Intermediate modes of larval development: bridging the gap between planktotrophy and lecithotrophy

Allen, Jonathan D.; Pernet, Bruno

doi:10.1111/j.1525-142x.2007.00202.x

Cited by 103 publications

(68 citation statements)

References 86 publications

(138 reference statements)

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“…In other words, we do not know if the last common ancestor of bilaterians was a direct or indirect developer. Although the dichotomy facilitates discourse, it does so at the expense of accuracy; in reality there are intermediate forms between absolute planktotrophic and lecithotrophic larvae (Allen and Pernet, 2007). Evolutionary scenarios have been proposed to explain the origin of indirect development, and compiled references can be found elsewhere (Page, 2009;Arenas-Mena, 2010;Sly et al, 2003).…”

Section: Broader Evolutionary Relevance Of Polychaete Feeding Trochopmentioning

confidence: 99%

Development of a feeding trochophore in the polychaete Hydroides elegans

Arenas-Mena¹,

Li²

2014

Int. J. Dev. Biol.

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Hydroides elegans is an indirectly developing polychaete with equal spiral cleavage, gastrulation by invagination, and a feeding trochophore. Expression of several transcription factors and differentiation genes has been characterized. Comparative analysis reveals evolutionarily conserved roles. For example, the synexpression of transcription factors FoxA and Brachyury suggests homology of primary and secondary gut openings in protostomes and deuterostomes, and the expression of Sall suggests similar regulatory controls in the posterior growth zone of bilaterians. Differences in gene expression suggest regulatory differences control gastrulation by invagination in polychaetes with a feeding trochophore and gastrulation by epiboly in polychaetes without a feeding trochophore. Association of histone variant H2A.Z with transcriptional potency and its expression suggest a developmental role during both embryogenesis and the larva-to-adult transformation. Methods are being developed for experimental exploration of the gene regulatory networks involved in trochophore development in Hydroides. It is unknown if polychaete feeding trochophores evolved from a larval stage already present in the life cycle of the last common ancestor of protostomes and deuterostomes. Previous evolutionary scenarios about larval origins overemphasize the discontinuity between larval and adult development and require the early evolution of undifferentiated and transcriptionally potent "set aside" cells. Indirect development may proceed by developmental remodeling of differentiated cells and could have evolved after gradual transformation of juveniles into larvae; undifferentiated and transcriptionally potent cells would have evolved secondarily. Comprehensive characterization of gene regulatory networks for feeding trochophore development may help resolve these major evolutionary questions. KEY WORDS: bilaterian, posterior growth, serpulid, annelidHydroides elegans, a polychaete with a feeding trochophore Characterization of polychaetes with a feeding trochophore, such as Hydroides elegans ( Fig. 1 and Table 1), is relevant to understand the developmental evolution of complex life cycles in spiralians. Embryonic development in polychaetes conforms to the presence or absence of a feeding trochophore (Fig. 2). In the genus Hydroides (Eupomatus), embryogenesis ends in a feeding trochophore endowed with an equatorial ciliary band, a protonephridium, various sensory organs, and a functional gut formed after gastrulation by invagination (Hatschek, 1885;Shearer, 1911). Blastomeres 4d and 2d22 are inconspicuous and fated to contribute to the mesodermal and ectodermal portions of the segmented body that will have primarily a reproductive role; the Int. J. Dev. Biol. 58: 575-583 (2014) growth and proliferation of 4d and 2d22 are feeding-dependent. In contrast, during embryogenesis in polychaetes without feeding larvae, blastomeres 4d and 2d are relatively large and immediately engage in the formation of segments (Fig. 2). In addition to la...

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Section: Broader Evolutionary Relevance Of Polychaete Feeding Trochopmentioning

confidence: 99%

Development of a feeding trochophore in the polychaete Hydroides elegans

Arenas-Mena¹,

Li²

2014

Int. J. Dev. Biol.

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“…Most of the published lineage tracing data comes from species that gastrulate by epiboly, likely because their eggs are large, develop slowly, and are easy to inject. It would be useful to generate more lineage data, and descriptions of gastrulation, from indirect developing species, or species that are facultative planktotrophs (Allen and Pernet, 2007). It will also be necessary to study gastrulation mechanisms in the lesser-known spiralian groups, and non-spiralian lophotrochozoans.…”

Section: Future Directionsmentioning

confidence: 99%

Ins and outs of Spiralian gastrulation

Lyons¹,

Henry²

2014

Int. J. Dev. Biol.

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Gastrulation is a critical stage of metazoan development during which endodermal and mesodermal tissues are internalized, and morphogenesis transforms the early embryo into each animal's unique body-plan. While gastrulation has been studied extensively in classic model systems such as flies, worms, and vertebrates, less is known about gastrulation at a mechanistic level in other taxa. Surprisingly, one particularly neglected group constitutes a major branch of animals: the Spiralia. A unique feature of spiralian development is that taxa with diverse adult body-plans, such as annelids, molluscs, nemerteans and platyhelminths all share a highly stereotyped suite of characters during embryogenesis called spiral cleavage. The spiral cleavage program makes it possible to compare distantly related embryos using not only morphological features, and gene expression patterns, but also homologous cell lineages. Having all three criteria available for comparison is especially critical for understanding the evolution of a complex process like gastrulation. Thus studying gastrulation in spiralians is likely to lead to novel insights about the evolution of body-plans, and the evolution of morphogenesis itself. Here we review relevant literature about gastrulation in spiralians and frame questions for future studies. We describe the internalization of the endoderm, endomesoderm and ectomesoderm; where known, we review data on the cellular and molecular control of those processes. We also discuss several morphogenetic events that are tied to gastrulation including: axial elongation, origins of the mouth and anus, and the fate of the blastopore. Since spiral cleavage is ancestral for a major branch of bilaterians, understanding gastrulation in spiralians will contribute more broadly to ongoing debates about animal body-plan divergence, such as: the origin of the through-gut, the emergence of indirect versus direct development, and the evolution of gene-regulatory networks that specify endomesoderm. We emphasize the fact that spiralian gastrulation provides the unique opportunity to connect well-defined embryonic cell lineages to variation in cell fate and cell behavior, making it an exceptional case study for evo-devo. KEY WORDS: spiralia, endomesoderm, ectomesoderm, blastopore, axial elongation, epiboly, invagination Gastrulation is a critical embryonic event during which presumptive endodermal and mesodermal cells are internalized (Stern, 2004). Gastrulation is closely tied to the development of key axial properties, and to the patterning of certain organ systems, such as the digestive tract; the openings of the mouth and/or anus often arise at or close to the site of gastrulation, called the blastopore (see Technau and Scholz, 2003;Hejnol and Martindale, 2009). Gastrulation also holds a pivotal role in evolutionary theories about the emergence and divergence of bilaterian body-plans (Arendt and Nübler-Jung,1997;Nielsen, 2001;Martindale and Hejnol, 2009 As evo-devo questions go, tracing the evolutionary history o...

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“…They arise from eggs that contain enough energy to support them through metamorphosis in the absence of food, but they also retain the ability to feed. As a mode of larval development, facultative feeding is quite rare; confirmed cases are limited to eight species in three phyla (Allen and Pernet, 2007). Of more than 250 echinoid (sea urchin, heart urchin, and sand dollar) species with known mode of development, two-thirds have obligately feeding larvae and the other third have nonfeeding larvae.…”

Section: Introductionmentioning

confidence: 99%

Egg Energetics, Fertilization Kinetics, and Population Structure in Echinoids With Facultatively Feeding Larvae

Zigler

Lessios

Raff

2008

The Biological Bulletin

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Abstract. Larvae of marine invertebrates either arise from small eggs and feed during their development or arise from large eggs that proceed to metamorphosis sustained only from maternal provisioning. Only a few species are known to posses facultatively feeding larvae. Of about 250 echinoid species with known mode of development, only two, Brisaster latifrons and Clypeaster rosaceus, are known to develop through facultatively planktotrophic larvae. To obtain more information on this form of development and its consequences, we determined egg size and egg energetic and protein content of these two species. We found that eggs of B. latifrons resemble those of species with nonfeeding larvae in these characteristics more than those of C. rosaceus. We also compared DNA sequences of the cytochrome oxidase (COI) gene from the Caribbean C. rosaceus to those of the sympatric planktotrophic developer C. subdepressus and also to those of the eastern Pacific species C. europacificus to estimate the degree of divergence between species with different developmental modes. Comparison of COI sequences of C. rosaceus from Panama and Florida revealed that there is no geographic differentiation in this species. Cross-fertilization experiments between C. rosaceus and C. subdepressus indicated that bidirectional gametic incompatibility has evolved between the two species.

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Intermediate modes of larval development: bridging the gap between planktotrophy and lecithotrophy

Cited by 103 publications

References 86 publications

Development of a feeding trochophore in the polychaete Hydroides elegans

Development of a feeding trochophore in the polychaete Hydroides elegans

Ins and outs of Spiralian gastrulation

Egg Energetics, Fertilization Kinetics, and Population Structure in Echinoids With Facultatively Feeding Larvae

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