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

Abstract

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.

Genetic diversity increases population productivity in a sessile marine invertebrate

“…First, if paternity is determined by the proximity of the nearest conspecific male, individuals in monoculture are more likely to breed with siblings, and thus smaller offspring size in monoculture could have been a result of inbreeding. Evidence for distance-based paternity biasing in organisms such as B. neritina is mixed (Yund and McCartney 1994, Bishop et al 2000, Johnson and Yund 2009), so we hesitate to speculate on the likelihood of inbreeding depression, but we note that such an effect is possible. However, studies have shown that paternity can determine maternal investment in offspring size (Hammerschmidt et al 2011), and is possible that mothers allocated fewer resources to offspring in monocultures because the sperm belonged to close relatives.…”

Efficient utilization of very dilute aquatic sperm: sperm competition may be more likely than sperm limitation when eggs are retained

“…The competitive interactions of sperm in these sorts of organisms are largely unknown, although the complexity of the female tract (Burighel & Martinucci 1994a,b), sperm precedence (Bishop et al 2000b) and potential sperm ageing effects (Pemberton et al 2003) have been documented in D. listerianum. Evidence of cryptic female 'control' over paternity in spermcast ascidians has been previously documented in terms of sexual compatibility (Scofield et al 1982;Bishop et al 1996) and frequency dependence of mate choice (Pemberton et al 2003).…”

The early sperm gets the good egg: mating order effects in free spawners

“…Although documented for a wide range of taxonomic groups (Smith 1984;Birkhead & Møller 1998;Simmons 2001), including sessile marine invertebrates (Bishop et al 2000), the influence of mating order on sperm use has never been described in free-spawning marine invertebrates, where both sexes shed gametes into the water column. Indeed, in free-spawning marine invertebrates, sexually selected forces are often considered of secondary importance to naturally selected processes such as sperm limitation (reviewed in Yund 2000).…”