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

  • ️Tue Jan 01 2013

Review

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

Claus Nielsen. BMC Evol Biol. 2013.

Abstract

Background: 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.

Results: 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.

Conclusions: 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.

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Figures

Figure 1
Figure 1

Theories about the origin of the indirect life cycles. The upper row shows the ontogenies of the ancestral organisms, and the lower row shows the ontogenies of the indirect, pelago-benthic organisms with the added life cycle stages indicated in red. The cnidarians have sessile adults instead of creeping adults.

Figure 2
Figure 2

Types of invertebrate life cycles. The definition of direct versus indirect development is not precise (see the text), and there are a few “facultative feeding” larvae, which feed in the plankton if food is available, but which are capable to go through metamorphosis without feeding.

Figure 3
Figure 3

Taxonomic overview of higher animal groups mentioned in the text.

Figure 4
Figure 4

Larval and adults shells of Lower Cambrian helcionellids. A, Apex of a centimeter-large adult showing the larval shell. B, A “small shelly fossil” showing the exact same morphology as the apex of the adult helcionellid. C, Detail of the sculpture of the adult shell. D, A whole fossil helcionellid. Modified from [48].

Figure 5
Figure 5

Developmental types of spatangoid echinoids. Left photos: Tests of a male and a female of the echinoid Brachysternaster chesheri. The brood pouches (bp) in the female and the difference in gonopore size in the two sexes are seen (gp; the male test is cleaned, whereas the female still has some of the organic material partially covering the gonopores; the black dot at the left side is inserted to indicate the size of the clean gonopore). Photos from

http://www.nhm.ac.uk/research-curation/research/projects/echinoid-directory/taxa/taxon.jsp?id=429

. Right diagram: Evolution of developmental types of Cretaceous spatangoid echinoids. Only the period from the Aptian to the Maastrictian is shown, but seven successive outgroups from the Valanginian to the Aptian all had pluteus larvae. Ap, Aptian; Al, Albian; Ce, Cenomanian; T, Turonian, C, Coniacian; S, Santonian; Ca, Campanian; M, Maastrichtian. Modified from [60].

Figure 6
Figure 6

Downstream-collecting ciliary complexes of trochophora larvae, SEM. A, The annelid Serpula oregonensis.B, The bivalve Barnea candida. C, The entoproct Loxosomella elegans. From [22].

Figure 7
Figure 7

The catch-up principle. Diagram of a cross-section of the velar edge of the gastropod Crepidula fornicata. The thick, compound cilia of prototroch and metatroch beat towards the band of single cilia of the adoral ciliary zone (food groove). The sequence of stages of the prototroch cilia are indicated by the small numbers. The prototroch cilia cut through the water, catch up with a food particle which is then pushed on to the adoral ciliary zone. This is apparently aided by the beat of the metatroch cilia. These cilia of the adoral zone carry the particles towards the mouth. From [66].

Figure 8
Figure 8

The occurrence of “direct” development in the gastropod genus Conus. Redrawn from [90]. The original paper distinguishes between species with planktonic larvae and non-planktonic development. Dr Alan Kohn (University of Washington) has informed me that all the planktonic larvae are planktotrophic.

Figure 9
Figure 9

“Direct” development in the gastropod Cassidaria sp. A, The fully differentiated veliger larva inside the cocoon collects yolk particles with the ciliary bands of the large velum and transports them to the mouth. B, The newly hatched juvenile has lost all traces of the velum. Modified from [96].

Figure 10
Figure 10

Occurrence of planktotrophic larvae in ambulacrarian clades. The small icons indicate the occurrence of the planktotrophic larval type in some species within the clade. Modified from [115].

Figure 11
Figure 11

Single egg capsule of the polychaete Pygospio elegans. The capsule contains one “intracapsular trochophore” ready for hatching as a pelagic larva and three embryos full of yolk and almost ready for hatching as small juveniles. From [142] with permission from Taylor & Francis Ltd.

http://www.tandfonline.com

.

Figure 12
Figure 12

The trochaea theory. The upper part of the left side shows the ancestral trochaea. The left side shows the life cycle of a trochaea which has added a creeping, benthic stage to its life cycle and established a functional tube-shaped gut by lateral compression of the lateral blastopore lips. The right side shows the life cycle of a protostomian ancestor which has developed a permanent tube-shaped gut by fusion of the lateral blastopore lips and differentiated the archaeotroch into the anterior proto- and metatroch around the mouth and the telotroch around the anus; prototroch and metatroch plus the adoral ciliary zone forms a downstream-collecting ciliary system. From [75].

Figure 13
Figure 13

Successive stages of the evolutionary transformation of the atrochal larva into a trochophore. A, A completely ciliated larva. B, Larva with an apical tuft and an equatorial band of cilia. C, Larva with mouth and anus. D, Larva with the ciliation restricted to a prototroch and a perioral ciliation. E, Larva with prototroch, adoral ciliary zone and metatroch. Modified from [154].

Figure 14
Figure 14

Occurrence of life cycle types in the Eumetazoa (Neuralia). Clades with planktotrophic (blue) and lecithotrophic/direct development (red) in major eumetazoan (neuralian) clades; blue/red clades indicate lineages of both types. The characteristic larval types, gastrula, trochophora and dipleurula are indicated. The ancestors of Eumetazoa (gastraea) and Protostomia (trochaea) are indicated, but the ancestors of Bilateria and Deuterostomia have not been envisaged.

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