Larval Planktotrophy—A Primitive Trait in the Bilateria?

Abstract

The concept of Gösta Jägersten of a primary biphasic metazoan life‐cycle, consisting of a planktotrophic larva and a benthic adult, forms the basis for several theories on metazoan phylogeny. In this paper the assumed planktotrophic life‐style of the larva is critically analyzed and reconsidered. It is shown, in particular for the Mollusca, that a biphasic life‐cycle with a lecithotrophic larva is probably the plesiomorphic condition. Character distribution and structural data suggest a parallel evolution of the downstream collecting system used in planktotrophic larvae or filter‐feeding adults of gastropods, bivalves and other spiralian or aschelminth taxa. In the basic metazoans (Parazoa, Placozoa, coelenterates) direct or lecithotrophic development dominates by far. For the acoelomate (Platyhelminthes, Gnathostomulida) and pseudocoelomate taxa direct development is probably the plesiomorphic condition. The structural similarities of the upstream collecting system in tentaculate and deuterostome phyla may also be explained by parallel events of heterochrony out of an ancestor with adult filter‐feeding. The main conclusion of this survey is that larval planktotrophy is likely to be secondary and not a plesiomorphic condition among the Bilateria. Accordingly, theories which are based on the assumed plesiomorphy of larval planktotrophy of the Bilateria, need careful reevaluation.

Indirect development, transdifferentiation and the macroregulatory evolution of metazoans

“…For example, the evolution of a complex pattern of transient H2A.Z silencing and reactivation would have to evolve in coordination with developmental and differentiation programmes for the eventual construction of an integrated larval stage with no actual precursor. This major coevolutionary constraint may explain why we find only the recent evolution of larval variants within the context of a biphasic life cycle (Haszprunar et al 1995;McHugh & Rouse 1998;Reitzel et al 2006), but no cases of recent evolution of indirect development from a life cycle that completely lacks a transiently differentiated stage.…”

Molecular paleoecology: using gene regulatory analysis to address the origins of complex life cycles in the late Precambrian

“…The only possible exception, according to Rigby and Milsom (2000), might be the ciliated larval stages of marine invertebrates because if trochophores and dipleurula larvae are descended from a holopelagic ancestor, as hypothesized by Ja¨gersten (1972) and Nielsen (2001), then the initial evolution of animals would have taken place in the pelagos and not on the benthos. This idea though has not received much acceptanceFmost authors have concluded that larval stages are products of convergent evolution intercalated into a benthic direct-developing strategy (e.g., Olive 1985;Chaffee and Lindberg 1986;Buckland-Nicks and Scheltema 1995;Haszprunar et al 1995;Conway Morris 1998;Valentine et al 1999;Budd and Jensen 2000;Hadfield 2000;Valentine and Collins 2000;Bagun˜a`et al 2001;Hadfield et al 2001;Jondelius et al 2002;Sly et al 2003;. Indeed, ecological considerations clearly show that feeding zooplankton could not have evolved much before the Tommotian (Butterfield 1997), and Nu¨tzel et al (2006 have recently shown that within gastropod molluscs planktotrophy did not evolve until the Cambrian-Ordovician transition around 490 Ma, as predicted by Signor and Vermeij (1994) and Peterson (2005;see Fig.…”

Comparative study of the apical ganglion in planktotrophic caenogastropod larvae: Ultrastructure and immunoreactivity to serotonin

“…Phylogenetic hypotheses suggest that a complex life cycle with a long-term, planktotrophic larvae is a primitive trait for both the Caenogastropoda and Heterobranchia, although feeding larvae may not have been ancestral for the gastropods as a whole (Haszprunar, 1988;Haszprunar et al, 1995;Ponder and Lindberg, 1997). We speculate that design features of the apical ganglion that are shared by planktotrophic larvae of both caenogastropods and heterobranchs arose in a common ancestor that also had a long-term larva and have been preserved in descendant species that have retained the complex life cycle.…”