Sexual differentiation and germ cell transfer in the colonial ascidian Botryllus schlosseri

Abstract

A B S T R A C TThe sexual differentiation in t h e colonial ascidian Botryllus schlosseri was considered with respect to colony sexualization and sexualization of t h e single zooids of t h e same blastogenic generation.The colony sexualization was investigated histologically in a series of young colonies reared in t h e laboratory and fixed periodically throughout a sequence of blastogenic generations. The newly set colonies lack gonad blastemata; next, germ cells appear and several generations are involved in various phases of hyposexuality prior to the appearance of generations in which mature both eggs and sperm.The sexual contribution of t h e zooids of the same generation was found to vary according to a n intrinsic bilateral asymmetry (the gonadogenic potential differs both contralaterally in each zooid and between zooids of a different, dextral or sinistral, parental origin) and in proportion to t h e quantity of germ cells that have been transferred from preceding generations.The transfer of germ cells from one to t h e following generations was investigated by fusing colonies of opposite pigment genotypes, then crossing t h e separated parabionts to a common genotype, and scoring t h e offspring pigment phenotypes. This experiment has shown t h a t not only immature oocytes but also undifferentiated germ cells were exchanged between t h e parabionts and then gradually matured as eggs or sperm in a prolonged series of generations.The primordial germ cells differ in size from hemoblasts, t h e source of hemocytes. However, further experiments a r e needed in order to decide between t h e two contrasting hypotheses of germ cell origin: either segregation from t h e atrial epithelium of buds or development from hemoblasts.The sexual differentiation in t h e colonies of Botryllus has been recently re-considered by Mukai and Watanabe ('76a,b). Nevertheless, many points still remain controversial.The hermaphroditic colonies reach sexual maturity only after having gone through several blastogenic generations. Male sexual maturity is attained first, though immature eggs are also present. Next, maturing gonads of either sex are produced in sequential generations. Seasonal sexual cycles in the wild, and succeeding cycles in t h e laboratory under constant temperature conditions have been described for B. schlosseri (Sabbadin, '55a, '60). Whether germ cells are present in the newly set colonies or during t h e periods or sexual inactivity and transferred to and gradually matured in t h e following generations

Botryllus schlosseri: A model ascidian for the study of asexual reproduction

“…The diverse combinations of these characters give rise to a variety of color morphs differing in both geographical and ecological distribution (Sabbadin and Graziani, 1967b;Sabbadin, 1978). The pigmentation pattern is a useful experimental marker, as it allows easy identification of colonies by simply ascertaining their color (Sabbadin, 1971;Sabbadin and Zaniolo, 1979;Laird et al, 2005b).…”

“…These studies were devoted either to the development of particular organs, such as the digestive system (Burighel, 1970), circulatory system (Brunetti and Burighel, 1969;Burighel and Brunetti, 1971), blood (Milanesi and Burighel, 1978;Burighel et al, 1983), heart (Nunzi et al, 1979), branchial basket (Casagrande et al, 1993), and nervous system (Burighel et al, 1997;, or to better comprehension of biological processes (Tables 3, 4), such as sexual reproduction (Sabbadin and Zaniolo, 1979;Manni et al, 1993Manni et al, , 1994 and take-over (Burighel and Schiavinato, 1984;Lauzon et al, 1993; see also Table 3 for references). Most of these studies describe bud development according to Sabbadin's (1955a) staging.…”

“…When the gonads appear, their maturation may require several generations, passing through the phase of incipient sexuality, with the appearance of undifferentiated gonad blastema in secondary buds, to a phase with abortive testes and oocytes not undergoing vitellogenesis, followed by the phase of male and then female sexual maturity (Sabbadin, 1960;Sabbadin and Zaniolo, 1979).…”

“…Colonial bilateral gonadal primordia appear in the secondary bud at stage 3 as clumps of undifferentiated cells on either side of the inner vesicle (Table 5; Sabbadin and Zaniolo, 1979): their lateral portion becomes an ovary. Oocytes appear in secondary buds (Fig.…”

EVOLUTIONARY GENETICS OF ALLORECOGNITION IN THE COLONIAL HYDROID HYDRACTINIA SYMBIOLONGICARPUS

“…Fusion may also allow partners to monopolize a shell, and prevent the subsequent colonization by competitors, more rapidly than a single col-ony could. However, there may also be substantial costs to intergenotypic fusion in terms of intraspecific parasitism, pathogen transmission, and developmental instability (Mukai 1976;Sabbadin and Zaniolo 1979;Buss 1982Buss , 1987Sabbadin and Astorri 1988;Shenk and Buss 1991;Grosberg 1992;Rinkevich and Weissman 1992a,b). Similarly, agonistic behavior is one of the principal ways that clonal cnidarians can acquire space occupied by other organisms; however, the production and deployment of structures that mediate aggressive interactions can exact substantial costs in terms of future growth and reproductive potential (Buss 1990;Buss and Grosberg 1990;Grosberg 1995, 1996).…”