Embryological perspective of sexual somatic development in ciliated protozoa: implications on immortality, sexual reproduction and inheritance of acquired characters

Abstract

This essay addresses somatic development during sexual reproduction of ciliated protozoa, which is interpreted as an embryological phenomenon resembling embryogenesis of multicellular organisms. The uniqueness of this somatic development, as distinct from asexual development, resides in its dependence on new information associated with the germ nucleus, and on its involvement of both maternal and postzygotic informational inputs. This understanding derives from experimental dissection of nuclear control of somatic development inParamecium, and in several hypotrichous ciliates. The embryological perspective enables us to reorganize our thinking on several historical issues of development and evolution: whether protozoa are immortal, and whether mortality only arose together with multicellularity; whether their sexual process can be regarded as reproduction, equivalent to sexual reproduction of multicellular organisms; whether the inheritance of acquired cortical variations of non- genic origins in ciliates constitutes a threat to neo-Darwinism. Conceptual predicaments on these issues have often stemmed from unwarranted parallelism drawn between asexual propagation of protozoa and sexual reproduction of multicellular organisms. The embryological reply to these questions is that ciliated protozoa are mortal, since during fertilization the maternal soma perishes by resorption, and is replaced by a new one which developsin situin the maternal soma. The consequence of their sexual process is the same as in sexually reproducing multicellular organisms, in that the post-fertilization protozoan is an ontogenetically new individual, equipped with a new soma unlike those generated during asexual propagation. On the basis of the characteristicin situdevelopment of the embryonic soma during sexual reproduction, two evolutionary perceptions are formulated. First, the extensiveness of resorption of the maternal soma, and release of development of the embryonic soma from cytotactic constraints imposed by the maternal soma, constitute major themes of phylogenetic evolution. Second, the evolutionary outcome of acquired cortical variations has to be evaluated in terms of the fidelity of perpetuation of such variations through sexual reproduction, and their potential of being assimilated into the genomic programme of embryonic development. The evolutionary predictions accordingly may turn out to be radically different from those based on the inheritance of such variations during asexual propagation alone.