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two successive rounds in the ancestor of vertebrates, and a third one specific to teleost fishes. Biased loss of most duplicates enriched the genome for specific genes, such as slow evolving genes, but this selective retention process is not well understood. To understand what drives the long-term preservation of duplicate genes, we characterized duplicated genes in terms of their expression patterns. We used a new method of expression enrichment analysis, TopAnat, applied to in situ hybridization data from thousands of genes from zebrafish and mouse. We showed that the presence of expression in the nervous system is a good predictor of a higher rate of retention of duplicate genes after whole-genome duplication. Further analyses suggest that purifying selection against the toxic effects of misfolded or misinteracting proteins, which is particularly strong in nonrenewing neural tissues, likely constrains the evolution of coding sequences of nervous system genes, leading indirectly to the preservation of duplicate genes after whole-genome duplication. Whole-genome duplications thus greatly contributed to the expansion of the toolkit of genes available for the evolution of profound novelties of the nervous system at the base of the vertebrate radiation.
AbstractThe American Eel (Anguilla rostrata) has an exceptional life cycle characterized by panmictic reproduction at the species scale, random dispersal, and selection in a highly heterogeneous habitat extending from subtropical to subarctic latitudes. The genetic consequences of spatially-varying selection in this species have been investigated for decades, revealing subtle clines in allele frequency at a few loci that contrast with complete panmixia on the vast majority of the genome. Because reproduction homogenizes allele frequencies every generation, sampling size, and genomic coverage are critical to reach sufficient power to detect selected loci in this context. Here, we used a total of 710 individuals from 12 sites and 12,098 high-quality single nucleotide polymorphisms to re-evaluate the extent to which local selection affects the spatial distribution of genetic diversity in this species. We used environmental association methods to identify markers under spatially-varying selection, which indicated that selection affects ∼1.5% of the genome. We then evaluated the extent to which candidate markers collectively vary with environmental factors using additive polygenic scores. We found significant correlations between polygenic scores and latitude, longitude and temperature which are consistent with polygenic selection acting against maladapted genotypes in different habitats occupied by eels throughout their range of distribution. Gene functions associated with outlier markers were significantly enriched for the insulin signaling pathway, indicating that the trade-offs inherent to occupying such a large distribution range involve the regulation of metabolism. Overall, this study highlights the potential of the additive polygenic scores approach in detecting selective effects in a complex environment.
AbstractBemisia tabaci threatens production of cassava in Africa through vectoring viruses that cause cassava mosaic disease (CMD) and cassava brown streak disease (CBSD). B. tabaci sampled from cassava in eight countries in Africa were genotyped using NextRAD sequencing, and their phylogeny and population genetics were investigated using the resultant single nucleotide polymorphism (SNP) markers. SNP marker data and short sequences of mitochondrial DNA cytochrome oxidase I (mtCOI) obtained from the same insect were compared. Eight genetically distinct groups were identified based on mtCOI, whereas phylogenetic analysis using SNPs identified six major groups, which were further confirmed by PCA and multidimensional analyses. STRUCTURE analysis identified four ancestral B. tabaci populations that have contributed alleles to the six SNP-based groups. Significant gene flows were detected between several of the six SNP-based groups. Evidence of gene flow was strongest for SNP-based groups occurring in central Africa. Comparison of the mtCOI and SNP identities of sampled insects provided a strong indication that hybrid populations are emerging in parts of Africa recently affected by the severe CMD pandemic. This study reveals that mtCOI is not an effective marker at distinguishing cassava-colonizing B. tabaci haplogroups, and that more robust SNP-based multilocus markers should be developed. Significant gene flows between populations could lead to the emergence of haplogroups that might alter the dynamics of cassava virus spread and disease severity in Africa. Continuous monitoring of genetic compositions of whitefly populations should be an essential component in efforts to combat cassava viruses in Africa.
AbstractLegionellaceae are intracellular bacteria known as important human pathogens. In the environment, they are mainly found in biofilms associated with amoebas. In contrast to the gammaproteobacterial family Enterobacteriaceae, which established a broad spectrum of symbioses with many insect taxa, the only instance of legionella-like symbiont has been reported from lice of the genus Polyplax. Here, we sequenced the complete genome of this symbiont and compared its main characteristics to other Legionella species and insect symbionts. Based on rigorous multigene phylogenetic analyses, we confirm this bacterium as a member of the genus Legionella and propose the name Candidatus Legionella polyplacis, sp.n. We show that the genome of Ca. Legionella polyplacis underwent massive degeneration, including considerable size reduction (529.746 bp, 484 protein coding genes) and a severe decrease in GC content (23%). We identify several possible constraints underlying the evolution of this bacterium. On one hand, Ca. Legionella polyplacis and the louse symbionts Riesia and Puchtella experienced convergent evolution, perhaps due to adaptation to similar hosts. On the other hand, some metabolic differences are likely to reflect different phylogenetic positions of the symbionts and hence availability of particular metabolic function in the ancestor. This is exemplified by different arrangements of thiamine metabolism in Ca. Legionella polyplacis and Riesia. Finally, horizontal gene transfer is shown to play a significant role in the adaptive and diversification process. Particularly, we show that Ca. L. polyplacis horizontally acquired a complete biotin operon (bioADCHFB) that likely assisted this bacterium when becoming an obligate mutualist.
Zika virus (ZIKV) has caused explosive epidemics in the Pacific and the Americas, posing a serious threat to public health. Conventional opinion advocates that ZIKV evolved into two distinct lineages, namely, African and Asian. Descendants of this latter lineage dispersed globally causing major epidemics. However, based on shared amino acid replacements and phylogenetic analyses, it was recently contentiously proposed that the Asian lineage was a direct descendant of the African lineage. To address this contentious issue, we reconstructed a phylogenetic tree of ZIKV using the method based on shared amino acid replacements and found that ZIKV evolved into two distinct lineages. This supports the conventional phylogenetic divergence pattern of ZIKV. Evidence of recombination and sequencing errors was identified among the large collection of ZIKV. As such problematic sequences could confound the phylogenetic analyses, they were removed. Bayesian phylogenetic analyses using the improved sequence data enabled estimates for the divergence time in the past of the African and Asian lineages of ∼180 years ago. Moreover, we found that the Asian lineage viruses did not evolve at an elevated rate. Our findings provide additional support for the conventional opinion that the Asian lineage of ZIKV diverged from the African lineage.