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

Abstract

Fertilization success may be severely limited in marine invertebrates that spawn both male and female gametes. In a diverse group of aquatic organisms only sperm are released, with sperm-egg fusion occurring at the mother. Here, we report fertilization kinetics data for two such 'brooding' or 'spermcast' species-representing each major clade of the animal kingdom. High levels of fertilization were achieved at sperm concentrations of two or three orders of magnitude lower than is common with broadcast spawning species. At a concentration of 100 sperm ml -1 , fertilization rates of a bryozoan and colonial ascidian were near maximum, whereas most broadcast spawners would have displayed near complete reproductive failure. A further experiment looked at the rate of uptake of sperm under natural conditions. Results suggested that sperm released at ca. 0.9 m from an acting female could be collected at a rate of 3-12 times greater than the minimum required simply to avoid sperm limitation. Thus, evolutionary pressures on gametic and other reproductive characteristics of many species that release sperm but retain eggs may be quite different from those of broadcast spawners and may confer on the former an enhanced scope for sperm competition and female choice.

Male reproductive success during spawning events of the octocoral Pseudopterogorgia elisabethae

“…Meidel & Yund (2001) found that sea urchin eggs had higher fertilization rates when they were able to 'time average' over 24 h of naturally occurring spawning events. The effect of time averaging is further magnified among species that actively pump water past eggs, and a number of studies have shown that tunicates can achieve high fertilization rates even when ambient sperm density is low (Bishop 1998, Pemberton et al 2003.…”

“…Meidel & Yund (2001) found that sea urchin eggs had higher fertilization rates when they were able to 'time average' over 24 h of naturally occurring spawning events. The effect of time averaging is further magnified among species that actively pump water past eggs, and a number of studies have shown that tunicates can achieve high fertilization rates even when ambient sperm density is low (Bishop 1998, Pemberton et al 2003.The expectation that large, nearby males will dominate the paternity of larvae on any single colony initially appears intuitive. However, the random success of males that occurred within an area of at least 400 m 2 suggests otherwise and has important implications for our understanding of reproductive systems.…”

Spatial distribution of ascidian sperm: two-dimensional patterns and short vs. time-integrated assays

“…Concerns about the fertilization consequences of rapid sperm dilution with distance from sperm source have led to an ongoing debate about the extent to which fertilization in these systems is limited by sperm availability (reviewed in Levitan & Petersen 1995, Yund 2000. In general, egg brooders that possess mechanisms to filter dilute sperm from the water appear to be less sperm-limited than egg broadcasters (Bishop 1998, Yund 2000, Pemberton et al 2003, Johnson & Yund 2004, Phillippi et al 2004. However, experimental approaches that incorporate life history adaptations that minimize gamete dilution effects (e.g.…”

“…Free-spawning marine invertebrates reproduce sexually by releasing sperm into the water, with fertilization occurring either externally (egg broadcasters) or internally (egg brooders, or spermcasters sensu Pemberton et al 2003). Evaluating the physical and biological conditions under which eggs are successfully fertilized is important for understanding the population dynamics of free-spawners.…”

Self-fertilization as an alternative mode of reproduction in the solitary tunicate Pyura chilensis

“…In sessile marine benthic invertebrates, the encounter between mating partners may be limited when broadcast gametes are exposed to wastage (Yund 1990, Yund & McCartney 1994. In broadcast spawning species in which sperm and eggs are released into the seawater, the rates of fertilization commonly vary between 0 and 100% (Levitan 1995, Pemberton et al 2003. Since fertilization success and mating distance in these species depend on the chance of intersection between sperm and eggs, the species should spawn synchronously to assure fertilization and to avoid the loss of sperm through dilution (e.g.…”