Sexual reproduction in the compound ascidian Diplosoma listerianum (Tunicata). I. Metamorphosis, storage and phagocytosis of sperm in female duct

Burighel, Paolo; Martinucci, G. B.

doi:10.1007/bf00350306

Cited by 17 publications

(22 citation statements)

References 19 publications

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“…Sperm released by the individual zooids leave the colony in the exhalant current and rapidly disperse into the surrounding water (Bishop & Ryland 1991). Entering another colony, sperm move up the fertilization canal (oviduct) of a zooid into the lumen of the ovary (Burighel et al 1986;Burighel & Martinucci 1994a;Bishop & Sommerfeldt 1996), where they may be stored (Bishop & Ryland 1991;Burighel & Martinucci 1994a;Bishop & Sommerfeldt 1996). True internal fertilization occurs around the time of ovulation of the fully-grown oocyte directly into the colonial tunic (Burighel & Martinucci 1994b), where brooding occurs.…”

Section: Introductionmentioning

confidence: 99%

Fertilization in the sea: are the hazards of broadcast spawning avoided when free–spawned sperm fertilize retained eggs?

Bishop

1998

Proc. R. Soc. Lond. B

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In broadcast-spawning marine animals, rapid dilution and short lifespan of sperm following release may impose severely localized patterns of mating. Partial or total failure of external fertilization due to sperm limitation appears commonplace. However, it is not clear to what extent the restrictive kinetics of fertilization in water also constrain mating in animals that release sperm but retain their eggs for fertilization.The compound ascidian Diplosoma listerianum liberates sperm that are dispersed to other colonies and taken in prior to internal cross-fertilization. The fertile lifespan of sperm was found to be long (half-life ca. 8 hours), and a substantial number of fertilizations occurred with 24-hour-old sperm. Fertilizations were obtained from sperm concentrations that would typically produce little or no external fertilization. In a separate experiment, a very small piece of D. listerianum (dry weight less than 2 mg) sired abundant progeny throughout a 3840 l tank. Paternity of progeny in these experiments was con¢rmed by molecular markers. The same markers were used to extend, to over seven weeks, the known maximum period of storage of exogenous sperm prior to fertilization in this species.The production of only a few thousand sperm at a time by each zooid, poor synchronization of release between zooids, and the existence of many well-spaced exhalant openings in large colonies suggest that D. listerianum is incapable of generating a dense plume of sperm, even close to the source. It is suggested that, unlike external fertilization, successful internal cross-fertilization in D. listerianum is not dependent upon the interception of a dense cloud of gametes just released by a near neighbour. It seems instead that dilute, long-lived sperm can be extracted e¤ciently from seawater by this suspension feeder, potentially over a period of time. This capability, and other features of the life history, make it unlikely that sperm limitation is an acute problem in this species and comparable taxa, a conclusion with potential signi¢cance for expected patterns of mating, sex allocation and gamete attributes in sessile aquatic invertebrates. Variance in reproductive success between individuals due to di¡erences in fertilization rate may be much lower than in broadcast spawners exhibiting external fertilization.

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Section: Introductionmentioning

confidence: 99%

Fertilization in the sea: are the hazards of broadcast spawning avoided when free–spawned sperm fertilize retained eggs?

Bishop

1998

Proc. R. Soc. Lond. B

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“…The anatomy of the ovary and pattern of sperm storage within it suggest that it is indeed entirely possible that the development of an oocyte is influenced by individual sperm. The ovary of Diplosoma listerianum is branched, and the stored sperm are distributed among narrow blind-ended diverticula that each penetrate the follicle cell layers of an immature oocyte and terminate in contact with its vitelline coat (Burighel & Martinucci 1994a,b, Bishop & Sommerfeldt 1996, with the furthest advanced sperm in each diverticulum thus in extreme proximity to the developing oocyte during vitellogenesis.…”

Section: Discussionmentioning

confidence: 99%

“…An alternative possibility, involving sexual conflict, is that sperm differs, according to its source, in its ability to manipulate the recipient colony to increase maternal investment. This might conceivably involve haploid gene expression in stored sperm (Immler 2008), a possibility further hinted at by the metamorphosis undergone by sperm of D. listerianum upon entry into the recipient ovary (Burighel & Martinucci 1994a). …”

Section: Discussionmentioning

confidence: 99%

Differential maternal allocation following mixed insemination contributes to variation in oocyte size in a sea squirt

Hammerschmidt

Pemberton²,

Michiels³

et al. 2011

Mar. Ecol. Prog. Ser.

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In many organisms, offspring fitness is markedly affected by size at hatching. Theoretical models predict offspring from one clutch to have the same optimal size, but empirical studies report within-clutch variation in offspring sizes for a wide range of species. According to the differential allocation hypothesis, this could be explained, at least in part, by multiply mated females selectively provisioning their offspring depending on the sperm donor. We tested this hypothesis in the internally fertilising, colonial sea squirt Diplosoma listerianum, whose larvae are non-feeding so that females' provisioning of oocytes provides all of the energy for larval dispersal and metamorphosis. We show that there is high within-clutch variation in offspring size in a natural D. listerianum population. When we then crossed laboratory clones pairwise in a fully factorial design in the laboratory, we found that the same acting female clone produced differently sized oocytes with different mating partners. This result does not reflect the effect of direct male benefits, as the water-borne sperm cell is the only contact between males and females, but nevertheless indicates that females allocate resources to their offspring in part influenced by the father's identity. This pattern would be expected to contribute to within-clutch variation in offspring size in mixed-paternity broods. KEY WORDS: Differential allocation · Oocyte size · Offspring fitness · Maternal investment · Diplosoma listerianumResale or republication not permitted without written consent of the publisher

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“…This is because compatible sperm move through the oviduct in a matter of hours but are subsequently stored in the ovary, potentially for weeks, prior to penetration of an ovum around the time of ovulation (Bishop & Ryland 1991;Burighel & Martinucci 1994a;Bishop & Sommerfeldt 1996;Bishop 1998); sperm arriving over a relatively long period might therefore compete for fertilizations. In the present experiments, egg penetration leading to the earliest progeny would typically have occurred in the presence of sperm from both sources.…”

Section: Discussionmentioning

confidence: 99%

“…Fertilizing sperm pass up the fertilization duct (oviduct) of a zooid and enter the lumen of the ovary (Burighel et al 1986;Burighel & Martinucci 1994a;Bishop & Sommerfeldt 1996). They may then be stored in the ovarian lumen for several weeks prior to fertilization (Bishop & Ryland 1991;Burighel & Martinucci 1994a;Bishop & Sommerfeldt 1996;Bishop 1998).…”

Section: (A) Biology Of Diplosoma Listerianummentioning

confidence: 99%

Sperm precedence in a novel context: mating in a sessile marine invertebrate with dispersing sperm

Bishop

Pemberton

Noble

2000

Proc. R. Soc. Lond. B

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The compound ascidian Diplosoma listerianum releases aquatic sperm which are dispersed passively to potential mates as individual gametes prior to storage of sperm, internal fertilization and brooding of embryos. The storage of exogenous sperm enables D. listerianum to produce a lengthy series of progeny following a brief period of mating. Molecular paternity analysis following sequential mating of colonies in laboratory culture revealed a consistent pattern with a clear initial bias in paternity towards the ¢rst of two acting males. The sites of sperm storage and fertilization and the morphology of the ovary in D. listerianum suggest that this bias re£ects ¢rst-in^¢rst-out use of individual stored gametes. The proportion of second-male paternity subsequently increased with time within the progeny arrays. This may have re£ected the ageing or passive loss of ¢rst-male sperm. It is also possible that the modular nature of the organism contributed to this temporal trend: any recently budded colony modules maturing in the interval between matings would have been available exclusively to second-male sperm as virgin zooids. Two sets of mating trials were run. In the ¢rst, the collection of progeny su¡ered an interruption of 13 days and each male gained a larger proportion of recorded paternity within the progeny analysed when mating ¢rst rather than when mating second. In one mating combination, the ¢rst male obtained almost 100% of recorded paternity. In the second set of trials, with di¡erent clonal combinations, the complete sequence of progeny was collected and the estimated overall proportion of second-male paternity (P 2 ) was consistently 4 0.5. Taken as a whole, the results suggest that the overall P 2 -value can vary widely within the population studied. Proposed mechanisms of mating-order e¡ects in species with copulatory mating include several which can have no counterpart in indirect aquatic mating since they involve the active removal, sealing o¡, volumetric displacement or incapacitation of ¢rst-male ejaculates. It is nevertheless clear that mating-order e¡ects can be pronounced during the type of non-copulatory mating examined here, which is widespread in marine invertebrates.

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Sexual reproduction in the compound ascidian Diplosoma listerianum (Tunicata). I. Metamorphosis, storage and phagocytosis of sperm in female duct

Cited by 17 publications

References 19 publications

Fertilization in the sea: are the hazards of broadcast spawning avoided when free–spawned sperm fertilize retained eggs?

Fertilization in the sea: are the hazards of broadcast spawning avoided when free–spawned sperm fertilize retained eggs?

Differential maternal allocation following mixed insemination contributes to variation in oocyte size in a sea squirt

Sperm precedence in a novel context: mating in a sessile marine invertebrate with dispersing sperm

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