Xenocoelomorpha is a phylum comprised of three clades of mostly marine worms: Xenoturbellida, Nemertodermatida and Acoela. Of the 452 currently described species in Xenocoelomorpha, order Acoela is the most speciose group, comprising 428 species (Flanders Marine Institute, 2021). Bursalia is the most complex and well-described suborder of Acoela, however the entire phylum is nonetheless distinguished from other marine worms by their simplicity and lack of features. Globally distributed and occupying a wide range of habitats, it is widely accepted that Xenocoelomorpha are the basal bilaterian and are thus of particular evolutionary interest.

Acoels exhibit a simple bilaterian body plan, characterised by a lack of features. The epidermis is completely ciliated, which allows for locomotion, and lacks a cuticle, giving rise to a soft-bodied organism (Jondelius et al, 2011). The body is flattened dorso-ventrally, with a distinct anterior and posterior end, the former possessing a statocyst (Ehlers, 1986). The position of the mouth, if it is present at all, is ventral and varies from the posterior to far anterior (Hejnol and Pang, 2016). Interestingly, this clade shows the most variation in mouth position of any animal group (Achatz et al, 2013). While the mouth of most Acoel species is positioned in the middle of the body, the Bursalia specimen observed in this instance had an anterior mouth. The suborder Bursalia are distinguished from other Acoels by the presence of two eyespots (ocelli) at the anterior end (Jondelius et al, 2011).

Acoels are very small, ranging from less than 1mm to 15mm in some species (Achatz et al, 2013). Most are translucent or milky-coloured, although some are coloured by pigmentation from algal symbionts (common in species residing in sun-exposed habitats), or glandular secretions called rhabdoids (Achatz et al, 2013). The Bursalia species described here is approximately 2mm long. The body is clear except for a yellow mass, which subsequently appears green under the microscope. This is likely an aggregation of gut cells, which form the syncytial mass Acoels utilise for digestion (Hejnol and Pang, 2016). Two ocelli were visible at the anterior end. Unfortunately, the statocyst could not be confidently discerned under the compound microscope, as the specimens were damaged due to their delicate nature.

Habitat

While the vast majority of Acoels are free-living marine worms, seven parasitic species and two freshwater species have been described (Achatz et al, 2013). Acoels inhabit a wide range of marine habitats, to which their body shape is related. Those living in sand are long and slender in order to move through the sediment, while Acoels in mud are often a compact, droplet shape, to allow effective locomotion through densely packed, fine sediment (Achatz et al, 2013). Acoels on reefs, or those living in rubble environments are often broader and flatter, to move over and between hard surfaces. Finally, pelagic Acoels tend to have a disc-shaped body, or enrolled sides, to move efficiently through the water column (Achatz et al, 2013). Bursalia are typically benthic, and the species observed in this instance hailed from a hard substrate, biofouling community and did not appear to be specialised to any particular environment based on body shape. Rather, it appeared to be a more generalised, flattened cylinder.

Feeding

Acoel diet again varies with habitat, and body size. Species of Acoel have been reported to feed on bacteria, unicellular organisms, crustaceans, molluscs and worms, including other Acoels. Some species have even been observed to engage in cannibalism, such as Conaperta flavibacillum (Achatz et al, 2013). The Bursalia specimens were observed to ingest particulate matter under the microscope. Most extant species of Acoel lack a muscular pharynx, so in order to ingest food, additional ventral muscles pull the posterior part of the body and the mouth forward, over the food (Jondelius et al, 2011).

Species interactions

There is very limited research into ecological interactions of free-living Acoels. Interestingly, the specimens observed in class appeared to be associated with a colonial ascidian. The worms moved over and into the ascidian and did not stray from it unless disturbed. One potential explanation is that the Acoels were utilising the ascidian as a food source. Alternatively, the ascidian may have served a protective role. If the ascidian was toxic, but the Acoels were immune to any effects, this could be an effective strategy to avoid predation. There is no research on any interactions between Acoels and ascidians. If this ecological interaction is documented again in the future, it may be worth investigating.

Life history and Reproduction

Acoels are hermaphrodites and can reproduce by sexual reproduction (Jondelius et al, 2011). Individuals have either paired or single ovaries and testes, or a single mixed gonad (Jondelius etal, 2011). Some species have secondary female organs, including a vagina and copulatory bursa, which allows for the storage and delivery of sperm (Jondelius et al, 2011). The presence of a copulatory bursa is a distinguishing characteristic of the suborder Bursalia (Jondelius et al, 2011). Secondary male organs include stylets and penes, which facilitate copulation (Petrov, 2007). Identification of Acoel species has historically relied on an examination of the morphology and anatomy of male copulatory organs under a microscope (Petrov, 2007). This makes identification of Acoels particularly complex, due to their small size and easily-damaged, soft bodies.

Fertilisation occurs internally via the male and female copulatory organs described above. Depending on the species, eggs are laid individually or in clusters through the mouth, female gonopore, or body wall rupture (Hejnol and Pang, 2016). One Bursalia specimen in class was observed to lay a cluster of around half a dozen grey-coloured eggs. When viewed under the microscope, the ocelli of the developing embryos were visible. Unfortunately, these photos were lost. During development, Acoels exhibit a unique pattern of cleavage unlike any other metazoan, known as ‘duet spiral cleavage’ (Henry, Martindale and Boyer, 2000).  Instead of perpendicular to the animal-vegetal axis, the second cleavage plan is an unequal ‘spiral’. Such cleavage pattern is an apomorphy of the Acoels (Ruiz-Trillo et al, 1999). Upon hatching, Acoels undergo direct development, which has been proposed to be the ancestral bilaterian condition, rather than a biphasic life cycle (Ruiz-Trillo et al, 1999).

Certain Acoel clades have also been observed to undergo asexual reproduction. Species of the family Paratomellidae undergo paratomy, which involves the preformation of organs before separation, resulting in a chain of zooids, ready to detach from the parent (Dorjes, 1966). On the other hand, architomy, whereby organs are formed after the separation of the parent and daughter, is common in the family Convolutidae (Bartolomaeus and Balzer, 1997). Finally, asexual budding has also been observed in one species of Acoel (Shannon and Achatz, 2007).

Behaviour

There is limited research into Acoel behaviour, likely owing to their small size. On the settlement plates, Acoels were observed to glide over surfaces in a group, with a number of smaller specimens following a larger one. Unfortunately, this behaviour was not able to be documented. The worms reacted to touch by using their mouth to strongly adhere to the substrate and were not easily moved. Once in the petri dish, the worms moved to the edges of the dish, likely seeking protection, and attempted to move away from disturbances.

One study of a Bursalia worm species, Symsagittifera roscoffensis, demonstrated that Acoel worms interact to coordinate their movements (Franks et al, 2016). At high densities, the worms engage in circular milling, whereby the worms move around in a distinct circular pattern. Proposed evolutionary advantages of this behaviour include protection by numbers, or rapid colonisation of substrate by formation of a biofilm (Franks et al, 2016). Even at low densities, the worms were observed to coordinate their movements and began to move in small polarised groups (Franks et al, 2016). While this would appear to be supported by observations from the settlement plates, it would be of future interest to observe this behaviour in other species.

Acoels are distinguished from other small worms by their very simple anatomy. As sister taxa to the Nephrozoa, Acoels lack an excretory, circulatory and respiratory system. For these processes, they rely on diffusion. They also lack a body cavity between the gut and epidermis – instead, this region is filled with parenchymal cells (Achatz et al, 2013).

Neuro-Muscular System

Unlike other members of Xenoacoelomoprha (Xenoturbellida and Nermertodermatida),Acoels possess a clear aggregation of neural cells, which in more derived forms, can be likened to a brain (Gavilan, Perea-Atienza and Martinez, 2016). Moreover, Acoels demonstrate high neuroanatomy plasticity, whereby basal clades look very different to more complex species within Acoela, thus the nervous system of different Acoels have been extensively studied to track evolution within the group (Achatz and Martinez, 2012).

While locomotion is achieved by ciliary gliding, Acoels havea diverse range of musculature to allow for contraction and bending. Dorso-ventral muscles allow the body to flatten, while a range of body wall and parenchymal muscles generate bending, shortening and lengthening (Achatz et al, 2010). Such a complicated range of motions requires coordination from a sufficiently advanced neural pathway with complex connectivity (Achatz and Martinez, 2012).

The Acoel neuro-muscular system is comprised of the statocyst, motor neurons and inner muscles (Achatz and Martinez, 2012). Owing to the Acoel statocyst morphology differing from other groups, its function is still unclear, as researchers believe it may not be able to function as a ‘true’ georeceptor (Gavilan, Perea-Atienza and Martinez, 2016). At the anterior end, an aggregation of neurons forms a brain or ‘statocyst ganglion’ around the statocyst. This aggregation can be barrel-shaped, ring-shaped, or a bi-lobed mass, with a complex network of connectives and commissures allowing for muscular coordination (Achatz et al, 2013). Basal Acoels appear to have ring- or barrel-shaped statocyst ganglions, while more complex forms develop a bi-lobed mass (Achatz etal, 2013). This complex and highly integrated nervous system allows Acoels to move faster, react to more types of stimuli and engage in highly coordinated processes such as copulation, unlike other members of Xenoacoelomorpha (Achatz and Martinez, 2012).

Digestive system

Digestion in Acoels occurs in a blind gut, lacking gastric subdivision, characterised by only one gut opening (Hejnol and Pang, 2016). Moreover, there is no gut lumen – instead, the gut is syncytial (Tyler and Hooge, 2004).The gut is lined by the gonads (Hejnol and Pang,2016). Moreover, there is no stomatogastric nervous system (Achatz and Martinez, 2012).

Stem cell system

While Acoels are no longer classified as a member of phylum Platyhelminthes, researchers have historically struggled to reconcile separating the two for a number of reasons (to be explored later), including that they share a very similar stem cell system (Egger et al, 2009). Stem cells in Acoels are located in the parenchyma (space between the gut and body walls) and are called neoblasts (Perea-Atienza et al, 2013). The stem cell system allows for growth and maintenance of the body, and as a result, possesses regenerative capabilities (Hejnol and Pang, 2016). Studies have shown that certain species of Acoel can completely regenerate all posterior structures within ten days, while few can regenerate their entire head, statocyst and ocelli (Perea-Atienza et al, 2013; Yamasu, 1991).

While most described species inhabit coastal sediment, their full global diversity is largely unknown, and recent studies suggest it may be greater than previously thought. Acoels have been found to inhabit a range of coastal and deep-sea benthos, as well as planktonic environments within temperate, tropical and equatorial latitudes (Arroyo et al, 2016). Fossil evidence of Acoels in the Antarctic has also been discovered (Arroyo et al, 2016). Moreover, molecular studies across these habitats show broader genetic diversity than anticipated (Arroyo et al, 2016).

The phylogenetic relationship of Xenocoelomorpha to other bilaterian lineages has been historically unstable. Until recently, Acoelomorphs were thought to be within the phylum Platyhelminthes, due to their physical appearance and similar regenerative capabilities (Egger et al, 2009). However, upon further investigation, researchers have distinguished the two. Morphologically speaking, Acoelomorpha do not possess protonephridia, the morphology of the spermatozoa differs and Acoelomorpha have a ciliary root structure in the epidermis that Platyhelminthes do not (Cannon et al, 2016). Moreover, on a molecular level, analyses of ribosomal DNA and transcriptomes from both phyla confirm that Acoelomorpha is distinguishable from Platyhelminthes, and is the basal bilaterian phylum (Cannon et al, 2016; Ruiz-Trillo et al, 1999). It follows then that Cnidaria are the sister taxa to Xenoacoelomorpha. This can be explained by the planuloid-acoeloid hypothesis, which posits that the first bilaterian was a cnidarian, planula larvae that evolved into a direct-developing benthic bilaterian (Arroyo et al, 2016).

This begs the question as to what the ancestral Acoel looked like. Some researchers propose that the last common bilaterian ancestor was a benthic, ciliated acoelomate worm, lacking excretory organs, coelomic cavities and nerve cords, which must have subsequently evolved once Nephrozoa diverged from Xenocoelomorpha (Cannon et al, 2016). Other researchers, however, suggest that perhaps the bilaterian last common ancestor was more common than thought. Following the discovery that Acoelomates have a portion of the Hox code in their DNA (Moreno, Permanyer and Martinez, 2011), the basal bilaterian could have been more complex than present-day Acoels, which could then be the result of regressive evolution. This theory is supported by long branching times of these basal organisms. (Achatz et al, 2013). Another study also suggests that the ancestral form had a muscular pharynx which was subsequently lost in some extant groups, rather than positing that this trait evolved independently multiple times(Jondelius et al, 2011). However, this idea of a more complex ancestral form is challenged by the likelihood of convergent evolution versus regressive evolution, and recent studies that suggest subsequent complexity has evolved independently (Gavilan, Perea-Atienza and Martinez, 2016).

Classification

As per the phylogeny below, the presence of ocelli indicates the specimen belongs to the suborder Bursalia. As discussed above, classification of Acoel species is difficult and often relies on information such as the anatomy of the male copulatory organ and molecular data. As this information was not available, the specimens were unable to be characterised beyond suborder Bursalia.

Phylum: Xenoacoelomoprha (Philippe et al, 2011)

Subphylum: Acoelomorpha (Ehlers, 1985)

Order: Acoela (Tyler, 2006)

Suborder: Bursalia (Jondelius et al, 2011)

It is difficult to estimate and track population sizes of Acoels due to their small size, global distribution and cryptic habits. Presently, Acoels are not considered threatened. However, as a marine species, they could be threatened by broad-scale processes that are likely to have widespread effects on virtually all species. Increasing turbidity and nutrification in coastal waters leads to a greater presence of algae, which in turn could increase the incidence of microbial mats, rendering previously available benthos uninhabitable for Acoels. Complex reef systems damaged by increasing extreme weather events would lead to a loss in habitat complexity, which for specialised hard substrate-dwellers, could lead to species losses. Moreover, global ocean acidification could impact the ability of all Acoels, including planktonic species, to grow and reproduce. Finally, continued removal of higher predators could lead to top-down food web effects, which could result in an unsustainable proliferation of Acoels due to the gradual removal of their nature predators.

Achatz, J., and Martinez, P. (2012). The nervous system of Isodiametra pulchra (Acoela) with a discussion on the neuroanatomy of the Xenacoelomorpha and its evolutionary implications. Frontiers in Zoology, 9, 1-21.

Achatz, J., Chiodin, M., Salvenmoser, W., Tyler, S., and Martinez, P. (2013). The Acoela: on their kind and kinships, especially with nemertodermatids and xenoturbellids (Bilateria incertae sedis). Organisms Diversity & Evolution, 13, 267-286.

Achatz, J., Hooge, M., Wallberg, A., Jondelius, U., and Tyler, S. (2010). Systematic revision of acoels with 9+0 sperm ultrastructure (Convolutida) and the. Journal of Zoological Systematics and Evolutionary Research, 48, 9-32.

Arroyo, S., Lopez-Escardo, D., de Vargas, C., and Ruiz-Trillo, I. (2016). Hidden diversity of Acoelomorpha revealed through metabarcoding. Biology Letters, 12, 1-5.

Bartolomaeus, T., and Balzer, I. (1997). Convolutriloba longifissura, nov. spec. (Acoela) - first case of longitudinal fission in Platyhelminthes. Microfauna Marina, 11, 7-18.

Cannon, J., Vellutini, B., Smith, J., Ronquist, F., Jondelius, U., and Hejnol, A. (2016). Xenacoelomorpha is the sister group to Nephrozoa. Nature, 530, 89-93.

Dorjes, J. (1966). Paratomella unichaeta nov. gen. nov. spec., representative of a new family of Turbellaria Acoela with asexual reproduction by paratomy. Publications for the Institute of Marine Research, 2, 187-200.

Egger, B., Steinke, D., Tarui, H., Mulder, K., Arendt, D., Borogonie, G., Funayama, N., Gschwentner, R., Hartenstein, V., Hobmayer, B., Hooge, M., Hrouda, M., Ishida, S., Kobayashi, C., Kuales, G., Nishimura, O., Pfister, D., Rieger, R., Salvenmoser, W., Smith, J., Technau, U., Tyler, S., Agata, K., Salzburger, W., and Ladurner, P. (2009). To Be or Not to Be a Flatworm: The Acoel Controversy. PLOS ONE, 4, 1-10.

Ehlers, U. (1986). Comments on a phylogenetic system of the Platyhelminthes. Hydrobiologia, 132, 1-12.

Flanders Marine Institute. (2021). Retrieved from World Register of Marine Species: http://www.marinespecies.org/index.php

Franks, N., Worley, A., Grant, K., Gorman, A., Vizard, V., Plackett, H., Doran, C., Gamble, M., Stumpe, M., and Sendova-Franks, A. (2016). Social behaviour and collective motion in plant-animal worms. Proceedings of the Royal Society B, 283, 1-9.

Gavilan, B., Perea-Atienza, E., and Martinez, P. (2016). Xenacoelomorpha: a case of independent nervous system centralization? Philosophical Transactions of the Royal Society B, 371, 1-14.

Hejnol, A., and Pang, K. (2016). Xenacoelomorpha's significance for understanding bilaterian evolution. Current Opinion in Genetics & Development, 39, 48-54.

Henry, J., Martindale, M., and Boyer, B. (2000). The Unique Developmental Program of the Acoel Flatworm, Neochildia fusca. Developmental Biology, 220, 285-295.

Jondelius, U., Wallberg, A., Hooge, M., and Raikova, O. (2011). How the Worm Got its Pharynx: Phylogeny, Classification and Bayesian Assessment of Character Evolution in Acoela. Systematic Biology, 60, 845-871.

Moreno, E., Permanyer, J., and Martinez, P. (2011).The Origin of Patterning Systems in Bilateria—Insights from the Hox and ParaHoxGenes in Acoelomorpha. Genomics Proteomics Bioinformatics, 9, 65-76.

Nielsen, C. (2011). Animal Evolution – Interrelationships of the Living Phyla. Oxford Scholarship Online.

Perea-Atienza, E., Botta, M., Salvenmoser, W., Gschwentner, R., Egger, B., Krisof, A., Martinez, P., and Achatz, J. (2013). Posterior regeneration in Isodiametra pulchra (Acoela, Acoelomorpha). Frontiers in Zoology, 10, 1-20.

Perea-Atienza, E., Gavilan, B., Chiodin, M., Abril, J., Hoff, K., Poustka, A., and Martinez, P. (2015). The nervous system of Xenacoelomorpha: a genomic perspective. Journal of Experimental Biology, 218, 618-628.

Petrov, A. (2007). Features of the Male Copulatory Organs in Acoels (Acoelomorpha) and Their Taxonomic Implications. Doklady biological Sciences, 413, 125-127.

Rieger, R., Tyler, S., Smith, J., and Rieger, G. (1991). Platyhelminthes: Turbellaria. In F. a. Harrison, Microscopic Anatomy of Invertebrates. Volume 3. Platyhelminthes and Nemertinea (pp. 7-140). New York: Wiley-Liss.

Ruiz-Trillo, I., Riutort, D., Littlewood, T., Herniou, E., and Baguna, J. (1999). Acoel Flatworms: Earliest Extant Bilaterian Metazoans, Not Members of Platyhelminthes. Science, 283, 1919-1923.

Shannon, T., and Achatz, J. (2007). Convolutriloba macropyga sp. nov., an uncommonly fecund acoel (Acoelomorpha) discovered in tropical aquaria. Zootaxa, 1525, 1-17.

Tyler, S., and Hooge, M. (2004). Comparative morphology of the body wall in flatworms (Platyhelminthes). Canadian Journal of Zoology, 82, 194-210.

Yamasu, T. (1991). Fine structure and function of ocelli and sagittocysts of acoel flatworms. Hydrobiologia, 227, 273-282.