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Willie J Swanson

Publications and source records attributed to Willie J Swanson.

At least 19 recordsLinked to original sources

Rapidly evolving zona pellucida domain proteins are a major component of the vitelline envelope of abalone eggs.

Proteins harboring a zona pellucida (ZP) domain are prominent components of vertebrate egg coats. Although less well characterized, the egg coat of the non-vertebrate marine gastropod abalone (Haliotis spp.) is also known to contain a ZP domain protein, raising the possibility of a common molecular basis of metazoan egg coat structures. Egg coat proteins from vertebrate as well as non-vertebrate taxa have been shown to evolve under positive selection. Studied most extensively in the abalone system, coevolution between adaptively diverging egg coat and sperm proteins may contribute to the rapid development of reproductive isolation. Thus, identifying the pattern of evolution among egg coat proteins is important in understanding the role these genes may play in the speciation process. The purpose of the present study is to characterize the constituent proteins of the egg coat [vitelline envelope (VE)] of abalone eggs and to provide preliminary evidence regarding how selection has acted on VE proteins during abalone evolution. A proteomic approach is used to match tandem mass spectra of peptides from purified VE proteins with abalone ovary EST sequences, identifying 9 of 10 ZP domain proteins as components of the VE. Maximum likelihood models of codon evolution suggest positive selection has acted among a subset of amino acids for 6 of these genes. This work provides further evidence of the prominence of ZP proteins as constituents of the egg coat, as well as the prominent role of positive selection in diversification of these reproductive proteins.

Adaptation, Biological↗

Molecular population genetics of the gene encoding the human fertilization protein zonadhesin reveals rapid adaptive evolution.

A hallmark of positive selection (adaptive evolution) in protein-coding regions is a d(N)/d(S) ratio >1, where d(N) is the number of nonsynonymous substitutions/nonsynonymous sites and d(S) is the number of synonymous substitutions/synonymous sites. Zonadhesin is a male reproductive protein localized on the sperm head, comprising many domains known to be involved in cell-cell interaction or cell adhesion. Previous studies have shown that VWD domains (homologous to the D domains of the von Willebrand factor) are involved directly in binding to the female zona pellucida (ZP) in a species-specific manner. In this study, we sequenced 47 coding exons in 12 primate species and, by using maximum-likelihood methods to determine sites under positive selection, we show that VWD2, membrane/A5 antigen mu receptor, and mucin-like domains in zonadhesin are rapidly evolving and, thus, may be involved in binding to the ZP in a species-specific manner in primates. In addition, polymorphism data from 48 human individuals revealed significant polymorphism-to-divergence heterogeneity and a significant departure from equilibrium-neutral expectations in the frequency spectrum, suggesting balancing selection and positive selection occurring in zonadhesin (ZAN) within human populations. Finally, we observe adaptive evolution in haplotypes segregating for a frameshift mutation that was previously thought to indicate that ZAN was a potential pseudogene.

Animals↗

Molecular evolution and population genetic analysis of candidate female reproductive genes in Drosophila.

Molecular analyses in several taxa have consistently shown that genes involved in reproduction are rapidly evolving and subjected to positive selection. The mechanism behind this evolution is not clear, but several proposed hypotheses involve the coevolution between males and females. In Drosophila, several male reproductive proteins (Acps) involved in male-male and male-female interactions show evidence of rapid adaptive evolution. What has been missing from the Drosophila literature is the identification and analysis of female reproductive genes. Recently, an evolutionary expressed sequence tag analysis of Drosophila female reproductive tract genes identified 169 candidate female reproductive genes. Many of these candidate genes still await further molecular analysis and independent verification of positive selection. Our goal was to expand our understanding of the molecular evolution of Drosophila female reproductive genes with a detailed polymorphism and divergence study on seven additional candidate female reproductive genes and a reanalysis of two genes from the above study. We demonstrate that 6 candidate female genes of the 9 genes surveyed show evidence of positive selection using both polymorphism and divergence data. One of these proteins (CG17012) is modeled to reveal that the sites under selection fall around and within the active site of this protease, suggesting potential differences between species. We discuss our results in light of potential function as well as interaction with male reproductive proteins.

Animals↗

Molecular evolution of seminal proteins in field crickets.

In sexually reproducing organisms, male ejaculates are complex traits that are potentially subject to many different selection pressures. Recent experimental evidence supports the hypothesis that postmating sexual selection, and particularly sexual conflict, may play a key role in the evolution of the proteinaceous components of ejaculates. However, this evidence is based almost entirely on the study of Drosophila, a species with a mating system characterized by a high cost of mating for females. In this paper, we broaden our understanding of the role of selection on the evolution of seminal proteins by characterizing these proteins in field crickets, a group of insects in which females appear to benefit from mating multiply. We have used an experimental protocol that can be applied to other organisms for which complete genome sequences are not yet available. By combining an evolutionary expressed sequence tag screen of the male accessory gland in 2 focal species (Gryllus firmus and Gryllus pennsylvanicus) with a bioinformatics approach, we have been able to identify as many as 30 seminal proteins. Evolutionary analyses among 5 species of the genus Gryllus suggest that seminal protein genes evolve more rapidly than genes encoding proteins that are not involved with reproduction. The rates of synonymous substitution (dS) are similar in genes encoding seminal proteins and genes encoding "housekeeping" proteins. For the same comparison, the rate of fixation of nonsynonymous substitutions (dN) is 3 times higher in genes encoding seminal proteins, suggesting that the divergence of seminal proteins in field crickets has been accelerated by positive Darwinian selection. In spite of the contrasting characteristics of the Drosophila and Gryllus mating systems, the mean selection parameter omega and the proportion of loci estimated to be affected by positive selection are very similar.

Analysis of Variance↗

TRPV6 exhibits unusual patterns of polymorphism and divergence in worldwide populations.

A striking footprint of positive selection was recently identified on chromosome 7q34-35 that spans at least 115 kb and encompasses four known genes (KEL, TRPV5, TRPV6, EPHB6). The signature of selection was observed in only one of the two populations analyzed suggesting the action of geographically restricted selective pressures. However, as only two populations were analyzed, it remains unknown whether the signature of selection extends to additional populations. To address this issue and begin to dissect the evolutionary history of this region in more detail, we performed an in-depth population genetic analysis on TRPV6, which is a calcium-permeable ion channel thought to mediate the rate-limiting step of dietary calcium absorption. We demonstrate that the rate of TRPV6 protein evolution is significantly accelerated in the human lineage, but only for a haplotype defined by three non-synonymous SNPs (C157R, M378V and M681T) that are nearly fixed for the derived alleles in non-African populations. Interestingly, we found that these three non-synonymous SNPs have high posterior probabilities for being targets of positive selection and are therefore strong candidates for mediating the population-specific signatures of selection in this region. In addition, we resequenced the exons corresponding to the C157R, M378V and M681T polymorphisms in 90 geographically diverse individuals and characterized their global allele frequency distribution by genotyping them in 1064 individuals from 52 populations. These data strongly suggest that the TRPV6 haplotype defined by the derived alleles at C157R, M378V and M681T conferred a selective advantage that varied spatially, and perhaps temporally, during human history.

Calcium Channels↗

Rapid evolution of reproductive proteins in abalone and Drosophila.

Observations from different taxa, including plants, protozoa, insects and mammals, indicate that proteins involved in reproduction evolve rapidly. Several models of adaptive evolution have been proposed to explain this phenomenon, such as sexual conflict, sexual selection, self versus non-self recognition and pathogen resistance. Here we discuss the potential role of sexual conflict in the rapid evolution of reproductive genes in two different animal systems, abalone (Haliotis) and Drosophila. In abalone, we reveal how specific interacting sperm-egg proteins were identified and discuss this identification in the light of models for rapid protein evolution and speciation. For Drosophila, we describe the genomic approaches taken to identify male accessory gland proteins and female reproductive tract proteins. Patterns of protein evolution from both abalone and Drosophila support the predicted patterns of rapid protein evolution driven by sexual conflict. We stress however that other selective pressures may contribute to the rapid evolution that is observed. We conclude that the key to distinguishing between sexual conflict and other mechanisms of protein evolution will be an integration of genetic, experimental and theoretical data.

Animals↗

Identification and comparative analysis of accessory gland proteins in Orthoptera.

Accessory reproductive gland proteins (Acps) in Drosophila evolve quickly and appear to play an important role in ensuring the fertilization success of males. Moreover, Acps are thought to be involved in establishing barriers to fertilization between closely related species. While accessory glands are known to occur in the males of many insect groups, the proteins that are passed on to females by males during mating have not been well characterized outside of Drosophila. To gain a better understanding of these proteins, we characterized ESTs from the accessory glands of two cricket species, Allonemobius fasciatus and Gryllus firmus. Using an expressed sequence tag (EST) approach, followed by bioinformatic and evolutionary analyses, we found that many proteins are secreted and, therefore, available for transfer to the female during mating. Further, we found that most ESTs are novel, showing little sequence similarity between taxa. Evolutionary analyses suggest that cricket proteins are subject to diversifying selection and indicate that Allonemobius is much less polymorphic than Gryllus. Despite rapid nucleotide sequence divergence, there appears to be functional conservation of protein classes among Drosophila and cricket taxa.

Amino Acid Sequence↗

Evolution of reproductive proteins from animals and plants.

Sexual reproduction is a fundamental biological process common among eukaryotes. Because of the significance of reproductive proteins to fitness, the diversity and rapid divergence of proteins acting at many stages of reproduction is surprising and suggests a role of adaptive diversification in reproductive protein evolution. Here we review the evolution of reproductive proteins acting at different stages of reproduction among animals and plants, emphasizing common patterns. Although we are just beginning to understand these patterns, by making comparisons among stages of reproduction for diverse organisms we can begin to understand the selective forces driving reproductive protein diversity and the functional consequences of reproductive protein evolution.

Animals↗

Speciation in birds: genes, geography, and sexual selection.

Molecular studies of speciation in birds over the last three decades have been dominated by a focus on the geography, ecology, and timing of speciation, a tradition traceable to Mayr's Systematics and the Origin of Species. However, in the recent years, interest in the behavioral and molecular mechanisms of speciation in birds has increased, building in part on the older traditions and observations from domesticated species. The result is that many of the same mechanisms proffered for model lineages such as Drosophila--mechanisms such as genetic incompatibilities, reinforcement, and sexual selection--are now being seriously entertained for birds, albeit with much lower resolution. The recent completion of a draft sequence of the chicken genome, and an abundance of single-nucleotide polymorphisms on the autosomes and sex chromosomes, will dramatically accelerate research on the molecular mechanisms of avian speciation over the next few years. The challenge for ornithologists is now to inform well studied examples of speciation in nature with increased molecular resolution-to clone speciation genes if they exist--and thereby evaluate the relative roles of extrinsic, intrinsic, deterministic, and stochastic causes for avian diversification.

Animals↗

Adaptive evolution in the SRZ chemoreceptor families of Caenorhabditis elegans and Caenorhabditis briggsae.

We investigated the possibility of positive selection acting on members of the putative seven-pass chemoreceptor superfamily in Caenorhabditis elegans, which comprises approximately 1,300 genes encoding seven-pass G protein-coupled receptors (GPCRs). Using a maximum-likelihood approach, we conducted statistical tests for evidence of codon sites where the ratio of nonsynonymous substitutions per nonsynonymous site to synonymous substitutions per synonymous site (d(N)/d(S)) was >1. Evidence for positive selection was found only for the srz family, about which virtually nothing specific is known. We extended the annotation of the srz gene family, establishing gene models for 60 srz genes in C. elegans and 28 srz genes in Caenorhabditis briggsae. d(N)/d(S) ratios varied dramatically in different regions of the SRZ proteins, peaking in predicted extracellular regions. These regions included 23 sites where evidence of positive selection was highly significant, corresponding remarkably well with regions implicated in ligand binding in other GPCR family members. We interpret these results as indicating that the srz family is under positive selection, probably driven by ligand binding.

Adaptation, Physiological↗

Pervasive adaptive evolution in primate seminal proteins.

Seminal fluid proteins show striking effects on reproduction, involving manipulation of female behavior and physiology, mechanisms of sperm competition, and pathogen defense. Strong adaptive pressures are expected for such manifestations of sexual selection and host defense, but the extent of positive selection in seminal fluid proteins from divergent taxa is unknown. We identified adaptive evolution in primate seminal proteins using genomic resources in a tissue-specific study. We found extensive signatures of positive selection when comparing 161 human seminal fluid proteins and 2,858 prostate-expressed genes to those in chimpanzee. Seven of eight outstanding genes yielded statistically significant evidence of positive selection when analyzed in divergent primates. Functional clues were gained through divergent analysis, including several cases of species-specific loss of function in copulatory plug genes, and statistically significant spatial clustering of positively selected sites near the active site of kallikrein 2. This study reveals previously unidentified positive selection in seven primate seminal proteins, and when considered with findings in Drosophila, indicates that extensive positive selection is found in seminal fluid across divergent taxonomic groups.

Animals↗

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.

Animals↗

A perforin-like protein from a marine mollusk.

Abalone (gastropod mollusks) express a protein, abMpeg1, which is a homolog of two mammalian proteins that share homology with mammalian perforin, a cytolytic and immune-regulatory protein of lymphocytes. One of the mammalian proteins, Mpeg1, is expressed in mature macrophage and prion-infected mouse brains, while the other, Epcs50, is expressed in ectoplacental cone cells of the invading placenta. Although the functions of these three proteins remain unknown, their structural similarity to mammalian perforin suggests that they may be involved in cell killing, the inflammatory response or tissue invasion. Consistent with these proposed functions, the Mpeg1 gene family shows the signature of positive Darwinian selection (adaptive evolution). The perforin-homology domain of abMpeg1 contains the cytolytic "helix-turn-helix" domain of perforin, supporting the idea that abMpeg1 is a cytolytic protein of the abalone innate immune system. The alpha-helices of abMpeg1 are amphipathic as are those of perforin. The conservation among abMpeg1, mammalian Mpeg1, and Epcs50 shows that Mpeg1 proteins represent a novel, ancient protein family of probable immunological function.

Amino Acid Sequence↗

Evolutionary expressed sequence tag analysis of Drosophila female reproductive tracts identifies genes subjected to positive selection.

Genes whose products are involved in reproduction include some of the fastest-evolving genes found within the genomes of several organisms. Drosophila has long been used to study the function and evolutionary dynamics of genes thought to be involved in sperm competition and sexual conflict, two processes that have been hypothesized to drive the adaptive evolution of reproductive molecules. Several seminal fluid proteins (Acps) made in the Drosophila male reproductive tract show evidence of rapid adaptive evolution. To identify candidate genes in the female reproductive tract that may be involved in female-male interactions and that may thus have been subjected to adaptive evolution, we used an evolutionary bioinformatics approach to analyze sequences from a cDNA library that we have generated from Drosophila female reproductive tracts. We further demonstrate that several of these genes have been subjected to positive selection. Their expression in female reproductive tracts, presence of signal sequences/transmembrane domains, and rapid adaptive evolution indicate that they are prime candidates to encode female reproductive molecules that interact with rapidly evolving male Acps.

Animals↗

Positive selection in the egg receptor for abalone sperm lysin.

The mechanism of speciation is a central problem in evolutionary biology. In free-spawning animals with no complex mating behavior, prezygotic reproductive isolation (speciation) could result from the rapid divergence of genes coding for sperm and egg proteins that bind each other during fertilization. In abalone, sperm lysin evolves rapidly by positive Darwinian selection. The egg vitelline envelope receptor for lysin had previously been shown to evolve neutrally and be subjected to concerted evolution. Several mathematical simulations predict that both male and female reproductive proteins should evolve rapidly by positive selection. Here we report that the sequence diversity of the amino-terminal end of the egg vitelline envelope receptor for lysin has been promoted by positive Darwinian selection. These data provide molecular support for theoretical models showing that the two sexes are locked in a "coevolutionary chase" that could be driven by processes such as sexual selection, sexual conflict, or microbial attack (pathogen avoidance). The result of this continuous coevolution of the gamete recognition system could be the splitting of one population into two that are reproductively isolated (speciation).

Animals↗

Adaptive evolution of genes and gene families.

The huge influx of genomic sequence and new statistical methods is making the discovery of genes subjected to adaptive evolution increasingly common. The use of comparative genomics to identify adaptive evolution is resulting in predictions of functionally important genes and gene regions. However, the selective pressure driving the adaptive evolution of most genes remains mysterious.

Adaptation, Physiological↗

Pervasive adaptive evolution in mammalian fertilization proteins.

Mammalian fertilization exhibits species specificity, and the proteins mediating sperm-egg interactions evolve rapidly between species. In this study, we demonstrate that the evolution of seven genes involved in mammalian fertilization is promoted by positive Darwinian selection by using likelihood ratio tests (LRTs). Several of these proteins are sperm proteins that have been implicated in binding the mammalian egg coat zona pellucida glycoproteins, which were shown previously to be subjected to positive selection. Taken together, these represent the major candidates involved in mammalian fertilization, indicating positive selection is pervasive amongst mammalian reproductive proteins. A new LRT is implemented to determine if the d(N)/d(S) ratio is significantly greater than one. This is a more refined test of positive selection than the previous LRTs which only identified if there was a class of sites with a d(N)/d(S) ratio >1 but did not test if that ratio was significantly greater than one.

Animals↗