Evolutionary history of Chaetognatha inferred from molecular and morphological data: a case study for body plan simplification

Background

Chaetognatha are a phylum of marine carnivorous animals which includes more than 130 extant species. The internal systematics of this group have been intensively debated since it was discovered in the 18^th century. While they can be traced back to the earlier Cambrian, they are an extraordinarily homogeneous phylum at the morphological level - a fascinating characteristic that puzzled many a scientist who has tried to clarify their taxonomy. Recent studies which have attempted to reconstruct a phylogeny using molecular data have relied on single gene analyses and a somewhat restricted taxon sampling. Here, we present the first large scale phylogenetic study of Chaetognatha based on a combined analysis of nearly the complete ribosomal RNA (rRNA) genes. We use this analysis to infer the evolution of some morphological characters. This work includes 36 extant species, mainly obtained from Tara Oceans Expedition 2009/2012, that represent 16 genera and 6 of the 9 extant families.

Results

Cladistic and phenetic analysis of morphological characters, geometric morphometrics and molecular small subunit (SSU rRNA) and large subunit (LSU rRNA) ribosomal genes phylogenies provided new insights into the relationships and the evolutionary history of Chaetognatha. We propose the following clade structure for the phylum: (((Sagittidae, Krohnittidae), Spadellidae), (Eukrohniidae, Heterokrohniidae)), with the Pterosagittidae included in the Sagittidae. The clade (Sagittidae, Krohnittidae) constitutes the monophyletic order of Aphragmophora. Molecular analyses showed that the Phragmophora are paraphyletic. The Ctenodontina/Flabellodontina and Syngonata/Chorismogonata hypotheses are invalidated on the basis of both morphological and molecular data. This new phylogeny also includes resurrected and modified genera within Sagittidae.

Conclusions

The distribution of some morphological characters traditionally used in systematics and for species diagnosis suggests that the diversity in Chaetognatha was produced through a process of mosaic evolution. Moreover, chaetognaths have mostly evolved by simplification of their body plan and their history shows numerous convergent events of losses and reversions. The main morphological novelty observed is the acquisition of a second pair of lateral fins in Sagittidae, which represents an adaptation to the holoplanktonic niche.

     

Some aspects of buoyancy adaptations of chaetognaths

Chaetognaths mainly keep to a preferred depth range by movement and resistance achieved by body shape. Some species, for exampleSagitta lyra andS. hexaptera, developed conspicuous, voluminous, gelatinous inner parts in the lateral fins. These are considered an aid toward buoyancy, as they compensate the increasing density caused by maturing gonads. Probably, the small size of the sexual organs ofS. enflata can also be regarded as a buoyancy adaptation. Member of the Taxonomy Group at the Biologische Anstalt Helgoland     

Internal morphology and function of paired fins in the epaulette shark,hemiscyllium ocellatum

Paired fins and associated internal structures of the epauletic sharkHemiscyllium ocellatum, were described on the basis of three specimens. A comparison with other genera showed the epaulette shark to be, characterized by two elongated basal cartilages articulating with a distally projecting articular condyle on the coracoid, a loosely separated radial series with an intermediate series, a levator pectoralis inferior muscle and an anterolaterally developed depressor pectoralis muscle in the pectoral fin, and an elongated anterior pelvic basal cartilage articulating with a distally projecting articular condyle and an anterolaterally developed depressor pelvicus muscle in the pelvic fin. In captivity, the sharks exhibited both upright and crawling behavior on the bottom by using the pectoral and pelvic fins and bending the body. The distinctive morphological characters are shared by otherHemiscyllium species and are suggested as important factors enabling their unique behavior associated with a complex coral reef habitat.     

The leopardChimaera, a new species of chimaeroid fish from New Zealand (Holocephali, Chimaeriformes, Chimaeridae)

A new species ofChimaera is described from three specimens collected from deep water fishing grounds off the North Island of New Zealand at depths ranging from 327–1020 m. This species is distinguished from all other members of the genus by gray coloration with chocolate brown reticulations and spots covering the body and fins, as well as additional external features such as rounded pelvic fins, first dorsal fin with distinct white margin, preopercular and oral lateral line canals sharing a common branch, and morphology of pelvic claspers in males bifid, the distal 1/3 divided, with pale colored fleshy, distal lobes. Comparisons are made toC. monstrosa andC. owstoni, the two most similar species in the genus. this represents the first species ofChimaera to be described from New Zealand.     

New genus and species of the family stichaeidae from Hokkaido,Japan

Specimens of a new genus and species of the stichaeid fish,Leptostichaeus pumilus, were collected from the Okhotsk Sea off Hokkaido in Japan. The present new genus and species clearly differs from all the other genera and species of the stichaeid fishes in the following characters: 3 or 4 pectoral fin rays; 10 or fewer caudal principal rays; 79–82 dorsal spines; no pelvic fin; last interneural spine supporting a single dorsal spine; infraorbital, occipital and lateral line canals absent; moderate size of dorsal spine shorter than eye diameter; membranes of dorsal and anal fins widely connected with caudal fin; a large black spot divided by a yellow band present just above gill cover.     

Littorellicola billhawkinsi n. gen., n. sp. (Digenea: Aporocotylidae) from the myocardial lacunae of Florida pompano, Trachinotus carolinus (Carangidae) in the Gulf of Mexico; with a comment on the interrelationships and functional morphology of intertrabecular aporocotylids

Littorellicola billhawkinsi n. gen., n. sp. infects the myocardial lacunae of the ventricle and atrium of Florida pompano, Trachinotus carolinus in the northern Gulf of Mexico. It differs from other aporocotylid genera by the combination of having a body 10–30× longer than wide, a posterolateral body protuberance, lateral spine rows, an aspinous anterior sucker comprising a slightly muscular rim circumscribing the mouth, asymmetrical posterior ceca 14–20× length of the anterior ceca and lacking diverticula or secondary rami, tens of testes distributing in a cobblestone-like field anterior and posterior to the distal ends of the posterior ceca, an oviducal seminal receptacle comprising the distal portion of the oviduct, and a post-cecal ovary plus by lacking rosethorn-shaped spines, a pharynx, and a Laurer's canal. The new species appears host specific to Florida pompano because no conspecific infection was detected in 134 carangids of 8 species in 4 genera captured nearby the type locality. Psettarium sebastodorum Holmes, 1971 is transferred to the new genus, as Littorellicola sebastodorum (Holmes, 1971) n. comb., because it and the new species differ from species of Psettarium by the combination of having multiple testes plus 8 other features detailed herein. This report brings the number of nominal Gulf of Mexico aporocotylids to 12 species of 8 genera, represents only the second record of an aporocotylid from a carangid there, and supports the notion that elongated, “thread-like” aporocotylids with lateral spine rows are seemingly well-adapted for infecting myocardial lacunae or embedding in the myocardium of their definitive fish hosts.     

Composition of the genus Leptosagitta of the family Sagittidae (Chaetognatha) with descriptions of four new species from coastal waters of the Northwestern Sea of Japan

Keys for the identification of the presently known species of the genus Leptosagitta (fam. Sagittidae) are presented. Four new species of this genus found in shallow waters of Vostok Bay, Amursky Bay (Peter the Great Bay), and Kievka Bay (all of the Sea of Japan) are described in detail: L. kiyashkoi sp. n., L. latyshevi sp. n., L. magna sp. n., and L. pauca sp. n.     

Three new genera representing novel lineages of Sordariomycetidae (Sordariomycetes, Ascomycota) from tropical freshwater habitats in Costa Rica

Three new genera are established in the Sordariomycetidae based on morphological and molecular data (SSU and LSU nrDNA) to accommodate five ascomycete species collected from submerged woody debris in freshwater habitats from Costa Rica. The genus Bullimyces contains three new species, B. communis, B. costaricensis and B. aurisporus. Bullimyces is characterized by globose to subglobose, membranous, black, ostiolate ascomata; deliquescent, hyaline, globose cells that fill the center of the centrum; unitunicate asci that deliquesce early in some species; and septate, thick-walled ascospores with or without gelatinous sheaths or appendages. Bullimyces species form a well supported clade with 100% bootstrap support, but the position of the genus in the Sordariomycetidae remains unclear. The second genus, Riomyces, is represented by a single species, R. rotundus. Riomyces is characterized by globose to subglobose, membranous, black, ostiolate ascomata, unitunicate, cylindrical asci, hyaline, globose cells that fill the hamathecium and septate, thick-walled ascospores with a gelatinous sheath. Although Riomyces is morphologically similar to Bullimyces, the two genera did not group together with support in any analysis. The third genus, Hydromelitis, is represented by a single species, H. pulchella. Hydromelitis is characterized by pyriform, membranous, black, ostiolate ascomata, unitunicate asci lacking an apical structure, simple, thin-walled, septate paraphyses and hyaline to golden yellow, multiseptate, thick-walled ascospores with a gelatinous sheath. Bullimyces, Riomyces and Hydromelitis were nested within an unsupported clade consisting of members of the Ophiostomatales, Magnaporthales and freshwater Annulatacaceae sensu lato and sensu stricto.     

Systematics of Chaetognatha under the light of molecular data, using duplicated ribosomal 18S DNA sequences

While the phylogenetic position of Chaetognatha has became central to the question of early bilaterian evolution, the internal systematics of the phylum are still not clear. The phylogenetic relationships of the chaetognaths were investigated using newly obtained small subunit ribosomal RNA nuclear 18S (SSU rRNA) sequences from 16 species together with 3 sequences available in GenBank. As previously shown with the large subunit ribosomal RNA 28S gene, two classes of Chaetognatha SSU rRNA gene can be identified, suggesting a duplication of the whole ribosomal cluster; allowing the rooting of one class of genes by another in phylogenetic analyses. Maximum Parsimony, Maximum Likelihood and Bayesian analyses of the molecular data, and statistical tests showed (1) that there are three main monophyletic groups: Sagittidae/Krohnittidae, Spadellidae/Pterosagittidae, and Eukrohniidae/Heterokrohniidae, (2) that the group of Aphragmophora without Pterosagittidae (Sagittidae/Krohnittidae) is monophyletic, (3) the Spadellidae/Pterosagittidae and Eukrohniidae/Heterokrohniidae families are very likely clustered, (4) the Krohnittidae and Pterosagittidae groups should no longer be considered as families as they are included in other groups designated as families, (5) suborder Ctenodontina is not monophyletic and the Flabellodontina should no longer be considered as a suborder, and (6) the Syngonata/Chorismogonata and the Monophragmophora/Biphragmophora hypotheses are rejected. Such conclusions are considered in the light of morphological characters, several of which are shown to be prone to homoplasy.     

Ericandersonia sagamia, a new genus and species of deep-water eelpouts (Perciformes: Zoarcidae) from Japan

A new genus and species of deep-water zoarcid fish, Ericandersonia sagamia, is described on the basis of four specimens collected from Sagami Bay, Japan, at depths of 880–930 m. This species is placed in the subfamily Gymnelinae and is distinguished from all genera of gymnelines by the following characters: pseudosubmental crest present; frontals partially fused dorsally; parietals meeting in midline; pelvic fins absent; ventral ramus of posttemporal weak; postorbital head pores 5; pectoral-fin rays 14. The phylogenetic analysis (based on 42 morphological characters) indicates that its position is outside the highly modified (= advanced) genera Seleniolycus, Melanostigma, Puzanovia, Nalbantichthys, Opaeophacus, and Andriashevia.     

MORPHOLOGICAL STUDIES IN A NEW SPECIES OF ACROSYMPHYTON (RHODOPHYCEAE)

Abbott , Isabella A. (Hopkins Marine Sta. of Stanford U., Pacific Grove, Calif.) Morphological studies in a new species of Acrosymphyton (Rhodophyceae). Amer. Jour. Bot. 49(8): 845–849. Illus. 1962.—Acrosymphyton taylori sp. nov. (Dumontiaceae, Cryptonemiales, Rhodophyceae) is shown to have a sexual cycle essentially similar to that of the 2 other species in the genus, but differs in some details of the sexual structures and the vegetative structure. Acrosymphyton taylori, from the Hawaiian Islands, is the only member of the genus from the Pacific. Acrosymphyton is only one of several genera of red algae possessing soft, gelatinous, uniaxial thalli. A study of specimens from various herbaria showed that specimens of Dudresnaya and Calosiphonia have been confused with Acrosymphyton.     

A new species of Chiliotrichiopsis (Asteraceae: Astereae) from Peru

Chiliotrichiopsis peruviana Nesom, H. Rob. & Granda, a new species from Dept. Ayacucho in southwestern Peru, is described and illustrated. It is the only rayless species of the genus, now expanded to four species, and the only one that occurs outside of Argentina.Chiliotrichiopsis is one of six shrubby South American genera of Astereae (subtribe Hinterhuberinae) with paleate receptacles. Observations on morphology and a key to these genera provide perspective for the generic placement of the new species.     

颈斑尖猪鱼——中国南海隆头鱼科新纪录种

本文根据采自海南岛的标本描述了中国南海一新记录种:颈斑尖猪鱼(Leptojulis lambdastigma)。本种的主要形态特征为:体长形,体长为体高的3.7~4.0倍,为头长的3.1~3.6倍;头长为吻长的2.7~3.3倍,为胸鳍长的1.45~1.65倍;头裸露无鳞;两颌前端各具2对大犬齿,外侧1对犬齿弯向外后方;背鳍Ⅸ-12,臀鳍Ⅲ-12,胸鳍i(不分支)+11-12(分支);侧线完整,侧线鳞27;颈部具一个"V"形大黑斑,胸鳍后部的上方、侧线的下方具一小黑斑。新鲜标本头部具2条黄色纵带,沿体侧分别经眼和胸鳍基部向后达尾鳍基部;体侧背部具1条浅棕黄色条带;胸鳍基部棕红色,后部浅色;臀鳍浅蓝色;尾鳍下部淡蓝色,上部橙色。本种与尾斑尖猪鱼(L.urostigma)形态较为相似,主要差别在于颈斑尖猪鱼的颈部具有一显著的"V"形黑斑,尾鳍基部无黑斑(尾斑尖猪鱼具此黑斑)。     

First Record of Fossil Ghost Pipefish (Solenostomidae,Gasterosteiformes) in Russia

A skeleton of a ghost pipefish (Solenostomidae) from the Pshekha Subformation of the Khadum Formation (Lower Oligocene) in the Republic of Adygea was discovered. This is the first fossil record of Solenostomidae in Russia; moreover, it is the only ghost pipefish found in the Oligocene. To date, only two fossil solenostomid genera and species from the Eocene of Monte Bolca (Italy) have been recorded. The only Recent genus of this family, Solenostomus Lacepède, 1903, contains four species. The new specimen is incompletely preserved; it lacks a fragment of the body and some fins, precluding the establishment of genus and species of this form. However, the unique geographical position and age of the new fossil expand our knowledge of the evolution and geographical range of the family Solenostomidae.     

A new batfish,Coelophrys bradburyae (Lophiiformes: Ogcocephalidae) from Japan, with comments on the evolutionary relationships of the genus

A new ogcocephalid batfish,Coelophrys bradburyae, is described on the basis of a single specimen collected from the Pacific coast off Aomori, Japan, at a depth between 557–595 m. The species differs from others of the genus by having a small eye (7.1 in head length), short upper jaw (3.7 in head length), short pectoral and pelvic fins (length 3.0 and 9.6 in head length, respectively), small illicial cavity (width 5.3 in head length), and no bifurcated tubercles on the lateral surface of the body. A key to the species ofCoelophrys is given and the evolutionary relationships of the genus discussed based on cladistic analyses: the sister relationship withHalieutopsis was confirmed and possible paedomorphic states, including the globose body, proposed as having evolved secondarily from a flat-bodied ogcocephalid ancestor.     

The origins of adipose fins: an analysis of homoplasy and the serial homology of vertebrate appendages

Adipose fins are appendages found on the dorsal midline between the dorsal and caudal fins in more than 6000 living species of teleost fishes. It has been consistently argued that adipose fins evolved once and have been lost repeatedly across teleosts owing to limited function. Here, we demonstrate that adipose fins originated repeatedly by using phylogenetic and anatomical evidence. This suggests that adipose fins are adaptive, although their function remains undetermined. To test for generalities in the evolution of form in de novo vertebrate fins, we studied the skeletal anatomy of adipose fins across 620 species belonging to 186 genera and 55 families. Adipose fins have repeatedly evolved endoskeletal plates, anterior dermal spines and fin rays. The repeated evolution of fin rays in adipose fins suggests that these fins can evolve new tissue types and increased structural complexity by expressing fin-associated developmental modules in these new territories. Patterns of skeletal elaboration differ between the various occurrences of adipose fins and challenge prevailing hypotheses for vertebrate fin origin. Adipose fins represent a powerful and, thus far, barely studied model for exploring the evolution of vertebrate limbs and the roles of adaptation and generative biases in morphological evolution.     

Ateleaspis tessellata Traquair, a non-cornuate cephalaspid from the Upper Silurian of Scotland

Ateleaspis tessellata Traquair, a non-cornuate cephalaspid from the U. Silurian of Scotland, is re-examined on the evidence of new material from the original localities. The species is found to be less 'primitive' than was previously thought in that the pectoral fins are separated from the trunk posteriorly by a distinct sinus and the two dorsal fins are developed essentially as in Aceraspis robustus Kiaer. The ventral visceral exoskeleton is described for the first time. Ateleaspis and Aceraspis are so close in so many respects that retention of separate genera is unnecessary; Aceraspis must be suppressed since Ateleaspis has priority. Revised diagnoses of the genus Ateleaspis and its two species, A. tessellata Traquair and A. robustus (Kiaer), are given and their relationships with other non-cornuate cephalaspids discussed.