Speciation and the evolution of gamete recognition genes: pattern and process

Abstract

Proteins on gamete surfaces are major determinants of fertilization success, particularly in free-spawning animals. Molecular analyses of these simple genetic systems show rapid evolution, positive selection, accelerated coalescence and, sometimes, extensive polymorphism. Careful analysis of the behavior of sperm produced by males with different gamete alleles shows that these alleles can deliver significant functional differences. Three forms of allele-specific fertilization advantage have been shown: assortative mating based on gamete type, rare allele advantage and heterozygote superiority. Models suggest that sperm and egg proteins may be coevolutionary partners that can alternate between directional selection for high fertilization ability and cyclic adaptation of eggs and sperm driven by sexual conflict. These processes act within allopatric populations and may accelerate their divergence if gamete adaptations in separate demes reduce cross-fertilization. Reproductive character displacement by reinforcement may play a diversifying role when previously allopatric populations rejoin. In circumstance that might prove to be common, divergence in sympatry can be driven by sexual conflict or by association of mating types with ecological differences. The ecology of fertilization, especially the degree of sperm competition and egg death via polyspermy, are important determinants of the strength and direction of selection on gametes. Freespawning animals allow careful analysis of gamete recognition -from the behavior of adults and interactions of gametes, to molecular patterns of allele divergence. Future research efforts on the evolutionary consequences of fertilization ecology, and the interaction between extensive variation in egg surface proteins and sperm fertilization ability, are particularly needed.

Characterization of the Sperm Molecule Bindin in the Sea Urchin Genus Paracentrotus

“…Proteins involved in reproduction and, more specifically, in gamete recognition-which control the binding and fusion of gametes-may play an essential role in reproductive isolation and speciation in marine organisms (reviewed in Palumbi 1994Palumbi , 1998Vacquier et al 1995;Swanson and Vacquier 2002;Lessios 2007). Reproductive isolation in broadcast spawners may be caused by a number of factors, such as nonoverlapping spawning times, chemical communication, or species-specific gamete interactions.…”

Is Sexual Conflict an "Engine of Speciation"?

“…A very large amount of experimental data coming from studies of sperm or pollen competition between closely related species (e.g., Arnold et al 1993;Wade et al 1994;Rieseberg 1995;Howard 1999), as well as from molecular studies of fertilization proteins (e.g., Aguade et al 1992;Lee and Vacquire 1992;Vacquier and Lee 1993;Metz and Palumbi 1996;Palumbi 1998;Howard 1999;Swanson and Vacquier 2002a,b;Galindo et al 2003;Landry et al 2003;Swanson et al 2003), indicates that in many diverging taxa, traits and proteins related to fertilization evolve extremely rapidly. At least in the case of marine organisms, there now appears to be a consensus that these data can be explained in large part by selection for avoidance of polyspermy (Levitan et al 2007;Palumbi 2009;Lessios 2011;Vacquier and Swanson 2011).…”

“…At least in the case of marine organisms, there now appears to be a consensus that these data can be explained in large part by selection for avoidance of polyspermy (Levitan et al 2007;Palumbi 2009;Lessios 2011;Vacquier and Swanson 2011). Sperm is under strong selection for increased efficiency in fertilizing eggs, but if more than one sperm penetrates the egg, the resulting zygote in usually inviable.…”

Crossing species boundaries : the hybrid histories of the true geese

“…There are several stages between insemination and copulation that may serve as barriers to heterospecific sperm Brillard, 2007, Eady, 2001): the transfer and storage of sperm may fail , the sperm may not be viable in the female reproductive tract (Gregory and Howard, 1994), the cross-attraction between sperm and egg may be lacking (Miller, 1997), or the gametes may be genetically incompatible (Palumbi, 1998, Vacquier, 1998.…”

“…The best studied form of gametic isolation is intrinsic gametic incompatibility, which is due to the failure of biochemical recognition mechanisms between heterospecific sperm and egg (Palumbi, 1998, Vacquier, 1998. These mechanisms have been studied extensively in the abalone genus Haliotus, in which successful fertilization depends on the complex interaction between the egg protein VERL ("Vitelline Envelope Receptor for Lysin") and the sperm protein lysin (Kresge et al, 2001).…”