Molecular evolutionary analysis of nematode Zona Pellucida (ZP) modules reveals disulfide-bond reshuffling and standalone ZP-C domains

This is the author accepted manuscript. The final version is available on open access from Oxford University Press via the DOI in this recordZona pellucida (ZP) modules mediate extracellular protein-protein interactions and contribute to important biological processes including syngamy and cellular morphogenesis. While some biomedically-relevant ZP modules are well-studied, little is known about the protein family’s broad-scale diversity and evolution. The increasing availability of sequenced genomes from “non-model” systems provides a valuable opportunity to address this issue, and to use comparative approaches to gain new insights into ZP module biology. Here, through phylogenetic and structural exploration of ZP module diversity across the nematode phylum, I report evidence that speaks to two important aspects of ZP module biology. First, I show that ZP-C domains—which in some modules act as regulators of ZP-N domain-mediated polymerization activity, and which have never before been found in isolation—can indeed be found as standalone domains. These standalone ZP-C domain proteins originated in independent (paralogous) lineages prior to the diversification of extant nematodes, after which they evolved under strong stabilizing selection, suggesting the presence of ZP-N domain-independent functionality. Second, I provide a much-needed phylogenetic perspective on disulfide bond variability, uncovering evidence for both convergent evolution and disulfide-bond reshuffling. This result has implications for our evolutionary understanding and classification of ZP module structural diversity and highlights the usefulness of phylogenetics and diverse sampling for protein structural biology. All told, these findings set the stage for broad-scale (cross-phyla) evolutionary analysis of ZP modules and position Caenorhabditis elegans and other nematodes as important experimental systems for exploring the evolution of ZP modules and their constituent domains.Royal Societ

Convergent evolution of small molecule pheromones in pristionchus nematodes

This is the final version. Available from eLife Sciences Publications via the DOI in this recordData availability: All data generated during this study are included in the manuscript and supporting files. Source data files have been provided.The small molecules that mediate chemical communication between nematodes—so-called “nematode-derived-modular-metabolites” (NDMMs)—are of major interest due to their ability to regulate development, behavior, and life-history. Pristionchus pacificus nematodes produce an impressive diversity of structurally complex NDMMs, some of which act as primer pheromones capable of triggering irreversible developmental switches. Many of these NDMMs have only ever been found in P. pacificus but no attempts had been made to study their evolution by profiling closely related species. This study was designed to bring a comparative perspective to the biochemical study of NDMMs via the systematic MS/MS and NMR-based analysis of exo-metabolomes from over 30 Pristionchus species. We identified 36 novel compounds and found evidence for the convergent evolution of complex NDMMs in separate branches of the Pristionchus phylogeny. Our results demonstrate that biochemical innovation is a recurrent process in Pristionchus nematodes, a pattern likely typical across the animal kingdom.Max Planck Societ

The genome of the Trinidadian guppy, Poecilia reticulata, and variation in the Guanapo population

For over a century, the live bearing guppy, Poecilia reticulata, has been used to study sexual selection as well as local adaptation. Natural guppy populations differ in many traits that are of intuitively adaptive significance such as ornamentation, age at maturity, brood size and body shape. Water depth, light supply, food resources and predation regime shape these traits, and barrier waterfalls often separate contrasting environments in the same river. We have assembled and annotated the genome of an inbred single female from a high-preda- tion site in the Guanapo drainage. The final assembly comprises 731.6 Mb with a scaffold N50 of 5.3 MB. Scaffolds were mapped to linkage groups, placing 95% of the genome assembly on the 22 autosomes and the X-chromosome. To investigate genetic variation in the population used for the genome assembly, we sequenced 10 wild caught male individu- als. The identified 5 million SNPs correspond to an average nucleotide diversity (π) of 0.0025. The genome assembly and SNP map provide a rich resource for investigating adap- tation to different predation regimes. In addition, comparisons with the genomes of other Poeciliid species, which differ greatly in mechanisms of sex determination and maternal resource allocation, as well as comparisons to other teleost genera can begin to reveal how live bearing evolved in teleost fish

RT-qPCR reveals opsin gene upregulation associated with age and sex in guppies (Poecilia reticulata) - a species with color-based sexual selection and 11 visual-opsin genes

<p>Abstract</p> <p>Background</p> <p>PCR-based surveys have shown that guppies (<it>Poecilia reticulata</it>) have an unusually large visual-opsin gene repertoire. This has led to speculation that opsin duplication and divergence has enhanced the evolution of elaborate male coloration because it improves spectral sensitivity and/or discrimination in females. However, this conjecture on evolutionary connections between opsin repertoire, vision, mate choice, and male coloration was generated with little data on gene expression. Here, we used RT-qPCR to survey visual-opsin gene expression in the eyes of males, females, and juveniles in order to further understand color-based sexual selection from the perspective of the visual system.</p> <p>Results</p> <p>Juvenile and adult (male and female) guppies express 10 visual opsins at varying levels in the eye. Two opsin genes in juveniles, <it>SWS2B </it>and <it>RH2-2</it>, accounted for >85% of all visual-opsin transcripts in the eye, excluding <it>RH1</it>. This relative abundance (RA) value dropped to about 65% in adults, as <it>LWS-A180 </it>expression increased from approximately 3% to 20% RA. The juvenile-to-female transition also showed <it>LWS-S180 </it>upregulation from about 1.5% to 7% RA. Finally, we found that expression in guppies' <it>SWS2-LWS </it>gene cluster is negatively correlated with distance from a candidate locus control region (LCR).</p> <p>Conclusions</p> <p>Selective pressures influencing visual-opsin gene expression appear to differ among age and sex. <it>LWS </it>upregulation in females is implicated in augmenting spectral discrimination of male coloration and courtship displays. In males, enhanced discrimination of carotenoid-rich food and possibly rival males are strong candidate selective pressures driving <it>LWS </it>upregulation. These developmental changes in expression suggest that adults possess better wavelength discrimination than juveniles. Opsin expression within the <it>SWS2-LWS </it>gene cluster appears to be regulated, in part, by a common LCR. Finally, by comparing our RT-qPCR data to MSP data, we were able to propose the first opsin-to-λ_maxassignments for all photoreceptor types in the cone mosaic.</p

Whole-genome sequences of Malawi cichlids reveal multiple radiations interconnected by gene flow.

The hundreds of cichlid fish species in Lake Malawi constitute the most extensive recent vertebrate adaptive radiation. Here we characterize its genomic diversity by sequencing 134 individuals covering 73 species across all major lineages. The average sequence divergence between species pairs is only 0.1-0.25%. These divergence values overlap diversity within species, with 82% of heterozygosity shared between species. Phylogenetic analyses suggest that diversification initially proceeded by serial branching from a generalist Astatotilapia-like ancestor. However, no single species tree adequately represents all species relationships, with evidence for substantial gene flow at multiple times. Common signatures of selection on visual and oxygen transport genes shared by distantly related deep-water species point to both adaptive introgression and independent selection. These findings enhance our understanding of genomic processes underlying rapid species diversification, and provide a platform for future genetic analysis of the Malawi radiation