Latent capacities for gametogenic cycling in the semelparous invertebrate Nereis.

Abstract

Most nereid polychaetes are strictly semelparous, a single episode of reproduction being invariably followed by death. Endocrine manipulation in Nereis diversicolor by the regular inplantation of cerebral ganglia from immature donors unveils characteristics associated with a capacity to engage in repeated gametogenic cycling. Such manipulation permits full maturation ofthe gametes but blocks spawning. Gamete resorption then leads on to another bout of gametogenesis and a new cohort of gametes is formed. The neurosecretory system adopts a cyclical pattern of activity, which parallels that of gametogenesis. Repair and maintenance of the soma continue throughout sexual maturation, as shown by the persistence of feeding and the capacity for regenerative segment proliferation. In consequence, life is extended apparently indefinitely. These latent capacities are reminiscent of features of iteroparous life histories, characterized by repeated breeding, and are postulated to be vestiges of an iteroparous ancestry. They also constitute a preadaptation for Iteroparity and reveal how readily a reversal to this condition could occur. The study suggests that reproductive strategies may be unexpectedly labile in even their most fundamental aspects.Two fundamentally distinct types of reproductive strategy are encountered among multicellular organisms, involving a single breeding episode or repeated episodes. A semelparous (1) [monotelic (2) or, in plants, monocarpic (3)] strategy involves an extreme form of "reproductive recklessness" (4), with resources being diverted from the soma for investment in reproduction on a scale that apparently precludes the possibility of survival by the parent [see review by Stearns (5)]. Semelparous organisms provide valuable models for the study of senescence because of the rapid and highly deterministic character of the process in these organisms. In contrast, an iteroparous (polytelic; polycarpic) life history involves repeated bouts ofreproductive activity during which repair and maintenance of the soma are maintained; the progress of senescence and the time ofdeath are not precisely "programmed."Most nereid polychaetes are strictly semelparous. Stages of larval and juvenile development are followed by a prolonged period of gametogonial proliferation resulting, in females, in the presence of oocytes at diverse stages of development (6). The final stages of oogenesis involve a process of "cohort formation," during which small oocytes disappear and all the gametes attain their full size, leading by a process of cytoplasmic transformation to the production of mature, fertile oocytes. The final stages of spermatogenesis involve the initiation of meiosis and the breakup of spermatocyte clusters to form motile spermatozoa. Mature nereids cease feeding and lack the capacity to regenerate caudal segments (7). In both sexes, gamete maturation is rapidly and invariably followed by spawning and death. In most species, although not in the estuarine Nereis diversicolor, sexual maturation is accom...

Gonadotrophic hormone inEulalia viridis(Polychaeta, Annelida): Stimulation of vitellogenesis

“…Declining production of the hormone in the later stages of maturation thus inhibit regeneration and somatic growth but free the processes which are characteristic of the later stages of maturation. Golding and Yuwono (1994) have shown that the deactivated ganglia of submature Nereidae can be reactivated, implying the possibility that an iteroparous mode of reproduction was previously present in the proto-Nereidae. The observations presented in this paper point to a more uniform pattern of endocrine control of reprodution in the various families of the Phyllodocida than had previously been thought to have been possible.…”

Discovery of methylfarnesoate as the annelid brain hormone reveals an ancient role of sesquiterpenoids in reproduction

“…In the related species Nereis diversicolor , it could be shown that implantation of ganglia from immature animals into the coelomic cavity of maturing animals, reversed the effects of the decreasing nereidin concentration. In particular, germ cells were resorbed and the ability to regenerate lost segments was re-established (Golding and Yuwono, 1994). These findings highlight the exceptional importance of neuroendocrine signals in semelparous reproduction and suggest that the underlying molecular mechanisms are conserved across different annelids (Hauenschild, 1956b, 1959; Golding, 1967a, 1967b; Durchon and Porchet, 1970; Hofmann, 1976; Cardon et al, 1981; Golding, 1983; Golding and Yuwono, 1994).…”

“…In particular, germ cells were resorbed and the ability to regenerate lost segments was re-established (Golding and Yuwono, 1994). These findings highlight the exceptional importance of neuroendocrine signals in semelparous reproduction and suggest that the underlying molecular mechanisms are conserved across different annelids (Hauenschild, 1956b, 1959; Golding, 1967a, 1967b; Durchon and Porchet, 1970; Hofmann, 1976; Cardon et al, 1981; Golding, 1983; Golding and Yuwono, 1994).

10.7554/eLife.17126.003Figure 1. Vitellogenin expression in eleocytes is a quantitative measure for the maturation stage of Platynereis , allowing for the establishment of a bioassay to purify the enigmatic brain hormone, nereidin.( A ) Scheme summarising the critical role of the brain hormone nereidin in energy expenditure, as derived from classical experiments: Before maturation (left), high nereidin levels sustain somatic growth, but repress reproduction; drops in nereidin activity levels initiate the generation of germ cells and sexual maturation (right).

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Endocrine and environmental control of reproduction in Polychaeta

“…Spawning never occurs, a situation that has occasionally been observed in iteroparous species (Olive et al 1981a). According to Golding and Yuwono (1994), this latent capacity is reminiscent of an iteroparous ancestry and may constitute a preadaptation to return to this condition.…”

“…As the level of endocrine activity of a transplanted brain removed from immature donors is maintained for some months after transfer into a host (Golding 1985(Golding , 1987, it is possible to cyclically increase the hormone titer by periodic (bimonthly) intracoelomic implantation of such cerebral ganglia (Golding and Yuwono 1994). When subjected to such experimental conditions, the worms achieve repeated cycles of gametogenesis, each cycle ending with resorption of the gametes, with no spawning.…”