Control of oocyte maturation, sperm activation and spawning in two lugworm species:Arenicola marina and A. defodiens

Abstract

In addition to the morphological differences between Arenicola defodiens (Cadman and Nelson-Smith, 1993) and Arenicola marina (L.) this study demonstrales clear differences in the reproductive biology, timing of reproduction at a population level, and endocrine control of reproduction in females. Fecundity IS significantly higher in females of A. marina and the mean diameter of their fully grown oocytes is also significantly larger than in A. defodiens. The timing of reproduction at a population level is also different with A. defodjens spawning approximately 1 to 2 mo later than sympatric A. marina. In vitro and in viva experiments have established fundamental differences as well as similarities in the hormonal control of reproduction of both sexes between the 2 species. Male A. defodienscan be induced to spawn by the injection of 8,11,14-eicosatrienoic acid into the coelomic cavity, putatively shown to be the natural sperm maturation factor and spawning hormone in A. marina. In females, injection of female prostomial homogenate from either species into the coelomic cavity induces oocyte maturation and subsequent spawning in both species. However, oocytes of A. marina, whilst maturing in the presence of CMF (Coelomic Maturation Factor) in vjtro, do not mature in the presence of prostomial homogenate of either species, whereas A. defodiens oocytes do. In A. marina, oocyte maturation and subsequent spawning is under the control of 2 hormones: (1) a substance from the prostomium, Prostom a l Maturation Hormone (PMH), which induces the production of (2) CMF whlch acts on the oocyte. In A. defodiens, we show that only PMH is required for oocyte maturation and spawning. The in vitro induction of oocyte maturation in A. marina, by a variety of chemicals and treatments that have already been shown to induce maturation in A. defodiens and species from other phyla, was investigated. None of the chen~icals and treatments tested induces maturation in A. marina or A. defodiens oocytes.

Calcium signals and oocyte maturation in marine invertebrates

“…1) In oocytes of polychaete annelids that arrest at metaphase I before fertilization (Fig. 1), induction of GVBD in isolated oocytes is triggered in various ways, including: i) transfer into natural, but not artificial, seawater in Chaetopterus (Ikegami et al, 1976); ii) exposure to a protease purified from digestive tract fluids in Sabellaria (Peaucellier, 1978), and iii) application of coelomic fluid supplemented with prostomial homogenates in Arenicola (Watson et al, 1998). Chaetopterus oocytes incubated in artificial seawater can be stimulated to undergo GVBD by excess K + in the presence of external Ca 2+ (Ikegami et al, 1976) and by A23187 even in Ca 2+ -free seawater (Eckberg and Carroll, 1982).…”

“…Chaetopterus oocytes incubated in artificial seawater can be stimulated to undergo GVBD by excess K + in the presence of external Ca 2+ (Ikegami et al, 1976) and by A23187 even in Ca 2+ -free seawater (Eckberg and Carroll, 1982). A23187 also triggers GVBD in Sabellaria oocytes (Peaucellier, 1978) but not in Arenicola oocytes (Meijer, 1979;Watson et al, 1998). Neither A23187 nor ionomycin induces GVBD in Pseudopotamilla oocytes (Nakano and Deguchi, unpublished observation), and instead an intraoocytic cAMP elevation seems to be essential for this process (Deguchi et al, 2011).…”

Unravelling mechanisms behind population dynamics, biological traits and latitudinal distribution in two benthic ecosystem engineers: A modelling approach

“…Given the really close phylogenetic relationship between A. marina and A. defodiens, the same abj-DEB model (accounting for metabolic acceleration between the first feeding and the end of metamorphosis) was used for both species with two different sets of parameters (see De Cubber et al, 2019;. The lifecycle of A. defodiens in a natural environment has barely been described, except for spawning events that have been reported from mid-December to early January (De Cubber et al, 2018;Watson et al, 1998). However, based on in situ pers.…”

CDK1/cyclin B regulation during oocyte maturation in two closely related lugworm species, Arenicola marina and Arenicola defodiens

“…In both species, the oocytes are arrested at prophase of meiosis I until spawning occurs. At this time, a hormone induces the transition from prophase to metaphase I and meiosis then is halted until fertilization occurs (Watson et al . 1998).…”

“…Regulation of MPF was examined in these two species of lugworm because of marked differences in their hormonal control of oocyte maturation despite their phylogenetic closeness. In A. defodiens , a single ‘prostomial maturation hormone’ (PMH) controls oocyte maturation on release from the brain (Watson et al . 1998).…”