Evolution Of Gamete Recognition Proteins Research Articles

Do Sperm Really Compete and Do Eggs Ever Have a Choice? Adult Distribution and Gamete Mixing Influence Sexual Selection, Sexual Conflict, and the Evolution of Gamete Recognition Proteins in the Sea.

The evolution of gametic compatibility and the effectiveness of compatibility, within and across species, depend on whether sperm from different males directly compete for an egg and whether eggs ever have a choice. Direct sperm competition and egg choice depend on whether sperm from different males arrive at an egg in the brief interval between first sperm contact and fertilization. Although this process may be relevant for all sexually reproducing organisms, it is most easily examined in aquatic external fertilizers. When sperm are released into the sea, packets of seawater at the spatial scale relevant to single eggs might contain sperm from only one male, eliminating the potential for direct sperm competition and egg choice. Field experiments and a simple heuristic model examining the degree of sperm mixing for the sea urchin Strongylocentrotus franciscanus indicate that degree of competitive fertilization depends on density and distribution of competing males and that the nature of this competition influences whether males with high- or low-affinity gamete recognition protein genotypes have higher reproductive success. These results provide a potential explanation for the generation and maintenance of variation in gamete recognition proteins and why effectiveness of conspecific sperm precedence can be density dependent.

Sperm competition and the evolution of gametic compatibility in externally fertilizing taxa.

Proteins expressed on the surface of sperm and egg mediate gametic compatibility and these proteins can be subject to intense positive selection. In this review, we discuss what is known about the patterns of adaptive evolution of gamete recognition proteins (GRPs). We focus on species that broadcast eggs and sperm into the environment for external fertilization, as the ease of observing and manipulating gamete interactions has allowed for greater advances in the understanding of GRP evolution, uncomplicated by confounding behavioral and physiological components that offer alternative evolutionary targets in internal fertilizers. We discuss whether interspecific mechanisms, such as selection to avoid fertilization between species (reinforcement selection), or intraspecific mechanisms, such as selection to increase (or decrease) the affinity between eggs and sperm based on the intensity of sperm competition, may be responsible for the pattern of GRP evolution observed. Variation in these proteins appears to influence gametic compatibility; GRP divergence among species is a better predictor of hybrid fertilization than neutral genetic markers and GRP variation within species predicts reproductive success among individuals within a population. Evidence suggests that sperm competition may play a large role in the evolution of gametic compatibility.

Adaptive Evolution of M3 Lysin—A Candidate Gamete Recognition Protein in the Mytilus edulis Species Complex

Marine invertebrate gamete recognition proteins (GRPs) are classic examples of rapid adaptive evolution of reproductive proteins, and hybridizing Mytilus blue mussels allow us to study the evolution of GRPs during speciation following secondary contact. Even with frequent hybridization, positive selection drives divergence of M7 lysin, one of the three Mytilus egg vitelline envelope (VE) lysins. Mytilus trossulus and M. edulis form a broad hybrid zone in the Canadian Maritimes and eastern Maine, isolated by strong (but partial) gamete incompatibility. M7 lysin, however, is an unlikely GRP controlling this gametic incompativility, as earlier studies showed either weak or no positive selection and extensive introgression between the two species. We used reverse transcriptase-polymerase chain reaction and cloned several alleles of M3 lysin, a potent VE lysin encoded by a nonhomologous gene whose evolution has not been studied. McDonald-Kreitman and HKA tests reveal strong positive selection, which PAML branch-site models detect in 19.7% of the codons. Protein structure predictions show that replacements map exclusively to one face of the carbohydrate recognition domain (CRD) of this C-type lectin, with codons under positive selection localizing to CRD regions known to control ligand specificity. Polymorphism/divergence analyses show that selective sweep has purged M. edulis but not M. trossulus of polymorphism, and unique to M3 is an absence of fixed substitutions and broad haplotype sharing between M. edulis and Mediterranean M. galloprovincialis. Taken together, these results suggest that different lysins serve as GRPs in different Mytilus hybrid zones, with M3 likely co-opted to play this role in the western Atlantic.

NATURAL HYBRIDIZATION IN THE SEA URCHIN GENUS PSEUDOBOLETIA BETWEEN SPECIES WITHOUT APPARENT BARRIERS TO GAMETE RECOGNITION

Marine species with high dispersal potential often have huge ranges and minimal population structure. Combined with the paucity of geographic barriers in the oceans, this pattern raises the question as to how speciation occurs in the sea. Over the past 20 years, evidence has accumulated that marine speciation is often linked to the evolution of gamete recognition proteins. Rapid evolution of gamete recognition proteins in gastropods, bivalves, and sea urchins is correlated with gamete incompatibility and contributes to the maintenance of species boundaries between sympatric congeners. Here, we present a counterexample to this general pattern. The sea urchins Pseudoboletia indiana and P. maculata have broad ranges that overlap in the Indian and Pacific oceans. Cytochrome oxidase I sequences indicated that these species are distinct, and their 7.3% divergence suggests that they diverged at least 2 mya. Despite this, we suspected hybridization between them based on the presence of morphologically intermediate individuals in sympatric populations at Sydney, Australia. We assessed the opportunity for hybridization between the two species and found that (1) individuals of the two species occur within a meter of each other in nature, (2) they have overlapping annual reproductive cycles, and (3) their gametes cross-fertilize readily in the laboratory and in the field. We genotyped individuals with intermediate morphology and confirmed that many were hybrids. Hybrids were fertile, and some female hybrids had egg sizes intermediate between the two parental species. Consistent with their high level of gamete compatibility, there is minimal divergence between P. indiana and P. maculata in the gamete recognition protein bindin, with a single fixed amino acid difference between the two species. Pseudoboletia thus provides a well-characterized exception to the idea that broadcast spawning marine species living in sympatry develop and maintain species boundaries through the divergence of gamete recognition proteins and the associated evolution of gamete incompatibility.

Evolutionary animation: how do molecular phylogenies compare to Mayr's reconstruction of speciation patterns in the sea?

Ernst Mayr used the geography of closely related species in various stages of increasing divergence to "animate" the process of geographic, or allopatric, speciation. This approach was applied to a wide set of taxa, and a seminal paper by Mayr used it to explore speciation patterns in tropical sea urchins. Since then, taxonomic information in several of these genera has been augmented by detailed molecular phylogenies. We compare Mayr's animation with the phylogenies of eight sea urchin genera placed by Mayr into four speciation groups. True to Mayr's predictions, early-stage genera have on average lower species divergence and more polytypic species than genera in later stages. For six of these genera, we also have information about the evolution of the gamete recognition protein bindin, which is critical to reproductive isolation. These comparisons show that later-stage genera with many sympatric species tend to be those with rapid bindin evolution. By contrast, early-stage genera with few sympatric species are not necessarily earlier in the divergence process; they happen to be those with slow rates of bindin evolution. These results show that the rate of speciation in sea urchins does not only depend on the steady accumulation of genome divergence over time, but also on the rate of evolution of gamete recognition proteins. The animation method used by Mayr is generally supported by molecular phylogenies. However, the existence of multiple rates in the acquisition of reproductive isolation complicates placement of different genera in an evolutionary series.

Positive Selection in the Carbohydrate Recognition Domains of Sea Urchin Sperm Receptor for Egg Jelly (suREJ) Proteins

A wealth of evidence shows that protein-carbohydrate recognition mediates the steps of gamete interaction during fertilization. Carbohydrate-recognition domains (CRDs) comprise a large family of ancient protein modules of approximately 120 amino acids, having the same protein fold, that bind terminal sugar residues on glycoproteins and polysaccharides. Sea urchin sperm express three suREJ (sea urchin receptor for egg jelly) proteins on their plasma membranes. suREJ1 has two CRDs, whereas suREJ2 and suREJ3 both have one CRD. suREJ1 binds the fucose sulfate polymer (FSP) of egg jelly to induce the sperm acrosome reaction. The structure of FSP is species specific. Therefore, the suREJ1 CRDs could encode molecular recognition between sperm and egg underlying the species-specific induction of the acrosome reaction. The functions of suREJ2 and suREJ3 have not been explored, but suREJ3 is exclusively localized on the plasma membrane over the sperm acrosomal vesicle and is physically associated with sea urchin polycystin-2, a known cation channel. An evolutionary analysis of these four CRDs was performed for six sea urchin species. Phylogenetic analysis shows that these CRDs were already differentiated in the common ancestor of these six sea urchins. The CRD phylogeny agrees with previous work on these species based on one nuclear gene and several mitochondrial genes. Maximum likelihood shows that positive selection acts on these four CRDs. Threading the suREJ CRDs onto the prototypic CRD crystal structure shows that many of the sites under positive selection are on extended loops, which are involved in saccharide binding. This is the first demonstration of positive selection in CRDs and is another example of positive selection acting on the evolution of gamete-recognition proteins.

Synopsis: 2003 Annual Meeting of the American Society of Andrology.

Synopsis: 2003 Annual Meeting of the American Society of Andrology.

Sexual selection at the protein level drives the extraordinary divergence of sex-related genes during sympatric speciation.

An increasing number of molecular studies are indicating that, in a wide variety of species, genes directly related to fertilization evolve at extraordinarily high rates. We try to gain insight into the dynamics of this rapid evolution and its underlying mechanisms by means of a simple theoretical model. In the model, sexual selection and sympatric speciation act together in order to drive rapid divergence of gamete recognition proteins. In this process, intraspecific competition for fertilizations enlarges male gamete protein variation by means of evolutionary branching, which initiates sympatric speciation. In addition, avoidance of competition for fertilizations between the incipient species drives the rapid evolution of gamete recognition proteins. This mechanism can account for both strong stabilizing selection on gamete recognition proteins within species and rapid divergence between species. Moreover, it can explain the empirical finding that the rate of divergence of fertilization genes is not constant, but highest between closely related species.

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.