Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

Nielsen, Claus

doi:10.1186/1471-2148-13-171

Cited by 69Marine Invertebrate Physiology and EcologyDevelopmental Biology and Gene RegulationEvolution and Paleontology Studies

Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

Open access

Nielsen, Claus·2013·BMC Evolutionary Biology

DOI 10.1186/1471-2148-13-171

Open this paper in CoChat — free account Open PDF

Abstract

Two theories for the origin of animal life cycles with planktotrophic larvae are now discussed seriously: The terminal addition theory proposes a holopelagic, planktotrophic gastraea as the ancestor of the eumetazoans with addition of benthic adult stages and retention of the planktotrophic stages as larvae, i.e. the ancestral life cycles were indirect. The intercalation theory now proposes a benthic, deposit-feeding gastraea as the bilaterian ancestor with a direct development, and with planktotrophic larvae evolving independently in numerous lineages through specializations of juveniles. Information from the fossil record, from mapping of developmental types onto known phylogenies, from occurrence of apical organs, and from genetics gives no direct information about the ancestral eumetazoan life cycle; however, there are plenty of examples of evolution from an indirect development to direct development, and no unequivocal example of evolution in the opposite direction. Analyses of scenarios for the two types of evolution are highly informative. The evolution of the indirect spiralian life cycle with a trochophora larva from a planktotrophic gastraea is explained by the trochophora theory as a continuous series of ancestors, where each evolutionary step had an adaptational advantage. The loss of ciliated larvae in the ecdysozoans is associated with the loss of outer ciliated epithelia. A scenario for the intercalation theory shows the origin of the planktotrophic larvae of the spiralians through a series of specializations of the general ciliation of the juvenile. The early steps associated with the enhancement of swimming seem probable, but the following steps which should lead to the complicated downstream-collecting ciliary system are without any advantage, or even seem disadvantageous, until the whole structure is functional. None of the theories account for the origin of the ancestral deuterostome (ambulacrarian) life cycle. All the available information is strongly in favor of multiple evolution of non-planktotrophic development, and only the terminal addition theory is in accordance with the Darwinian theory by explaining the evolution through continuous series of adaptational changes. This implies that the ancestor of the eumetazoans was a holopelagic, planktotrophic gastraea, and that the adult stages of cnidarians (sessile) and bilaterians (creeping) were later additions to the life cycle. It further implies that the various larval types are of considerable phylogenetic value.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Integrity signals

Registry

Crossref · 10.1186/1471-2148-13-171

Cites

148 of 148 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

If the first nervous system arose in a small animal, especially a larva, this probably lessens the need for internal-coordination functions in behaviour.
“If the first nervous system arose in a small animal, especially if it first appeared in the larval stage [91], this will probably reduce the need for IC functions in behaviour.”
From An option space for early neural evolution (2015) · cites this paper as [91]

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Part of this paper’s reference list could not be split into single entries.

The Growth of Biological Thought: Diversity, Evolution, and Inheritance
Mayr, E. (1982) · CERN Document Server (European Organization for Nuclear Research) · Cited by 2,295 · see citing works
Oxford Oxford University
Funnekotter, B. (2005) · Amsterdam University Press eBooks · doi:10.1017/9789048505418.012 · Cited by 1,672 · see citing works
Animal evolution: interrelationships of the living phyla
(2012) · Choice Reviews Online · doi:10.5860/choice.50-1469 · Cited by 1,041 · see citing works
Three-dimensional preservation of algae and animal embryos in a Neoproterozoic phosphorite
Xiao, S., Zhang, Y., & Knoll, A. H. (1998) · Nature · doi:10.1038/35318 · Cited by 783 · see citing works
The Deep Roots of Eukaryotes
Baldauf, S. L. (2003) · Science · doi:10.1126/science.1085544 · Cited by 782 · see citing works
Ecology of Marine Invertebrate Larvae
McEdward, L. R. (2020) · CRC Press eBooks · doi:10.1201/9780138758950 · Cited by 710 · see citing works
Origin and Evolutionary Radiation of the Mollusca
(1995) · doi:10.1093/oso/9780198549802.001.0001 · Cited by 706 · see citing works
Systematics and ecology of the Isefjord marine fauna (Denmark)
Rasmussen, E. (1973) · Ophelia · doi:10.1080/00785326.1973.10430115 · Cited by 692 · see citing works
Systematics and Evolution of Littorina
Reid, D. G. (1999) · Cited by 473 · see citing works
Hox genes and the evolution of the arthropod body plan1
Hughes, C. L., & Kaufman, T. C. (2002) · Evolution & Development · doi:10.1046/j.1525-142x.2002.02034.x · Cited by 433 · see citing works
Embryology: constructing the organism
(1998) · Choice Reviews Online · doi:10.5860/choice.35-3280 · Cited by 423 · see citing works
The earliest Cambrian record of animals and ocean geochemical change
Maloof, A. C., Porter, S. M., Moore, J. L., Dudas, F. O., Bowring, S. A., Higgins, J. A., Fike, D. A., & Eddy, M. P. (2010) · Geological Society of America Bulletin · doi:10.1130/b30346.1 · Cited by 419 · see citing works
Phylogenomic analyses unravel annelid evolution
Struck, T. H., Paul, C., Hill, N., Hartmann, S. A., Hösel, C., Kube, M., Lieb, B., Meyer, A., Tiedemann, R., Purschke, G., et al. (2011) · Nature · doi:10.1038/nature09864 · Cited by 406 · see citing works
The Invertebrates, Vol. II: Platyhelminthes and Rhynchocoela
Goodrich, A. L., & Hyman, L. H. (1951) · Transactions of the American Microscopical Society · doi:10.2307/3223296 · Cited by 346 · see citing works
Six major steps in animal evolution: Are we derived sponge larvae?
Nielsen, C. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00231.x · Cited by 343 · cited 1× · see citing works
“feeding adult through “neoteny” is almost identical to the process proposed by me [21], except that I now call the”
Self-citation
The invertebrates : Platyhelminthes and Rhynchocoela, the acoelomate Bilateria.
Hyman, L. H. (1951) · Cited by 336 · see citing works
Invertebrate neurophylogeny: suggested terms and definitions for a neuroanatomical glossary
Richter, S., Loesel, R., Purschke, G., Schmidt‐Rhaesa, A., Scholtz, G., Stach, T., Vogt, L., Wanninger, A., Brenneis, G., Döring, C., et al. (2010) · Frontiers in Zoology · doi:10.1186/1742-9994-7-29 · Cited by 334 · see citing works
The phylogeny and classification of post-Palaeozoic echinoids
Kroh, A., & Smith, A. B. (2010) · Journal of Systematic Palaeontology · doi:10.1080/14772011003603556 · Cited by 326 · see citing works
EVOLUTION OF THE METAZOAN LIFE CYCLE
Hedgpeth, J. W. (1974) · Evolution · doi:10.1111/j.1558-5646.1974.tb00804.x · Cited by 320 · see citing works
Higher-level metazoan relationships: recent progress and remaining questions
Edgecombe, G. D., Giribet, G., Dunn, C. W., Hejnol, A., Kristensen, R. M., Neves, R. C., Rouse, G. W., Worsaae, K., & Sørensen, M. V. (2011) · Organisms Diversity & Evolution · doi:10.1007/s13127-011-0044-4 · Cited by 291 · see citing works
Small Bilaterian Fossils from 40 to 55 Million Years Before the Cambrian
Chen, J.-Y., Bottjer, D. J., Oliveri, P., Dornbos, S. Q., Gao, F., Ruffins, S., Chi, H., Li, C.-W., & Davidson, E. H. (2004) · Science · doi:10.1126/science.1099213 · Cited by 284 · see citing works
The Fossils of the Burgess Shale
Briggs, D., Erwin, D. H., & Collier, F. J. (1994) · Bristol Research (University of Bristol) · Cited by 257 · see citing works
Cnidarian phylogenetic relationships as revealed by mitogenomics
Kayal, E., Roure, B., Philippe, H., Collins, A. G., & Lavrov, D. V. (2013) · BMC Evolutionary Biology · doi:10.1186/1471-2148-13-5 · Cited by 240 · see citing works
Evidence of giant sulphur bacteria in Neoproterozoic phosphorites
Bailey, J. V., Joye, S. B., Kalanetra, K. M., Flood, B. E., & Corsetti, F. A. (2006) · Nature · doi:10.1038/nature05457 · Cited by 219 · see citing works
The Biogeography of Marine Invertebrate Life Histories
Marshall, D. J., Krug, P. J., Kupriyanova, E. K., Byrne, M., & Emlet, R. B. (2011) · Annual Review of Ecology Evolution and Systematics · doi:10.1146/annurev-ecolsys-102710-145004 · Cited by 215 · see citing works
SUSPENSION FEEDING BY MARINE INVERTEBRATE LARVAE: CLEARANCE OF PARTICLES BY CILIATED BANDS OF A ROTIFER, PLUTEUS, AND TROCHOPHORE
Strathmann, R. R., Jahn, T. L., & Fonseca, J. R. (1972) · Biological Bulletin · doi:10.2307/1540326 · Cited by 210 · see citing works
Trochophore concepts: ciliary bands and the evolution of larvae in spiralian Metazoa
Rouse, G. W. (1999) · Biological Journal of the Linnean Society · doi:10.1111/j.1095-8312.1999.tb01920.x · Cited by 201 · see citing works
Cellular and Subcellular Structure of Neoproterozoic Animal Embryos
Hagadorn, J. W., Xiao, S., Donoghue, P. C. J., Bengtson, S., Gostling, N. J., Pawlowska, M., Raff, E. C., Raff, R. A., Turner, F. R., Chongyu, Y., et al. (2006) · Science · doi:10.1126/science.1133129 · Cited by 199 · see citing works
The comparative morphology, phylogeny and evolution of the gastropod family littorinidae
Reid, D. G. (1989) · Philosophical transactions of the Royal Society of London. Series B, Biological sciences · doi:10.1098/rstb.1989.0040 · Cited by 198 · see citing works
Reproduction and development of marine invertebrates
Wilson, W. H., Stricker, S. A., & Shinn, G. L. (1994) · Johns Hopkins University Press eBooks · Cited by 196 · see citing works
A placozoan affinity for Dickinsonia and the evolution of late Proterozoic metazoan feeding modes
Sperling, E. A., & Vinther, J. (2010) · Evolution & Development · doi:10.1111/j.1525-142x.2010.00404.x · Cited by 194 · see citing works
Precambrian animal diversity: Putative phosphatized embryos from the Doushantuo Formation of China
Chen, J.-Y., Oliveri, P., Li, C.-W., Zhou, G.-Q., Gao, F., Hagadorn, J. W., Peterson, K. J., & Davidson, E. H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4457 · Cited by 187 · see citing works
Parallel Evolution of Nonfeeding Larvae in Echinoids
Wray, G. A. (1996) · Systematic Biology · doi:10.1093/sysbio/45.3.308 · Cited by 181 · see citing works
Late Larval Development and Onset of Symbiosis in the Scleractinian Coral Fungia scutaria
Schwarz, J. A., Krupp, D. A., & Weis, V. M. (1999) · Biological Bulletin · doi:10.2307/1543169 · Cited by 180 · see citing works
Fossilized Nuclei and Germination Structures Identify Ediacaran “Animal Embryos” as Encysting Protists
Huldtgren, T., Cunningham, J. A., Yin, C., Stampanoni, M., Marone, F., Donoghue, P. C. J., & Bengtson, S. (2011) · Science · doi:10.1126/science.1209537 · Cited by 171 · see citing works
Entoproct life-cycles and the entoproct/ectoproct relationship
Nielsen, C. (1971) · Ophelia · doi:10.1080/00785326.1971.10430095 · Cited by 168 · see citing works
Self-citation
Developmental shifts and species selection in gastropods
Duda, T. F., & Palumbi, S. R. (1999) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.96.18.10272 · Cited by 162 · see citing works
Acoel development supports a simple planula-like urbilaterian
Hejnol, A., & Martindale, M. Q. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2239 · Cited by 161 · see citing works
A molecular phylogeny of bryozoans
Waeschenbach, A., Taylor, P. D., & Littlewood, D. T. J. (2011) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.11.011 · Cited by 154 · see citing works
Origins of the other metazoan body plans: the evolution of larval forms
Raff, R. A. (2008) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2007.2237 · Cited by 154 · see citing works
The origin of Metazoa: a transition from temporal to spatial cell differentiation
Mikhailov, K. V., Константинова, А. В., Nikitin, M. A., Troshin, P. V., Rusin, L. Y., Lyubetsky, V., Panchin, Y. V., Mylnikov, A. P., Moroz, L. L., Kumar, S., et al. (2009) · BioEssays · doi:10.1002/bies.200800214 · Cited by 151 · see citing works
High-resolution fate map of the snail Crepidula fornicata: The origins of ciliary bands, nervous system, and muscular elements
Hejnol, A., Martindale, M. Q., & Henry, J. J. (2007) · Developmental Biology · doi:10.1016/j.ydbio.2007.01.044 · Cited by 150 · see citing works
Trochophora larvae: Cell‐lineages, ciliary bands, and body regions. 1. Annelida and Mollusca
Nielsen, C. (2004) · Journal of Experimental Zoology Part B: Molecular and Developmental Evolution · doi:10.1002/jez.b.20001 · Cited by 150 · see citing works
Self-citation
PHYLOGENETIC EFFECTS, THE LOSS OF COMPLEX CHARACTERS, AND THE EVOLUTION OF DEVELOPMENT IN CALYPTRAEID GASTROPODS
Collin, R. (2004) · Evolution · doi:10.1111/j.0014-3820.2004.tb01729.x · Cited by 141 · see citing works
The earliest fossil record of the animals and its significance
Budd, G. E. (2008) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2007.2232 · Cited by 140 · see citing works
Regulatory evolution and the origin of the bilaterians
Peterson, K. J., & Davidson, E. H. (2000) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.97.9.4430 · Cited by 139 · see citing works
The active evolutionary lives of echinoderm larvae
Raff, R. A., & Byrne, M. (2006) · Heredity · doi:10.1038/sj.hdy.6800866 · Cited by 136 · see citing works
Bilaterian Origins: Significance of New Experimental Observations
Peterson, K. J., Cameron, R. A., & Davidson, E. H. (2000) · Developmental Biology · doi:10.1006/dbio.1999.9475 · Cited by 133 · see citing works
Hox gene expression in larval development of the polychaetes Nereis virens and Platynereis dumerilii (Annelida, Lophotrochozoa)
Kulakova, M. A., Бакаленко, Н. И., Novikova, E. L., Cook, C. E., Eliseeva, E., Steinmetz, P. R. H., Kostyuchenko, R. P., Dondua, A. K., Arendt, D., Akam, M. E., et al. (2006) · Development Genes and Evolution · doi:10.1007/s00427-006-0119-y · Cited by 123 · see citing works
Larval stages of a living sea lily (stalked crinoid echinoderm)
Nakano, H., Hibino, T., Oji, T., Hara, Y., & Amemiya, S. (2003) · Nature · doi:10.1038/nature01236 · Cited by 123 · see citing works
Expression of anterior Hox genes during larval development of the gastropod Haliotis asinina
Hinman, V. F., O’Brien, E., Richards, G. S., & Degnan, B. M. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03056.x · Cited by 120 · see citing works
The Cambrian Fossils of Chengjiang, China
(2003) · Wiley eBooks · doi:10.1002/9780470999950 · Cited by 120 · see citing works
New data on Kimberella , the Vendian mollusc-like organism (White Sea region, Russia): palaeoecological and evolutionary implications
Fedonkin, M. A., Simonetta, A., & Ivantsov, A. Y. (2007) · Geological Society, London, Special Publications · doi:10.1144/sp286.12 · Cited by 116 · see citing works
Life Cycle Evolution in Asteroids: What is a Larva?
McEdward, L. R., & Janies, D. A. (1993) · Biological Bulletin · doi:10.2307/1542444 · Cited by 114 · see citing works
Deuterostomes in a twist: the origins of a radical new body plan
Smith, A. B. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2008.00260.x · Cited by 113 · see citing works
The significance of moulting in Ecdysozoan evolution
Valentine, J. W., & Collins, A. G. (2000) · Evolution & Development · doi:10.1046/j.1525-142x.2000.00043.x · Cited by 112 · see citing works
Evolving Pathways
Fusco, G. (2008) · Cambridge University Press eBooks · doi:10.1017/cbo9780511541582 · Cited by 111 · see citing works
Trochophora larvae: cell-lineages, ciliary bands and body regions. 2. Other groups and general discussion
Nielsen, C. (2005) · Journal of Experimental Zoology Part B Molecular and Developmental Evolution · doi:10.1002/jez.b.21050 · Cited by 111 · see citing works
Self-citation
A molecular palaeobiological hypothesis for the origin of aplacophoran molluscs and their derivation from chiton-like ancestors
Vinther, J., Sperling, E. A., Briggs, D. E. G., & Peterson, K. J. (2011) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2011.1773 · Cited by 111 · see citing works
The development of the larval nervous system, musculature and ciliary bands of Pomatoceros lamarckii (Annelida): heterochrony in polychaetes
McDougall, C., Chen, W.-C., Shimeld, S. M., & Ferrier, D. E. K. (2006) · Frontiers in Zoology · doi:10.1186/1742-9994-3-16 · Cited by 111 · see citing works
Requirement of the Manx Gene for Expression of Chordate Features in a Tailless Ascidian Larva
Swalla, B. J., & Jeffery, W. R. (1996) · Science · doi:10.1126/science.274.5290.1205 · Cited by 108 · see citing works
Who came first--larvae or adults? origins of bilaterian metazoan larvae
Sly, B. J., Smith, M. S., & Raff, R. A. (2003) · The International Journal of Developmental Biology · doi:10.1387/ijdb.14756338 · Cited by 105 · see citing works
Filter-feeding in fifteen marine ectoprocts (Bryozoa):particle capture and water pumping
Riisgård, H. U., & Manríquez, P. H. (1997) · Marine Ecology Progress Series · doi:10.3354/meps154223 · Cited by 104 · see citing works
Apical organs in echinoderm larvae: insights into larval evolution in the Ambulacraria
Byrne, M., Nakajima, Y., Chee, F. C., & Burke, R. D. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00189.x · Cited by 98 · see citing works
Embryonic and post‐embryonic development of the Early Cambrian cnidarian Olivooides
Zhao, Y. J., & Bengtson, S. (1999) · Lethaia · doi:10.1111/j.1502-3931.1999.tb00538.x · Cited by 96 · see citing works
A Description of Spawning and Post-Gastrula Development of the Cool Temperate Coral, Caryophyllia Smithi
Tranter, P. R. G., Nicholson, D., & Kinchington, D. (1982) · Journal of the Marine Biological Association of the United Kingdom · doi:10.1017/s0025315400070387 · Cited by 96 · see citing works
Tentacle structure and filter-feeding in Crisia eburnea and other cyclostomatous bryozoans, with a review of upstream-collecting mechanisms
Nielsen, C., & Riisgård, H. U. (1998) · Marine Ecology Progress Series · doi:10.3354/meps168163 · Cited by 94 · see citing works
Self-citation
Multiple origins of anural development in ascidians inferred from rDNA sequences
Hadfield, K. A., Swalla, B. J., & Jeffery, W. R. (1995) · Journal of Molecular Evolution · doi:10.1007/bf00164028 · Cited by 92 · see citing works
Functional Constraints on the Evolution of Larval Forms of Marine Invertebrates: Experimental and Comparative Evidence
Emlet, R. B. (1991) · American Zoologist · doi:10.1093/icb/31.4.707 · Cited by 90 · see citing works
The Biphasic Life Cycle—A Central Theme of Metazoan Evolution
Rieger, R. M. (1994) · American Zoologist · doi:10.1093/icb/34.4.484 · Cited by 90 · see citing works
The epitome of hand waving? Larval feeding and hypotheses of metazoan phylogeny
Rouse, G. W. (2000) · Evolution & Development · doi:10.1046/j.1525-142x.2000.00063.x · Cited by 90 · see citing works
Embryos, polyps and medusae of the Early Cambrian scyphozoan Olivooides
Dong, X., Cunningham, J. A., Bengtson, S., Thomas, C., Liu, J., Stampanoni, M., & Donoghue, P. C. J. (2013) · Proceedings of the Royal Society B Biological Sciences · doi:10.1098/rspb.2013.0071 · Cited by 89 · see citing works
A novel ontogenetic pathway in hybrid embryos between species with different modes of development
Raff, E. C., Popodi, E. M., Sly, B. J., Turner, F. R., Villinski, J. T., & Raff, R. A. (1999) · Development · doi:10.1242/dev.126.9.1937 · Cited by 87 · see citing works
Anatomy, ecology and affinities of the Australian Early Cambrian bivalve Pojetaia runnegari Jell
Runnegar, B. N., & Bentley, C. (1983) · Journal of Paleontology · Cited by 87 · see citing works
Patterns of gene expression: homology or homocracy?
Nielsen, C., & Martı́nez, P. (2003) · Development Genes and Evolution · doi:10.1007/s00427-003-0301-4 · Cited by 86 · see citing works
Self-citation
Downstream collecting in ciliary suspension feeders: the catch-up principle
Riisgård, H. U., Nielsen, C., & Larsen, P. S. (2000) · Marine Ecology Progress Series · doi:10.3354/meps207033 · Cited by 86 · see citing works
Self-citation
A Silurian armoured aplacophoran and implications for molluscan phylogeny
Sutton, M. D., Briggs, D. E. G., Siveter, D. J., Siveter, D. J., & Sigwart, J. D. (2012) · Nature · doi:10.1038/nature11328 · Cited by 80 · see citing works
Molecular Phylogenetic and Embryological Evidence That Feeding Larvae Have Been Reacquired in a Marine Gastropod
Collin, R., Chaparro, Ó. R., Winkler, F. M., & Véliz, D. (2007) · Biological Bulletin · doi:10.2307/25066586 · Cited by 79 · see citing works
Resolving phylogenetic signal from noise when divergence is rapid: a new look at the old problem of echinoderm class relationships.
Pisani, D., Feuda, R., Peterson, K., & Smith, A. B. T. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2011.08.028 · Cited by 79 · see citing works
Shell microstructure of the early bivalve Pojetaia and the independent origin of nacre within the mollusca
Vendrasco, M. J., Checa, A. G., & Kouchinsky, A. (2011) · Palaeontology · doi:10.1111/j.1475-4983.2011.01056.x · Cited by 74 · see citing works
Complex embryos displaying bilaterian characters from Precambrian Doushantuo phosphate deposits, Weng'an, Guizhou, China
Chen, J., Bottjer, D. J., Li, G., Hadfield, M. G. ‏., Gao, F., Cameron, R. A., Zhang, C., Xian, D., Tafforeau, P., Liao, X., et al. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0904805106 · Cited by 74 · see citing works
Phylogenetic analysis of four nuclear protein-encoding genes largely corroborates the traditional classification of Bivalvia (Mollusca)
Sharma, P. P., González, V. L., Kawauchi, G. Y., Andrade, S. C. S., Guzmán, A., Collins, T. M., Glover, E. A., Harper, E. M., Healy, J. M., Mikkelsen, P. M., et al. (2012) · Molecular Phylogenetics and Evolution · doi:10.1016/j.ympev.2012.05.025 · Cited by 73 · see citing works
Feeding behavior and acquisition of zooxanthellae by planula larvae of the sea anemone Anthopleura elegantissima
Schwarz, J. A., Weis, V. M., & Potts, D. C. (2002) · Marine Biology · doi:10.1007/s00227-001-0736-y · Cited by 71 · see citing works
The Lower Metazoa.
Barnes, R. D., & Dougherty, E. C. (1964) · The American Midland Naturalist · doi:10.2307/2423524 · Cited by 70 · see citing works
Programmed Cell Death in the Apical Ganglion During Larval Metamorphosis of the Marine MolluscIlyanassa obsoleta
Gifondorwa, D. J., & Leise, E. M. (2006) · Biological Bulletin · doi:10.2307/4134600 · Cited by 68 · see citing works
Levels of selection and macroevolutionary patterns in the turritellid gastropods
Lieberman, B. S., Allmon, W. D., & Eldredge, N. (1993) · Paleobiology · doi:10.1017/s0094837300015876 · Cited by 68 · see citing works
Modes of larval development in Early Tertiary neogastropods
Hansen, T. A. (1982) · Paleobiology · doi:10.1017/s0094837300007119 · Cited by 67 · see citing works
Modes of Larval Development and Rates of Speciation in Early Tertiary Neogastropods
Hansen, T. A. (1983) · Science · doi:10.1126/science.220.4596.501 · Cited by 66 · see citing works
Homology of ciliary bands in Spiralian Trochophores
Henry, J. J., Hejnol, A., Perry, K. J., & Martindale, M. Q. (2007) · Integrative and Comparative Biology · doi:10.1093/icb/icm035 · Cited by 66 · see citing works
Structure and swimming behavior of the larva of Haliclona tubifera (Porifera: Demospongiae)
Woollacott, R. M. (1993) · Journal of Morphology · doi:10.1002/jmor.1052180306 · Cited by 65 · see citing works
Persistent Ancestral Feeding Structures in Nonfeeding Annelid Larvae
Pernet, B. (2003) · Biological Bulletin · doi:10.2307/1543293 · Cited by 63 · see citing works
Development of the enteropneust Ptychodera flava: Ciliary bands and nervous system
Nielsen, C., & Hay‐Schmidt, A. (2007) · Journal of Morphology · doi:10.1002/jmor.10533 · Cited by 61 · see citing works
Self-citation
A molecular and morphological revision of genera of Asterinidae (Echinodermata: Asteroidea)
O’Loughlin, P. M., & Waters, J. M. (2004) · Memoirs of Museum Victoria · doi:10.24199/j.mmv.2004.61.1 · Cited by 60 · see citing works
Zur Morphologie und Embryogenese des Darmtraktes und der transitorischen Organe bei Prosobranchiern (Mollusca, Gastropoda)
Fioroni, P. (1966) · Revue suisse de zoologie · doi:10.5962/bhl.part.75848 · Cited by 60 · see citing works
Reorganization of the nervous system during metamorphosis of a hydrozoan planula
Martina, V. J. (2000) · Invertebrate Biology · doi:10.1111/j.1744-7410.2000.tb00011.x · Cited by 57 · see citing works
Unusual Development of the Mitraria Larva in the Polychaete Owenia collaris
Smart, T. I., & von Dassow, G. (2009) · Biological Bulletin · doi:10.1086/bblv217n3p253 · Cited by 56 · see citing works
Indirect development, transdifferentiation and the macroregulatory evolution of metazoans
Arenas‐Mena, C. (2010) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2009.0253 · Cited by 56 · see citing works
Bias? What bias? The evolution of downstream larval‐feeding in animals
Rouse, G. W. (2000) · Zoologica Scripta · doi:10.1046/j.1463-6409.2000.00040.x · Cited by 56 · see citing works
An Attempt to Reconstruct the System of Animal Classification
Hadži, J. (1953) · Systematic Biology · doi:10.2307/sysbio/2.4.145 · Cited by 55 · see citing works
Rare and remarkable animals of Scotland, represented from living subjects: with practical observations on their nature
Dalyell, J. G. (1847) · doi:10.5962/bhl.title.5984 · Cited by 54 · see citing works
Fractionation ofPneumocystis carinii developmental stages by counterflow centrifugal elutriation and sequential filtrations
Stefano, J. A. D., Foy, J., Sullivan, D. W., Dawes, S. M., Cushion, M. T., Babcock, G. F., Sleight, R. G., van HALBEEK, H., & Walzer, P. D. (1994) · Parasitology Research · doi:10.1007/bf00932616 · Cited by 50 · see citing works
Poecilogony and larval ecology in the gastropod genus Alderia*
Krug, P. J. (2007) · American Malacological Bulletin · doi:10.4003/0740-2783-23.1.99 · Cited by 50 · see citing works
An Attempt to Reconstruct the System of Animal Classification
Hadzi, J. (1953) · Systematic Zoology · doi:10.2307/2411558 · Cited by 48 · see citing works
Feeding by larvae of two different developmental modes in Streblospio benedicti (Polychaeta: Spionidae)
Pernet, B., & McArthur, L. (2006) · Marine Biology · doi:10.1007/s00227-006-0266-8 · Cited by 47 · see citing works
Methods of ciliary filter feeding in adult Phoronis muelleri (phylum Phoronida) and in its free-swimming actinotroch larva
rd, H. R. X. E. (2002) · Marine Biology · doi:10.1007/s00227-002-0802-0 · Cited by 46 · see citing works
Time and Extent of Ciliary Response to Particles in a Non-Filtering Feeding Mechanism
Strathmann, R. R. (2007) · Biological Bulletin · doi:10.2307/25066587 · Cited by 44 · see citing works
Ciliary filter‐feeding structures in adult and larval gymnolaemate bryozoans
Nielsen, C. (2002) · Invertebrate Biology · doi:10.1111/j.1744-7410.2002.tb00065.x · Cited by 43 · see citing works
Self-citation
Morphology and wall ultrastructure of leiosphaeric and acanthomorphic acritarchs from the Ediacaran of Australia
Willman, S. (2008) · Geobiology · doi:10.1111/j.1472-4669.2008.00178.x · Cited by 43 · see citing works
Aspects of feeding, growth and stage development by trochophora larvae of the boreal polychaete Mediomastus fragile (Rasmussen) (Capitellidae)
Hansen, B. W. (1993) · Journal of Experimental Marine Biology and Ecology · doi:10.1016/0022-0981(93)90224-c · Cited by 41 · see citing works
Co‐option and dissociation in larval origins and evolution: the sea urchin larval gut
Love, A. C., Lee, A. E., Andrews, M. E., & Raff, R. A. (2008) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00215.x · Cited by 41 · see citing works
Ciliary Bands in Echinoderm Larvae: Evidence for Structural Homologies and a Common Plan
Lacalli, T. C. (1993) · Acta Zoologica · doi:10.1111/j.1463-6395.1993.tb01229.x · Cited by 41 · see citing works
Apical skeletons of sea urchins (Echinodermata: Echinoidea): two methods for inferring mode of larval development
Emlet, R. B. (1989) · Paleobiology · doi:10.1017/s009483730000943x · Cited by 40 · see citing works
A merciful death for the “earliest bilaterian,” Vernanimalcula
Bengtson, S., Cunningham, J. A., Yin, C., & Donoghue, P. C. J. (2012) · Evolution & Development · doi:10.1111/j.1525-142x.2012.00562.x · Cited by 40 · see citing works
The origin of the pelagobenthic metazoan life cycle: what's sex got to do with it?
Degnan, B. M., & Degnan, B. M. (2006) · Integrative and Comparative Biology · doi:10.1093/icb/icl028 · Cited by 37 · see citing works
Structure and occurrence of cyphonautes larvae (bryozoa, ectoprocta)
Nielsen, C., & Worsaae, K. (2010) · Journal of Morphology · doi:10.1002/jmor.10856 · Cited by 36 · see citing works
Self-citation
Versatile ciliary behaviour in capture of particles by the bryozoan cyphonautes larva
Strathmann, R. R. (2006) · Acta Zoologica · doi:10.1111/j.1463-6395.2006.00224.x · Cited by 35 · see citing works
Size of the earliest mollusks: Did small helcionellids grow to become large adults?
Mus, M. M., Palacios, T., & Jensen, S. (2008) · Geology · doi:10.1130/g24218a.1 · Cited by 35 · see citing works
Larval ciliary bands and metazoan phylogeny
Nielsen, C. (1979) · Research at the University of Copenhagen (University of Copenhagen) · Cited by 34 · see citing works
Self-citation
Origin of planktotrophy—evidence from early molluscs: a response to Freeman and Lundelius
Nützel, A., Lehnert, O., & Frýda, J. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00166.x · Cited by 33 · see citing works
How to make a protostome
Nielsen, C. (2012) · Invertebrate Systematics · doi:10.1071/is11041 · Cited by 31 · see citing works
Self-citation
Regulatory punctuated equilibrium and convergence in the evolution of developmental pathways in direct‐developing sea urchins
Raff, E. C., Popodi, E. M., Kauffman, J. S., Sly, B. J., Turner, F. R., Morris, V. B., & Raff, R. A. (2003) · Evolution & Development · doi:10.1046/j.1525-142x.2003.03054.x · Cited by 31 · see citing works
First record of a bivalved larval shell in Early Cambrian tommotiids and its phylogenetic significance
Holmer, L. E., Skovsted, C. B., Larsson, C. M., Brock, G. A., & Zhang, Z. (2011) · Palaeontology · doi:10.1111/j.1475-4983.2010.01030.x · Cited by 30 · see citing works
No evidence for planktotrophy in Cambrian molluscs
Runnegar, B. N. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00165.x · Cited by 27 · see citing works
Nervous system development of two crinoid species, the sea lily Metacrinus rotundus and the feather star Oxycomanthus japonicus
Nakano, H., Nakajima, Y., & Amemiya, S. (2009) · Development Genes and Evolution · doi:10.1007/s00427-010-0317-5 · Cited by 27 · see citing works
Phylogeny of Palaeozoic Gastropods Inferred from Their Ontogeny
Frýda, J. (2012) · Springer eBooks · doi:10.1007/978-90-481-3428-1_12 · Cited by 26 · see citing works
Morphogenesis and phenotypic divergence in two developmental morphs of Streblospio benedicti (Annelida, Spionidae)
Gibson, G., MacDonald, K., & Dufton, M. (2010) · Invertebrate Biology · doi:10.1111/j.1744-7410.2010.00213.x · Cited by 25 · see citing works
The internal structure of Early Cambrian fossil embryo Olivooides revealed in the light of Synchrotron X-ray Tomographic Microscopy
Chen, F., & Dong, X. (2008) · 中国科学通报：英文版 · doi:10.1007/s11434-008-0452-9 · Cited by 24 · see citing works
Some aspects of spiralian development
Nielsen, C. (2009) · Acta Zoologica · doi:10.1111/j.1463-6395.2009.00421.x · Cited by 24 · see citing works
Self-citation
Functional and Evolutionary Implications of Opposed Bands, Big Mouths, and Extensive Oral Ciliation in Larval Opheliids and Echiurids (Annelida)
Miner, B. G., Sanford, E., Strathmann, R. R., Pernet, B., & Emlet, R. (1999) · Biological Bulletin · doi:10.2307/1542993 · Cited by 23 · see citing works
THE REPRODUCTIVE BIOLOGY OF EURYTHOE COMPLANATA (PALLAS, 1766), (POLYCHAETA: AMPHINOMIDAE)
Kudenov, J. D. (1974) · UA Campus Repository (The University of Arizona) · Cited by 20 · see citing works
The other gastropod larvae: Larval morphogenesis in a marine neritimorph
Page, L. R., & Ferguson, S. (2012) · Journal of Morphology · doi:10.1002/jmor.20103 · Cited by 19 · see citing works
Analysis of ciliary band formation in the mollusc Ilyanassa obsoleta
Gharbiah, M., Nakamoto, A., & Nagy, L. M. (2013) · Development Genes and Evolution · doi:10.1007/s00427-013-0440-1 · Cited by 17 · see citing works
Origin of planktotrophy—evidence from early molluscs: a response to Nützel et al. (2006)
Freeman, G., & Lundelius, J. W. (2007) · Evolution & Development · doi:10.1111/j.1525-142x.2007.00164.x · Cited by 14 · see citing works
The Development of Form: Causes and Consequences of Developmental Reprogramming Associated with Rapid Body Plan Evolution in the Bilaterian Radiation
Martindale, M. Q., & Lee, P. N. (2013) · Biological Theory · doi:10.1007/s13752-013-0117-z · Cited by 14 · see citing works
Effects of extra‐embryonic provisioning on larval morphology and histogenesis in Boccardia proboscidea (Annelida, Spionidae)
Gibson, G., & Carver, D. (2012) · Journal of Morphology · doi:10.1002/jmor.20071 · Cited by 14 · see citing works
Opposed Ciliary Bands in the Feeding Larvae of Sabellariid Annelids
Pernet, B., & Strathmann, R. R. (2011) · Biological Bulletin · doi:10.1086/bblv220n3p186 · Cited by 14 · see citing works
The rise of bilaterians
Freeman, G. (2009) · Historical Biology · doi:10.1080/08912960903295843 · Cited by 13 · see citing works
Petrographic analysis of new specimens of the putative microfossil Vernanimalcula guizhouena (Doushantuo Formation, South China)
Petryshyn, V. A., Bottjer, D. J., Chen, J., & Gao, F. (2011) · Precambrian Research · doi:10.1016/j.precamres.2011.08.003 · Cited by 13 · see citing works
Filter feeding mechanism in the phoronid Phoronopsis harmeri (Phoronida, Lophophorata)
Temereva, E. N., & Malakhov, V. V. (2010) · Russian Journal of Marine Biology · doi:10.1134/s1063074010020057 · Cited by 13 · see citing works
[On the morphology and embryogenesis of the intestinal tract and transitory organs in Prosobranchia (Mollusca, Gastropoda)].
Fioroni, P. (1966) · PubMed · Cited by 10 · see citing works
Ontogeny of the spiralian brain
Nielsen, C. (2008) · Cambridge University Press eBooks · doi:10.1017/cbo9780511541582.027 · Cited by 9 · see citing works
Self-citation
Coordinated shifts to non-planktotrophic development in spatangoid echinoids during the Late Cretaceous
Cunningham, J. A., & Jeffery, C. H. (2009) · Biology Letters · doi:10.1098/rsbl.2009.0302 · Cited by 8 · see citing works
Larval Forms: Their Nature, Origin, and Affinities
Balfour, F. M. (1880) · Journal of Cell Science · doi:10.1242/jcs.s2-20.80.381 · Cited by 7 · see citing works
Ontogeny, systematics, and phylogenetics: Perspectives of future synthesis and a new model of the evolution of bilateria
Martynov, A. V. (2012) · Biology Bulletin · doi:10.1134/s106235901205010x · Cited by 6 · see citing works
Sutton MD, Briggs DEG, Siveter DaJ, Siveter DeJ & Sigwart JD (2012) A Silurian armoured aplacophoran and implication for molluscan phylogeny. Nature, 490: 94-97(Earth Science Today)
高橋, 正. (2013) · 地球科學 · Cited by 6 · see citing works
The origin and phylogenetic significance of the trochophoran larvae. 2. Evolutionary significance of the larvae of coelomate worms and molluscs
Ivanova-Kazas, O. M. (1985) · Зоологический журнал · Cited by 5 · see citing works
Untitled work
Dewel (2000) · doi:10.1002/(sici)1097-4687(200001)243:1
Ediacarian sponge spicule clusters from southwestern Mongolia and the origins of the Cambrian fauna
(1997) · doi:10.1130/0091-7613(1997)025

Flagged first, then by citations

3 of the 151 references couldn’t be matched to a known paper.

Research works printed but not linked: 7

Raikova EV: Life cycle, cytology, and morphology of Polypodium hydriforme, a coelenterate parasite of the eggs of the acipenseriform fishes. J Parasitol 1994, 80:1-22.
Phil Trans R Soc B 2008, 363(1496):1425-1434.
Ockelmann KW: Developmental types in marine bivalves and their distribution along the Atlantic coast of Europe. In Proceedings of the 1st European Malacological Congress. Edited by Cox LR, Peake JF. London: Choncological Society of Great Britan and Ireland and Malacological Society of London; 1965:25-35.
Jeffery CH: Dawn of echinoid nonplanktotrophy: Coordinated shifts in development indicate environmental instability prior to the K-T boundary. Geology 1997, 25(11):991-994.
Rouse GW: Polychaetes have evolved feeding larvae numerous times. Bull Mar Sci 2000, 67(1):391-409.
Woltereck R: Wurm"kopf", Wurmrumpf und Trochophora. Zool Anz 1904, 28:273-322.
Hadfield MG, Iaea DK: Velum of encapsulated veligers of Petaloconchus (Gastropoda), and the problem of Re-evolution of planktotrophic larvae. Bull Mar Sci 1989, 45(2):377-386.

Sorted by citations

The onset of the ‘Ordovician Plankton Revolution’ in the late Cambrian
Servais, T., Perrier, V., Danelian, T., Klug, C., Martin, R., Munnecke, A., Nowak, H., Nützel, A., Vandenbroucke, T., Williams, M., et al. (2016) · Palaeogeography Palaeoclimatology Palaeoecology · doi:10.1016/j.palaeo.2015.11.003 · Cited by 157 · see citing works
An option space for early neural evolution
Jékely, G., Keijzer, F., & Godfrey-Smith, P. (2015) · Philosophical Transactions of the Royal Society B: Biological Sciences · doi:10.1098/rstb.2015.0181 · Cited by 171 · see citing works
The origin of animal body plans: a view from fossil evidence and the regulatory genome
Erwin, D. H. (2020) · Development · doi:10.1242/dev.182899 · Cited by 133 · see citing works
Myoinhibitory peptide regulates feeding in the marine annelid Platynereis
Williams, E. A., Conzelmann, M., & Jékely, G. (2015) · Frontiers in Zoology · doi:10.1186/s12983-014-0093-6 · Cited by 120 · see citing works
Evolution of Sexual Reproduction in Marine Invertebrates
Ostrovsky, A. N. (2013) · Springer eBooks · doi:10.1007/978-94-007-7146-8 · Cited by 111 · see citing works
The origins of molluscs
Vinther, J. (2015) · Palaeontology · doi:10.1111/pala.12140 · Cited by 102 · see citing works
Larval ecology and morphology in fossil gastropods
Nützel, A. (2014) · Palaeontology · doi:10.1111/pala.12104 · Cited by 88 · see citing works
Phototaxis and the origin of visual eyes
Randel, N., & Jékely, G. (2015) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.2015.0042 · Cited by 82 · see citing works
Evolution of the bilaterian mouth and anus
Nielsen, C., Brunet, T., & Arendt, D. (2018) · Nature Ecology & Evolution · doi:10.1038/s41559-018-0641-0 · Cited by 70 · see citing works
Self-citation
Evolutionary transcriptomics of metazoan biphasic life cycle supports a single intercalation origin of metazoan larvae
Wang, J., Zhang, L., Lian, S., Qin, Z., Zhu, X., Dai, X., Huang, Z., Ke, C., Zhou, Z., Wei, J., et al. (2020) · Nature Ecology & Evolution · doi:10.1038/s41559-020-1138-1 · Cited by 68 · see citing works
The Influence of Bacteria on Animal Metamorphosis
Cavalcanti, G. S., Alker, A. T., Delherbe, N., Malter, K. E., & Shikuma, N. J. (2020) · Annual Review of Microbiology · doi:10.1146/annurev-micro-011320-012753 · Cited by 62 · see citing works
The Origin of Mucosal Immunity: Lessons from the Holobiont Hydra
Schröder, K., & Bosch, T. C. G. (2016) · mBio · doi:10.1128/mbio.01184-16 · Cited by 58 · see citing works
Origin of the trochophora larva
Nielsen, C. (2018) · Royal Society Open Science · doi:10.1098/rsos.180042 · Cited by 56 · see citing works
Self-citation
The Haeckelian shortfall or the tale of the missing semaphoronts
Faria, L. R. R., Pie, M. R., Salles, F. F., & Soares, E. D. G. (2020) · Journal of Zoological Systematics & Evolutionary Research · doi:10.1111/jzs.12435 · Cited by 55 · see citing works
A Screen for Gene Paralogies Delineating Evolutionary Branching Order of Early Metazoa
Erives, A., & Fritzsch, B. (2020) · G3 Genes|Genomes|Genetics · doi:10.1534/g3.119.400951 · Cited by 49 · see citing works
The origin of tetraradial symmetry in cnidarians
Dzik, J., Baliński, A., & Sun, Y. (2017) · Lethaia · doi:10.1111/let.12199 · Cited by 50 · see citing works
The Evolutionary Ecology of Metamorphosis
ten Brink, H., de Roos, A. M., & Dieckmann, U. (2019) · The American Naturalist · doi:10.1086/701779 · Cited by 41 · see citing works
Larval nervous systems: true larval and precocious adult
Nielsen, C. (2015) · Journal of Experimental Biology · doi:10.1242/jeb.109603 · Cited by 39 · see citing works
Self-citation
Lower Cambrian helcionelloid macromolluscs from South Australia
Jacquet, S., & Brock, G. A. (2015) · Gondwana Research · doi:10.1016/j.gr.2015.06.012 · Cited by 39 · see citing works
High expression of new genes in trochophore enlightening the ontogeny and evolution of trochozoans
Xu, F., Domazet‐Lošo, T., Fan, D., Dunwell, T. L., Li, L., Fang, X., & Zhang, G. (2016) · Scientific Reports · doi:10.1038/srep34664 · Cited by 37 · see citing works
Cephalopod ontogeny and life cycle patterns
Vidal, É. A. G., & Shea, E. K. (2023) · Frontiers in Marine Science · doi:10.3389/fmars.2023.1162735 · Cited by 36 · see citing works
Metamorphic remodeling of morphology and the body cavity in Phoronopsis harmeri (Lophotrochozoa, Phoronida): the evolution of the phoronid body plan and life cycle
Temereva, E. N., & Malakhov, V. V. (2015) · BMC Evolutionary Biology · doi:10.1186/s12862-015-0504-0 · Cited by 29 · see citing works
Ctenophores are direct developers that reproduce continuously beginning very early after hatching
Edgar, A., Ponciano, J. M., & Martindale, M. Q. (2022) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2122052119 · Cited by 28 · see citing works
Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensis
Gilbert, E., Teeling, C., Lebedeva, T. S., Pedersen, S., Chrismas, N. A. M., Genikhovich, G., & Modepalli, V. (2022) · Development · doi:10.1242/dev.200833 · Cited by 26 · see citing works
Review of data for a morphological look on Xenacoelomorpha (Bilateria incertae sedis)
Haszprunar, G. (2015) · Organisms Diversity & Evolution · doi:10.1007/s13127-015-0249-z · Cited by 27 · see citing works
The early history of the metazoa—a paleontologist’s viewpoint
Zhuravlev, A. Y. (2015) · Biology Bulletin Reviews · doi:10.1134/s2079086415050084 · Cited by 26 · see citing works
Development and organization of the larval nervous system in Phoronopsis harmeri: new insights into phoronid phylogeny
Temereva, E. N., & Tsitrin, E. B. (2014) · Frontiers in Zoology · doi:10.1186/1742-9994-11-3 · Cited by 25 · see citing works
Organization and metamorphic remodeling of the nervous system in juveniles of Phoronopsis harmeri (Phoronida): insights into evolution of the bilaterian nervous system
Temereva, E. N., & Tsitrin, E. B. (2014) · Frontiers in Zoology · doi:10.1186/1742-9994-11-35 · Cited by 23 · see citing works
Evolution of deuterostomy - and origin of the chordates
Nielsen, C. (2015) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12229 · Cited by 20 · see citing works
Self-citation
Larval anatomy of the pterobranch Cephalodiscus gracilis supports secondarily derived sessility concordant with molecular phylogenies
Stach, T. (2013) · Die Naturwissenschaften · doi:10.1007/s00114-013-1117-3 · Cited by 17 · see citing works
Evolution of Metazoan Life Cycles and the Origin of Pelagic Larvae
Malakhov, V. V., Bogomolova, E., Kuzmina, T. V., & Temereva, E. N. (2019) · Russian Journal of Developmental Biology · doi:10.1134/s1062360419060043 · Cited by 17 · see citing works
Does the frontal sensory organ in adults of the hoplonemertean Quasitetrastemma stimpsoni originate from the larval apical organ?
Magarlamov, T. Y., Dyachuk, V. A., & Chеrnyshev, A. V. (2020) · Frontiers in Zoology · doi:10.1186/s12983-019-0347-4 · Cited by 14 · see citing works
Development of the Nervous System of Carinina ochracea (Palaeonemer-tea, Nemertea)
von Döhren, J. (2016) · PLoS ONE · doi:10.1371/journal.pone.0165649 · Cited by 14 · see citing works
Hydrodynamics in early animal evolution
Nielsen, C. (2022) · Biological reviews/Biological reviews of the Cambridge Philosophical Society · doi:10.1111/brv.12909 · Cited by 14 · see citing works
Self-citation
Nemertea
von Döhren, J. (2015) · Springer eBooks · doi:10.1007/978-3-7091-1871-9_8 · Cited by 14 · see citing works
Gene Regulatory Network that Shaped the Evolution of Larval Apical Organ in Cnidaria
Gilbert, E., Craggs, J., & Modepalli, V. (2023) · Molecular Biology and Evolution · doi:10.1093/molbev/msad285 · Cited by 13 · see citing works
The Fortunian (lowermost Cambrian) Qinscyphus necopinus (Cnidaria, Scyphozoa, Coronatae) underwent direct development
Shao, T., Liu, Y., Duan, B., Zhang, H., Hu, Z., Qi, W., Zhang, Y., & Qin, J. (2018) · Neues Jahrbuch für Geologie und Paläontologie - Abhandlungen · doi:10.1127/njgpa/2018/0755 · Cited by 12 · see citing works
Macroevolution of Animal Body Plans: Is There Science after the Tree?
Jenner, R. A. (2014) · BioScience · doi:10.1093/biosci/biu099 · Cited by 12 · see citing works
Ground plan of the larval nervous system in phoronids: Evidence from larvae of viviparous phoronid
Temereva, E. N. (2017) · Evolution & Development · doi:10.1111/ede.12231 · Cited by 12 · see citing works
Perspective—Nervous System Development in Bilaterian Larvae: Testing the Concept of ‘Primary Larvae’
Richter, S., Stach, T., & Wanninger, A. (2015) · Oxford University Press eBooks · doi:10.1093/acprof:oso/9780199682201.003.0025 · Cited by 11 · see citing works
Non-directional Photoreceptors in the Pluteus of Strongylocentrotus purpuratus
Valero‐Gracia, A., Petrone, L., Oliveri, P., Nilsson, D., & Arnone, M. I. (2016) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2016.00127 · Cited by 11 · see citing works
The oldest known larva and its implications for the plesiomorphy of metazoan development
Zhang, H., & Dong, X. (2015) · 中国科学通报：英文版 · doi:10.1007/s11434-015-0886-9 · Cited by 10 · see citing works
Vertebrate origins are informed by larval lampreys (ammocoetes): a response to Miyashitaet al., 2021
Mallatt, J. M. (2022) · Zoological Journal of the Linnean Society · doi:10.1093/zoolinnean/zlac086 · Cited by 9 · see citing works
Renewed perspectives on the sedentary-pelagic last common bilaterian ancestor
Martynov, A. V., & Korshunova, T. (2022) · Bijdragen tot de Dierkunde · doi:10.1163/18759866-bja10034 · Cited by 7 · see citing works
Cnidarian Larvae: True Planulae, Other-Than-Planulae, and Planulae That Don’t Look Like Planulae
Kraus, Y. A. (2023) · Russian Journal of Developmental Biology · doi:10.1134/s1062360423070044 · Cited by 7 · see citing works
Duplicated FoxA genes in the leech Helobdella: Insights into the evolution of direct development in clitellate annelids
Kuo, D., & Hsiao, Y. (2018) · Developmental Dynamics · doi:10.1002/dvdy.24621 · Cited by 7 · see citing works
Evolutionary Development of Marine Larvae
(2017) · Oxford University Press eBooks · doi:10.1093/oso/9780198786962.003.0002 · Cited by 7 · see citing works
Modelling the effects of short and random proto-neural elongations
de Wiljes, O. O., van Elburg, R. A. J., & Keijzer, F. (2017) · Journal of The Royal Society Interface · doi:10.1098/rsif.2017.0399 · Cited by 6 · see citing works
Origin and Diversity of Marine Larvae
Nielsen, C. (2017) · doi:10.1093/oso/9780198786962.003.0001 · Cited by 6 · see citing works
Self-citation
The 3D architecture of the ctenophore aboral organ and the evolution of complex integrative centers in animals
Ferraioli, A., Digel, L., Sturm, D., Colgren, J. J., Goff, C. L., Jan, A., Soto-Angel, J. J., Naumann, B. T., Kittelmann, M., & Burkhardt, P. (2026) · Science Advances · doi:10.1126/sciadv.aea8399 · Cited by 7 · see citing works
Neurons with larval synaptic targets pioneer the later nervous system in the annelid Malacoceros fuliginosus
Seybold, A., Kumar, S., Tumu, S. C., & Hausen, H. (2025) · Frontiers in Neuroscience · doi:10.3389/fnins.2024.1439897 · Cited by 4 · see citing works
Expression of GATA and POU transcription factors during the development of the planktotrophic trochophore of the polychaete serpulid Hydroides elegans
Wong, K. S., & Arenas‐Mena, C. (2016) · Evolution & Development · doi:10.1111/ede.12196 · Cited by 5 · see citing works
Anatomy and the type concept in biology show that ontologies must be adapted to the diagnostic needs of research
Vogt, L., Mikó, I., & Bartolomaeus, T. (2022) · Journal of Biomedical Semantics · doi:10.1186/s13326-022-00268-2 · Cited by 5 · see citing works
A LATE ORDOVICIAN PLANKTIC ASSEMBLAGE WITH EXCEPTIONALLY PRESERVED SOFT-BODIED PROBLEMATICA FROM THE MARTINSBURG FORMATION, PENNSYLVANIA
Meyer, M., Ganis, G. R., Wittmer, J., Zalasiewicz, J., & Baets, K. D. (2018) · Palaios · doi:10.2110/palo.2017.036 · Cited by 5 · see citing works
Contrasting the development of larval and adult body plans during the evolution of biphasic lifecycles in sea urchins
McDonald, B. D., Massri, A. J., Berrío, A., Byrne, M., McClay, D. R., & Wray, G. A. (2024) · Development · doi:10.1242/dev.203015 · Cited by 5 · see citing works
Multiple Losses of Planktotrophic Development in the Cosmopolitan Bivalve GenusLasaea*
Li, J., & Foighil, D. Ó. (2015) · American Malacological Bulletin · doi:10.4003/006.033.0210 · Cited by 4 · see citing works
[Early history of the Metazoa--a palaeontologist's viewpoint].
Zhuravlev, A. Y. (2014) · PubMed · Cited by 4 · see citing works
Molecular and cellular architecture of the larval sensory organ in the cnidarian Nematostella vectensisPreprint
Teeling, C., Gilbert, E., Pedersen, S., Chrismas, N. A. M., & Modepalli, V. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.05.10.443235 · Cited by 4 · see citing works
The larva problem: homology, evolvability, terminology
Minelli, A. (2025) · Invertzool · doi:10.15298/invertzool.22.1.07 · Cited by 3 · see citing works
Diversity in the Development of the Neuromuscular System of Nemertean Larvae (Nemertea, Spiralia)
von Döhren, J. (2021) · Frontiers in Ecology and Evolution · doi:10.3389/fevo.2021.654846 · Cited by 3 · see citing works
Pelagic Shrimps (Crustacea, Decapoda, Dendrobranchiata, and Caridea) in the Southeast Pacific
Guzmán, G., & Olguin, C. N. (2020) · Springer eBooks · doi:10.1007/978-3-030-58410-8_12 · Cited by 2 · see citing works
Unraveling the microRNA regulatory network underlying the planktonic-to-benthic transition in the Pacific oyster
Xie, Y., Yang, M., Sun, H., & Xu, F. (2025) · Aquaculture Reports · doi:10.1016/j.aqrep.2025.103304 · Cited by 1 · see citing works
Evolution of Reproductive Patterns in Cheilostomata
Ostrovsky, A. N. (2013) · Springer eBooks · doi:10.1007/978-94-007-7146-8_3 · Cited by 1 · see citing works
Eric Davidson and deep time
Erwin, D. H. (2017) · History & Philosophy of the Life Sciences · doi:10.1007/s40656-017-0156-z · Cited by 1 · see citing works
Gene regulatory network that shaped the evolution of larval sensory organ in CnidariaPreprint
Gilbert, E., Craggs, J., & Modepalli, V. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.09.14.557727 · Cited by 1 · see citing works
Genetic Mechanisms Regulating the Spatiotemporal Modulation of Proliferation Rate and Mode in Neural Progenitors and Daughter Cells during Embryonic CNS Development
Salmani, B. Y. (2018) · doi:10.3384/diss.diva-147736 · Cited by 1 · see citing works
From skin to brain: modelling a whole-body coordination scenario of nervous system origin
de Wiljes, O. (2020) · doi:10.33612/diss.123420732
Additional file 1 of Anatomy and the type concept in biology show that ontologies must be adapted to the diagnostic needs of research
Vogt, L., Mikó, I., & Bartolomaeus, T. (2022) · Figshare · doi:10.6084/m9.figshare.20167827
Nervous system evolution : insights from the sea urchin
Formery, L. (2019) · theses.fr (ABES) · doi:10.70675/146c0b8aza71az47ecza2c7zc12baf0f5794

Authors: Nielsen, C.
Affiliations: University of Copenhagen (DK)
Corresponding author: Nielsen, Claus
ORCID: Nielsen, Claus
Venue: BMC Evolutionary Biology
Publisher: Springer Science and Business Media LLC
Published: 2013
Volume: 13
Issue: 1
Pages: 171
ISSN: 1471-2148 (ISSN-L)
DOI: 10.1186/1471-2148-13-171
OpenAlex: W2122337391
Cited by: 69
References: 151
Citations by year: 2026: 1 · 2025: 3 · 2024: 1 · 2023: 4 · 2022: 7 · 2021: 2 · 2020: 7 · 2019: 4 · 2018: 6 · 2017: 6 · 2016: 5 · 2015: 14 · 2014: 6 · 2013: 3
FWCI: 1.08
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
Locations: BMC Evolutionary Biology (publishedVersion, cc-by)
Europe PMC (PubMed Central) (publishedVersion, cc-by)
Research at the University of Copenhagen (University of Copenhagen) (submittedVersion, cc-by)
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: planktotrophic larvae, indirect development, direct development, trochophore, larval evolution, ciliates

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review

Life cycle evolution: was the eumetazoan ancestor a holopelagic, planktotrophic gastraea?

Abstract

Integrity signals

Claims the paper makes

Claims other papers make about this one

Self-check

Cites

Cited by

Related

Record

About these checks