Homology of the lophophore and its evolution within lophophorates

Abstract

The lophophore is a tentaculated organ -a specificity of Lophophorata. Since molecular phylogeny has yielded contradictory data on the monophyly of lophophorates, results of comparative morphology are used here to shed light on the question about the homology of the lophophore in different groups of lophophorates. We compare the morphology of the lophophore and the organization of its coelomic, nervous, and muscular systems in three different phyla of lophophorates: phoronids, bryozoans, and brachiopods. The morphology of the lophophore and the structure of all lophophoral organ systems are examined in respect to the standard criteria of homology. The comparative analysis supports the homology of the lophophore and suggests the monophyly of the lophophorates. We present a hypothetical scenario of lophophore evolution based on our analyses. Accordingly, the ancestral lophophore of lophophorates had a horseshoe-shaped brachial axis and was innervated by supraenteric and subenteric nerve centers, which were connected by circumenteric connectives and a circumoral nerve. This ancestral lophophore then evolved in three different phyla by two pathways: (i) by complication and (ii) by simplification.

Structure of the oral tentacles of early ontogeny stage in brachiopod Hemithiris psittacea (Rhynchonelliformea, Rhynchonellida)

“…Thus, the shape of tentacles in cross sections depends on the length of brachial axis of the lophophore. Since lophophorates' ancestor apparently had a horseshoe shaped lophophore with a short brachial axis (Temereva & Kuzmina, 2022), its tentacles had a round shape in transverse section.…”

“…The tentacles of all lophophorates have prominent zonality, which is expressed in the presence of several ciliated zones that are colocalized with nerves and muscle bundles (Figure 7; Temereva & Kuzmina, 2022; Temereva & Malakhov, 2010; Temereva, et al, 2021). In phoronids and bryozoans, there are 6 ciliary zones: frontal, two latero‐frontal, two lateral and an abfrontal.…”

“…The lophophore is mainly used for filtration of food particles and respiration. This tentacular organ is regarded as a synapomorphy of three animal phyla, which are gathered into a united clade called Lophophorata: Phoronida, Bryozoa, and Brachiopoda (see review in Temereva & Kuzmina, 2022). The monophyly of the lophophorates was supported by some authors (Jang & Hwang, 2009; Marlétaz et al, 2019; Nesnidal et al, 2013; Zverkov et al, 2019).…”

Phoronida—A small clade with a big role in understanding the evolution of lophophorates

“…Therefore, the lophophore can be divided into the oral and anal sides. The shape and arrangement of the lophophore are one of the most variable and taxonomically important features of the phoronid body plan (e.g., Emig, 1982;Temereva & Kuzmina, 2022;Temereva et al, 2016;Temereva, 2019aTemereva, , 2020. In some of the species, the bases of tentacles form almost an oval field, while in others the lophophore is horseshoe-shaped, extending into branches that bend towards the anal side (Figure 1b).…”

“…Phoronids are coelomate animals and their coelom is divided into three compartments-the vestigial protocoel that occupies a small flap of tissue covering the mouth opening (the so-called epistome), mesocoel that forms the coelomic cavity of the lophophoral tentacles, and the metacoel that represents major coelomic cavity occupying most of the trunk (Emig, 1973b(Emig, , 1982Hermann, 1997;Temereva & Kuzmina, 2022;Temereva & Malakhov, 2011, 2015. However, it remains debatable whether protocoel is a coelomic cavity at all (Bartolomaeus, 2001).…”