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Synchronous multispecific spawning on coral reefs: potential for hybridization and roles of gamete recognition.

Problems of gamete recognition in corals and other mass-spawning invertebrates are potentially great. In 'mass spawnings', closely-related species or genera commonly spawn at the same time, or within 1 or 2 h of each other, increasing the potential for hybridization. Among mass-spawning corals, most of the species involved are hermaphrodites that package the gametes in buoyant bundles that float to the sea surface before breaking up. Local hydrodynamic features frequently act to aggregate gametes from many different species into slicks where both eggs and sperm can be viable for extended periods. Other mass-spawning invertebrate taxa, such as molluscs, polychaetes and various echinoderms, do not have buoyant gametes but also spawn with a high level of synchrony. Gametes of organisms participating in these spawning events must be able to successfully recognize conspecifics. If they cannot do this, either through sperm chemotaxis or by mechanisms at the level of sperm binding and penetration, there may be high levels of gamete wastage through hybridization. Alternatively, viable hybrids may be formed, a factor that could have contributed to the evolutionary history of mass-spawning taxa, as well as to the taxonomic difficulties that have plagued the taxonomy of groups such as reef-building corals. Within some mass-spawning taxa, pre-zygotic barriers to fertilization suggest relatively recent molecular evolution at gamete recognition loci.

Animals↗

Protein-carbohydrate complementarity in mammalian gamete recognition.

Recent studies suggest that gamete recognition in a number of species is mediated by complementary proteins and carbohydrates on opposing gamete surfaces. Studies in invertebrates and vertebrates have shown that carbohydrate-binding proteins on the sperm surface recognize and bind to complementary glycoconjugates on the egg's extracellular coat. This chapter reviews our current knowledge of gamete recognition in the mouse. The complementary receptors for both mouse sperm and egg have been identified, purified, and characterized. Their synthesis during gametogenesis has been defined, as have the effects of sperm capacitation and of the acrosome reaction on their expression and distribution. Their relationship to gamete receptors that function in other species is discussed. Finally, evidence is presented that suggests that one of the receptors that mediate mouse gamete recognition belongs to a family of cell surface receptors that function during multiple cellular interactions in development.

Animals↗

Genomic and Structural Analysis of Gamete Recognition Proteins in a Broadcast Spawning Echinoderm Mesocentrotus franciscanus.

Gamete recognition proteins are expressed on the surfaces of sperm and eggs, where they mediate interactions between gametes. The genetic basis for gamete recognition proteins, as well as their structure and interactions, have yet to be fully resolved. Using a new high-quality de novo genome assembly for the sea urchin Mesocentrotus franciscanus, we investigated the genomic structure, expression, and protein forms of several gamete recognition proteins: sperm bindin, egg receptor for sperm (HSP110), and egg bindin receptor (EBR1), as well as the receptor for egg jelly (REJ) and its paralogs. To inform future population genetic and evolutionary studies, we resolve the genomic structure of the large EBR1 protein, identifying fewer tandem CUB-TSP1 repeats in EBR1 compared to the initial characterization of this protein. As expected for an egg receptor for sperm, EBR1 is highly expressed in female reproductive tissues (eggs and female gonad), compared to other tissues. In contrast, HSP110 shows similar levels of expression across male and female reproductive tissues, as well as across non-reproductive tissues and development stages. HSP110 might be a pleiotropic gene that in part influences fertilization. Using protein structural modeling and functional domain predictions, we propose hypotheses about potential interactions among EBR1, bindin, and HSP110 proteins that may provide insight into sperm-egg interactions in sea urchins. Resolving the genomic structure of genes encoding gamete recognition proteins, in combination with functional annotations and protein structural modeling, enables deeper investigation into the consequences of variation in gamete recognition proteins and the evolution of reproductive isolation.

Mesocentrotus franciscanus↗

Positive selection and sequence rearrangements generate extensive polymorphism in the gamete recognition protein bindin.

Bindin is a gamete recognition protein of sea urchins that mediates species-specific attachment of sperm to an egg-surface receptor during fertilization. Sequences of bindin from closely related urchins show fixed species-specific differences. Within species, highly polymorphic bindin alleles result from point substitution, insertion/deletion, and recombination. Since speciation, positive selection favoring allelic variants has generated diversity in bindin polypeptides. Intraspecific bindin variation can be tolerated by the egg receptor, which suggests functional parallels between this system and other flexible recognition systems, including immune recognition. These results show that polymorphism in mate recognition loci required for rapid evolution of sexual isolation can arise within natural populations.

Alleles↗

Gamete recognition: sperm proteins that interact with the egg zona pellucida.

The gamete recognition and initial binding processes that are crucial for the success of mammalian fertilization are mediated by moieties associated with the extracellular matrix of the egg (the zona pellucida) and the head of the fertilizing spermatozoon. The zona proteins involved have been characterized in some detail, with ZP3 and ZP2 generally acknowledged to be responsible for the initial (primary) and secondary interactions, respectively. However, the identity of the complementary molecules on the sperm surface is highly contentious and remains unresolved. This review summarizes the current knowledge and controversies in this research area. The credentials of some of the major candidates and the probability of the involvement of multiple sperm receptors with different binding characteristics are assessed. Resolving this very important gap in our understanding is an essential prerequisite to understanding fully the molecular and signal transduction events that cause sperm acrosomal exocytosis. Such fundamental information is also imperative for the development of novel forms of contraception (or sterilization) targeted against specific sperm epitopes. Moreover, this information may contribute to our understanding of certain types of male infertility.

Acrosome Reaction↗

Evolution of gamete recognition proteins.

REVIEW Although fertilization has been studied for more than a century, the cell surface proteins mediating the process are only now becoming known. Gamete interaction in animals appears to be molecularly complex. Although it is difficult to generalize at present, diversity of structure may be a recurring theme in the evolution of fertilization proteins. Examples of rapid evolution of fertilization proteins by positive selection are known, and concerted evolution can influence the differentiation of gamete recognition proteins between closely related species.

Animals↗

Role of sperm-surface glycoproteins in gamete recognition in two mouse species.

In-vitro fertilization and sperm binding to the zona pellucida within and between Mus musculus (laboratory mouse) and Mus caroli (Asian wild field mouse) were examined. Maximum homologous sperm binding in M. musculus was 12.3 +/- 0.3 spermatozoa bound/egg and in M. caroli, 9.2 +/- 0.2. In heterologous crosses, sperm-zona binding was significantly reduced (M. musculus eggs with M. caroli spermatozoa, 1.9 +/- 0.14; M. caroli eggs with M. musculus spermatozoa, 5.5 +/- 0.2). Homologous sperm-zona interaction was inhibited by different sugars in the two mouse species (M. caroli by alpha-methyl mannose, M. musculus by sialic acid). The data suggest that gamete recognition is highly species specific and that hapten sugars play a significant role in sperm-zona binding.

Animals↗

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

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.

Alleles↗

Fertilization in brown algae. II. Evidence for lectin-sensitive complementary receptors involved in gamete recognition in Fucus serratus.

Fertilization in Fucus serratus is directly proportional to the number of sperm added, saturating at approximately 250 sperm per egg with an apparent Km of 120 sperm per egg. The effect of a range of lectins on fertilization has been tested. Preincubation of gametes with Con A and fucose-binding protein (FBP) inhibited fertilization. At low concentrations this was by specifically binding to eggs; at high concentrations pretreatment of either gametes inhibited fertilization probably due to cytotoxicity. Fertilization was not inhibited by simple sugar haptens, but polysaccharides containing fucosyl or mannosyl residues (yeast mannan, fucoidan, ascophyllan) inhibited fertilization by binding to sperm. Pretreatment of eggs with alpha-fucosidase or alpha-mannosidase was effective in inhibiting fertilization. All the results indirectly demonstrate that fertilization in Fucus serratus is based on an association between fucosyl- and mannosyl-containing ligands on the egg surface and specific carbohydrate-binding receptors on the sperm surface.

Carbohydrates↗

Members of the 70 kDa heat shock protein family specifically recognize sulfoglycolipids: role in gamete recognition and mycoplasma-related infertility.

We have previously shown that several mycoplasma species associated with infertility bind specifically to sulfated glycolipids isolated from the mammalian reproductive tract. We now show that a germ cell-specific sulfoglycolipid binding protein (SLIP 1), which is a potent inhibitor of sperm/egg binding in vitro, is immunologically related to the heat shock protein(Hsp) 70 family of stress proteins and that Hsps are surface antigens in male germ cells. Our present data demonstrate that several mycoplasma and mammalian Hsps share this glycolipid binding specificity in vitro, and suggest that surface Hsps can function as adhesins which mediate sulfoglycolipid recognition in infectious disease and normal reproductive physiology.

Animals↗

Molecular mechanisms of gamete recognition and fusion at fertilization.

Advances in many areas of reproductive technology have been rapid and, in many respects, have outstripped our knowledge of the fundamental processes of human and animal sperm-egg interactions at fertilization. This is particularly true of human fertilization, where the availability of eggs for research purposes is severely restricted. As a consequence of this, most of the significant advances in our understanding of mammalian fertilization have resulted from studies on animals, particularly the mouse. This review summarizes our current knowledge of the molecular aspects of mammalian fertilization from the point of view of the fertilizing spermatozoon. Particular reference is made to those advances in our knowledge of human fertilization mechanisms. Further understanding of the molecular basis of human fertilization is of paramount importance for the development of new methods of contraception and also for the rational diagnosis and treatment of certain forms of infertility.

Acrosome↗

[Gamete recognition in mammals: sperm and zona pellucida interactions].

Association of sperm with the acellular protective envelope of the oocyte, the zona pellucida, and their penetration is a determinant step in fertilization process. It is at this stage that species barriers take place to prevent cross fertilizations. This association is dependent upon binding of ZP3 oligosaccharides to specific sperm receptors. Their activation triggers the acrosome reaction via transduction pathways and release of proteolytic enzymes that dissociate the zona pellucida network. Then, secondary binding to zona pellucida components allows sperm to penetrate and cross the zona pellucida barrier. Several sperm surface proteins are putative receptors for zona pellucida partners. Repercussion of these studies on human fertility are discussed.

Acrosin↗

The species recognition system: a new corollary for the human fetoembryonic defense system hypothesis.

We have previously suggested that the human fetus is protected during human development by a system of both soluble and cell surface associated glycoconjugates that utilize their carbohydrate sequences as functional groups to enable them to evoke tolerance. The proposed model has been referred to as the human fetoembryonic defense system hypothesis (hu-FEDS). In this paradigm, it has previously been proposed that similar oligosaccharides are used to mediate crucial recognition events required during both human sperm-egg binding and immune-inflammatory cell interactions. This vertical integration suggested to us that the sperm-egg binding itself is related to universal recognition events that occur between immune and inflammatory cells, except that in this case recognition of 'species' rather than recognition of 'self' is being manifested. In this paper, we have designated this component of hu-FEDS as the species recognition system (SRS). We propose that the SRS is an integral component of the hu-FEDS used to enable sperm-egg recognition and protection of the gametes from potential immune responses. Recent structural data indicates that the glycan sequences implicated in mediating murine gamete recognition are also expressed on CD45 in activated murine T lymphocytes and cytotoxic T lymphocytes. This overlap supports our contention that there is an overlap between the immune and gamete recognition systems. Therefore the hu-FEDS paradigm may be a subset of a larger model that also applies to other placental mammals. We therefore propose that the hu-FEDS model for protection should in the future be referred to as the eutherian fetoembryonic defense system hypothesis (eu-FEDS) to account for this extension. The possibility exists that the SRS component of eu-FEDS could predate eutherians and extend to all sexually reproducing organisms. Future investigation of the interactions between the immune and gamete recognition system will be required to determine the degree of overlap.

Embryo, Mammalian↗