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Kimberella and Controversial Relationships — A Chronological Synopsis, Continued

Photo: Kimberella, by the paleobear from Lontananza, Loreto, Peru / CC BY (https://creativecommons.org/licenses/by/2.0).

Editor’s note: We are delighted to present a series of posts by paleontologist Günter Bechly on the Ediacaran organism Kimberella. If identified as an animal, it would “predate the Cambrian explosion of bilaterian animal phyla as a kind of ‘advance guard.’” The question is of interest for debates about evolution and arguments about intelligent design raised by Stephen Meyer, among others. Find the full series about Kimberella here.

In an article about the origins of multicellularity, Knoll (2011) said that “Kimberella, shares many features with mollusks, although in toto its preserved characters suggest a stem-group bilaterian.” He also postulated that “these animals must have had coordinated muscles capable of sustained locomotion, a digestive system for processing food captured using a radula-like oral apparatus, and a circulatory system that freed Kimberella from diffusional constraints,” even though none of these characters is preserved in any of the Kimberella fossils (note: Fedonkin et al. 2007b actually said that “a true circulatory system may have been absent in Kimberella“).

Nielsen (2012) provided an updated standard textbook on animal evolution and the interrelationships of animal phyla. As in the first edition of his book (Nielsen 2001), he remained unconvinced by previous attributions of Kimberella and remarked: “The Late Precambrian Kimberella has been interpreted as a mollusc …, but the reconstruction shows a periphery with a ‘crenellated zone’ that does not resemble any known structure from living molluscs, and there is no sign of foot, mouth, or radula. Long scratches in the microbial mat near the anterior end of some specimens have been interpreted as radular marks …, but the relationships of Kimberella still seem uncertain.”

Ivantsov (2010b, 2012) listed several characters (dorsal sclerites, mouth with teeth, foot adapted for crawling) that he considered to be “sufficient to assume a molluscan affinity of Kimberella,” but also listed several conflicting characters (e.g., different feeding apparatus and movement, absence of sensor processes, dorsal muscles). He concluded that “probably, Kimberella is only closely related to mollusks, but it is not a mollusk itself. It is probably related to one of the early evolution stages of trochophore animals, when their extant phyla had not been yet formed.” He closed his article with the clear statement that the “available fossils give us no solid evidences of mollusks’ occurrence in the Precambrian.”

“Fossil Problematica”

Vendrasco (2012) criticized previous attributions of Kimberella to the stem of mollusks and said “their hypothesis lacks strong support, and this is exacerbated by the uncertain placement of Kimberella.” Therefore, he preferred to classify Kimberella among the Ediacaran “fossil problematica.”

Erwin & Valentine (2013) considered Kimberella “to be one of the few Ediacaran body fossils that require placement higher than the Cnidaria” (quoted in Budd & Jensen 2017).

Ivantsov (2013) simply stated that in his opinion “Kimberella had little to do with mollusks, although it was probably a primitive trochophoran animal (Trochozoa).”

Scherholz et al. (2013) only briefly mentioned that the attribution of Kimberella to the crown- or stem-group of mollusks is uncertain and presented evidence that simple worm-like aplacophoran mollusks evolved from more complex polyplacophoran ancestors. This is also supported by the fossil armored aplacophoran Kulindroplax perissokomos described by Sutton et al. 2012 from the Silurian of England. This finding of course undermines the claim that Kimberella resembles the assumed molluscan ground plan.

Stöger et al. (2013) said that “The Vendian (555 Ma) body fossil Kimberella was discussed as a mollusc, but not widely accepted as such, and rather treated as lophotrochozoan stem member or ‘no more specifically than as a bilaterian.’” However, because all their molecular time trees placed the origin of mollusks in the Precambrian, Stöger et al. at least considered that “Kimberella appears late enough in the fossil record to be considered as a potential stem mollusc.” Furthermore, they maintained that “Kimberella corresponds to the description of molluscan stem-group features” because it seems to share the following four characters as putative synapomorphies with molluscs in their cladistic analysis: bipartite radula, foot with gliding sole, circumpedal mantle cavity, separate mantle covered with cuticula. It is interesting that none of these characters is really unequivocally established as present in Kimberella. It is also noteworthy that their reconstruction of internal mollusk relationships is contradicted by virtually all other recent studies (Ponder & Lindberg 2008, Nielsen 2012, Kocot 2013, Schrödel & Stöger 2014, Vinther 2014, 2015, Sigwart & Lindberg 2015, Parkhaev 2017, Giribet & Edgecombe 2020, Kocot et al. 2020) and thus has to be considered as highly controversial and doubtful. Anyway, the authors concluded: 

Our assessment of potential morphological apomorphies and the molecular clock results would suggest that the Vendian (555 Ma) Kimberella is a candidate stem-group mollusc appearing before the evolution of a dorsal shell field. The interpretation of Kimberella is controversial, but the true stem molluscs probably did have a large, bilaterally symmetrical body with subapical mouth on a snout with a likely bipartite radula, a broad ventral foot, many dorsoventral muscle bundles, and a dorsal mantle covered with a resistant dorsal cuticle with mineralised spicules, which are all molluscan features, but lacking a shell.

Uncertain Affinities

Gehling et al. (2014) found that Kimberichnus “supports previous trace fossil evidence that bilaterians existed globally before the Cambrian explosion of life” and “point to the systematic feeding excavation of seafloor microbial mats by large bilaterians of molluscan grade.” However, they also cautioned that “closer examination of the K. teruzzii arrays provides some contrary evidence” to a molluscan affinity of the trace-maker. They emphasized that extant gastropods always move forward in the direction of their radular feeding, but never backward unlike Kimberella. They concluded that “Kimberella and its feeding scratches are best explained as evidence of basal crown group bilaterians with lophotrochozoan affinities,” but they considered the affinities of Kimberella to be uncertain.

Grazhdankin (2014) called Kimberella a “tissue-grade organism,” which he attributed to a newly created Ediacaran phylum called Bilateralomorpha, also comprising the potentially related genera Brachina and Solza as well as very different problematic organisms with bilateral body symmetry like for example Parvancorina and Temnoxa.

Schrödl & Stöger (2014) thought that recent phylogenomic studies, which “recovered Mollusca as a basal offshoot of a lophotrochozoan (spiralian) clade,” are well “consistent with their Precambrian dating in molecular clock approaches.” They also speculated that characters like a sinusoidal body cavity and a ciliated foot could be plesiomorphic ground plan characters “for Kimberella and other molluscs.”

Scheltema (2014) said that “besides being a grazer, Kimberella appears to be a stem belonging to the total group Mollusca. As defined here, it has a stiff, noncalcareous, organic dorsal covering (but see Ivantsov 2009), a ventral muscular, flat-soled foot, and a space (mantle cavity) between dorsum and ventrum containing folded tissue — the basic body plan for Mollusca although with many variations.”

Shu et al. (2014) referred to Kimberella as “a possible soft-bodied mollusk,” but just two pages later as “possible stem lophotrochozoan.” Obviously, a lot is possible.

Sperling et al. (2015), who studied the Ediacaran-Cambrian oxygenation, said that “large triploblastic Ediacaran organisms, such as Kimberella (commonly but not definitively thought to be related to the mollusks; …), moved across the seafloor, making extensive scratch marks on the sediment surface,” and therefore claimed that the “combination of Kimberella’s size, locomotion, and feeding mode would have required both a blood vascular system and much higher minimum oxygen levels.”

Vinther (2015) concluded that “Kimberella from the latest Ediacaran exhibits several molluscan traits, which justifies its position as a molluscan stem-group member, rather than as a more basal Lophotrochozoan.” He emphasized that “these impressions resemble a molluscan body plan in having a distinct creeping sole (foot) and a surrounding mantle separated by a mantle cavity,” and “the dorsal surface exhibits a cuticular shield with tubercular nodes.” His main argument for a mollusk affinity was the association with “creeping and scraping marks suggestive of a ciliary gliding organism with a molluscan-style radula” (Vinther et al. 2012) as well as the presence of a paired structure at the tubular end, which he interpreted as resembling esophageal pouches that are only known in mollusks like monoplacophorans, chitons, and gastropods. However, Vinther acknowledged that “Kimberella does not offer any characters for establishing character polarity in molluscan evolution as it does not possess a biomineralized skeleton.”

Bowyer et al. (2017) considered Kimberella as a “bilaterian organism” and “probably motile early molluscan organism.”

A Careful and Thorough Review

Budd & Jensen (2017), after a careful and thorough review of all the published evidence, were much more prudent. In spite of all the previous attributions to bilaterian animals, they mentioned that “there is a curious similarity of some elongate Kimberella to fronds …, the rounded terminal structures would be attachments and the radiating ridges would be interpreted as body fossil parts.” On the other hand they said that “general similarities can also be found between Kimberella and Palaeophragmodictya spinosa (Serezhnikova, 2009), with an outer zone and an inner zone with ‘hand’-like structures that in Kimberella have been interpreted as longitudinal muscle. The possibility that Kimberella is coelenterate grade should therefore not be excluded (see also Erwin, 2008).” They found that “although likely a metazoan, its placement remains problematic; it may be on the bilaterian stem group rather than within the stem group of any particular phylum — this is not incompatible with it retaining some coelenterate-grade features,” and conclude that “the affinities of Kimberella remain highly uncertain, but there seems to be no good reason to regard it as a mollusc; its most likely placement is in the stem-group of the Bilateria.”

Cunningham et al. (2017) agreed that “the presence of differentiated anterior-posterior anatomy and bilateral symmetry, comparatively large size, a possible radula-like structure, and evidence of movement suggest that Kimberella was a total-group bilaterian.” However, they cautioned that “suggestions of a more derived affinity place too much credence on the inference of a molluscan radula, and the nature of the mantle-like structure.” Concerning the feeding traces, they remarked that “there remain unresolved questions regarding how these scratches were formed and by what kind of structure …, and there is insufficient evidence to test whether the structure that produced them was homologous with a molluscan radula.”

Droser et al. (2017) listed Kimberella as a “putative stem-mollusk.”

Ivantsov (2017) said that Kimberella is “representing the Bilateria” and “probably, could belong to the Trochozoa … and probably, was close to the ancestors of mollusks.”

Parkhaev (2017) discussed the arguments for a molluscan affinity of Kimberella and considered this assignment as doubtful, mainly because the reconstruction of Kimberella does not conform to the mollusk archetype. The biggest issue is “the direction of movement, since all of the mollusks crawl head first. Secondly, the style of feeding is absolutely untypical for mollusks, because when they ‘scrape’ the food substrate by a radula, they make translational movements forward rather than backward (Ivanov, 1990, text-fig. 6), since that radula is located on their tongue within the throat, but not on the anterior appendage of the head. Therefore, obviously there is no homology between the ‘teeth’ of Kimberella and the radula of mollusks.” He also rejected the dorsal sclerites as evidence for a molluscan nature, because they are only indirectly inferred and are found in various phyla. He concluded that “it is difficult to assign Kimberella to any known phylum of metazoans, definitely it is undoubtedly the representative of Bilateria,” and that any ancestors of mollusks cannot be detected yet among the soft-bodied organisms of the Vendian biota.

Vinther et al. (2017) described the Ordovician Calvapilosa kroegeri, which is a siphonogonuchid and very similar to halkieriids. It definitely proved the presence of a true radula and established the molluscan affinity of halkieriids (also see Wanninger & Wollesen 2019). In their phylogenetic analyses (see extended data figure 8 in their supplementary information), which included most early fossils of lophotrochozoans, they resolved Kimberella within the stem group of mollusks.

Darroch et al. (2018) listed Kimberella in their tree as lophotrochozoan and maintained that “Kimberella is the best candidate for a bilaterian metazoan, possessing a number of mollusk-like characteristics: Kimberella was likely mobile, preserves evidence for a muscular ‘foot’, and is commonly associated with scratch marks (Kimberichnus isp.), illustrating possession of paired radula-like structures.”

A Change of Mind

Ivantsov et al. (2019) considered Kimberella as “a bilateral symmetric organism close to mollusks.” This was unlike his earlier papers until 2013, when he still claimed that it “had little to do with mollusks” (see above). It is interesting that this apparent change of mind is not based on any new fossil evidence, but maybe rather on peer pressure.

Wanninger & Wollesen (2019) discussed the similarities of Kimberella with basal mollusks and placed Kimberella as most basal branch of stem mollusk in their tree of molluscan phylogeny and evolution. They listed the presence of a single shell and dorso-ventral muscles as only putative synapomorphies, even though both characters are highly doubtful for Kimberella.

Kocot et al. (2020) presented the most recent phylogenetic analysis of mollusks, as well as a molecular clock study that placed the origin of mollusks in the Precambrian about 584 million years ago. They commented: 

The Ediacaran fossil genus Kimberella has been hypothesized to represent a stem-group mollusc by some, but the molluscan affinity of Kimberella has been criticized by others who instead view it as an early-branching bilaterian, in part because of its old age (~555 MYA). Although broad, our and other recent estimates for the divergence of molluscs are at least compatible with hypotheses regarding Kimberella as an early offshoot of the molluscan stemline. However, if Kimberella was indeed a mollusc, it differed from most extant molluscs in its lack of a shell (although sclerites may have been present) and, more significantly, a bizarre rake-like mode of feeding unlike that of any modern mollusc.

Giribet & Edgecombe (2020) did not take a position in their most up-to-date textbook on the invertebrate tree of life, but merely mentioned that “the possibility that the Ediacaran fossil Kimberella quadrata … could be a mollusc or a mollusclike bilaterian has been explored numerous times since that idea was first formalized.”

Last but not least, the constantly updated Paleobiology Database lists Kimberella within Metazoa in the unranked clade Kimberellomorpha, thus neither as a bilaterian nor as a stem mollusk.

Next, “Kimberella Is No Solution to the Cambrian Conundrum.”