Category Archives: worms

Male resistance: when females disappear and hermaphrodites don’t like you

by Piter Kehoma Boll

During the evolution of life, sex was certainly a great innovation. It allows organisms to reproduce while mixing their genes with that of another individual. Although it usually makes your offspring to have only half of your genes, which does not seem to be as great as an offspring that carries you as a whole into the next generation, there are certainly advantages in mixing. The most evident advantage is that your genes can combine with other versions and, as a result, produce a better team of genes than the one that you had. Even though each of your children carries only half of you, that half is more likely to survive than a child that carries you as a whole. In other words, sex gives the possibility for a population of genes (those that make up an individual) to get rid of some of the less efficient ones and replace them with better copies.

As you know, most sexual organisms make such a recombination by fusing two sexual cells, the gametes, and those are usually of two different kinds: a small one (the male) and a large one (the female).

In some species, each individual can only produce either male or female gametes, therefore being either a male organism or a female organism. In such species, sexual reproduction requires a male to mate with a female. This is the pattern found, for example, in most vertebrates and arthropods.

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A female (large) and a male (small) of the tick Ixodes ricinus mating. Image by Jana Bulantová.*

In other species, each individual can produce both male and female gametes, therefore being called a hermaphrodite. The advantage of such a system is that hermaphrodites can mate with any individual of their species, sometimes even with themselves! One of the main problems with hermaphroditism is when you decide to play only one role, which may lead to conflict during sex.

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Two snails Helix pomatia (hermaphrodites) making love. Photo by Wikimedia user Jangle1969.**

Now what evolved first? Dioecious species (those having male and female individuals) or hermaphrodites (allso called monoecious species)? It’s hard to tell, but we can be sure that during evolution many lineages switched from one system to the other and back. And the coolest part is that such switches still happen today.

You may know that most flowering plants are hermaphrodites. Flowers usually have both male and female organs, although they are rarely able to fertilize themselves (self-fertilization). Among plants, the cases of dioecious species seem to be mainly due to some mutation that ended up partially sterilizing an individual. For example, a mutation could appear that makes the plant unable to produce male organs, thus becoming only female. Other individuals in the population that lack this mutation continue to be hermaphrodites, so we have an “unbalanced” species with two sexes, females and hermaphrodites, but no males. Although unusual at first, such a system can remain stable if reproduction occurs through cross-fertilization and not self-fertilization. As both females and hermaphrodites need pollen (which produces the male gametes) from other plants, they can coexist as long as the pollinator carries pollen to both sexes. The same happens if the sexes are male and hermaphrodite. As long as the pollinator carries the male’s pollen to hermaphrodite flowers, both sexes can do just fine.

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The plant Geranium sylvaticum includes hermaphrodites and females, but no males. Photo by Enrico Blasutto.**

Species composed of males and hermaphrodites are called androdioecious (from Greek andro-, man, male + di-, two + oikos, home, house; therefore “male in two “houses”, i.e., in two different kinds of organisms), while those composed of females and hermaphrodites are called gynodioecious (from Greek gyno-, woman, female; therefore “female in two different kinds of organisms).

Androdioecious and gynodioecious species occur among animals as well, but in this case their existance indicates something happening in the other direction, i.e., it is a transition from a dioecious species (with males and females) to a hermaphrodite species. And this is much more complicated that the other way round. Actually, it can get really, really bad for the “single-sex sex”.

This unbalanced sexual system in animals usually happens like this. There is a happily dioecious species with male and female individuals, but one day a new mutation appears and allows one of the sexes to produce both male and female gametes, thus becoming an hermaphrodite. However, such hermaphrodites are usually unable to play the role of the new sex while mating, i.e., they have the gametes, but not the tool to mate using them. Thus, the only way to use both gametes is to fertilize themselves.

One problem that comes from doing that is inbreeding. When you fertilize yourself, you are not increasing genetic diversity. On the contrary, you have very high chances of producing offspring with two copies to the same gene, thus decreasing genetic diversity. In order to continue to have recombination, you must mate with the single-sex individuals, which means you can only play the role of your original sex and your hermaphroditism is irrelevant. You are producing useless gametes. Or are you?

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A male and a hermaphrodite of the nematode Caenorhabditis elegans an androdioecious species. Credit to Worm Atlas.

The problem with inbreeding happens when an organism ends up with two copies of a deleterious gene, which is fairly common in species where cross-fertilization is the rule and such deleterious genes are maintained in the population through individuals with a single copy that is not enough to cause any trouble. That is why having kids with your parents, children of siblings is usually a bad idea. When a species evolves from a system of cross-fertilization to one of self-fertilization, inbreeding can be a serious problem at first, producing many descendants that will die soon. However, eventually this will “purge” the set of genes. If individuals only mate with themselves, the number of deleterious genes will sharply decrease after some generations and inbreeding will not be such a big problem anymore.

When this happens in a species with unbalanced sex, the single-sex individuals will be in trouble. Two androdioecious animals have been studied regarding this conflict, the nematode and model organism Caenorhabditis elegans and clam shrimps of the genus Eulimnadia, such as Eulimnadia texana. In both groups, the hermaphrodites do not seem to be very interested in mating with males. They have even lost most phenotypic clues that help males identify them as potential mates. The only thing left for the males is to insist, to look for hermaphrodites and force them to mate with them, but it is a hard battle. Even when mating does occur, the hermaphrodite usually discards the male’s sperm.

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A hermaphrodite (left) and a male (right) of the clam shrimp Eulimnadia texana. Credits to arizonafairyshrimp.com

The persistence of males in the population depends basically on their ability to fertilize hermaphrodites against their will and the sex-determination system of the species. When hermaphrodites produce males by self-fertilization, they are destined to remain for at least some time even if they cannot fertilize that much. Now if self-fertilization only produce hermaphrodites, the poor males have to be really persistent or otherwise they will soon perish.

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You may also like:

Having more females makes you gayer… if you are a beetle

Endosperm: the pivot of the sexual conflict in flowering plants

Gender Conflict: Who’s the man in the relationship?

Male dragonflies are not as violent as thought

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References and further reading:

Chasnov JR 2010. The evolution from females to hermaphrodites results in a sexual conflict over mating in androdioecious nematode worms and clam shrimp. Journal of Evolutionary Biology 23: 539–556.

Ellis RE & Schärer L 2014. Rogue Sperm Indicate Sexually Antagonistic Coevolution in Nematodes. PLoS Biol 12: e1001916.

Ford RE & Weeks SC 2018. Intersexual conflict in androdioecious clam shrimp: Do androdioecious hermaphrodites evolve to avoid mating with males? Ethology 124: 357–364.

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Friday Fellow: C. elegans

by Piter Kehoma Boll

Despite its small size, today’s fellow is one of the most important organisms in current scientific research. Named Caenorhabditis elegans and usually called simply C. elegans, this worms is a nematode and reaches about 1 mm in length and lives in the soil of temperate areas.

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An adult hermaphrodite of C. elegans. Photo by Bob Goldstein.*

There are only four bands of muscles that run along the body of C. elegans and they only alow the worm to bend the body dorsally or ventrally, but not to the sides. Thus, while moving on a horizontal surface, the worms are forced to lie on their left or ride side.

The main food source of C. elegans are bacteria that live on decaying organic matter, although they can also feed on some yeast species. Therefore, they thrive in soils rich in organic matter, where bacteria occur in abundance.

The sex of C. elegans is unusual. An adult organism can be either a male or a hermaphrodite, without a pure female form. Hermaphrodites are the most common form and usually self-fertilize, although they can, and apparently prefer, to mate with males. The larvae pass through four larval stages before reaching the adult stage, but this happens very quickly, since in ideal conditions the lifespan of C. elegans is of about 2 to 3 weeks. However, in conditions of insufficient food, an alternative third larval stage called dauer can be formed. The dauer stage has the body sealed, including the mouth, which doesn’t allow it to take in food, and can remain as such for a few months until the conditions are good again.

As most nematodes, C. elegans presents eutely, i.e., the adult worm has a genetically determined number of cells in the body. This number is fixed and does not change, because cell division ceases in adults. Male C. elegans have 1031 cells and hermaphrodites have 959 cells.

Due to its small size, small and fixed number of cells, transparent body and because it is easy to raise it in the lab, C. elegans became a perfect model organism. It was the first organism to have its genome fully sequenced and up to now it is the only organism with a complete connectome (the map of his neuron connections). It has been used in studies related to ageing, development, apoptosis and all sort of gene expressions.

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References and further reading:

Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics 77(1): 71-94.

Klass, M. R. (1977) Aging in the nematode Caenorhabditis elegans: Major biological and environmental factors influencing life span. Mechanisms of Ageing and Development 6: 413–429. https://doi.org/10.1016/0047-6374(77)90043-4

Peden, E.; Killian, D. J.; Xue, D. (2008) Cell death specification in C. elegans. Cell Cycle 7(16): 2479–2484. https://doi.org/10.4161/cc.7.16.6479

Wikipedia. Carnorhabditis elegans. Available at < https://en.wikipedia.org/wiki/Caenorhabditis_elegans >. Access on April 16, 2018.

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Planarian: a living vessel built by unicellular organisms?

by Piter Kehoma Boll

Not long ago I talked about the peculiar genome of the freshwater planarian Schmidtea mediterranea and how it challenges our view of many cellular processes. Now what if I told you that planarians also challenge our view of what a multicellular organism is?

We all know that organisms may be either unicellular or multicellular, but sometimes it is hard to tell them apart, especially in what are called colonial organisms, in which clones of unicellular individuals may live together.

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Green algae of the genus Volvox are somehow at the boundary between unicellular and multicellular organisms. Although usually considered a colony of unicellular organisms, they behave somewhat like a multicellular organism. Photo by Frank Fox.*

So where lies the boundary between gathered unicellular organisms and true multicellular organisms? One of the ideas is that for a group of cells to be considered a single unit (an organism) they must have high levels of cooperation and low levels of conflict between each other and, perhaps more important than that, they have to be dependent on the association in order to survive.

As most recent evolutionary theories predict, cooperation increases with genetic similarity. As a result, multicellular organisms are (almost) always composed of cells having the exact same genetic material, i.e., they are all clones. We know, however, that during DNA replication mutations may occur, so that eventually at least some cells of an adult and many-celled organism may have become genetically distinct. This leads to a need to find a way to fix this problem by reincreasing genetic similarity, and the way most organisms found to do that is by allowing only one lineage of their cells, the germ cells (which produce the gametes) to generate the next generation. Thus, each transition from one generation to the next passes through a “zygotic bottleneck”, i.e., a new organism is always generated from a single original cell, the zygote, which assures that the genetic similarity is always brought back.

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A developing new egg, with an embryo that is created from a single original cell, the zygot, assuring a higher genetic similarity of the cells in the whole organism. Photo by Stéphanie Bret.**

The zygotic bottleneck is not a rule for a lot of species though. Many animals and plants are able to reproduce asexually by budding, fission or many other ways. In such cases, the new organism usually is built from several different lineages of the parent organism. For example, some succulent plants may generate a new organism from a dettached leaf and several cells of the original leaf start to reproduce and together they build the new plant and, as each lineage may have suffered different mutations, the offspring is not necessarily composed of genetically identical cells. Nevertheless, even such organisms, which are able to reproduce asexually, still retain the ability to generate zygotes through sexual reproduction, which eventually “cleans that mess”.

But in planarians things get really strange. First of all, let’s explain some basic things about planarians. They have, as you know, a remarkable regeneration ability. This happens due to the presence of stem cells called neoblasts that fill their bodies. Those neoblasts are able to generate all cell types that make up the planarian’s body. In fact, all cells in a planarian must come from neoblasts, because, as weird as it may be, all differentiated cells in a planarian body ARE UNABLE TO UNDERGO MITOSIS! Once a neoblast differentiates into any kind of cell, it is condemned to die in a few days without ever letting descendants. All cells in a planarian body are therefore constantly replaced by new ones coming from neoblasts. The only lineage of differentiated cells that is still able to reproduce is that of the germ cells, which, as in other multicellular organisms, assure that the next generation will consist of organisms with genetically homogeneous cells.

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Girardia tigrina, a freshwater planarian. Photo by Wikimedia user Slimguy.**

Several freshwater planarians, however, have lost their ability to generate sexual organs and, as a result, germ cells. In order to reproduce, they must rely on a form of asexual reproduction, which in this case happens by transversal fission of the body and posterior regeneration of the missing parts. In these populations, the zygotic bottleneck disappeared completely and, as a result, any non-lethal mutation in the neoblasts is retained in the organism, leading to a population of genetically distinct neoblasts inside a planarian.

Therefore, considering the fact that asexual planarians are not genetically homogeneous, having several different neoblast lineages in the same body, and that the neoblasts are the only cells able to reproduce and continue the species, a recent publication by Fields and Levin (see references) suggests that asexual planarians are nothing more than a very complex environment built by neoblasts in order to survive. Considering that each neoblast is an independent cell, which only needs the environment (the planarian) to survive, but does not need other neoblasts, planarians, at least the asexual ones, do not seem to have reached completely the requirements of high internal cooperation and low internal competition to be considered multicellular organisms.

We could interpret the neoblasts as unicellular organisms that live together, cooperating to build a complex environment, the planarian body, with their own sterile descendants (the differentiated cells), as if they were a group of queen ants living among sterile castes. Kind of mind blowing, huh? But it actually makes sense.

If you want to read more about it and understand every detail in this theory, read the references below.

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Maybe you’d like:

Endosperm: the pivot of the sexual conflict in flowering plants

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References:

Fields, C; Levin, M. (2018) Are Planaria Individuals? What Regenerative Biology is Telling Us About the Nature of Multicellularity. Evolutionary Biology: 1–11.

West, S. A.; Fisher, R. M.; Gardner, A.; Kiers, E. T. (2015) Major evolutionary transitions in individuality. PNAS 112 (33): 10112-10119. https://doi.org/10.1073/pnas.1421402112

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Friday Fellow: Green-Banded Broodsac

by Piter Kehoma Boll

Parasites are very speciose, and I often feel that I’m not giving enough space for them here, especially when I bring you a flatworm, which is likely the group with the largest number of parasite species. So let’s talk about one today at last.

The first parasitic flatworm I am introducing to you is Leucochloridium paradoxum, the green-banded broodsac. It is a member of the flatworm group Trematoda, commonly known as flukes and, as all flukes, it has a complex life cycle.

Adults of the green-banded broodsac live in the intestine of various passerine birds of North America and Europe. The eggs they lay reach the environment through the bird’s feces and are eventually ingested by land snails of the genus Succinea.

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Adult individual of Leucochloridium paradoxum (left), an infected intermediate hose, a sail of the genus Succinea (center) and the sporocysts along the snail’s internal organs (right). Images not to scale. Extracted from http://medbiol.ru/medbiol/dog/0011a975.htm

Adults of Leucochloridium paradoxum are very similar to the adults of other species of the genus Leucochloridium, the main differences being seen in the larval stages. Inside the body of the snail, the eggs hatch into the first larval stage, the miracidium, which inside the snail’s digestive system develops into the next stage, the sporocyst.

The sporocyst has the form of a long and swollen sac (the broodsac, hence the common name) that is filled with many cercariae, which are the next larval stage. The sporocyst than migrates towards the snail’s eye tentacles, invading them and turning them into a swollen, colorful and pulsating structure that resembles a caterpillar. In this stage of infection, the poor snail is most likely blind and cannot avoid light as it normally does. As a result, it becomes exposed to birds that mistake it for a juicy caterpillar, eating it eagerly.

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A poor snail of the species Succinea putris with a broodsac in its left eye stalk. There is only one terrible fate for this creature. Photo by Thomas Hahmann.*

When the snail is eaten, the sporocyst burst and the several cercariae are released. In the bird’s intestine, they develop into adults and restart the nightmarish cycle.

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References:

Rząd, I.; Hofsoe, R.; Panicz, R.; Nowakowski, J. K. (2014) Morphological and molecular characterization of adult worms of Leucochloridium paradoxum Carus, 1835 and L. perturbatum Pojmańska, 1969 (Digenea: Leucochloridiidae) from the great tit, Parus major L., 1758 and similarity with the sporocyst stages. Journal of Helminthology 88(4): 506-510. DOI: 10.1017/S0022149X13000291

Wikipedia. Leucochloridium paradoxum. Available at < https://en.wikipedia.org/wiki/Leucochloridium_paradoxum >. Access on March 8, 2018.

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Friday Fellow: Bobbit Worm

by Piter Kehoma Boll

Today’s Friday Fellow probably looks like a creature coming directly from hell to the poor sea animals that are its prey. Well, it looks quite scary even for humans! Its name is Eunice aphroditois, a beautiful name. Popularly it is known as the Bobbit worm and looks like a colorful nightmare.

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Anterior portion of a bobbit worm coming out of the sand. Photo by Jenny Huang.*

The Bobbit worm is a polychate worm and is one of the largest known annelids, with several records of individuals reaching up to 1 m in length, and even one record of a specimen that was almost 3 m long. It is found in warm waters all around the world, in the Atlantic, the Indian and the Pacific oceans.

Being an ambush predator, the Bobbit worm buries itself into the ocean floor, among the sediments, and waits for a delicious meal to swim over it. Once a prey is detected, the Bobbit worm projects itself forward and captures it with its sharp teeth.

The name “Bobbit worm” was coined in 1996 and refers to Lorena Bobbitt, who became publicly known in 1993 after cutting off her husband’s penis with a knife while he was asleep. The name seems to be inspired in the worm’s scissor-like jaws and has nothing to do with the female cutting off the male’s penis. In fact, those worms release the gametes in the water, so that there isn’t even a sexual intercourse.

Despite its popularity, being even raised as a “pet” sometimes, little is known about the Bobbit worm’s ecology. If you happen to have one in your fishtank, make some research and publish it!

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References:

Uchida, H.; Tanase, H.; Kubota, S. (2009) An extraordinarily large specimen of the polychaete worm Eunice aphroditois (Pallas) (Order Eunicea) from Shirahama, Wakayama, central Japan. Kuroshio Biosphere 5: 9-5.

Wikipedia. Eunice aphroditois. Available at < https://en.wikipedia.org/wiki/Eunice_aphroditois >. Access on January 31, 2017.

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You know nothing, humans! A planarian genome challenges our understanding of how life works

by Piter Kehoma Boll

We finally have a rather complete sequencing of a planarian’s genome, more precisely, of the planarian Schmidtea mediterranea, which is an important model organism for the study of stem cells and regeneration.

In case you don’t know, planarians have a remarkable ability of regeneration, so that even tiny pieces are able to regenerate into a whole organism. They are like a real-life Wolverine, but somewhat cooler! This amazing ability is possible due to the presence of a group of stem cells called neoblasts that can differentiate into any cell type found in the planarian’s body. In fact, all differentiated cell types in planarians are unable to undergo mitosis, so that neoblasts are responsible for constantly replacing cells in every tissue. But we are not here to explain the details of planarian regeneration. We are here to talk about Schmidtea mediterranea‘s genome!

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Look at its little cock eyes saying “I will destroy everything you think you know, humans!” Photo by Alejandro Sánchez Alvarado.*

A rather complete genome of S. mediterranea has been recently published and its analysis reveal some astonishing features.

First of all, 61.7% of S. mediterranea‘s genome is formed by repeated elements. Repeated elements are basically DNA strands that occur in multiple copies throught the genome of an organism. They are thought to come from the DNA of virus that was incorporated to the host’s DNA. In humans, about 46% of the genome is formed by repeated elements. Most repeated elements of S. mediterranea belong to unidentified families of retroelements, thus suggesting that they are new undescribed families. Those repeats are very long, having more than 30 thousand base pairs, which are not known to exist in other animals. The only other group of repeated elements with a similar size is found in plants and known as OGRE (Origin G-Rich Repeated Elements). The long repeat found in Schmidtea was therefore called Burro (Big, unknown repeat rivaling Ogre).

But certainly the most surprising thing about S. mediterranea‘s genome is the lack of many highly conserved genes that are found in most eukaryotes and that were thought to be essential for cells to function properly.

Schmidtea mediterranea lacks genes responsible for repairing double-stranded breaks (DSBs) in DNA, which would make them very likely to suffer a lot of mutations and sensitive to anything that induces DSBs. However, planarians are known to have an extraordinary resistance to gamma radiation that induces DSBs. Do they have other repairing mechanisms or is our current understanding about this process flawed?

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Several “essential” genes and their presence (in green) or absence (in red) in several animals. Schmidtea mediterranea lacks them all. Image extracted from Grohme et al. (2018).**

Another important gene that was not found in S. mediterranea is the Fatty Acid Synthase (FASN) gene, which is essential for an organism to synthesize new fatty acids. Planarians therefore would have to rely on the lipids acquired from the diet. This gene is also absent in parasitic flatworms and was at first thought to be an adaptation to parasitism but since it is absent in free-living species as well, it does not seem to be the case. Could it be a synapomorphy of flatworms, i.e., a character that identifies this clade of animals?

That is not enough for little Schmidtea, though. More than that, this lovely planarian seems to lack the MAD1 and MAD2 genes, which are found in virtually all eukaryotes. Those genes are responsible for the Spindle Assembly Checkpoint (SAC), an important step during cell division that prevents the two copies of a chromosome to separate from each other before they are all connected to the spindle apparatus. This assures that the chromosomes will be evenly distributed in both daughter cells. Errors in this process lead to aneuploidy (the wrong number of chromosomes in each daughter cell), which is the cause of some genetic disorders such as the Down syndrome in humans. Planarians do not have any trouble in distributing their chromosomes properly, so what is going on? Have they developed a new way to prevent cellular chaos or, again, is our current understanding about this process flawed?

Let’s wait for the next chapters.

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Reference:

Grohme, M. A.; Schloissnig, S.; Rozanski, A.; Pippel, M.; Young, G. R.; Winkler, S.; Brandl, H.; Henry, I.; Dahl, A.; Powell, S.; Hiller, M.; Myers, E.; Rink, J. C. (2018). “The genome of Schmidtea mediterranea and the evolution of core cellular mechanisms”. Nature. doi:10.1038/nature25473

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Xenoturbella, a growing group of weirdoes

by Piter Kehoma Boll

You may never have heard of Xenoturbella, and I wouldn’t blame you. Despite being a fascinating feature of evolution, little is known about it and its magic has been hidden from most of us.

The first Xenoturbella was described in 1949 and named Xenoturbella bocki. At the time, it was considered a strange flatworm, hence its name, from Greek xenos, strange + turbella, from Turbellaria, free-living flatworms. Xenoturbella bocki is a marine animal measuring up to 3 cm in length and looking like a flat worm… a flatworm! Well, actually more like a folded worm, because its body has a series of folds running londitudinally that make it have a W shape in cross section.

Found in the cold waters around northern Europe, its body lacks a centralized nervous system, having only a net of neurons inside the epidermis. There are also no reproductive organs, neither anything similar to a kidney or any other organ beside a mouth and a gut and some structures on its surface.

For decades, X. bocki was the only species of Xenoturbella known to us. A second species was described in 1999 as X. westbladi, but molecular analyses revealed that it was the same species as X. bocki, so we continued having only one species. Thanks to molecular studies, we also figured out that Xenoturbella is not a flatworm at all, but belongs to a group of very primitive bilaterian animals, being closely related to another group of former flatworms, the acoelomorphs. Together, Xenoturbella and the acoelomorphs (a good name for a rock band, right?) form the group called Xenacoelomorpha.

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Xenoturbella churro, “head” to the right. Photo by Greg Rouse.*

Forming its own phylum (or perhaps class if it is grouped in a single phylum with the acoelomorphs) named Xenoturbellida, X. bocki recently discovered that it is not alone in the world. In 2016, four new species were described from the waters of the Pacific Ocean near the coasts of Mexico and the USA, being named Xenoturbella monstrosa, X. churro, X. profunda and X. hollandorum. Considering the small size of X. bocki, some of them were monsters, especially X. monstrosa, which reaches 20 cm in length!

Four new species was quite a finding. The phylum suddenly was five times bigger than before. As someone particularly interested in obscure animal groups, especially those that once were members of the lovely phylum Plathyelminthes, I was very excited by this discovery, but I wasn’t expecting at all what happened after that.

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Photo of the only known specimen of Xenoturbella japonica until now. “Head” to the left. Credits to Nakano et al. (2017).*

In December 2017, one more species was found, this time on the other side of the Pacific, near Japan. Named Xenoturbella japonica, the fifth member of the Xenoturbella genus is very welcome. The new species was based on two specimens, an adult “female” specimen (are they hermaphrodites? I don’t think we can be sure about it yet…) and a juvenile specimen. One more exciting thing is that the juvenile may actually be yet another species! But we need more material to be sure.

You can read the article describing Xenoturbella japonica here.

See also: Acoelomorpha, a phylogenetic headache

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References:

Nakano, H.; MIyazawa, H.; Maeno, A.; Shiroishi, T.; Kakui, K.; Koyanagi, R.; Kanda, M.; Satoh, N.; Omori, A.; Kohtsuka, H. (2017) A new species of Xenoturbella from the western Pacific Ocean and the evolution of XenoturbellaBMC Evolutionary Biology17: 245. https://doi.org/10.1186/s12862-017-1080-2

Rouse, G.W.; Wilson N.G.; Carvajal, J.I.; Vrijenhoek, R.C. (2016) New deep-sea species of Xenoturbella and the position of Xenacoelomorpha. Nature, 530:94–7. doi:10.1038/nature16545.

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