All males are not created equal: Fertility differences depend on gamete recognition polymorphisms in sea urchins

Abstract

Behaviors, morphologies, and genetic loci directly involved in reproduction have been increasingly shown to be polymorphic within populations. Explaining how such variants are maintained by selection is crucial to understanding the genetic basis of fertility differences, but direct tests of how alleles at reproductive loci affect fertility are rare. In the sea urchin genus Echinometra, the protein bindin mediates sperm attachment to eggs, evolves quickly, and is polymorphic within species. Eggs exposed to experimental sperm mixtures show strong discrimination on the basis of the males' bindin genotype. Different females produce eggs that nonrandomly select sperm from different males, showing that variable egg-sperm interactions determine fertility. Eggs select sperm with a bindin genotype similar to their own, suggesting strong linkage between female choice and male trait loci. These experiments demonstrate that alleles at a single locus can have a strong effect on fertilization and that reproductive loci may retain functional polymorphisms through epistatic interactions between male and female traits. They also suggest that positive selection at gamete recognition loci like bindin involves strong selection within species on mate choice interactions.

Natural and sexual selection against hybrid flycatchers

“…However, the increased levels of extra-pair young may partly be caused by hybrid sperm inviability or sperm incompatibility (e.g. Wade et al 1994;Price 1997;Birkhead 1998;Hellberg & Vacquier 1999;Palumbi 1999), or perhaps an early embryonic death of backcross offspring. We did not detect any reduction in male hybrid fitness through sexual selection through female fecundity (here estimated by clutch size).…”

Female polymorphisms, sexual conflict and limits to speciation processes in animals

“…However, we should expect to find such polymorphisms, given the presence of additive genetic variation for female resistance to male mating attempts (see above) and molecular evidence for allelic polymorphisms at reproductive loci in both males and females (Palumbi 1999). It is important to underscore that sexual polymorphisms may not always be possible to detect visually, but may be cryptic and only detectable by molecular analyses of the underlying reproductive loci.…”

“…It is important to underscore that sexual polymorphisms may not always be possible to detect visually, but may be cryptic and only detectable by molecular analyses of the underlying reproductive loci. For instance, studies of the molecular basis of gamete recognition loci in the sea urchin genus Echinometra have revealed extensive polymorphisms in traits important to fertilization success among male sperm haplotypes (Palumbi 1999). It seems likely that there may be additional hidden phenotypic differences among female genotypes in their reproductive performance.…”

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

“…The cycle could continue, possibly producing round after round of directional selection on egg and sperm. Experiments on assortative mating based on egg and sperm genotypes showed that this mechanism was plausible (Palumbi, 1999). But this mechanism requires a continuous generation of novel alleles of the receptor, new mutation of the sperm genes to match them and replacement of the old alleles by the new.…”

“…) urchins, bindin genes show a very different pattern, with a large amount of polymorphism within species as well as large differences between them. For example, in the Hawaiian sea urchin E. mathaei, there are at least five major clades of bindin alleles (Figure 2; see also Palumbi, 1999). Controlled crosses in which males homozygous for bindin clades A and B compete for access to eggs show that these different alleles confer different fertilization abilities (Palumbi, 1999).…”