Research Article |
Corresponding author: Natsumi Kanzaki ( nkanzaki@affrc.go.jp ) Academic editor: David Fitch
© 2014 Natsumi Kanzaki, Erik Ragsdale, Robin Giblin-Davis.
This is an open access article distributed under the terms of the Creative Commons Attribution License (CC BY 4.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Citation:
Kanzaki N, Ragsdale E, Giblin-Davis R (2014) Revision of the paraphyletic genus Koerneria Meyl, 1960 and resurrection of two other genera of Diplogastridae (Nematoda). ZooKeys 442: 17-30. https://doi.org/10.3897/zookeys.442.7459
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Recent inferences of phylogeny from molecular characters, as well as a reexamination of morphological and biological characters, reject the monophyly of the nematode genus Koerneria Meyl, 1960 (Diplogastridae). Here, Koerneria sensu lato is revised. The genus, which previously consisted of 40 species, is separated into three genera. Almost all of the transferred species are moved to the resurrected genus Allodiplogaster Paramonov & Sobolev in Skrjabin et al. (1954). Koerneria and Allodiplogaster are distinguished from each other by a weakly vs. clearly striated body surface, an undivided vs. divided stomatal cheilostom, and arrangement of the terminal ventral triplet of male genital papillae, namely in that v5 and v6 are paired and separated from v7 vs. v5–v7 being close to each other. Allodiplogaster is further divided into two groups of species, herein called the henrichae and striata groups, based on both morphological and life-history traits. The henrichae group is characterized by papilliform labial sensilla and male genital papillae, a conical tail in both males and females, and an association with terrestrial habitats and insects, whereas the striata group is characterized by setiform labial sensilla and male genital papillae, an elongated conical tail in both sexes, and an association with aquatic habitats. A second genus, Anchidiplogaster Paramonov, 1952, is resurrected to include a single species that is characterized by its miniscule stoma and teeth, unreflexed testis, and a distinct lack of male genital papillae or stomatal apodemes. Lastly, one further species that was previously included in Koerneria sensu lato is transferred to the genus Pristionchus Kreis, 1932. The revision of Koerneria sensu lato is necessitated by the great variability in its subordinate taxa, which occupy a variety of habitats, in addition to the increased attention to Diplogastridae as a model system for comparative mechanistic biology.
Allodiplogaster , Anchidiplogaster , Koerneria , Pristionchus , revision, phylogeny, taxonomy
Koerneria Meyl, 1960 heretofore consisted of 40 nominal species, following the revision by
In their revision of Diplogastridae,
Paraphyly of Koerneria sensu lato. Tree is simplified from
In this article, we revise the genus Koerneria by examining the original and subsequent descriptions of its nominal species. Based on morphological, biological, and molecular evidence, we separate Koerneria sensu lato into three genera. All renamed groups are hypothesized to be monophyletic and follow the precedent of previous classification systems (
Species of Koerneria sensu lato are classified herein into four typological groups (three genera, with one genus further separated into two morphological and ecological groups) based on the following characters or traits, which were selected due to their high availability and reliability, being relatively accurate even in old descriptions:
(1) Stomatal morphology, specifically the separation of cheilostom and presence of apodemes
(2) Male tail morphology, including shape and arrangement of genital papillae
(3) Female tail morphology
(4) Life-history characters, particularly habitat preferences
In addition to published literature, several species available in culture were examined for typological characters: Koerneria luziae, isolated from stag beetles from Japan (
Previous inferences of the phylogeny of Koerneria spp. indicate that two species, K. luziae (Körner, 1954) Meyl, 1960 and K. ruehmi Atighi, Pourjam, Kanzaki, Giblin-Davis, De Ley, Mundo-Ocampo & Pedram, 2013, form a well-supported clade that is the sister group to most or all other sequenced Diplogastridae (
Fig.
Schematic drawings of the generic characters of Koerneria and Allodiplogaster. From left to right: stenostomatous form, eurystomatous form, female tail, and male tail characters. From top to bottom: Koerneria, aquatic Allodiplogaster (“striata” species group) and two types of terrestrial Allodiplogaster (“henrichae” species group). For the stenostomatous form of A. sudhausi (not shown), see
Generic diagnosis
1) Stomatal dimorphism occasionally present
2) Body-wall cuticle with weak vertical striations
3) Cheilostom usually forming short, undivided tube; rugae absent
4) Stegostom with dorsal claw-like tooth, right subventral tooth, and left subventral serrated figs or ridges
5) Postdental region of stegostom with left and right apodemes directed subventrad
6) Female gonad amphidelphic
7) Anterior two ventral and distal pairs of genital papillae (v5 and v6) close to each other, the posterior pair (v7) being clearly apart from v6
8) Short and conical male tail (c’ is usually ≤ 3) usually with short spike or with small, bursa-like or membranous appendage at tail tip
9) Known from terrestrial habitats, often in association with insects
Type species
Diplogaster goffarti Körner, 1954
comb. Koerneria goffarti Meyl, 1960
Other species
K. erlangensis (Sachs, 1950) Sudhaus & Fürst von Lieven, 2003
K. luziae (Körner, 1954) Meyl, 1960
K. ruehmi Atighi, Pourjam, Kanzaki, Giblin-Davis, De Ley, Mundo-Ocampo & Pedram, 2013
K. sinodendroni (Körner, 1954) Meyl, 1960
K. systenoceri (Körner, 1954) Meyl, 1960
Following this restricted definition of Koerneria, most of the remaining species of Koerneria sensu lato are transferred to the resurrected genera Anchidiplogaster and Allodiplogaster. One species, which was previously combined as K. dubia (Hnatewytsch, 1929) Sudhaus & Fürst von Lieven, 2003 is returned to Anchidiplogaster based on a suite of characters unique to this taxon as well as by the lack of stomatal apodemes, an absolute character of Koerneria as defined both previously and herein:
Generic diagnosis
1) Miniscule, undivided stoma with two small, similarly sized pyramidal teeth (one dorsal and one right subventral)
2) Stomatal apodemes absent
3) Male genital papillae absent
4) Testis without flexure
Type and only species
=Diplogaster dubia Hnatewytsch, 1929
comb. Anchidiplogaster Paramonov, 1952
All but one of the remaining species of Koerneria sensu lato are transferred to the other resurrected genus, Allodiplogaster. This name has priority (ICZN 23.1) over other names that are available for this taxonomic grouping, which consist of Diplenteron Andrássy, 1964, Glauxinemella Gagarin, 1998, and Gobindonema Khera, 1970. Furthermore, Allodiplogaster is separated into two putatively monophyletic groups of species, which we designate as the “henrichae group” and “striata group” based on morphological and biological evidence.
Fig.
=Diplenteron Andrássy, 1964: D. colobocercus Andrássy, 1964
=Gobindonema Khera, 1970: G. filicaudata Khera, 1970
nec Gobindonema Sood & Prashad, 1974 (Trichostrongylidae)
=Glauxinemella Gagarin, 1998: G. striata Gagarin, 1998
Generic diagnosis
1) Stomatal dimorphism occasionally present
2) Body-wall cuticle with clear vertical striations
3) Cheilostom separated into six per- and interradial figs or rugae
4) Stegostom with dorsal claw-like tooth, right subventral tooth, and left subventral serrated figs or ridges
5) Postdental region of stegostom with left and right apodemes directed subventrad
6) Female gonad amphidelphic; rarely prodelphic
7) Distal triplet papillae of males (v5-7) close to each other
8) Tail of male and females highly variable in shape
9) Known from variable habitats including terrestrial insect associates and aquatic species
Type species
Diplogaster henrichae Sachs, 1950
comb. Allodiplogaster henrichae Paramonov & Sobolev in Skrjabin, Shikobalova, Sobolev, Paramonov & Sudarikov, 1954
Other species
henrichae group of Allodiplogaster
1) Labial sensilla usually papilliform
2) Female tail usually conical with or without filiform tip
3) Male tail usually conical with short spike
4) Male genital papillae short and papilliform
5) Known from terrestrial habitats, often in association with insects
A. colobocerca (Andrássy, 1964), comb. n.
=Mononchoides potohikus Yeates, 1969
A. hirschmannae (Sachs, 1950), comb. n.
A. histophora (Weingärtner, 1955), comb. n.
A. hylobii (Fuchs, 1915), comb. n.
A. incurva (Körner, 1954), comb. n.
A. labiomorpha (Kühne, 1995), comb. n.
A. lepida (Andrássy, 1958), comb. n.
A. lucani (Körner, 1954), comb. n.
A. pierci (Massey, 1967), comb. n.
A. pini (Fuchs, 1931), comb. n.
A. robinicola (Rühm, 1956), comb. n.
A. sudhausi (Fürst von Lieven, 2008), comb. n.
striata group of Allodiplogaster
1) Labial sensilla setiform
2) Male and female tail usually elongate-conical, with or without filiform tip
3) Male genital papillae setiform
4) Known from aquatic habitats
A. angarensis (Gagarin, 1983), comb. n.
A. aquatica (Dassonville & Heyns, 1984), comb. n.
A. baicalensis (Tsalolichin, 1972), comb. n.
A. carinata (Zullini, 1981), comb. n.
A. didentata (Hnatewytsch, 1929), comb. n.
=Diplogaster curvidentatus Altherr, 1938
=Diplogaster obscuricola Altherr, 1938
=Diplogaster quadridentatus Altherr, 1938
A. filicaudata (Khera, 1970), comb. n.
A. ivanegae (Gagarin, 1983), comb. n.
A. lupata (Shoshin, 1989), comb. n.
A. mordax (Shoshin, 1989), comb. n.
A. mulveyi (Ebsary, 1986), comb. n.
A. pantolaba (Shoshin, 1989), comb. n.
A. pararmata (Schneider, 1938), comb. n.
=Diplogaster armatus apud Filipjev, 1930, nec Hofmänner, 1913
A. regia (Shoshin, 1989), comb. n.
A. ruricula (Gagarin, 1983), comb. n.
A. sphagni (Soós, 1938), comb. n.
A. strenua (Gagarin, 1983), comb. n.
A. striata (Gagarin, 1998), comb. n.
A. tenuipunctata (Altherr, 1938), comb. n.
A. terranova (Ebsary, 1986), comb. n.
The single remaining species previously included in Koerneria sensu lato is transferred to Pristionchus Kreis, 1932. This transfer is supported by the absence of subventral apodemes, the key character diagnosing Koerneria sensu lato:
Pristionchus macrospiculum (Altherr, 1938), comb. n.
The separation of Koerneria as circumscribed herein from Allodiplogaster, Anchidiplogaster, and Pristionchus is strongly supported by the structure of the cheilostom, arrangement of male genital papillae, and phylogeny as inferred independently from molecular sequence characters (
The distinct morphology of Anchidiplogaster dubia, especially its lack of genital papillae in several observed male specimens separates this species from all other Diplogastridae and supports its reestablishment in that genus. Further indicating the distinctness of this species from most other known Diplogastridae is its unreflexed testis flexure, as a flexure was previously considered a plesiomorphic character of the entire family (
The split of Allodiplogaster into the henrichae and striata groups is also supported by morphology, principally by the tail of both sexes, which is usually much longer in striata group than in henrichae group, and by the male genital papillae and labial sensilla, which are distinctly setiform in striata group. The separation of the two proposed groups of Allodiplogaster is only confounded by overlapping morphological characters, namely the fish-bone-like swellings along the pharyngeal lumen that are present in henrichae group species, Allodiplogaster spp. RGD227 and RGD228, as well as in one species of the striata group, A. carinata, although not in another striata group species such as A. pararmata (
Other morphological characters may further support to separate henrichae group from as a monophyletic clade distinct from the striata group and from Koerneria.
Dimorphism has been confirmed in at least two species in this group, including one undescribed species (Kanzaki and Ragsdale et al. unpubl. obs.)
Species status and several key characters of Koerneria sensu lato in the revised genera.
Data type: Summary of typological characters as a spread sheet.
Explanation note: Taxonomic history, morphological (typological) characters, and life-history traits of Koerneria sensu lato in the revised genera.