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

Abstract

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...

Population assignment and local adaptation along an isolation‐by‐distance gradient in Pacific cod (Gadus macrocephalus)

“…Second, locus 8253 had the second largest overall F ST value ( F ST  = 0.46), was identified as an outlier in both coastal analyses, and aligned to an intron of the folliculogenesis‐specific bHLH transcription factor, which may regulate the expression of the reproductively important zona pellucida genes (Liang, Soyal, & Dean, 1997). Zona pellucida has been previously identified to undergo rapid selection in other species (Aagaard, Yi, MacCoss, & Swanson, 2006; Heras, McClintock, Sunagawa, & Aguilar, 2015), and both changes to coding regions as well as differences in expression patterns may be important to diversification in Pacific cod.…”

Postcopulatory sexual selection: Darwin's omission and its consequences

“…The abalone sperm molecule lysin, which digests a hole in the vitelline egg membrane, has evolved up to 15 times faster than introns (85), and there is a link between sites of positive selection and functional changes (83). Egg molecules with which lysin interacts have also undergone rapid divergence under selection (75,86). Similarly, the bindin molecule of sea urchin sperm, which both attaches the acrosomal process of the sperm to the glycoprotein bindin receptor molecules in the egg's vitelline layer and promotes fusion of egg and sperm membranes, also shows rapid divergence (84).…”

The role of linkage disequilibrium in the evolution of premating isolation

“…In many systems, however, loci involved in eggsperm incompatibilities, sperm storage or other specific features directly affecting fertility may not be likely to also be explicit targets of mate choice (this also applies to loci that directly cause higher mortality between mating and offspring production); remember that it is not enough that they be genetically associated with such targets, to truly be a magic trait these loci must themselves directly act as mating cues. One potential exception, depending on semantics, comes in the VERL/ lysin gamete recognition protein system of abalone (and potentially likewise in other gamete recognition systems); here positive selection, most likely driven by some form of sexual conflict such as polyspermy avoidance, has acted directly on the VERL receptor, driving evolution in both components of the system (for example, Aagaard et al, 2006). This example only works, however, if we consider gamete recognition systems not to have a 'choosing sex'-if we consider 'choice' to occur through the female component of the system, then the positive selection in this example is acting on the wrong component of the system to technically be a magic trait (that is, not on lysin, the 'mating cue').…”