From incipient to substantial: evolution of placentotrophy in a phylum of aquatic colonial invertebrates.

Andrew N Ostrovsky

doi:10.1111/evo.12039

Abstract

Matrotrophy has long been known in invertebrates, but it is still poorly understood and has never been reviewed. A striking example of matrotrophy (namely, placentotrophy) is provided by the Bryozoa, a medium-sized phylum of the aquatic colonial filter feeders. Here I report on an extensive anatomical study of placental analogues in 21 species of the bryozoan order Cheilostomata, offering the first review on matrotrophy among aquatic invertebrates. The first anatomical description of incipient placentotrophy in invertebrates is presented together with the evidence for multiple independent origins of placental analogues in this order. The combinations of contrasting oocytic types (macrolecithal or microlecithal) and various degrees of placental development and embryonic enlargement during incubation, found in different bryozoan species, are suggestive of a transitional series from the incipient to the substantial placentotrophy accompanied by an inverse change in oogenesis, a situation reminiscent of some vertebrates. It seems that matrotrophy could trigger the evolution of sexual zooidal polymorphism in some clades. The results of this study show that this phylum, with its wide variety of reproductive patterns, incubation devices, and types of the simple placenta-like systems, offers a promising model for studying parallel evolution of placentotrophy in particular, and matrotrophy in general.

Highlights

Key evolutionary novelties are often considered as a driving force of progressive evolution
The results of this study show that this phylum, with its wide variety of reproductive patterns, incubation devices, and types of the simple placenta-like systems, offers a promising model for studying parallel evolution of placentotrophy in particular, and matrotrophy in general
In addition to contributing new data on oogenesis and the variety of placental analogues, the results of this study suggest the presence in cheilostome bryozoans of the so-called incipient placentotrophy

Summary

Introduction

Key evolutionary novelties are often considered as a driving force of progressive evolution. Only salps, nonmonotreme mammals, and scorpions possess placentas or placenta-like organs Another striking example is the phylum Bryozoa, a medium-sized group of aquatic colonial filter-feeders, which is unique among invertebrates in possessing matrotrophy in all its major classes: all the living representatives of the classes Stenolaemata and Phylactolaemata and many species from the class Gymnolaemata are known to be matrotrophic (for review and history of the research see Reed 1991; Ostrovsky et al 2009a, see Supplementary Materials 1). It seems that most, if not all, bryozoans with EEN are placentotrophic. The understanding of reproductive patterns employing the simplest placenta-like systems in invertebrates may be important for reconstructing the evolution of matrotrophy in general

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Discussion

Conclusion