Frequent lineage-specific substitution rate changes support an episodic model for protein evolution

Since the inception of the molecular clock model for sequence evolution, the investigation of protein divergence has revolved around the question of a more or less constant change of amino acid sequences, with specific overall rates for each family. Although anomalies in clock-like divergence are well known, the assumption of a constant decay rate for a given protein family is usually taken as the null model for protein evolution. However, systematic tests of this null model at a genome-wide scale have lagged behind, despite the databases’ enormous growth. We focus here on divergence rate comparisons between very closely related lineages since this allows clear orthology assignments by synteny and reliable alignments, which are crucial for determining substitution rate changes. We generated a high-confidence dataset of syntenic orthologs from four ape species, including humans. We find that despite the appearance of an overall clock-like substitution pattern, several hundred protein families show lineage-specific acceleration and deceleration in divergence rates, or combinations of both in different lineages. Hence, our analysis uncovers a rather dynamic history of substitution rate changes, even between these closely related lineages, implying that one should expect that a large fraction of proteins will have had a history of episodic rate changes in deeper phylogenies. Furthermore, each of the lineages has a separate set of particularly fast diverging proteins. The genes with the highest percentage of branch-specific substitutions are ADCYAP1 in the human lineage (9.7%), CALU in chimpanzees (7.1%), SLC39A14 in the internal branch leading to humans and chimpanzees (4.1%), RNF128 in gorillas (9%), and S100Z in gibbons (15.2%). The mutational pattern in ADCYAP1 suggests a biased mutation process, possibly through asymmetric gene conversion effects. We conclude that a null model of constant change can be problematic for predicting the evolutionary trajectories of individual proteins

Fast adjustment of pace‐of‐life and risk‐taking to changes in food quality by altered gene expression in house mice

The pace-of-life syndrome hypothesis provides a framework for the adaptive integration of behaviour, physiology and life history between and within species. It suggests that behaviours involving a risk of death or injury should co-vary with a higher allocation to fast reproduction. Empirical support for this hypothesis is mixed, presumably because important influencing factors such as environmental variation, are usually neglected. By experimentally manipulating food quality of wild mice living under semi-natural conditions for three generations, we show that individuals adjust their life history strategies and risk-taking behaviours as well as trait covariation (Nindividuals = 1442). These phenotypic differences are correlated to differences in transcriptomic gene expression of primary metabolic processes in the liver while no changes in gene frequencies occurred. Our discussion emphasises the need to integrate the role of environmental conditions and phenotypic plasticity in shaping relationships among behaviour, physiology and life history in response to changing environmental conditions

Multiple Pristionchus pacificus genomes reveal distinct evolutionary dynamics between de novo candidates and duplicated genes

The birth of new genes is a major molecular innovation driving phenotypic diversity across all domains of life. Although repurposing of existing protein-coding material by duplication is considered the main process of new gene formation, recent studies have discovered thousands of transcriptionally active sequences as a rich source of new genes. However, differential loss rates have to be assumed to reconcile the high birth rates of these incipient de novo genes with the dominance of ancient gene families in individual genomes. Here, we test this rapid turnover hypothesis in the context of the nematode model organism Pristionchus pacificus We extended the existing species-level phylogenomic framework by sequencing the genomes of six divergent P. pacificus strains. We used this data to study the evolutionary dynamics of different age classes and categories of origin at a population level. Contrasting de novo candidates with new families that arose by duplication and divergence from known genes, we find that de novo candidates are typically shorter, show less expression, and are overrepresented on the sex chromosome. While the contribution of de novo candidates increases towards young age classes, multiple comparisons within the same age class showed significantly higher attrition in de novo candidates than in known genes. Similarly, young genes remain under weak evolutionary constraints with de novo candidates representing the fastest evolving subcategory. Altogether, this study provides empirical evidence for the rapid turnover hypothesis and highlights the importance of the evolutionary time-scale when quantifying the contribution of different mechanisms towards new gene formation

Are orphan genes protein-coding, prediction artifacts, or non-coding RNAs?

Background: Current genome sequencing projects reveal substantial numbers of taxonomically restricted, so called orphan genes that lack homology with genes from other evolutionary lineages. However, it is not clear to what extent orphan genes are real, genomic artifacts, or represent non-coding RNAs. Results: Here, we use a simple set of assumptions to test the nature of orphan genes. First, a sequence that is transcribed is considered a real biological entity. Second, every sequence that is supported by proteome data or shows a depletion of non-synonymous substitutions is a protein-coding gene. Using genomic, transcriptomic and proteomic data for the nematode Pristionchus pacificus, we show that between 4129-7997 (42-81 %) of predicted orphan genes are expressed and 3818-7545 (39-76 %) of orphan genes are under negative selection. In three cases that exhibited strong evolutionary constraint but lacked expression evidence in 14 RNA-seq samples, we could experimentally validate the predicted gene structures. Comparing different data sets to infer selection on orphan gene clusters, we find that the presence of a closely related genome provides the most powerful resource to robustly identify evidence of negative selection. However, even in the absence of other genomic data, the availability of paralogous sequences was enough to show negative selection in 8-10 % of orphan genes. Conclusions: Our study shows that the great majority of previously identified orphan genes in P. pacificus are indeed protein-coding genes. Even though this work represents a case study on a single species, our approach can be transferred to genomic data of other non-model organisms in order to ascertain the protein-coding nature of orphan genes

Single-Molecule Sequencing Reveals the Chromosome-Scale Genomic Architecture of the Nematode Model Organism Pristionchus pacificus

The nematode Pristionchus pacificus is an established model for integrative evolutionary biology and comparative studies with Caenorhabditis elegans. While an existing genome draft facilitated the identification of several genes controlling various developmental processes, its high degree of fragmentation complicated virtually all genomic analyses. Here, we present a de novo genome assembly fromsingle-molecule, long-read sequencing data consisting of 135 P. pacificus contigs. When combined with a genetic linkage map, 99% of the assembly could be ordered and oriented into six chromosomes. This allowed us to robustly characterize chromosomal patterns of gene density, repeat content, nucleotide diversity, linkage disequilibrium, and macrosynteny in P. pacificus. Despite widespread conservation of synteny between P. pacificus and C. elegans, we identified one major translocation from an autosome to the sex chromosome in the lineage leading to C. elegans. This highlights the potential of the chromosome-scale assembly for future genomic studies of P. pacificus

Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulation

Species-specific, new, or "orphan" genes account for 10%-30% of eukaryotic genomes. Although initially considered to have limited function, an increasing number of orphan genes have been shown to provide important phenotypic innovation. How new genes acquire regulatory sequences for proper temporal and spatial expression is unknown. Orphan gene regulation may rely in part on origination in open chromatin adjacent to preexisting promoters, although this has not yet been assessed by genome-wide analysis of chromatin states. Here, we combine taxon-rich nematode phylogenies with Iso-Seq, RNA-seq, ChIP-seq, and ATAC-seq to identify the gene structure and epigenetic signature of orphan genes in the satellite model nematode Pristionchus pacificus Consistent with previous findings, we find young genes are shorter, contain fewer exons, and are on average less strongly expressed than older genes. However, the subset of orphan genes that are expressed exhibit distinct chromatin states from similarly expressed conserved genes. Orphan gene transcription is determined by a lack of repressive histone modifications, confirming long-held hypotheses that open chromatin is important for new gene formation. Yet orphan gene start sites more closely resemble enhancers defined by H3K4me1, H3K27ac, and ATAC-seq peaks, in contrast to conserved genes that exhibit traditional promoters defined by H3K4me3 and H3K27ac. Although the majority of orphan genes are located on chromosome arms that contain high recombination rates and repressive histone marks, strongly expressed orphan genes are more randomly distributed. Our results support a model of new gene origination by rare integration into open chromatin near enhancers

Deep taxon sampling reveals the evolutionary dynamics of novel gene families in Pristionchus nematodes

The widespread identification of genes without detectable homology in related taxa is a hallmark of genome sequencing projects in animals, together with the abundance of gene duplications. Such genes have been called novel, young, taxon-restricted, or orphans, but little is known about the mechanisms accounting for their origin, age, and mode of evolution. Phylogenomic studies relying on deep and systematic taxon sampling and using the comparative method can provide insight into the evolutionary dynamics acting on novel genes. We used a phylogenomic approach for the nematode model organism Pristionchus pacificus and sequenced six additional Pristionchus and two outgroup species. This resulted in 10 genomes with a ladder-like phylogeny, sequenced in one laboratory using the same platform and analyzed by the same bioinformatic procedures. Our analysis revealed that 68%-81% of genes are assignable to orthologous gene families, the majority of which defined nine age classes with presence/absence patterns that can be explained by single evolutionary events. Contrasting different age classes, we find that older age classes are concentrated at chromosome centers, whereas novel gene families preferentially arise at the periphery, are weakly expressed, evolve rapidly, and have a high propensity of being lost. Over time, they increase in expression and become more constrained. Thus, the detailed phylogenetic resolution allowed a comprehensive characterization of the evolutionary dynamics of Pristionchus genomes indicating that distribution of age classes and their associated differences shape chromosomal divergence. This study establishes the Pristionchus system for future research on the mechanisms that drive the formation of novel genes

An empirical study of link quality estimation techniques for disconnection detection in WBANs

Sensor nodes in many Wireless Body Area Network (WBAN) architectures are supposed to deliver sensed data to a gateway node on the body. To satisfy the data delivery requirements, the network needs to adapt itself to the changes in connection status of the body nodes to the gateway. As a prerequisite, Link Quality Estimation (LQE) needs to be done to detect the connection status of the nodes. The quality of links in WBANs is highly time-varying. The LQE technique should be agile to react fast to such link quality dynamics while avoiding frequent fluctuations to reduce the network adaptation overhead. In this paper, we present an empirical study on using different LQE methods for detecting the connection status of body nodes to the gateway in WBANs. A set of experiments using 16 wireless motes deployed on a body are performed to log the behavior of the wireless links. We explore the trade-offs made by each LQE method in terms of agility, stability, and reliability in detecting connection changes by analyzing the experimental data. Moreover, different LQE methods are used in an adaptive multi-hop WBAN mechanism, as a case study, and their impact on the Quality-of-Services (QoS) are investigated. © 2013 ACM