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Cited by 158Marine Invertebrate Physiology and EcologyDevelopmental Biology and Gene RegulationEvolution and Paleontology Studies

Origin and evolution of animal life cycles

NIELSEN, CLAUS·1998·Biological Reviews of the Cambridge Philosophical Society
DOI 10.1017/s0006323197005136
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Abstract

ABSTRACT The ‘origin of larvae’ has been widely discussed over the years, almost invariably with the tacit understanding that larvae are secondary specializations of early stages in a holobenthic life cycle. Considerations of the origin and early radiation of the metazoan phyla have led to the conclusion that the ancestral animal (= metazoan) was a holopelagic organism, and that pelago‐benthic life cycles evolved when adult stages of holopelagic ancestors became benthic, thereby changing their life style, including their feeding biology. The literature on the larval development and phylogeny of animal phyla is reviewed in an attempt to infer the ancestral life cycles of the major animal groups. The quite detailed understanding of larval evolution in some echinoderms indicates that ciliary filter‐feeding was ancestral within the phylum, and that planktotrophy has been lost in many clades. Similarly, recent studies of the developmental biology of ascidians have demonstrated that a larval structure, such as the tail of the tadpole larva, can easily be lost, viz. through a change in only one gene. Conversely, the evolution of complex structures, such as the ciliary bands of trochophore larvae, must involve numerous genes and numerous adaptations. The following steps of early metazoan evolution have been inferred from the review. The holopelagic ancestor, blastaea, probably consisted mainly of choanocytes, which were the feeding organs of the organism. Sponges may have evolved when blastaea‐like organisms settled and became reorganized with the choanocytes in collar chambers. The eumetazoan ancestor was probably the gastraea, as suggested previously by Haeckel. It was holopelagic and digestion of captured particles took place in the archenteron. Cnidarians and ctenophores are living representatives of this type of organization. The cnidarians have become pelago‐benthic with the addition of a sessile, adult polyp stage; the pelagic gastraea‐like planula larva is retained in almost all major groups, but only anthozoans have feeding larvae. Within the Bilateria, two major lines of evolution can be recognized: Protostomia and Deuterostomia. In protostomes, trochophores or similar types are found in most spiralian phyla; trochophore‐like ciliary bands are found in some rotifers, whereas all other aschelminths lack ciliated larvae. It seems probable that the trochophore was the larval type of the ancestral, pelago‐benthic spiralian and possible that it was ancestral in all protostomes. Most of the non‐chordate deuterostome phyla have ciliary filter‐feeding larvae of the dipleurula type, and this strongly indicates that the ancestral deuterostome had this type of larva.

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  • The latest common ancestor of eleutherozoans (node E of Fig. 2) must have utilized maximal indirect development.

    “Given that all other eleutherozoan groups (i.e., asteroids, ophiuroids, echinoids, and holothurians, which is to say all modern echinoderm groups except crinoids) also have primary larval stages, the latest common ancestor of eleutherozoans (Fig. 2, node E) must have utilized maximal indirect development as well (see also Smith, 1997;Nielsen, 1998).”

    From Bilaterian Origins: Significance of New Experimental Observations (2000) · cites this paper as Nielsen, 1998

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Authors
NIELSEN, C.
Affiliations
University of Copenhagen (DK)
Corresponding author
NIELSEN, CLAUS
ORCID
NIELSEN, CLAUS
Venue
Biological Reviews of the Cambridge Philosophical Society
Publisher
Wiley
Published
1998-05
Volume
73
Issue
2
Pages
125-155
ISSN
0006-3231 (ISSN-L)
DOI
10.1017/s0006323197005136
OpenAlex
W2153478536
Cited by
158
References
0
Citations by year
2026: 8 · 2025: 2 · 2024: 3 · 2023: 3 · 2022: 6 · 2021: 5 · 2020: 2 · 2019: 6 · 2018: 1 · 2017: 1 · 2016: 1 · 2015: 3 · 2013: 5 · 2012: 2
FWCI
11.08
Type
journal article
Language
en
Open access
closed
Licence
doi.wiley.com/10.1002/tdm_license_1 (tdm, 6332 d)
Locations
  • Biological reviews/Biological reviews of the Cambridge Philosophical Society (publishedVersion)
  • Research at the University of Copenhagen (University of Copenhagen) (submittedVersion)
Topics
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Marine Invertebrate Physiology and Ecology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
  • Physical Sciences › Earth and Planetary Sciences › Paleontology › Evolution and Paleontology Studies
Keywords
animal life cycle, animal evolution, planktotrophy, trochophore larvae, ciliary bands, sponge evolution, choanocytes, planula larvae

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