Dickinsonia costata — the first evidence of neoteny in Ediacaran organisms

Abstract

Some of the most famous organisms of the Late Precambrian are representatives
of the genus Dickinsonia. Four species of Dickinsonia are found throughout the
section, characterized by macrofossils, on the southeastern White Sea area. However, their
distribution is uneven. Two species, D. costata and D. tenuis are the most common, while
the other two occur sporadically. At the lower levels (Verkhovka Formation) thinsegmented
D. tenuis is the most frequently encountered. There are few imprints that can be
attributed to D. costata, and all of them are of small size. Numerous specimens of D. costata,
representing all available for study stages of ontogeny, are present only at the upper
stratigraphic levels — in the Zimnie Gory and Erga formations. The statistical analysis of
Dickinsonia imprints from a number of fossil assemblages in the southeastern White Sea
shows an existence of two distinct groups that could represent different stages of ontogeny
of a single species — D. tenuis. All the features of the juvenile D. tenuis — a round body,
enlarged head part and a small number of trunk isomers — are distinctive features of D.
costata. These features are preserved in mature D. costata. The most likely explanation of
this phenomenon is the origin of D. costata from D. tenuis by neoteny.

Full text

© INVERTEBRATE ZOOLOGY, 2017Invertebrate Zoology, 2017, 14(1): 92–98
Dickinsonia costata — the first evidence of neoteny
in Ediacaran organisms
M.A. Zakrevskaya, A.Yu. Ivantsov
A.A. Borissiak Paleontological Institute of RAS, Profsoyuznaya st., 123, Moscow, 117647, Russia.
E-mail: mariazakrevskaya@gmail.com ivancov@paleo.ru
ABSTRACT: Some of the most famous organisms of the Late Precambrian are represen-
tatives of the genus Dickinsonia. Four species of Dickinsonia are found throughout the
section, characterized by macrofossils, on the southeastern White Sea area. However, their
distribution is uneven. Two species, D. costata and D. tenuis are the most common, while
the other two occur sporadically. At the lower levels (Verkhovka Formation) thin-
segmented D. tenuis is the most frequently encountered. There are few imprints that can be
attributed to D. costata, and all of them are of small size. Numerous specimens of D. costata,
representing all available for study stages of ontogeny, are present only at the upper
stratigraphic levels — in the Zimnie Gory and Erga formations. The statistical analysis of
Dickinsonia imprints from a number of fossil assemblages in the southeastern White Sea
shows an existence of two distinct groups that could represent different stages of ontogeny
of a single species — D. tenuis. All the features of the juvenile D. tenuis — a round body,
enlarged head part and a small number of trunk isomers — are distinctive features of D.
costata. These features are preserved in mature D. costata. The most likely explanation of
this phenomenon is the origin of D. costata from D. tenuis by neoteny.
How to cite this article: Zakrevskaya M.A., Ivantsov A.Yu. 2017. Dickinsonia costata —
the first evidence of neoteny in Ediacaran organisms // Invert. Zool. Vol.14. No.1. P.92–98.
doi: 10.15298/invertzool.14.1.13
KEY WORDS: Ediacaran biota, Vendian, Metazoa, Invertebrate paleontology, Dickin-
sonia.
Dickinsonia costata — первое свидетельство неотении
у эдиакарских организмов
М.А. Закревская, А.Ю. Иванцов
Палеонтологический институт им. А.А. Борисяка РАН, Профсоюзная ул., 123, Москва,
117647, Россия. E-mail: mariazakrevskaya@gmail.com ivancov@paleo.ru
РЕЗЮМЕ: Одними из самых известных организмов позднего докембрия являются
представители рода Dickinsonia. На территории Юго-Восточного Беломорья 4 вида
дикинсоний встречаются по всему разрезу, охарактеризованному макроископаемы-
ми. Однако распределение их неравномерно. Наибольшее распространение имеют
два вида D. costata и D. tenuis, а два других встречаются спорадически. На нижних
уровнях (верховская свита) наиболее часто встречается тонкосегментная D. tenuis, а
отпечатков, которые можно было бы отнести к D. costata мало и все они мелкого
размера. Многочисленные остатки D. costata, отражающие все доступные для на-

93Dickinsonia costata — the first evidence of neoteny in Ediacaran organisms
Introduction
Dickinsonia Sprigg, 1947 is one of the most
typical and world-known fossil taxa of the Edi-
acaran (Vendian) age. It was described original-
ly from the upper Ediacaran (Pound Quartzite)
of the Flinders Ranges in South Australia. The
genus is common in marine strata of eastern
Europe and South Australia. The flat bilaterally
symmetrical body of Dickinsonia consists of
two parts — head and trunk ones. The trunk part
is divided into numerous transverse elements —
isomers, located on both sides of the body in an
alternating pattern. The head part of mature
individuals is almost indistinguishable from iso-
mers by its overall size and size ratios.
Dickinsonia costata Sprigg, 1947 is the type
species of the genus. It is characterized by a
round shape with the length/width ratio ap-
proaching 1:1, by a small number of isomers
with relatively large width, and by the enlarged
head part.
During 70 years of the study of Dickinsonia,
understanding of this genus was changed radi-
cally. At the beginning, Dickinsonia was inter-
preted as coelenterates of uncertain origin
(Sprigg, 1949) and as annelids (Glaessner, Wade,
1966). D. Seilacher combined Dickinsonia along
with the rest of the Vendian biota into the special
extinct kingdom of Vendobionta on the basis of
their specific features, such as the chambered
construction, the symmetry of the sliding reflec-
tion, a presumable absence of the oral opening
and distinct inner structures (Seilacher, 1989,
1992). He suggested that Dickinsonia was feed-
ing by absorbing dissolved organic matter by
the entire body surface using chemo- or photo-
symbionts. Later on, Seilacher reduced the com-
position of the Vendobionta and lowered the
rank of this group to a class level within rhizo-
pod protozoans (Seilacher et al., 2003). G. Re-
tallack suggested that Dickinsonia was remains
of fungi or lichens on the basis of its leaf shape
and unlimited growth (Retallack, 1994). E. Sper-
ling and J. Vinther proposed a hypothesis on the
placozoan level of organization of alike Vendi-
an organisms, based on the assumption that
Dickinsonia fed by external digestion (Sper-
ling, Vinther, 2010). Dickinsonia was also in-
terpreted as ancestral chordates (Dzik, 2003).
According to the most compelling suggestions,
Dickinsonia is classified as the Proarticulata, an
extinct phylum of benthic mobile multicellular
animals (Fedonkin, 1990). This statement was
confirmed by the finds of Dickinsonia trace
fossils in association with the body imprints of
the trace maker (Ivantsov, Malakhovskaya, 2002;
Gehling et al., 2005; Evans et al., 2015). The
pattern of Dickinsonia trace fossils revealed
that this animal fed on upper surface of micro-
bial mats using its ventral side (Ivantsov, 2011,
2013). Distinct internal structures, interpreted
as digestive-distributive systems, were also
found in some specimens of Dickinsonia (Ivan-
блюдения стадии онтогенеза этого вида, присутствуют только на верхних уровнях —
в зимнегорской и ергинской свитах. Проведенный статистический анализ совокуп-
ности отпечатков дикинсоний из ряда захоронений Юго-Восточного Беломорья
показал существование 2 четких групп, которые могут представлять собой различ-
ные стадии онтогенеза одного вида — D. tenuis. Все признаки ювенильных D. tenuis —
округлое тело, широкий головной отдел и небольшое количество туловищных
изомеров — являются характерными признаками D. costata и сохраняются у нее во
взрослом состоянии. Наиболее вероятным объяснением выявленного феномена
является происхождение D. costata от D. tenuis путем неотении.
Как цитировать эту статью: Zakrevskaya M.A., Ivantsov A.Yu. 2017. Dickinsonia
costata — the first evidence of neoteny in Ediacaran organisms // Invert. Zool. Vol.14.
No.1. P.92–98. doi: 10.15298/invertzool.14.1.13
КЛЮЧЕВЫЕ СЛОВА: эдиакарская биота, вендский период, Metazoa, палеонтология
беспозвоночных, Dickinsonia.

94 M.A. Zakrevskaya, A.Yu. Ivantsov
tsov, 2004). An indirect evidence of this organ-
ism mobility can also be derived from the study
of paleocommunities. In paleocommunities con-
sisting of juveniles only and almost lacking
mature individuals, very large single individu-
als of Dickinsonia costata occur. Such individ-
uals, representing the previous generation, prob-
ably migrated from nearby areas and gave the
birth to juveniles that formed a new paleocom-
munity (Zakrevskaya, 2014).
Dickinsonia is the richest genus of the late
Precambrian macroorganisms. At present, nine
species of this genus were described: D. costa-
ta, D. tenuis, D. lissa, D. menneri, D. rex, D.
brachina, D. minima, D. spriggi, and D. elon-
gata. However, the majority of these species
probably are synonyms. In the White Sea sec-
tions, four species only are found, namely D.
costata, D. tenuis, D. lissa, D. menneri. They
differ primarily by ratios of body dimensions
and by the width of transverse elements (iso-
mers) and the head part. Of them, D. costata and
D. tenuis only are present in a significant num-
ber to use statistical analysis.
Materials and methods
Dickinsonia specimens are collected in the
southeastern White Sea area (Arkhangelsk re-
gion) by the Precambrian team of the A.A.
Borissiak Paleontological Institute of RAS and
housed in the Laboratory of Precambrian Or-
ganisms of this institute.
The fossils were preserved in situ as im-
prints on sandstone bottom surfaces (Flinders-
type preservation; Narbonne, 2005), as a result
of burial of benthic paleocommunities by storm
sediments. In the White Sea section, a series of
successive burials is observed at different strati-
graphic levels embracing an interval of over 3
million years (Martin et al., 2000; Llanos et al.,
2005). Dickinsonia is found throughout the sec-
tion, characterized by macrofossils. However,
generally only thin-segmented D. tenuis occurs
at the lower levels (the Verkhovka Formation)
while imprints that can be attributed to D. cos-
tata are few and small. Numerous specimens of
D. costata preserving all the stages of ontogeny
available for study are restricted to the upper
levels, in the Zimnie Gory and Erga formations.
For the statistical analysis of the fossil im-
prints, over 500 specimens, presumably belong-
ing to different species of Dickinsonia, were
measured. The length and the width of each
imprint (with 0.1 mm precision), the number of
its isomers, and the width of the first isomer at its
widest dimension are measured in 220 speci-
mens of Dickinsonia. Fragmentary preservation
of other specimens does not allow us to include
them in our analysis. However, an excellent
preservation of the majority of the White Sea
specimens bearing the finest details provides an
opportunity to make necessary measurements
even in the smallest individuals.
Results and discussion
A statistical analysis has been applied to the
imprints of both D. tenuis and D. costata from
a number of burials in the Verkhovka and Erga
formations, respectively, of the Karakhta and
Zimnie Gory localities (Zakrevskaya, Ivantsov,
2015). Due to certain peculiarities of the forma-
tion of Flinders-type localities, each fossil as-
semblages of a burial reflects directly the pre-
burial state of populations and is not enriched or
depleted during posthumous processes. The re-
sulting plots show a variation in the number of
isomers and the width of the first isomer of
Dickinsonia in relation to the body size (length,
width). The body length of D. tenuis being
figured against the width of its first isomer
reveals a bimodal distribution of these dimen-
sions (Fig. 1). The first group is represented by
small-sized specimens with a wide head part,
and the second group — by larger specimens
with a narrow head part. These two sets of
individuals are distinct and their ratio variables
do not overlap.
The ratio of the length to the number of
isomers also demonstrates a similar division
into two groups for D. tenuis (Fig. 2), where the
first group is characterized by a small number of
isomers and a small body size, and the second
one — by a large number of isomers and a bigger

95Dickinsonia costata — the first evidence of neoteny in Ediacaran organisms
Fig. 1. Ratio of length to width of the head part of Dickinsonia tenuis from Karakhta locality.
Рис. 1. Соотношение длины и ширины головного отдела Dickinsonia tenuis из Карахтинского
местонахождения.
Fig. 2. Ratio of length to number of isomers in Dickinsonia tenuis from Karakhta locality and D. costata from
Zimnie Gory locality.
Рис. 2. Соотношение длины и количества изомеров у Dickinsonia tenuis из Карахтинского и Dickinsonia
costata из Зимнегорского местонахождения.

96 M.A. Zakrevskaya, A.Yu. Ivantsov
size. The plot shows that the size ratios of the
first group correlate with same ratios of D.
costata from the Zimnie Gory locality (marked
by black triangles) and together these data com-
pile a single linear trend. Such a pattern keeps
pass in D. costata throughout the entire length
range up to very large specimens (up to 140 mm
in length). In D. tenuis, as the size increases, the
linear trend abruptly changes its direction, and
the growth in the number of isomers overcomes
the increase in size of larger individuals com-
pared to smaller ones.
The same pattern is observed on the plot
showing the ratio of the number of isomers to the
width of the first isomer for the same specimens
of D. tenuis and D. costata (Fig. 3). An overlap
of dimensions of the smallest D. tenuis with
those of D. costata is observed, where the latter
is distinguished by the presence of a wide head
part and a small total number of isomers. Over
specimens of D. tenuis form a separate set that
does not overlap with the previous one and is
characterized by a gradually increasing total
number of isomers and a constant very small
relative width of the head part, which is much
inferior to the width of the head part in speci-
mens from the first set.
In fossil assemblages of the Karakhta local-
ity, all small individuals of Dickinsonia are
characterized by body dimensions of D. costa-
Fig. 3. Ratio of number of isomers to width of the head part in the widest section of Dickinsonia tenuis from
Karakhta and D. costata from Zimnie Gory locality.
Рис. 3. Соотношение количества изомеров и ширины головного отдела в самой широкой его части
у Dickinsonia tenuis из Карахтинского и Dickinsonia costata из Зимнегорского местонахождения.

97Dickinsonia costata — the first evidence of neoteny in Ediacaran organisms
ment can be indicative of the fact that Dickinso-
nia had a distinct juvenile stage and this stage
was characterized by an ecology different from
that of mature individuals.
It can be seen that all the features of juvenile
D. tenuis — the round body, the wide first
isomer and a small number of isomers – are
characteristics of D. costata and remain so at
mature stages (Fig. 3, 4). These observations
can indicate a probable origin of D. costata
from D. tenuis by the neoteny. This is the first
case of neoteny being observed in Precambrian
organisms.
ta, and all larger individuals have features typ-
ical of D. tenuis (Fig. 4). The transition from the
first set to the second one is abrupt but no gap in
the sequence is observed. In this regard, we
suggest that both sets represent different stages
of ontogeny of the same species — D. tenuis.
The transition is accompanied by a discontinu-
ous growth and by a sharp, almost double in-
crease in the number of trunk isomers, as well as
a reduction in the width of the head part. Thus,
the body assumes the appearance of a typical D.
tenuis. The well-marked morphological differ-
ences between early and later stages of develop-
Fig. 4. Individual development of Dickinsonia. 1–8 — a part of the ontogeny series of D. tenuis based on
specimens from Karakhta locality (1–3 — juveniles); 9, 10 — D. costata from Zimnie Gory locality; latex
casts of the specimens from the PIN RAS collection, nos.: 1 — specimen PIN, No 4852/38, 2 — 4852/39,
3 — 4852/33, 4 — 4852/79, 5 — 4852/60, 6 — 4852/30, 7 — 4852/44, 8 — 4852/17, 9 — 3993/5107, 10
— 3993/5243. Scale bar 1 cm.
Рис. 4. Возрастные преобразования тела дикинсоний. 1–8 — фрагмент онтогенетического ряда
Dickinsonia tenuis по материалам Карахтинского местонахождения (1–3 — ювенильная стадия); 9,
10 — Dickinsonia costata из Зимнегорского местонахождения; латексные слепки с экземпляров
коллекции ПИН РАН, №№: 1 — 4852/38, 2 — 4852/39, 3 — 4852/33, 4 — 4852/79, 5 Ї 4852/60, 6 —
4852/30, 7 — 4852/44, 8 — 4852/17, 9 — 3993/5107, 10 — 3993/5243. Длина масштабного отрезка —
1 см.

98 M.A. Zakrevskaya, A.Yu. Ivantsov
Martin M.W., Grazhdankin D.V., Bowring S.A., Evans
D.A.D., Fedonkin M.A., Kirschvink J.L. 2000. Age of
Neoproterozoic Bilatarian Body and Trace Fossils,
White Sea, Russia: Implications for Metazoan Evolu-
tion // Science. Vol.288. No.5467. P.841–845.
Narbonne G.M. 2005. The Ediacara biota: Neoproterozoic
origin of animals and their ecosystems // Annual
Review Earth Planet. Science. Vol.33. P.421–442.
Retallack G.J. 1994. Were the Ediacaran fossils lichens? //
Paleobiology. Vol.20. P.523–544.
Seilacher A. 1989. Vendozoa: Organismic construction in
the Proterozoic biosphere // Lethaia. Vol.22. No.3.
P.229–239.
Seilacher A. 1992. Vendobionta and Psammocorallia: lost
constructions of Precambrian evolution // Journal of
the Geological Society. London. Vol.149. No.4. P.607–
613.
Seilacher A., Grazhdankin D., Legouta A. 2003. Ediaca-
ran biota: The dawn of animal life in the shadow of
giant protests // Paleontological research. Vol.7. No.1.
P.43–54.
Sperling E.A., Vinther J. 2010. A placozoan affinity for
Dickinsonia and the evolution of late Proterozoic
metazoan feeding modes // Evolution & Develop-
ment. Vol.12. P.201–209.
Sprigg R.C. 1947. Early Cambrian (?) Jellyfishes from the
Flinders Ranges, South Australia // Transactions of
The Royal Society of South Australia. Vol.71. No.2.
P.212–224.
Sprigg R.C. 1949. Early Cambrian “Jellyfishes” of Edi-
acara, South Australia and Mouth John, Kimberley
District, Western Australia // Transactions of The Roy-
al Society of South Australia. Vol.73. No.1. P.72–99.
Zakrevskaya M.A. 2014. Paleoecological reconstruction
of the Ediacaran benthic macroscopic communities of
the White Sea (Russia) // Palaeogeography, Palaeocli-
matology, Palaeoecology. Vol.410. P.27–38.
Zakrevskaya M.A., Ivantsov A.Yu. 2015. [Evolution of
views on the nature of Dickinsonia costata (metazoan
of the Vendian period)] // Sovremennye problemy
paleontologii. Materialy LXI sessii Paleontolo-
gicheskogo obshchestva pri RAN. Sankt-Peterburg.
P.40–42 [in Russian].
Responsible editor E.N. Temereva
The work was supported by the RFBR grant
No. 17-05-02212-a.
References
Dzik J. 2003. Anatomical information content in the
Ediacaran fossils and their possible zoological affin-
ities // Integrative and Comparative Biology. Vol.43.
P.114–126.
Evans S.D., Droser M.L., Gehling J.G. 2015. Dickinsonia
liftoff: Evidence of current derived morphologies //
Palaeogeography, Palaeoclimatology, Palaeoecology.
Vol.434. P.28–33.
Fedonkin M.A. 1990. Systematic description of the Ven-
dian Metazoa // B. Sokolov, A. Ivanovski (eds.). The
Vendian System 1, Paleontology. New York: Spring-
er-Verlag. P.71–120.
Gehling J.G., Droser M.L., Jensen S., Runnegar B.N.
2005. Ediacaran organisms: relating form to function
// D.E.G. Briggs (ed.). Evolving Form and Function:
Fossils and Development. Proceedings of a Sympo-
sium Honoring Adolf Seilacher for His Contributions
to Palaeontology in Celebration of His 80th Birthday.
New Haven: Yale University. P.43–67.
Glaessner M.F., Wade M. 1966. The Late Precambrian
fossils from Ediacara, South Australia // Palaeontolo-
gy. Vol.9. P.599–628.
Ivantsov A.Yu. 2004. New Proarticulata from the Vendian
of Arkhangelsk Region // Paleontological Journal.
Vol.38. No.3. P.247–253.
Ivantsov A.Yu. 2011. Feeding Traces of Proarticulata —
the Vendian Metazoa // Paleontological Journal.
Vol.45. No.3. P.237–248.
Ivantsov A.Yu. 2013. Trace Fossils of Precambrian Meta-
zoans “Vendobionta” and “Mollusks” // Stratigraphy
and Geological Correlation. Vol.21. No.3. P.252–
264.
Llanos M.P.I., Tait J.A., Popov V., Abalmassova A. 2005.
Palaeomagnetic data from Ediacaran (Vendian) sedi-
ments of the Arkhangelsk region, NW Russia: an
alternative apparent polar wander path of Baltica for
the Late Proterozoic — Early Palaeozoic // Earth and
Planetary Science Letters. Vol.240. P.732–747.