Detailed reconstruction of the musculature in Limnognathia maerski (Micrognathozoa) and comparison with other Gnathifera

Abstract

IntroductionLimnognathia maerski is the single species of the recently described taxon, Micrognathozoa. The most conspicuous character of this animal is the complex set of jaws, which resembles an even more intricate version of the trophi of Rotifera and the jaws of Gnathostomulida. Whereas the jaws of Limnognathia maerski previously have been subject to close examinations, the related musculature and other organ systems are far less studied. Here we provide a detailed study of the body and jaw musculature of Limnognathia maerski, employing confocal laser scanning microscopy of phalloidin stained musculature as well as transmission electron microscopy (TEM).ResultsThis study reveals a complex body wall musculature, comprising six pairs of main longitudinal muscles and 13 pairs of trunk dorso-ventral muscles. Most longitudinal muscles span the length of the body and some fibers even branch off and continue anteriorly into the head and posteriorly into the abdomen, forming a complex musculature. The musculature of the jaw apparatus shows several pairs of striated muscles largely related to the fibularium and the main jaws. The jaw articulation and function of major and minor muscle pairs are discussed. No circular muscles or intestinal musculature have been found, but some newly discovered muscles may supply the anal opening.ConclusionsThe organization in Limnognathia maerski of the longitudinal and dorso-ventral muscle bundles in a loose grid is more similar to the organization found in rotifers rather than gnathostomulids. Although the dorso-ventral musculature is probably not homologous to the circular muscles of rotifers, a similar function in body extension is suggested. Additionally, a functional comparison between the jaw musculature of Limnognathia maerski, Rotifera and Gnathostomulida, emphasizes the important role of the fibularium in Limnognathia maerski, and suggests a closer functional resemblance to the jaw organization in Rotifera.

Spiralian Phylogeny Informs the Evolution of Microscopic Lineages

“…Despite the microscopic size and understudied biology of most gnathiferan lineages (e.g., male micrognathozoans having not been observed), this topology has been supported previously with morphological data [6, 36, 37], albeit not using conventional molecular markers [38]. The main synapomorphies of Rotifera + Micrognathozoa have been uncovered in ultrastructural studies of the epidermis [39] and of the jaw apparatus composed of rod-like structures [37], with Rotifera + Micrognathozoa having some common supporting musculature [7].…”

“…Examples of such important ''Problematica'' are Lobatocerebromorpha [3,12,13], Diurodrilida [4,5], Micrognathozoa [6,7], and Loricifera [14], representing among the smallest animals ever discovered, which have received phylum-level affiliations or remain of uncertain position within Protostomia. We present here the first nuclear protein-coding data from representatives of all four clades, incorporating these and other new and published protein-coding surveys into a 402-ortholog, 90-taxon supermatrix comprising all free-living lineages of Spiralia (Table S1).…”

“…interstitial annelids originally considered ''ancestral'' to the other annelid taxa [25,26], other members of which have recently been shown to be non-monophyletic and derived from macrofaunal ancestors [27,28]. However, for Diurodrilus, several authors have also proposed a relationship outside of Annelida, specifically to the recently discovered Micrognathozoa, with which they share, e.g., characteristic mid-ventral trunk ciliophores and a ventral muscular plate of the pharynx [5][6][7]. Equally complicated is the case of Lobatocerebrum, originally described as ''a turbellariomorph member of the annelid line of evolution'' [3], i.e., an intermediate between Platyhelminthes and Annelida-a position maintained by Rieger [12] and Hazprunar et al [2] (who erected for it the phylum Lobatocerebromorpha), which we aimed to test here.…”

“…Moreover, they show unique features such as an inverted body-wall musculature or a novel pharyngeal organ. This and their ciliated epidermis have led some to propose relationships with other microscopic spiralians, namely Platyhelminthes, Gastrotricha, and in the case of Diurodrilus, with Micrognathozoa [6,7]-lineages that are grouped by some analyses into ''Platyzoa,'' a clade whose status remains uncertain [1,[8][9][10][11]. Here, we assess the interrelationships among the meiofaunal and macrofaunal members of Spiralia using 402 orthologs mined from genome and transcriptome assemblies of 90 taxa.…”

Nervous system and ciliary structures of Micrognathozoa (Gnathifera): evolutionary insight from an early branch in Spiralia

“…in rotifers [6–8], one genus of Gnathostomulida [9,10] and Micrognathozoa [11]. On the other hand, CLSM studies on the nervous system of Gnathifera are quite scarce (e.g.…”