Joel W. Martin

Arthropod relationships revealed by phylogenomic analysis of nuclear protein-coding sequences

The remarkable antiquity, diversity and ecological significance of arthropods have inspired numerous attempts to resolve their deep phylogenetic history, but the results of two decades of intensive molecular phylogenetics have been mixed. The discovery that terrestrial insects (Hexapoda) are more closely related to aquatic Crustacea than to the terrestrial centipedes and millipedes (Myriapoda) was an early, if exceptional, success. More typically, analyses based on limited samples of taxa and genes have generated results that are inconsistent, weakly supported and highly sensitive to analytical conditions. Here we present strongly supported results from likelihood, Bayesian and parsimony analyses of over 41 kilobases of aligned DNA sequence from 62 single-copy nuclear protein-coding genes from 75 arthropod species. These species represent every major arthropod lineage, plus five species of tardigrades and onychophorans as outgroups. Our results strongly support Pancrustacea (Hexapoda plus Crustacea) but also strongly favour the traditional morphology-based Mandibulata (Myriapoda plus Pancrustacea) over the molecule-based Paradoxopoda (Myriapoda plus Chelicerata). In addition to Hexapoda, Pancrustacea includes three major extant lineages of ‘crustaceans’, each spanning a significant range of morphological disparity. These are Oligostraca (ostracods, mystacocarids, branchiurans and pentastomids), Vericrustacea (malacostracans, thecostracans, copepods and branchiopods) and Xenocarida (cephalocarids and remipedes). Finally, within Pancrustacea we identify Xenocarida as the long-sought sister group to the Hexapoda, a result confirming that ‘crustaceans’ are not monophyletic. These results provide a statistically well-supported phylogenetic framework for the largest animal phylum and represent a step towards ending the often-heated, century-long debate on arthropod relationships.

Decapod crustacean phylogenetics

Overviews of Decapod Phylogeny On the Origin of Decapoda, F. R. Schram Decapod Phylogenetics and Molecular Evolution, A. Toon, M. Finley, J. Staples, and K. A. Crandall Development, Genes, and Decapod Evolution, G. Scholtz, A. Abzhanov, F. Alwes, C. Biffis, and J. Pint Mitochondrial DNA and Decapod Phylogenies: The Importance of Pseudogenes and Primer Optimization, C. D. Schubart Phylogenetic Inference Using Molecular Data, F. Palero and K. A. Crandall Decapod Phylogeny: What Can Protein-Coding Genes Tell Us?, K. H. Chu, L. M. Tsang, K. Y. Ma1, T.-Y. Chan, and P. K. L. Ng Spermatozoal Morphology and its Bearing On Decapod Phylogeny, C. Tudge Evolution of Mating Systems in Decapod Crustaceans, A. Asakura A ShrimpaEURO (TM)s Eye View of Evolution: How Useful are Visual Characters in Decapod Phylogenetics?, M. L. Porter and T. W. Cronin Crustacean Parasites as Phylogenetic Indicators in Decapod Evolution, C. C. Boyko and J. D. Williams The Bearing of Larval Morphology on Brachyuran Phylogeny, P. F. Clark Advances in our Knowledge of Shrimp-like Decapods Evolution and Radiation of Shrimp-like Decapods: an Overview, C. H. J. M. Fransen and S. De Grave A Preliminary Phylogenetic Analysis of the Dendrobranchiata based on Morphological Characters, C. Tavares, C. Serejo and J. W. Martin Phylogeny of the Infraorder Caridea based on Mitochondrial and Nuclear Genes (Crustacea: Decapoda), H. D. Bracken, S. De Grave, and D. L. Felder Advances in our Knowledge of Thalassinoid and Lobsterlike Groups Molecular Phylogeny of the Thalassinidea based on Nuclear and Mitochondrial Genes, R. Robles, C. C. Tudge, P. C. Dworschak, G. C. B. Poore, and D. L. Felder Molecular Phylogeny of the Family Callianassidae based on Preliminary Analyses of Two Mitochondrial Genes, D. L. Felder and R. Robles The Timing of the Diversification of the Freshwater Crayfishes, J. Breinholt, M. PA (c)rez-Losada, and K. A. Crandall Phylogeny of Marine Clawed Lobster Families Nephropidae Dana, 1852, and Thaumastochelidae Bate, 1888, based on Mitochondrial Genes, D. Tshudy, R. Robles, T.-Y. Chan, K. C. Ho, K. H. Chu, S. T. Ahyong, and D. L. Felder The Polychelidan Lobsters: Phylogeny and Systematics (Polychelida: Polychelidae), S. T. Ahyong Advances in our Knowledge of the Anomura Anomuran Phylogeny: New Insights from Molecular Data, S. T. Ahyong, K. E. Schnabel, and E. W. Maas Advances in our Knowledge of the Brachyura Is the Brachyura Podotremata a Monophyletic Group?, G. Scholtz and C. L. Mclay Assessing the Contribution of Molecular and Larval Morphological Characters in a Combined Phylogenetic Analysis of the Superfamily Majoidea, K. M. Hultgren, G. Guerao, F. P. L. Marques, and F. P. Palero Molecular Genetic Re-examination of Subfamilies and Polyphyly in the Family Pinnotheridae (Crustacea: Decapoda), E. Palacios-Theil, J. A. Cuesta, E. Campos, and D. L. Felder Evolutionary Origin of the Gall Crabs (Family Cryptochiridae) based on 16S rDNA Sequence Data, R. Wetzer, J. W. Martin, and S. L. Boyce Systematics, Evolution, and Biogeography of Freshwater Crabs, N. Cumberlidge and P. K. L. Ng Phylogeny and Biogeography of Asian Freshwater Crabs of the Family Gecarcinucidae (Brachyura: Potamoidea), S. Klaus, D. Brandis, P. K. L. Ng, D. C. J. Yeo, and C. D. Schubart A Proposal for a New Classification of Portunoidea and Cancroidea (Brachyura: Heterotremata) based on Two Independent Molecular Phylogenies, C. D. Schubart and S. Reuschel Molecular Phylogeny of Western Atlantic Representatives of the Genus Hexapanopeus (Decapoda: Brachyura: Panopeidae), B. P. Thoma, C. D. Schubart, and D. L. Felder Molecular Phylogeny of the Genus Cronius Stimpson, 1860, with Reassignment of C. tumidulus and Several American Species of Portunus to the Genus Achelous De Haan, 1833 (Brachyura: Portunidae), F. L. Mantelatto, R. Robles, C. D. Schubart, and D. L. Felder Index Color Insert

External morphology of the male of Cyclestheria hislopi (Baird, 1859) (Crustacea, Branchiopoda, Spinicaudata), with a comparison of male claspers among the Conchostraca and Cladocera and its bearing on phylogeny of the ‘bivalved’ Branchiopoda

The adult male of Cyclestheria hislopi, sole member of the spinicaudate conchostracan clam shrimp family Cyclestheriidae and a species of potential phylogenetic importance, is described for the first time. Several previously unknown features are revealed. Among these are (1) the morphology of the dorsal organ, which is roughly similar in shape to the supposedly homologous structure in other clam shrimps but bears a relatively large, centrally located pore unique to the species; (2) an anterior cuticular pore presumably leading to the ‘internal’ space surrounding the compound eyes, and thereby homologous to the same pore in other clam shrimps and in the Notostraca; (3) the spination and setation of the antennae and thoracopods, and (4) the mature male first thoracopods (claspers). The male claspers are paired and essentially equal in size and shape on right and left sides of the body. The second pair of thoracopods are not modified as claspers, a situation different from all other spinicaudate families but shared (plesiomorphic we propose) with the laevicaudatans and most cladocerans. The claspers bear a field of special spine‐like setae on the extremity of the ‘palm’; this setal type, previously unrecognized, is unique to Cyclestheria. The palm of the clasper also bears two palps (one very small), as in other conchostracan species (both laevicaudatans and spinicaudatans). The movable finger of the clasper, modified from the thoracopod endopod, bears a row of long setae along its outer extremity, also unique. Cyclestheria exhibits a mixture of characters, some unique and others typical of the Spinicaudata (Conchostraca). Cladoceran clasper types are briefly reviewed. as are the claspers in the Spinicaudata and Laevicaudata (Conchostraca). Morphology of the clasper of Cyclestheria shows typical spinicaudate characters. It is suggested that claspers on the first thoracopods may be a synapomorphy for the Conchostraca and the Cladocera. The possible role of Cyclestheria or a Cyclestheria‐like ancestor in cladoceran phylogeny is briefly discussed in light of recent suggestions (Martin and Cash‐Clark, 1995) of cladoceran monophyly and possible ancestral relationships with this genus. Some possibilities concerning the phylogenetic position of Cyclestheria–either as a sister group to the rest of the Spinicaudata or as a sister group to the Cladocera—are discussed.

The external morphology of the onychopod ‘cladoceran’ genus Bythotrephes (Crustacea, Branchiopoda, Onychopoda, Cercopagididae), with notes on the morphology and phylogeny of the order Onychopoda

The onychopod ‘cladoceran’ genus Bythotrephes Leydig is reviewed and redescribed based on introduced material of the B. cederstroemi‘form’ from the Great Lakes of North America. Reviewed briefly are the systematic history, introduction into North America, and natural history of the genus. Using S.E.M. and light microscopy, we then illustrate a mixture of plesiomorphic and (predominantly) derived features, most of which can be explained as modifications for predation. An emended generic diagnosis includes unique and previously poorly known characters that serve to distinguish Bythotrephes from the confamilial genus Cercopagis, such as a distinctly bilobed labrum, spinose anterior mandibular process, small (exopodal?) spines on the external face of thoracopods 1–3, and a gnathobasic process (proximal endite) on thoracopod 1. A redescription, combined with observations on the external morphology, highlights several morphological peculiarities. These include the strongly bilobed labrum, the loss of one of the original two pairs of maxillae (with a question raised as to which pair has been lost), an unusual point of origin for the ‘proximal endite’ (termed herein the ‘gnathobasic process’ because of uncertainty of homology) on thoracopods two and three, a bulbous process of unknown significance located just posterior to the last thoracopod, and the presence of what might be a remnant of the food groove believed to have been present in a hypothesized ancestral group leading to the Onychopoda. The problem of whether Bythotrephes contains one dimorphic species or two species, B. Iongimanus and B. cederstroemi, is reviewed briefly, and the morphological feature in which these forms differ (the caudal process) is described in detail for the cederstroemi form. Comparison with descriptions of other cercopagidids suggests that Bythotrephes is a highly derived taxon, with short‐abdomen genera of the Podonidae and Polyphemidae (e.g., Polyphemus) appearing closer to the onychopod phyletic stem, and with the more closely related genus Cercopagis more derived still. Phylogeny within the Cladocera, and the possible origin of the Cladocera from a cyclestheria‐like ancestor among the spinicaudate conchostracans, is reconsidered. A hypothesis of evolutionary relationships is presented that depicts the ctenopods and anomopods as having arisen from a hypothetical Cyclestheria‐like ancestor, with the predatory cladoceran taxa Haplopoda and Onychopoda being derived from the base of the anomopod lineage. Some of the many problems in the suggested phylogeny are discussed.

Evolutionary genomics of the cold-adapted diatom Fragilariopsis cylindrus

The Southern Ocean houses a diverse and productive community of organisms. Unicellular eukaryotic diatoms are the main primary producers in this environment, where photosynthesis is limited by low concentrations of dissolved iron and large seasonal fluctuations in light, temperature and the extent of sea ice. How diatoms have adapted to this extreme environment is largely unknown. Here we present insights into the genome evolution of a cold-adapted diatom from the Southern Ocean, Fragilariopsis cylindrus, based on a comparison with temperate diatoms. We find that approximately 24.7 per cent of the diploid F. cylindrus genome consists of genetic loci with alleles that are highly divergent (15.1 megabases of the total genome size of 61.1 megabases). These divergent alleles were differentially expressed across environmental conditions, including darkness, low iron, freezing, elevated temperature and increased CO2. Alleles with the largest ratio of non-synonymous to synonymous nucleotide substitutions also show the most pronounced condition-dependent expression, suggesting a correlation between diversifying selection and allelic differentiation. Divergent alleles may be involved in adaptation to environmental fluctuations in the Southern Ocean.

The complete sequence of human chromosome 5

Chromosome 5 is one of the largest human chromosomes and contains numerous intrachromosomal duplications, yet it has one of the lowest gene densities. This is partially explained by numerous gene-poor regions that display a remarkable degree of noncoding conservation with non-mammalian vertebrates, suggesting that they are functionally constrained. In total, we compiled 177.7 million base pairs of highly accurate finished sequence containing 923 manually curated protein-coding genes including the protocadherin and interleukin gene families. We also completely sequenced versions of the large chromosome-5-specific internal duplications. These duplications are very recent evolutionary events and probably have a mechanistic role in human physiological variation, as deletions in these regions are the cause of debilitating disorders including spinal muscular atrophy.

Eulimnadia belki, a new clam shrimp from Cozumel, Mexico (Conchostraca: Limnadiidae), with a review of central and South American species of the genus Eulimnadia

ABSTRACT A new species of Eulimnadia, E. belki, is described from the Chankanaab National Park in Cozumel, State of Quintana Roo, Yucatan Peninsula, Mexico. The species also occurs in Venezuela. Eulimnadia belki can be distinguished from all other species of the Limnadiidae in the New World by the unusual morphology of the eggs. The morphology of the external egg shell, a promising taxonomic character, is compared to that of all species of Eulimnadia known from Central and South America.

Review of the clam shrimp family Lynceidae Stebbing, 1902 (Branchiopoda: Conchostraca), in the Americas

ABSTRACT The North, South, and Central American species of the Lynceidae Stebbing are reviewed. Morphological characters that distinguish the family, including several not previously known or not recognized as being of familial importance, are illustrated and discussed. Of the three known genera in the family, only two, Lynceus Muller and Paralimnetis Gurney, are known from North, Central, and South America; the genus Lynceiopsis Daday, known only from Africa, is described and discussed for comparative purposes. Taxonomic characters that can be reliably used to identify American species are primarily those of the male first thoracopods (claspers) and head region (rostrum). All American species are redescribed, with two exceptions. The validity of two species, Lynceus tropicus and L. rotundirostris. is questioned on the basis of the poor condition of type material and inadequate original descriptions. One new species of Paralimnetis Gurney is described from Texas. A key to the American species is included.

Austinograea williamsi, new genus, new species, a hydrothermal vent crab(Decapoda: Bythograeidae) from the Mariana Back-Arc Basin, western Pacific

Austinograea williamsi is described from hydrothermal vents in the Mariana Back-Arc Basin, a spreading center in the western North Pacific, at depths of 3,595-3,660 m. This is the first bythograeid crab described from the western Pacific, extending the range of the Bythograeidae approximately 12,500 km from the nearest previous collection sites along the East Pacific Rise. The species differs remarkably from all other brachyuran crabs in lacking eyes or moveable eyestalks; the possible remnant of the eyestalk is fused to the surrounding orbital region of the carapace and bears no cornea or pigment. The species is further distingushed by the coxa of the third maxilliped, which is nearly covered by the juxtaposition of the margin of the carapace with the sternum and chelipedal coxa, a character proposed herein to be of generic importance. Other characters serving to separate A. williamsi from species in the genera Bythograea and Cyanagraea are the presence of setose fields on the subhepatic surface and on the ventral dactylar surface of the chelae in both sexes, densely setose ventral margins on the merus and basi-ischium of all walking legs, chelipeds with fingers that meet along their entire occluding margins in both sexes (i.e., do not gape), and a relatively straight male first pleopod that bears small spinules and is longer than the second pleopod. The third maxillipeds and male pleopods of Cyanagraea, previously unknown, are described from a specimen taken at 13?N on the East Pacific Rise; the pleopods are more similar to those of Austinograea than to those of Bythograea. A key to the genera of the Bythograeidae is provided. Crabs of the family Bythograeidae are known only from deep waters at marine hydrothermal vents. The family was originally erected by Williams (1980) to accommodate Bythograea thermydron from the Galapagos vent fields. Subsequent to that species description there have been scattered reports of other bythograeids from the Galapagos and from other vent areas of the Pacific and Atlantic Oceans. Bythograea microps Saint Laurent, 1984, was described on the basis of one adult female (the 23.5mm carapace length holotype) and several subadults or juveniles. Saint Laurent (1984) also erected a second genus and a third species, Cyanagraea praedator, to accommodate two large adult females taken from the vicinity of black smokers at the 13?N vent fields on the East Pacific Rise. Subsequently, more specimens of C. praedator have been collected; three of them, including two males, were among material collected by physiologists of the Scripps Institution of Oceanography on the French Hydronaut Expedition to the same locality. More recently, Saint Laurent (1988) erected a fourth species, Bythograea intermedia, on the basis of a single megalopa larva and on the assumption that some of the smaller juveniles described by Williams (1980) were of this previously unrecognized species. Finally, Williams (1988) described Bythograea mesatlantica from vents along the Mid-Atlantic Ridge. Guinot (in press) erected the genus Segonzacia on the basis of this species. In the present paper, we describe a new genus and species of the Bythograeidae from hydrothermal vents on the spreading center of the Mariana Back-Arc Basin in the western North Pacific Ocean. This find extends the known range of the family Bythograeidae approximately 12,500 km to the west from the nearest previous collection sites along the East Pacific Rise. MATERIALS AND METHODS The material forming the basis of this report was collected during a series of dives with the submarine Alvin in April-May 1987. The collection sites consisted of 3 active vent fields along the spreading center of the Mariana Back-Arc Basin at about 18?N, just west of the Mariana Island Arc. These vent fields were spaced along 3.5 km of the ridge crest at depths between 3,595 and 3,660 m (Hessler et al., 1988). Most of the crabs were caught in baited traps actually intended for obtaining scavenging amphipods (Ingram and Hessler, 1983, fig. 2a). Consequently, the opening at the inner end of the entrance funnel was smaller than

Phylogenetics links monster larva to deep-sea shrimp

Mid-water plankton collections commonly include bizarre and mysterious developmental stages that differ conspicuously from their adult counterparts in morphology and habitat. Unaware of the existence of planktonic larval stages, early zoologists often misidentified these unique morphologies as independent adult lineages. Many such mistakes have since been corrected by collecting larvae, raising them in the lab, and identifying the adult forms. However, challenges arise when the larva is remarkably rare in nature and relatively inaccessible due to its changing habitats over the course of ontogeny. The mid-water marine species Cerataspis monstrosa (Gray 1828) is an armored crustacean larva whose adult identity has remained a mystery for over 180 years. Our phylogenetic analyses, based in part on recent collections from the Gulf of Mexico, provide definitive evidence that the rare, yet broadly distributed larva, C. monstrosa, is an early developmental stage of the globally distributed deepwater aristeid shrimp, Plesiopenaeus armatus. Divergence estimates and phylogenetic relationships across five genes confirm the larva and adult are the same species. Our work demonstrates the diagnostic power of molecular systematics in instances where larval rearing seldom succeeds and morphology and habitat are not indicative of identity. Larval–adult linkages not only aid in our understanding of biodiversity, they provide insights into the life history, distribution, and ecology of an organism.