Bursosaphia, DORJES, 1968 AND

Atherton, Sarah & Jondelius, Ulf, 2022, Phylogenetic assessment and systematic revision of the acoel family Isodiametridae, Zoological Journal of the Linnean Society 194, pp. 736-760 : 746-747

SYNONYMIZATION OF BURSOSAPHIA DÖRJES, 1968 AND PRAEAPHANOSTOMA DÖRJES, 1968

Dörjes (1968) placed great emphasis on the presence and structure of the bursa in his classification system, and numerous genera were created or separated based on small differences of this organ. When Dörjes (1968) described the species Bursosaphia baltalimaniaformis Dörjes, 1968 , he justified the creation of a new genus based on what he interpreted as bursal tissue (‘ bursales Gewebe ’) in which the true bursa was embedded. However, Dörjes (1968) was somewhat unclear in his description of the bursal tissue that surrounds the female system, stating only that it is a tissue that stores foreign sperm, that it is separate from the parenchyma of the rest of the body and that it similarly is present in species of Archaphanstoma (= Baltalimania ), which otherwise lack a true bursa. Dörjes (1968) also stated that bursal tissue may occur in other genera, but will typically disappear after a true bursa has formed. Unfortunately, this character has not been assessed for any species with a true bursa in any of the literature outside Dörjes’ (1968) description of Bursosaphia and, therefore, it is unclear how prevalent it is within Isodiametridae .

Unfortunately, no sequences of B. baltalimaniaformis are currently available, and so the relationship between this species and other acoels cannot be directly tested at this time. Regardless, results from our phylogenetic analyses suggest that bursal tissue is not a good character for distinguishing genera, since the only species other than B. baltalimaniaformis known to possess it – Baltalimania macrospiriferum and B. agile – do not on their own form a clade, but instead group with species of Baltalimania without bursal tissue ( Fig. 1 ). Given these results, and that there is no difference in the morphology of Bursosaphia and Praeaphanostoma apart from the bursal tissue, we propose to synonymize the two genera, with Bursosaphia the junior synonym for Praeaphanostoma .

REASSIGNMENT OF HAPLOGONARIA SCHILLINGI HOOGE & TYLER, 2015 TO THE GENUS PRAEAPHANOSTOMA DÖRJES, 1968

Our results show Haplogonaria schillingi to be nested in Praeaphanstoma and closely related to Praeaphanostoma rubrum . Sequences of the 18S, 28S and COI genes were published for H. schillingi and used in several phylogenetic analyses before the species was formally described. Jondelius et al. (2011) found the species (denoted there as Haplogonaria ‘ schillingi ’) positioned closely to Pseudaphanostoma smithrii and transferred the species to Pseudaphanostoma on this basis. Later, Nilsson et al. (2011) and Kånneby & Jondelius (2013) used the sequences in their phylogenetic analyses with results congruent to Jondelius et al. (2011), but still listing the species as Haplogonaria schillingi . Of note, at the time of all three publications, no sequences of any species of Praeaphanstoma were available and, indeed, results from our analysis show that P. smithrii is the closest sister to all other species of Praeaphanstoma. Hooge & Tyler (2015) eventually described the species, but found that the male copulatory organ lacks a muscular, tubular penis. Because such morphology is incongruous with the diagnostic character of Isodiametridae, Hooge & Tyler (2015) dubbed the species Haplogonaria schillingi and assumed the molecular data resulted from an error in handling specimens.

Our results, with the additional sequence data of Praeaphanstoma longum and especially P. rubrum , contradict the assertion that the position of H. schillingi in the phylogenetic analyses was due to some error. The morphology of H. schillingi is generally consistent with species of Praeaphanostoma . Praeaphanostoma is in part characterized by a moderate to small frontal organ, a muscular seminal vesicle, a seminal bursa with well-defined walls but without nozzles and a welldefined vagina with a sphincter, all characters that H. schillingi also possesses. Praeaphanostoma longum is additionally morphologically similar to H. shillingi in the shared possession of an unpaired ovary, common gonopore, diagonal muscles restricted to the anterior end and a characteristic bright-red pigmentation. The two species differ only in the size of the rhabdoids (small in P. longum , large in H. schillingi ), possession of a genital atrium (absent in P. longum , present in H. schillingi ) and, of course, the penis (present in P. longum , absent in H. schillingi ). Given such similarities, the position of H. schillingi is conceivable, and the absence of a penis could potentially represent a secondary loss. Praeaphanostoma includes several species – including those in our analysis that were the closest to H. schillingi – where the penis is a simple inpocketing of the epidermis, a condition that in Isodiametridae is only otherwise present in Proaphanostoma .

Thus, based on the positioning of the species in our phylogenetic analyses and the morphological similarity, we formally reassign Haplogonaria schillingi to Praeaphanostoma in Isodiametridae .

REDESCRIPTION OF PSEUDAPHANOSTOMA HYALINORHABDOIDA KÅNNEBY & JONDELIUS, 2013 AND REASSIGNMENT TO PRAEAPHANOSTOMA DÖRJES, 1968

Following a re-examination of the original collection notes and materials, it is clear from both photographs of live animals and from fixed, sectioned animals that Kånneby & Jondelius (2013) incorrectly interpreted the morphology of the reproductive system of Pseudaphanostoma hyalinorhabdoida in their original description. The female bursa was described as the seminal vesicle; the actual seminal vesicle and connecting vas deferens were dismissed as patches of free sperm outside the male copulatory organ, and the penis was not identified. Kånneby & Jondelius (2013) based the inclusion of the species in Pseudaphanostoma on the mistaken lack of female accessory organs and the relationship between this species and Pseudaphanostoma smithrii in their phylogenetic tree.

It is clear that this species does possess a female bursa, ciliated vagina and gonopore common to both the male and female system ( Figs 6–7 ). The presence of an unadorned female bursa is a characteristic of species of Praeaphanostoma , while species of Pseudaphanostoma lack all female accessory organs. Further, results from our DNA analyses confirm a close relationship between this species with Praeaphanostoma longum and P. rubrum ( Fig. 1 ), neither of which had sequences available when Kånneby & Jondelius (2013) performed their analysis. The morphological inaccuracies of the original description require that the species be redescribed, and the updated morphology and phylogenetic relationships support the transference of the species from Pseudaphanostoma to Praeaphanstoma.

Figures

Figure 1. Concatenated 28S, 18S and COI gene tree summary. Percent bootstrap values are given at each node. Sequences from six species of Isodiametridae and Actinoposthiidae represented only by 18S sequences downloaded from GenBank (Table S1) were excluded.

Figure 6. Praeaphanostoma hyalinorhabdoida. A, micropictograph of posterior end, male pore indicated by arrow. B, drawing of whole body. C, micropictograph of whole body. D, micropictograph of posterior end, focus on reproductive anatomy. b, bursa; eg, egg; f, frontal organ; i, intestine; m, mouth; mco, male copulatory organ; p, penis; r, rhabdoid glands; st, statocyst; t, testis; v, vacuole; vd, vas deferens.

Figure 7. Praeaphanostoma hyalinorhabdoida, sagittal view. A, drawing of whole body. B, sagittal section of whole body stained with haematoxylin–eosin. b, bursa; eg, egg; f, frontal organ; i, intestine; mco, male copulatory organ; p, penis; r, rhabdoid glands; st, statocyst; v, vacuole.