Development of a feeding trochophore in the polychaete Hydroides elegans

Abstract

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...

Expression of GATA and POU transcription factors during the development of the planktotrophic trochophore of the polychaete serpulid Hydroides elegans

“…The independent evolution of epibolic gastrulation in Platynereis and Capitella would be consistent with the observed variability of GATA4/5/6 expression. Similarly consistent with this scenario is the expression of Otx and Brachyury reported in Capitella and Hydroides but not in Platynereis , as previously discussed (Arenas‐Mena ; Arenas‐Mena and Li ). One would expect substantial differences in regulatory gene expression between H. elegans embryos and the utterly different epibolic embryos of Capitella (Arenas‐Mena and Li ).…”

“…Similarly consistent with this scenario is the expression of Otx and Brachyury reported in Capitella and Hydroides but not in Platynereis , as previously discussed (Arenas‐Mena ; Arenas‐Mena and Li ). One would expect substantial differences in regulatory gene expression between H. elegans embryos and the utterly different epibolic embryos of Capitella (Arenas‐Mena and Li ). The relatively conserved regulatory gene expression may be due to a dual function for GATA4/5/6 in endoderm germ layer specification and morphogenesis during gastrulation.…”

“…The results are discussed in a broader regulatory and evolutionary context that explores how lecithotrophic and planktotrophic development could have evolved. The present study supplements previous regulatory gene expression studies in H. elegans embryos, currently the best characterized among planktotrophic polychaetes (Arenas‐Mena and Li ). The combined evidence favors scenarios proposing that lecithotrophic development evolved from planktotrophic development in polychaetes.…”

Origin of the trochophora larva

“…This development soon became established already in the larva (through the process called adultation [ 19 ]). This type of blastopore closure, called amphistomy, is observed directly in the annelid Hydroides , where the posterior opening finally closes, but a new anus develops in the same region [ 20 ] and with modifications in many spiralians [ 4 , 5 ]. In the larva, the anterior part of the archaeotroch was retained around the mouth as the prototroch + metatroch (on the anterior and posterior sides of the adoral ciliary zone, respectively), functioning as a downstream-collecting system (see below), and the posterior part remaining around the anus as the telotroch.…”

“…The few studies on gene expression, e.g. on Patella [ 23 ] and Hydroides [ 20 , 24 , 25 ], are too scattered to contribute to the discussion.…”