The ecological and evolutionary consequences of sperm chemoattraction

Abstract

Chemical communication between sperm and egg is a critical factor mediating sexual reproduction. Sperm attractants may be significant evolutionarily for maintaining species barriers, and important ecologically for increasing gamete encounters. Still unresolved, however, are the functional consequences of these dissolved signal molecules. Here, we provide experimental evidence that sperm chemoattraction directly affects the magnitude of fertilization success. The recent discovery of L-tryptophan as a potent attractant to red abalone (Haliotis rufescens) sperm affords the opportunity to quantify how navigation affects gamete interactions. Sperm behavioral responses to manipulations of the natural tryptophan gradient around individual eggs reveals that both chemotaxis and chemokinesis significantly promote contacts. Our results show further that attractant release by means of diffusion effectively doubles the target size of red abalone eggs, which in turn significantly increases fertilization success. Although long theorized as potential barriers to hybridization, species-specific sperm attractants in red and green (Haliotis fulgens) abalone are only minor contributors to maintaining reproductive isolation. Because abalone typically live in dense, multispecies aggregations, chemically mediated navigation would prevent sperm from pointlessly tracking heterospecific eggs. Thus, even though reproductive isolation fundamentally resides at the level of membrane recognition proteins, species-specific sperm attractants may evolve to locate the right target within mixed gamete suspensions of closely related species.

Mating system variation in the hermaphroditic brooding coral, Seriatopora hystrix

“…However, these systems do vary in fundamentally different ways, which are likely to have important implications for fertilization success. First, pheromones and other chemotactic attractants may be used by some marine animals to increase fertilization success and outcrossing (for example, Coll et al, 1995;Riffell et al, 2002Riffell et al, , 2004, while filter feeding species have been shown to actively filter out and store sperm from conspecific individuals (Yund, 2000;Hughes et al, 2002). Nevertheless, levels of selfing may be more common in marine animals than is currently recognized and more research is clearly needed to determine the extent of selffertilization and the factors important in maintaining mixed reproductive strategies.…”

“…While some plants have evolved associations with pollinators to assist in the transfer of pollen from one individual to another, no such associations are known for marine taxa. Although pheromones and other chemotactic attractants may be used by some marine taxa to increase fertilization success (for example, Coll et al, 1995;Riffell et al, 2002Riffell et al, , 2004, and despite the potential for decreased fitness due to inbreeding through selfing, the capacity to ensure fertilization in the absence of potential mates or under sperm-limited conditions means that self-fertilization may be an important reproductive tactic for hermaphroditic brooding and broadcast spawning species (for example, Sabbadin, 1971;Heyward and Babcock, 1986;Yund and McCartney, 1994;Cohen, 1996, Brazeau et al, 1998.…”

Chemically moderated gamete preferences predict offspring fitness in a broadcast spawning invertebrate

“…Sperm chemokinesis, on the other hand, describes a change in the steady-state speed of sperm cells, independent of direction, which is governed by the concentration of the chemical stimulus [16]. Both processes (hereafter 'sperm chemoattraction') can simultaneously contribute to the accumulation of sperm around unfertilized eggs [17,18].…”

Gamete plasticity in a broadcast spawning marine invertebrate

“…Many marine invertebrate eggs have accessory structures, such as follicle cells or jelly coats, that increase the overall target size for searching sperm (48,49). Furthermore, the eggs of some species release sperm chemoattractants that increase the virtual size of eggs, increasing their chances of being contacted by sperm (50,51). Such egg accessory devices are thought to be energetically inexpensive relative to the actual ovicell itself (52), and so some have argued that selection due to the sperm environment will act more strongly on accessory structures than ovicell size per se (49).…”