[Body]
Close-up of female stolen – one of the independent reproductive units – from the worm Ramisyllis kingghidorahi. It has already sprouted eyes and is swimming free to find a stolon of the opposite sex with which to reproduce.
As a supposed product of intelligent design, the reproductive process of the branching marine worm Ramisyllis kingghidorahi is nothing short of bizarre—especially when one considers that many of its marine worm relatives manage perfectly well with far more straightforward, functional reproductive strategies, free from the Heath-Robinson complexity seen in R. kingghidorahi.
This remarkable worm comprises a branching network of segments, the ends of which can transform into free-living reproductive units known as stolons. These stolons firstly grow a pair of eyes then detach from the main body and swim off in search of a partner—another stolon of the opposite sex.
Yet the most pressing question for biologists isn’t why such a labyrinthine reproductive system evolved, but how it is controlled and coordinated across the worm’s sprawling body. This is precisely the mystery tackled by a team of researchers from Georg-August-Universität Göttingen, Germany.
Their research has just been published, open access, in the journal BMC Genomics.
What information do you have on Ramisyllis kingghidorahi? Ramisyllis kingghidorahi – The Branching Marine Worm TaxonomyThe researchers also explain their research in a press release from Georg-August-Universität Göttingen:
- Kingdom Animalia
- Phylum Annelida
- Class Polychaeta
- Family Syllidae
- Genus Ramisyllis
- Species R. kingghidorahi
Discovery
- Year Described 2022
- Discovered In Sea of Japan, near Sado Island, Japan
- Habitat Lives within the internal canals of sponges belonging to the genus Petrosia
Notable Features
- Body Structure Possesses a unique branching body plan with a single head and multiple posterior branches, each capable of independent function.
- Reproduction Reproduces through a process called stolonization, where specialized reproductive units (stolons) develop at the ends of branches, grow eyes, detach, and swim away to mate .
- Genetic Insights Recent studies have mapped the worm's gene expression, revealing that different body regions exhibit distinct genetic activity, particularly the stolons, which show upregulation of genes related to gamete production and eye development .
Etymology
- Named after "King Ghidorah," the three-headed, two-tailed monster from the Godzilla franchise, due to its branching morphology reminiscent of the creature .
Conservation Status
- As of now, there is no specific conservation status assigned to R. kingghidorahi. Further research is needed to determine its population size and any potential threats.
Interesting Fact
- R. kingghidorahi is one of only three known species of branching annelid worms, making it an exceptional subject for studies on body plan evolution and reproductive strategies in marine invertebrates.
A head and a hundred tails: how a branching worm manages reproductive complexity
International research team led by Göttingen University produces genetic activity map for rare worm
Scientists have uncovered the genetic underpinnings of one of the ocean’s most bizarre animals: a branching marine worm named Ramisyllis kingghidorahi that lives inside sea sponges and reproduces in a truly extraordinary way. Living hidden in tropical waters, this worm grows multiple body branches within a host sponge, each tail capable of producing separate living reproductive units called “stolons”. But how does a single animal coordinate sexual reproduction across so many branches? To find out, researchers led by the University of Göttingen analysed gene expression across different body regions and between male, female and juvenile specimens. This provides the first complete “genetic activity map” – or transcriptome – of any branching worm, revealing how this creature manages to control reproduction across its branching body. Their findings were published in BMC Genomics.
The researchers found clear patterns in their analyses: differences in gene activity were more pronounced between different body regions in the same worm than between the sexes. The stolons – short-lived reproductive units that break off from the branches and swim away to mate – had the most distinctive genetic signatures when comparing males and females, probably reflecting their specialised role in gamete production and metamorphosis.
We were surprised to find that the head of the worm, which was previously thought to house a sex-specific control system, didn’t show the dramatic differences we expected between males and females. Instead, the stolons emerged as the true hotspots of gene activity during sexual development.
Dr Guillermo Ponz-Segrelles, first author
IES El Burgo-Ignacio-Echeverría
Las Rozas de Madrid, Madrid, Spain.
An overlooked but key feature of the reproductive stolons is that they sprout eyes before detaching from the main worm body in search of a mate. This study revealed upregulation of genes related to eye development, providing the first clues about how the tip of a branch of the worm body metamorphoses into an independent stolon. Interestingly, the data also hint at the possibility of partial genome duplication in Ramisyllis, which may help explain the complexity of its biology and reproductive system. Despite some challenges in identifying conserved signalling pathways, the results point to a unique genetic toolkit in Ramisyllis and highlight how little we still know about reproduction in marine invertebrates.
This worm and its surreal, tree-like body made headlines around the world in 2021 and 2022, yet it continues to amaze us. It challenges our understanding of how animal bodies can be organized, and how such strange forms of reproduction are orchestrated at the molecular level.
Dr. Thilo Schulze, co-first author
Animal Evolution & Biodiversity
Georg-August-Universität Göttingen
Göttingen, Germany.
With many aspects of branching worms’ reproductive biology still a mystery, the team hopes this new genetic resource will open the door to deeper investigations into how life evolves in unexpected directions – even in the hidden corners of our oceans.
Branched worm inside a sea sponge.Ponz Segrelles, Aguado & Glasby.Female reproductive unit of new species of branching worm (Ramisyllis kingghidorahi) "shaking".Female reproductive units of new species of branching worm reacting to the light.PublicationNew species of branching worm (Ramisyllis kingghidorahi) digesting food.
The reproductive system of Ramisyllis kingghidorahi is a compelling counterpoint to creationist assertions of intelligent design. Far from being a paragon of engineering efficiency, this worm’s method of reproduction is a masterclass in evolutionary kludging—cobbled together not for elegance, but functionality under specific constraints over time. The species produces free-swimming reproductive units, or stolons, which grow eyes, detach from a highly branched, sedentary parent body, and swim off in search of a mate. This process is not only energy-intensive and complex but also involves a decentralised network of genetic regulation across the worm’s ramified body, which makes little sense as a product of foresight or design.Abstract
Background
Ramisyllis kingghidorahi (Annelida, Syllidae) is one of few annelid species with a ramified body, one anterior end and hundreds of posterior ends. R. kingghidorahi belongs to the family Syllidae, whose members reproduce by forming stolons, small autonomous reproductive units, at the posterior end. Molecular mechanisms controlling sexual reproduction are still poorly understood, but previous studies support an important role of the anterior end and stolons. The roles of different body regions during sexual reproduction in a complex branched body where there is only one head but multiple posterior ends, which develop hundreds of simultaneous stolons, have never been investigated. Consequently, we aimed to research the transcriptomic basis of sexual maturation and stolonization in R. kingghidorahi by performing differential gene expression analyses.
Results
Transcriptomes were assembled from different body regions (anterior end, midbody, and stolons) of male, female, and non-reproductive individuals. Comparative analyses revealed that body region had a greater impact on gene expression profiles than sex, with the anterior end and stolons showing extensive gene upregulation. Across-sex comparisons revealed sex-specific processes in all body regions, with stolons exhibiting the most differences in differential expression, likely related to gametogenesis and external sexual dimorphism. Fewer genes than expected were differentially expressed in the anterior region, a result for which different possible explanations are discussed. Surprisingly, key genes typically associated with segmentation and metamorphosis, such as Wnt and Hox, showed little differential expression, aligning with recent findings that stolon segments lack a specific segment identity.
Conclusions
This study presents the first transcriptomic data for a branched annelid species and offers new insights into the complex genetic regulation of reproduction in R. kingghidorahi. Additionally, it provides the first glimpse into the mechanisms of sexual maturation in branched syllids, which must coordinate stolonization across multiple posterior ends. These findings enhance our understanding of annelid reproductive biology and highlight the need for further research to uncover the physiological and molecular pathways regulating sexual maturation and stolonization in syllids and other annelids.
Background
Annelids of the family Syllidae Grube, 1850 [1] are characterized by two main features: the presence of a proventricle, and the post-embryonic metamorphic changes associated with sexual maturation [2,3,4]. The proventricle is an apomorphic structure of the digestive tract that lies immediately posterior to the more strongly-cuticularized, partially-eversible axial pharynx, and is composed of a prominent layer of radially-arranged muscle cells [2,3,4,5,6]. During sexual maturation, many syllid species develop reproductive units (stolons) formed by a few segments at the posteriormost tip of the body. These units contain the gonads and gametes and they are detachable from the rest of the body and usually develop characteristic anterior anatomical features like eyes and brains in addition to swimming chaetae, which allow them to swim and find a mating partner independently [6,7,8,9,10]. This process is known as schizogamy or stolonization.
For several decades, the leading hypothesis about the physiological mechanisms regulating sexual maturation in syllids was that stolonization is constantly suppressed by a Stolonization-Inhibiting Hormone (SIH) associated with the proventricle or the proventricle region and, when the right light and temperature conditions are met, a Stolonization-Promoting Hormone (SPH) produced and/or released by the prostomium inhibits SIH and triggers sexual maturation and stolonization [11,12,13,14,15]. However, later research has shown that hormonal control of sexual maturation in annelids is usually significantly more complex [16,17,18,19,20,21,22,23,24] and, based on this increasing knowledge, gene expression studies have been performed in syllids to further understand the role of the anterior region in the onset and control of stolonization, refining the original hypothesis. Álvarez-Campos et al. [25] found differential expression of genes involved in methylfarnesoate synthesis in stolonizing Syllis Magdalena Wesenberg-Lund, 1962 [26], and have proposed that it acts together with dopamine and serotonin in regulating sexual maturation and influencing the expression of several genes involved in gametogenesis and other reproduction-related processes. Similarly, Ponz-Segrelles et al. [27] discussed the issue of sex determination and its possible relation with irreversible gene expression changes during the worms’ lives. More recently, Nakamura et al. [24] studied the expression patterns of several candidate genes, including stem cell markers and Hox genes, during stolonization in Megasyllis nipponica (Imajima, 1966) [28]. Yet, there is still much to learn about the mechanisms involved in the many changes associated with sexual maturation in Syllidae. For example, despite the extreme metamorphic changes that take place, there is still no information concerning the mechanisms involved in stolon formation, which must include, but may not be limited to, axis patterning, nervous system and eye development, chaetae formation, gonad development, gametogenesis, and behaviour.
On top of this, syllid reproduction includes a variety of different types of stolonization (i.e. scissiparity and several kinds of gemmiparity) [29], with those present in the Ribbon Clade (sensu [29, 30]) being the most remarkable [7, 29]. This clade includes species that produce only one stolon per reproductive event (scissiparity), but also others that simultaneously produce multiple stolons (gemmiparity), which may be clustered in bunches attached ventrally at the posteriormost one or two parental segments, or individually attached to different posterior segments [31,32,33,34]. However, the most striking species of the Ribbon Clade are those with a branched body [29, 35, 36], something that was initially thought to be restricted to a single species, but is now known in three, presumably related different species from a wide geographic range and will likely be described for related, newly-described species in the future [37].
Branched syllids obligatorily inhabit sponges and exhibit a body plan unique among the annelids (Figs. 1A, B). These animals show a single anterior end with a regular head and foregut that is followed by a ramified body in which the body recursively branches laterally [35,36,37] (Figs. 1A, C). Lateral branches are known to include all longitudinal internal organs and are, therefore, considered to be complete bifurcations of the anteroposterior axis of the animal [38]. Notably, such branched bodies result in the existence of hundreds or thousands of complete posterior ends, each of them potentially capable of stolonization [36]. This way, a single stolonizing specimen of branched syllid can produce hundreds of stolons simultaneously [36, 37]. Stolons (Fig. 1D) show sexual dimorphism in their external anatomy, and each sexually mature specimen produces either male or female stolons exclusively during each stolonization cycle [35,36,37,38]. Unfortunately, branched syllids have proven to be very elusive and have only been occasionally found in very limited places since they were first discovered [35,36,37]. Thus, due to their specific habitats, difficult accessibility for sampling, the challenges of studying symbiotic organisms both in the lab and field, and the many difficulties faced in the past when trying to obtain sequence data, not much is known about these enigmatic animals. However, the peculiar anatomy of branched syllids of the genus Ramisyllis have been recently explored in detail, and it has been proposed that physiological innovations must also be present in these species since basic processes like digestion or blood circulation are likely to be affected by their branched bodies [38].
As explained, syllids show great diversity in relation to the metamorphic changes associated with sexual maturation, including extremes such as those described for Ramisyllis. However, up to now, all available gene expression information comes only from species producing stolons through scissiparity [24, 25, 27, 39]. Thus, the true complexity and variability of the many mechanisms that must be involved in controlling sexual maturation in syllids remains virtually unknown. Studying these mechanisms in syllids with different reproductive modes is particularly interesting, as it is unclear whether the anterior end and stolons, known to regulate sexual maturation in scissiparous syllids, also function similarly in branched syllids, which have numerous posterior ends requiring stolonization control. Considering the previous studies and proposed stolonization control hypotheses [7, 24, 25], the single head of these animals must play a highly important role in regulating the reproductive processes occurring in hundreds of posterior ends. Thus, the aim of this study is to characterize gene expression changes associated with stolonization and examine what regions are involved in reproductive processes in such huge and complex branched bodies.Fig. 1
Stereomicroscopy images of living specimens of Ramisyllis kingghidorahi and in situ underwater photography of its host sponge Petrosia sp. A, Fragment of the anterior region including the prostomium, proventricle, and first branches, dorsal view. Arrowhead points to the anterior end. B, Host sponge Petrosia sp. in its natural habitat [modified from 54]. C, Fragment of a R. kingghidorahi specimen including several posterior ends. Arrow points towards the direction of the anterior end, which is missing. D, Developing male stolon attached to its parental stalk. Dashed line indicates the boundary between the stalk (left) and the stolon (right). Scale bars: 2 mm (A, C); 1 cm (B); 250 µm (D)
Here we present an exploratory analysis of gene expression in stolon-bearing male and female specimens of the branched syllid Ramisyllis kingghidorahi Aguado et al., 2022 [37]. We used transcriptome-based differential gene expression analyses to compare the expression profiles from three body regions (anterior ends, midbody fragments, and stolons) in reproductive males and females as well as non-reproductive individuals, and focused on the expression patterns of those transcripts that we identified as potentially involved in processes related to sexual maturation/reproduction.
From a biological perspective, this form of reproduction only makes sense as a response to the worm’s unusual lifestyle: living embedded in sponge tissue where mobility is limited. In such an environment, a traditional form of mating would be highly inefficient or outright impossible. The decentralised production of stolons along many branches allows for multiple, simultaneous chances at reproduction, increasing the likelihood of success despite the constraints. Evolution, with its trial-and-error tinkering, can produce such baroque solutions precisely because it is unguided and works with whatever materials are at hand—no matter how convoluted the outcome.
If R. kingghidorahi had been designed by an intelligent entity, who inexplicably chose to design it to live in such a contrained environment as the inside of a sponge in the first place, one must wonder why the designer opted for a solution so biologically costly and prone to failure. Intelligent design proponents often claim nature exhibits irreducible complexity or optimal design. Yet here we see a process that is not only reducible but almost certainly evolved through a patchwork of adaptations to ecological pressures. The worm’s reproductive strategy is not evidence of foresight, but rather a living demonstration of how messy, contingent, and ultimately powerful the evolutionary process can be.
As I pointed out in my book, The Unintelligent Designer: Refuting the Intelligent Design Hoax, complexity is not a characteristic of good, intelligent design; intelligent design is minimally complex. Complexity in living systems is evidence of an unintelligent, utilitarian natural process, operating without a plan and with natural selection favouring the least bad solution.
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