Selection for High Gamete Encounter Rates Explains the Success of Male and Female Mating Types

Abstract

Sexual reproduction occurs in many small eukaryotes by fusion of similar gametes (isogamy). In the absence of distinguishable sperm and eggs, male and female mating types are missing. However, species with distinct males and females have so prospered that almost all familiar plants and animals have these mating types. Why has sexual reproduction involving sperm and eggs been so successful? An answer is obtained by considering physical limitations on encounter rates between gametes. A biophysical model based on well-established relationships produces "tness landscapes for the evolution of gamete size and energy allocation between motility and pheromone production. These landscapes demonstrate that selection for high gamete encounter rates favors large, pheromone-producing eggs and small, motile sperm. Thus, broadcast-spawning populations with males and females can reproduce at lower population densities and survive under conditions where populations lacking males and females go extinct. It appears that physical constraints on gamete encounter rates are su$cient to explain the "rst two steps in the isogamyPanisogamyPoogamyPinternal fertilization evolutionary sequence observed in several lineages of the eukaryotes. Unlike previous models, assumptions concerning zygote "tness or decreasing speed of swimming with increasing gamete size are not required.

A comparative test of a theory for the evolution of anisogamy

“…Assuming isogamy is the ancestral condition we can ask why did the gametes change in relative size? A number of theories have been presented (Parker et al 1972;Cosmides & Tooby 1981;Hoekstra 1982;Cox & Sethian 1985;Dusenbery 2000) (for a review see Hoekstra 1987). Here we test the dominant explanation for the evolution of gamete dimorphism (Parker et al 1972;Maynard Smith 1978;Bulmer 1994).…”

Ecological Models Explaining the Success of Distinctive Sperm and Eggs (Oogamy)

“…Contrary claims (Hoekstra, 1984(Hoekstra, , 1987 are based on unreasonably throwing out the volume/number trade-off for gametes. It has been argued (Dusenbery, 2000;Dusenbery & Snell, 1995) that the best assumption for the relation between swimming speed and sperm size is direct proportionality, but this assumption has been criticized (Randerson & Hurst, 2001). In any case, it is clear that this assumption is not necessary in the pheromone model (Table 1FPheromone; Dusenbery, 2000).…”

“…It has been argued (Dusenbery, 2000;Dusenbery & Snell, 1995) that the best assumption for the relation between swimming speed and sperm size is direct proportionality, but this assumption has been criticized (Randerson & Hurst, 2001). In any case, it is clear that this assumption is not necessary in the pheromone model (Table 1FPheromone; Dusenbery, 2000). In fact, Dusenbery's assumption makes selection for dimorphism more difficult.…”

“…A variety of other explanations have been proposed over several decades (Charlesworth, 1978;Cox & Sethian, 1985;Dusenbery, 2000;Hoekstra, 1984;Hoekstra et al, 1984;Parker et al, 1972;Schuster & Sigmund, 1982;Scudo, 1967), but disagreement about their plausibility and misunderstanding of their underlying assumptions continues. Most alternative explanations are ecological in the sense that they focus on allocation of resources, selection on size, and/or behavioral interactions between gametes.…”

The role of structured stirring and mixing on gamete dispersal and aggregation in broadcast spawning

“…Once released into the water column, sperm and ova may coalesce as a result of passive transport by turbulence, or by active sperm swimming. Models and experiments suggest that a combination of large, pheromoneproducing eggs and small, motile sperm increases gamete encounter rates (Dusenbery, 2000;Dusenbery, 2002;Podolsky, 2001;Podolsky, 2002). Turbulent stirring and mixing produces long-term dilution of gamete concentrations (Csanady, 1973;Denny et al, 1992), but the dilution may be mitigated by releasing gametes in a viscous matrix (Thomas, 1994a;Marshall, 2002;Yund and Meidel, 2003), or through gamete sequestration in surge channels (Denny et al, 1992) and tide pools (Pearson and Brawley, 1996).…”