Tag Archives: Bilateria

Who came first? The comb or the sponge?

by Piter Kehoma Boll

The endless question is here again, but this time it appears to be settled. What animal group is the earliest of all? Who came first?

It is clear that there are five animal lineages that are usually regarded as monophyletic: sponges, placozoans, comb jellies, cnidarians and bilaterians. Let’s take a brief look at each of them:

Sponges (phylum Porifera) are always sessile, i.e., they do not move and are fixed to the substrate. They have a very simple anatomical structure. Their body is consisted of a kind of tube, having a large internal cavity and two layers of cells, an outer one and an inner one around the cavity. There are several small openings connecting the cavity to the outside, called pores, and one or more large cavities, called oscula (singular: osculum). Between the two cell layers there is a jelly-like mesohyl containing unspecialized cells, as well as the skeleton structures, including fibers of spongine and spicules of calcium carbonate or silica. Some species also secrete an outer calcium carbonate skeleton over which the organic part grows. Sponges lack muscles, nervous system, excretory system or any other kind of system. They simply live by beating the flagella of the choanocytes (the cells of the inner layer), creating a water flow entering through the pores and exiting through the osculum. The choanocytes capture organic particles in the water and ingest them by phagocytosis. All sponge cells can change from one type to another and migrate from one layer to another, so there are no true tissues.

porifera_body_structures_01

Body structures found in sponges. Picture by Philip Chalmers.*

Placozoans (phylum Placozoa) are even simpler than sponges, but they actually have true tissues. They are flat amoeboid organisms with two layers of epithelium, one dorsal and one ventral, and a thin layer of stellate cells. The ventral cell layer is slightly concave and appears to be homologous to the endoderm (the “gut” layer) of other animals, while the upper layer is homologous to the ectoderm (the “skin” layer).

701px-trichoplax_adhaerens_photograph

Trichoplax adhaerens, the only species currently in the phylum Placozoa. Photo by Bernd Schierwater.**

Comb jellies (phylum Ctenophora) resemble jellyfishes, but a closer look reveals many differences. Externally they have an epidermis composed by two layers, an outer one that contains sensory cells, mucus-secreting cells and some specialized cells, like colloblasts that help capturing prey and cells containing multiple cilia used in locomotion, and an inner layer with a nerve net and muscle-like cells. They have a true mouth that leads to a pharynx and a stomach. From the stomach, a system os channels distribute the nutrients along the body. Opposite to the mouth there is a small anal pore that may excrete small unwanted particles, although most of the rejected material is expelled through the mouth. There is a layer of jelly-like material (mesoglea) between the gut and the epidermis.

bathocyroe_fosteri

The comb jelly Bathocyroe fosteri.

Cnidarians (phylum Cnidaria) have a structure similar to comb jellies, but not as complex. They also have an outer epidermis, but this is composed by a single layer of cells, and a sac-like gut surrounded by epthelial cells (gastrodermis), as well as a mesoglea between the two. Around the mouth there is one or two sets of tentacles. The most distinguishing feature of cnidarians is the presence of harpoon-like nettle cells, the cnidocytes, which are used as a defense mechanism and to help subdue prey.

800px-cross_section_jellyfish_en-svg

Body structure of a cnidarian (jellyfish). Picture by Mariana Ruiz Villarreal.

Bilaterians (clade Bilateria) includes all other animals. They are far more complex and are characterized by a bilateral body, cephalization (they have heads) and three main cell layers, the ectoderm, which originates the epidermis and the nervous system, the mesoderm, which give rise to muscles and blood cells, and the endoderm, which develops into the digestive and endocrine systems.

500px-bilaterian-plan-svg

Basic bilaterian structure.

Traditionally, sponges were always seen as the most primitive animals due to their lack of true tissues, muscular cells, nervous cells and all that stuff. However, some recent molecular studies have put the comb jellies as the most primitive animals. This was highly unexpected, as comb jellies are far more complex than sponges and placozoans, which would suggest that muscles and a nervous system evolved twice in the animal kingdom, or that sponges are some weird simplification of a more complex ancestor, which would be very hard to explain. The nervous system of comb jellies is indeed quite unusual, but not so much that it needs an independent origin.

However, now things appear to be settled. A study published this month on Current Biology by Simion et al. reconstructed a phylogenetic tree using 1719 genes of 97 animal species, and applying new and more congruent methods. With this more refined dataset, they recovered the classical reconstruction that puts sponges at the base of the animal tree, a more plausible scenario after all.

But why other studies have found comb jellies as the most basal group? Well, it seeems that comb jellies have unusually high substitution rates, meaning that their genes evolve faster. This leads to a problem called “long branch attraction” in phylogenetic reconstructions. As DNA has only four different nucleobases, namely adenine, guanine, cytosine and thymine, each one can only mutate into one of the other three. When mutations occur very often, they may go back to what they were in long lost ancestor, leading to misinterpretations in the evolutionary relationships. That seems to be what happens with comb jellies.

So, it seems that after all the sponge indeed came first.

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References and further reading:

Borowiec ML, Lee EK, Chiu JC, & Plachetzki DC 2015. Extracting phylogenetic signal and accounting for bias in whole-genome data sets supports the Ctenophora as sister to remaining Metazoa. BMC Genomics 16: 987. DOI: 10.1186/s12864-015-2146-4

Littlewood DTJ 2017. Animal Evolution: Last Word on Sponges-First? Current Biology 27: R259–R261. DOI: 10.1016/j.cub.2017.02.042

Simion P, Philippe H, Baurain D, Jager M, Richter DJ, Di Franco A, Roure B, Satoh N, Quéinnec É, Ereskovsky A, Lapébie P, Corre E, Delsuc F, King N, Wörheide G, & Manuel M 2017. A Large and Consistent Phylogenomic Dataset Supports Sponges as the Sister Group to All Other Animals. Current Biology 27: 958–967. DOI: 10.1016/j.cub.2017.02.031

Wallberg A, Thollesson M, Farris JS, & Jondelius U 2004. The phylogenetic position of the comb jellies (Ctenophora) and the importance of taxonomic sampling. Cladistics 20: 558–578. DOI: 10.1111/j.1096-0031.2004.00041.x
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Acoelomorpha: A Phylogenetic Headache

ResearchBlogging.orgby Piter Kehoma Boll

Take a look at these guys:

The green worm Symsagittifera roscoffensis (Graff, 1891). Photograph by Vincent Maran. Extracted from doris.ffessm.fr

Green worms Symsagittifera roscoffensis (Graff, 1891). Photograph by Vincent Maran. Extracted from doris.ffessm.fr

It’s a member of the group Acoelomorpha, animals which are still a puzzle in phylogeny. That means no one knows for sure where in the animals’ evolutionary tree they are exactly.

But first, let’s take a look about what makes an acoelomorph.

Those little guys are small worms, usually measuring less than 1 mm in length and living in marine or brackish waters or as symbionts. There are two groups of acoelomorphs: Acoela and Nemertodermatida. Acoels are the simplest ones; they have a mouth, but lack a gut, so that the food ingested goes directly to the internal tissues. In Nemertodermatida, there is a blind gut, i.e., with only one opening, like in the primitive cnidarians or in flatworms. In fact, they were initially classified as flatworms, but several features later challenged their position inside this phylum. The main differences are:

  • Acoelomorphs have an epidermis (“skin”) with cilia whose roots are interconnected in a hexagonal pattern, while other flatworms have independent cilia.
  • Acoelomorphs lack protonephridia (primitive kidney-like organs) and all other groups of animals have at least one of those or more complex organs with similar function.
  • While flatworms and all other protostomes (arthropods, annelids, mollusks, nematodes…) have ventral nerve cords and deuterostomes (chordates, echinoderms…) have dorsal ones, in acoelomorphs there are several nerve cords distributed radially along the body length.
Distribution of nerve chords in Acoelomorpha, Protostomia and Deuterostomia. Picture by myself, Piter K. Boll.

Distribution of nerve chords in Acoelomorpha, Protostomia and Deuterostomia. Picture by myself, Piter K. Boll.

Analyzing such features, it seems obvious that Acoelomorpha is a basal group of bilateral animals and may be the reminiscent of a primitive group of animals later almost completely extinct by their most complex descendants, the true protostomes and deuterostomes. The original radially-distributed nerve cords were simplified in dorsal or ventral ones in higher groups, but remained radial in Acoelomorpha.

Several phylogenetic studies indicate that Acoelomorpha is indeed a basal group of bilateral animals. They also lack several important Hox genes (responsible for determining body plan and organs’ distribution in animals) and it is quite unlikely that they would have lost most of them by secondary simplification.

Another group of simple animals, the Xenoturubellida, was sometimes proposed as a sister group for Acoelomorpha. Their proximity would be explained by several shared features, mainly the simple nervous system, the lack of a stomatogastric (mouth-gut) system, the structure of the epidermal cilia and the unusual fact that, in both groups, epidermal degenerated cells as resorbed in the gastrodermis.

A Xenoturbella worm. Photograph extracted from bioenv.gu.se/english/staff/Hiroaki_Nakano_eng/

A Xenoturbella worm. Photograph extracted from bioenv.gu.se/english/staff/ Hiroaki_Nakano_eng/

The group Xenoturbellida, however, has been placed in Deuterostomia in some molecular studies and recently Philippe et al. 2011 proposed that Acoelomorpha would also belong to the the Deuterostomia! But how could such a thing be possible when they obviously have primitive and unique features, like the radially placed nerve cords? The group’s explanation is that Acoelomorpha, as well as Xenoturbellida, have a sequence of microRNA (miR-103/107/2013) which is exclusive to Deuterostomia, so they would also be deuterostomes.

But wait a minute! What do they mean by “exclusive to Deuterostomia”? It means that that microRNA sequence is found in deuterostomes, but not in protostomes. Now think with me. We have 4 bilateral groups here: Acoelomorpha, Xenoturbellida, Deuterostomiaa and Protostomia. If you look at them this way, we can see that the statement “miR-103/107/2013 is exclusive to Deuterostomia” is false. The truth is that this sequence is absent in Protostomia, but present in all other groups. Wouldn’t it be more logical to think that, instead of deuterostomes acquiring this sequence, what really happened is that it was a primitive microRNA and protostomes have lost it?

If you consider Xenoturbellida and Acoelomorpha inside Deuterostomia, you have to assume that they passed through a huge simplification, and you maintain the radial nerve cords unexplained. Now if you think of them as primitive groups, the only thing necessary is to analyze protostomes as having lost a microRNA sequence. Quite a simpler explanation which doesn’t let open gaps.

Phylogenetic position of Acoelomorpha and Xenoturbellida according to Philippe et al. 2011. It means that (1) the bilaterians' ancestor had a complex set of Hox Genes; (2) miR-103/107/2013 appeared in an ancestor of true Deuterostomes+Xenacoelomorpha (Xenoturbellida + Acoelomorpha); (3) Xenacoelomorpha passed through a huge loss of Hox genes, loss of most internal organs and a mysterious set of radial nerve cords appear. Very complicated.

Phylogenetic position of Acoelomorpha and Xenoturbellida according to Philippe et al. 2011. It means that (1) the bilaterians’ ancestor had a complex set of Hox genes, being a complex animal; (2) miR-103/107/2013 appeared in an ancestor of true Deuterostomes+Xenacoelomorpha (Xenoturbellida + Acoelomorpha); (3) Xenacoelomorpha passed through a huge loss of Hox genes, loss of most internal organs and a mysterious set of radial nerve cords appear. Very complicated.

Position of Xenacoelomorpha as a basal group. It means that (1)

Phylogenetic position of Acoelomorpha and Xenoturbellida according to Boll et al. 2013 (that’s me!) based on a review of previous studies, as a basal group. It means that (1) the bilaterian’s ancestor was a simple animal, with a simple set of Hox genes, having miR-103/107/2013 and radial nerve cords; (2) the set of Hox genes became more complex and the nerve cords where simplified to either dorsal or ventral; (3) miR-103/107/2013 is lost in Protostomia. Way simpler.

You can read more in the references listed below.

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References:

Boll, P., Rossi, I., Amaral, S., Oliveira, S., Müller, E., Lemos, V., & Leal-Zanchet, A. (2013). Platyhelminthes ou apenas semelhantes a Platyhelminthes? Relações filogenéticas dos principais grupos de turbelários. Neotropical Biology and Conservation, 8 (1), 41-52 DOI: 10.4013/nbc.2013.81.06

Egger, B., Steinke, D., Tarui, H., De Mulder, K., Arendt, D., Borgonie, 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., & Ladurner, P. (2009). To Be or Not to Be a Flatworm: The Acoel Controversy. PLoS ONE, 4 (5) DOI: 10.1371/journal.pone.0005502

Hejnol, A., Obst, M., Stamatakis, A., Ott, M., Rouse, G., Edgecombe, G., Martinez, P., Baguna, J., Bailly, X., Jondelius, U., Wiens, M., Muller, W., Seaver, E., Wheeler, W., Martindale, M., Giribet, G., & Dunn, C. (2009). Assessing the root of bilaterian animals with scalable phylogenomic methods. Proceedings of the Royal Society B: Biological Sciences, 276 (1677), 4261-4270 DOI: 10.1098/rspb.2009.0896

Moreno, E., Nadal, M., Baguñà, J., & Martínez, P. (2009). Tracking the origins of the bilaterian
patterning system: insights from the acoel flatworm. Evolution & Development, 11 (5), 574-581 DOI: 10.1111/j.1525-142X.2009.00363.x

Mwinyi, A., Bailly, X., Bourlat, S., Jondelius, U., Littlewood, D., & Podsiadlowski, L. (2010). The phylogenetic position of Acoela as revealed by the complete mitochondrial genome of Symsagittifera roscoffensis. BMC Evolutionary Biology, 10 (1) DOI: 10.1186/1471-2148-10-309

Philippe, H., Brinkmann, H., Copley, R., Moroz, L., Nakano, H., Poustka, A., Wallberg, A., Peterson, K., & Telford, M. (2011). Acoelomorph flatworms are deuterostomes related to Xenoturbella. Nature, 470 (7333), 255-258 DOI: 10.1038/nature09676

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Filed under Evolution, Molecular Biology, Zoology