indirectly (clearance method). Direct measurement was possible here, as ammocoetes remain apparently undisturbed in glass tubes that allow the separation of inhalent from exhalent ventilatory currents. Problems arise in attempting to use clearance methods to determine flow rates in burrowed suspension feeders, and these problems are discussed.Ammocoete flow rates are exceptionally low compared to the rates of other suspensi...

Reconstructing the Life Cycle and the Feeding of Ancestral Vertebrates

One goal of this symposium is to examine the earliest evolution of the vertebrates. This problem can be approached from an ecological perspective, by considering possible habitats and feeding modes of ancestral Paleozoic fish. This chapter will expand and re-evaluate some ideas put forth recently (Mallatt, 1984b). It deals with the initial vertebrate adaptive radiation, which occurred between the Cambrian and the Devonian periods, from about 550 to 375 million years ago. Fossil documentation of this radiation is fragmentary, so extant animals and habitats must be used to help interpret their Paleozoic ancestors and analogues. Except for its latest phase, this earliest radiation of fishes was probably confined to shallow marine environments (Denison, 1956; Spjeldnaes, 1967; Ritchie and Gilbert-Tomlinson, 1977; Repetski, 1978; Darby, 1982). The fossil record, while incomplete, is unambiguous on this point: there are no demonstrably freshwater fossil vertebrates known until the late Silurian (Denison, 1956).

Branchial ion fluxes and toxicant extraction efficiency in lamprey (Petromyzon marinus) exposed to methylmercury

Abstract This study used tubes to hold eel-like freshwater fish, larval lampreys (Petromyzon marinus). This apparatus allowed convenient measurement of: (1) how toxicants affect flux rates of Na+ and Cl− across the pharynx; and (2) the efficiency with which the pharynx extracts toxicant from solution. Methylmercury was presented to lampreys for 2–4 h at 13°C in an aqueous medium (0.2 mM NaCl and KHCO3) at a concentration of 180 μg Hg/l (about a 40-h LC50). Compared to control lampreys, animals exposed to methylmercury exhibited a significantly lower influx of Cl− (by 30%: 0.15 vs. 0.21 μM/g per h), a greater efflux of Na+ (by 30%: 0.34 vs. 0.26 μM/g per h), and a greater efflux of Cl− (by 22%: 0.36 vs. 0.3 μM/g per h). Influx of Na+ (0.23 μM/g per h) was not affected by methylmercury. The elevated efflux of Na+ and Cl− from the gills is consistent with established hypotheses that methylmercury increases the permeability of cell membranes to cations and other small molecules. Our data do not, however, support an oftenstated hypothesis that methylmercury inhibits the enzyme responsible for Na+ uptake into cells, Na+K+ATPase. Lampreys extracted methylmercury from solution with efficiencies of 41–66%, higher percentages than are recorded for other fish. Such exceptional extraction efficiencies may relate to the soft water used in this study.

Categorization of the mitochondria-rich cells in the gill epithelium of the freshwater phases in the life cycle of lampreys

Abstract The distribution and ultrastructure of the mitochondria-rich (MR) cells in the gills of larval (ammocoetes) and adult lampreys (Petromyzon marinus and Geotria australis) have been studied. One type of MR cell, which is found only in ammocoetes, occurs in groups on and between gill lamellae. Freeze-fracture replicas show that the apical membrane of this ammocoete MR cell contains globular particles. The second type of MR cell, which is present in both ammocoetes and adults in freshwater, is located between lamellae and at the base of the filament. This cell usually occurs singly and is typically intercalated between ammocoete MR cells in larval lampreys and between pavement cells and pavement and chloride cells in adult lampreys. It contains rod-shaped particles in either the apical membrane (subtype A) or, far less frequently, the lateral membrane (subtype B) and in membranes of cytoplasmic vesicles and tubules. These features characterize this intercalated MR cell as a member of a group of MR cells that are also found in urinary epithelia of tetrapods and the amphibian epidermis, where they are involved in H+ and HCO3- secretion. Because this type of MR cell disappears when the young adult lamprey enters the sea and reappears immediately after the fully grown adult re-enters freshwater on its spawning run, it is presumably essential for osmoregulation in freshwater. On the basis of electrophysiological studies on frog skin, it is proposed that the subtype A of the branchial intercalated MR cell of lampreys provides the driving force for the Na+ uptake by active H+ secretion. By analogy with urinary epithelia, the subtype B cells may exchange Cl- for HCO3-.

Pikaia gracilens Walcott: stem chordate, or already specialized in the Cambrian?

For the past 35 years, the Cambrian fossil Pikaia gracilens was widely interpreted as a typical basal chordate based on short descriptions by Conway Morris. Recently, Conway Morris and Caron (CMC) (2012, Biol Rev 87:480-512) described Pikaia extensively, as a basis for new ideas about deuterostome evolution. This new Pikaia has characters with no clear homologues in other animals, so they could be phylogenetically uninformative autapomorphies. These characters include a dorsal organ, posterior ventral area, posterior fusiform structure, and anterior dorsal unit. Yet CMC interpret most of the unusual characters as primitive for chordates, thereby interpreting Pikaia as an even more convincing stem chordate than before. Moreover, they claim that segment (myomere) shape is a reliable guide for defining a chordate and even for assigning animals to their correct place in deuterostome phylogeny. By defining sigmoidal segments as a basal chordate character, they situate Pikaia at the base of the chordates and banish fossil yunnanozoans (which have straight segments) to a position deep within the deuterostomes. In addition, they consider amphioxus, with its conspicuously chevron-shaped segments, to be so highly derived that it is of little use for reconstructing the first chordates. We question their overemphasis on the phylogenetic value of segment shape and their marginalizing of amphioxus. We deduce that Pikaia, not amphioxus, is specialized. We performed a cladistic analysis that showed the character interpretations of CMC are consistent with their wide-ranging evolutionary scenario, but that these interpretations leave unresolved the position of Pikaia within chordates.

High tolerance of lampreys to Kepone® toxicity

Larval sea lampreys (Petromyzon marinus) were exposed to the organochlorine insecticide Kepone® in freshwater solution in a continuous flow diluter system at 12 and 20°C. At 12°, the 36-hr LC50, 96-hr LC50, and incipient lethal concentrations were 1,100, 444 and 145 μg Kepone/ L, respectively, while at 20°, the 96-hr LC50 was 414 μg/L. These are the highest LC50 values for Kepone ever reported for a fish species. Rates at which larval lampreys accumulate and clear Kepone were measured at 12°C. The depuration rate constant (Kd: 0.13–0.46 per day) was the highest ever reported in a fish species, so rapid elimination may contribute to the exceptional ability of lampreys to survive acute Kepone poisoning. The uptake rate constant (Ku) was 450–650 per day, and the bioconcentration factor averaged about 1900. The most likely source of high tolerance of lampreys to Kepone is an ability to withstand high tissue levels: Lampreys survived body burdens of 500–600 μg Kepone/g, exceeding all other known vertebrates. Technical difficulties associated with the use of Kepone solutions are discussed, such as precipitation and loss from solution through apparent volatilization.

Comparative Analysis of Mitochondrial Genomes in Diplura (Hexapoda, Arthropoda): Taxon Sampling Is Crucial for Phylogenetic Inferences

Two-pronged bristletails (Diplura) are traditionally classified into three major superfamilies: Campodeoidea, Projapygoidea, and Japygoidea. The interrelationships of these three superfamilies and the monophyly of Diplura have been much debated. Few previous studies included Projapygoidea in their phylogenetic considerations, and its position within Diplura still is a puzzle from both morphological and molecular points of view. Until now, no mitochondrial genome has been sequenced for any projapygoid species. To fill in this gap, we determined and annotated the complete mitochondrial genome of Octostigma sinensis (Octostigmatidae, Projapygoidea), and of three more dipluran species, one each from the Campodeidae, Parajapygidae, and Japygidae. All four newly sequenced dipluran mtDNAs encode the same set of genes in the same gene order as shared by most crustaceans and hexapods. Secondary structure truncations have occurred in trnR, trnC, trnS1, and trnS2, and the reduction of transfer RNA D-arms was found to be taxonomically correlated, with Campodeoidea having experienced the most reduction. Partitioned phylogenetic analyses, based on both amino acids and nucleotides of the protein-coding genes plus the ribosomal RNA genes, retrieve significant support for a monophyletic Diplura within Pancrustacea, with Projapygoidea more closely related to Campodeoidea than to Japygoidea. Another key finding is that monophyly of Diplura cannot be recovered unless Projapygoidea is included in the phylogenetic analyses; this explains the dipluran polyphyly found by past mitogenomic studies. Including Projapygoidea increased the sampling density within Diplura and probably helped by breaking up a long-branch-attraction artifact. This finding provides an example of how proper sampling is significant for phylogenetic inference.