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.
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.adaptive evolution ͉ egg coat proteins ͉ gamete recognition M etazoan eggs are surrounded by a fibrous coat referred to as the zona pellucida, as the vitelline or perivitelline envelope, or as the chorion. The constituent proteins of these structures, which we collectively refer to as egg coats, have been well characterized among vertebrate taxa, including species of mammals (1), teleost fish (2), amphibians (3), and birds (4). These studies show the principle constituents of vertebrate egg coats to be glycosylated proteins sharing a common structural motif of Ϸ260 aa known as the zona pellucida (ZP) domain. ZP domain proteins are found among diverse eukaryotic structures, facilitating protein polymerization through intramolecular disulfide bonds among conserved cysteine resides within the ZP domain (5). For example, the predominant model of mouse egg coat (zona pellucida) formation posits filaments of arrays of two ZP proteins (ZP2 and ZP3) crosslinked via a third (ZP1), resulting in a fibrous matrix completely enclosing the egg (1). Although orthologs of these mammalian proteins are known from egg coat structures across vertebrate lineages (6, 7), non-vertebrate taxa are less well studied and it is not yet clear whether ZP proteins are similarly prominent features of egg coats across metazoans. For example, all known proteins comprising Drosophila egg coat structures lack ZP domains (8). However, a large glycoprotein from the egg coat [vitelline envelope (VE)] of the m...
Identifying fertilization molecules is key to our understanding of reproductive biology, yet only a few examples of interacting sperm and egg proteins are known. One of the best characterized comes from the invertebrate archeogastropod abalone (Haliotis spp.), where sperm lysin mediates passage through the protective egg vitelline envelope (VE) by binding to the VE protein vitelline envelope receptor for lysin (VERL). Rapid adaptive divergence of abalone lysin and VERL are an example of positive selection on interacting fertilization proteins contributing to reproductive isolation. Previously, we characterized a subset of the abalone VE proteins that share a structural feature, the zona pellucida (ZP) domain, which is common to VERL and the egg envelopes of vertebrates. Here, we use additional expressed sequence tag sequencing and shotgun proteomics to characterize this family of proteins in the abalone egg VE. We expand 3-fold the number of known ZP domain proteins present within the VE (now 30 in total) and identify a paralog of VERL (vitelline envelope zona pellucida domain protein [VEZP] 14) that contains a putative lysin-binding motif. We find that, like VERL, the divergence of VEZP14 among abalone species is driven by positive selection on the lysin-binding motif alone and that these paralogous egg VE proteins bind a similar set of sperm proteins including a rapidly evolving 18-kDa paralog of lysin, which may mediate sperm-egg fusion. This work identifies an egg coat paralog of VERL under positive selection and the candidate sperm proteins with which it may interact during abalone fertilization.
Conspecific pollen precedence (CPP) is a major component of reproductive isolation between many flowering plant taxa and may reveal mechanisms of gametophytic evolution within species, but little is known about the genetic basis and evolutionary history of CPP. We systematically investigated the genetic architecture of CPP using patterns of transmission ratio distortion (TRD) in F2 and backcross hybrids between closely related species of Mimulus (Phrymaceae) with divergent mating systems. We found that CPP in Mimulus hybrids was polygenic and was the majority source of interspecific TRD genome-wide, with at least eight genomic regions contributing to the transmission advantage of M. guttatus pollen grains on M. guttatus styles. In aggregate, these male-specific transmission ratio distorting loci (TRDLs) were more than sufficient to account for the 100% precedence of pure M. guttatus pollen over M. nasutus pollen in mixed pollinations of M. guttatus. All but one of these pollen TRDLs were styledependent; that is, we observed pollen TRD in F 1 and/or M. guttatus styles, but not in M. nasutus styles. These findings suggest that species-specific differences in pollen tube performance accumulate gradually and may have been driven by coevolution between pollen and style in the predominantly outcrossing M. guttatus.
Species-specific recognition between egg and sperm, a crucial event that marks the beginning of fertilization in multicellular organisms, mirrors the binding between haploid cells of opposite mating type in unicellular eukaryotes such as yeast. However, as implied by the lack of sequence similarity between sperm-binding regions of invertebrate and vertebrate egg coat proteins, these interactions are thought to rely on completely different molecular entities. Here, we argue that these recognition systems are, in fact, related: despite being separated by 0.6-1 billion years of evolution, functionally essential domains of a mollusc sperm receptor and a yeast mating protein adopt the same 3D fold as egg zona pellucida proteins mediating the binding between gametes in humans.
Thirty-six nuclear-encoded RAPD loci and 20 allozyme loci were studied to compare levels of diversity and differentiation among populations and races of the widespread North American conifer, Douglas-fir [Pseudotsuga menziesii (Mirb.) Franco]. RAPD assays used diploid seed embryo DNA from 22 to 36 trees in each of six populations that sampled the three major races (two populations per race). A comparable allozyme data set for nearby populations was constructed from a published study. RAPDs of organelle origin were excluded by hybridization of blotted RAPD gels with chloroplast and mitochondrial DNA-enriched probes. RAPD and allozyme markers had similar levels of diversity within populations (H S = 0.22<0.03 and 0.16<0.03, respectively) and differentiation among populations (G ST = 0.34<0.07 and 0.29<0.07, respectively). When the allozyme data set was transformed into dominant, biallelic markers to study how RAPDs may bias diversity estimates, resampling studies showed that simulated H S and H T were reduced by half regardless of sample size. Because observed diversity for RAPDs was equivalent to, or higher than, that of allozymes, our simulations suggest that RAPD markers may contain substantially higher levels of inherent, but hidden, diversity. In contrast, the simulations showed that estimates of G ST using RAPDs should not be significantly biased at the population sizes we employed.
Racial differentiation and genetic variability were studied between and within the coastal, north interior, and south interior races of Douglas-fir using RAPD and allozyme markers. Nearly half of all RAPD bands scored (13: 45%) were found to be amplified from mitochondrial DNA. They exhibited maternal inheritance among hybrids and backcrosses between the races, and were much more highly differentiated (GST = 0.62 for haplotype frequencies) than were allozymes (GST = 0.26). No evidence of hybridization or introgression was detected where the coastal and interior races come into proximity in central Oregon.
The genetic basis for the evolution of development includes genes that encode proteins expressed on the surfaces of sperm and eggs. Previous studies of the sperm acrosomal protein bindin have helped to characterize the adaptive evolution of gamete compatibility and speciation in sea urchins. The absence of evidence for bindin expression in taxa other than the Echinoidea has limited such studies to sea urchins, and led to the suggestion that bindin might be a sea urchin-specific molecule. Here we characterize the gene that encodes bindin in a broadcast-spawning asterinid sea star (Patiria miniata). We describe the sequence and domain structure of a full-length bindin cDNA and its single intron. In comparison to sea urchins, P. miniata bindin is larger but the two molecules share several general features of their domain structure and some sequence features of two domains. Our results extend the known evolutionary history of bindin from the Mesozoic (among the crown group sea urchins) into the early Paleozoic (and the common ancestor of eleutherozoans), and present new opportunities for understanding the role of bindin molecular evolution in sexual selection, life history evolution, and speciation among sea stars.
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