Genetic assimilation of ancestral plasticity during parallel adaptation

Phenotypic plasticity in ancestral populations is hypothesised to facilitate adaptation, but evidence supporting its contribution is piecemeal and often contradictory. Further, whether ancestral plasticity increases the probability of parallel genetic and phenotypic adaptive changes has not been explored. The most general finding is that nearly all ancestral gene expression plasticity is reversed following adaptation, but this is usually examined transcriptome-wide rather than focused on the genes directly involved in adaptation. We investigated the contribution of ancestral plasticity to adaptive evolution of gene expression in two independently evolved lineages of zinc-tolerant Silene uniflora. We found that the general pattern of reversion is driven by the absence of a widespread stress response in zinc-adapted plants compared to ancestral, zinc-sensitive plants. Our experiments show that reinforcement of ancestral plasticity plays an influential role in the evolution of plasticity in derived populations and, surprisingly, one third of constitutive differences between ecotypes are the result of genetic assimilation of ancestral plasticity. Ancestral plasticity also increases the chance that genes are recruited repeatedly during adaptation. However, despite a high degree of convergence in gene expression levels between independently adapted lineages, genes with ancestral plasticity are as likely to have similar expression levels in adapted populations as genes without. Overall, these results demonstrate that ancestral plasticity does play an important role in adaptive parallel evolution, particularly via genetic assimilation across evolutionary replicates.

Co-option of the same ancestral gene family gave rise to mammalian and reptilian toxins

Background Evolution can occur with surprising predictability when organisms face similar ecological challenges. For most traits, it is difficult to ascertain whether this occurs due to constraints imposed by the number of possible phenotypic solutions or because of parallel responses by shared genetic and regulatory architecture. Exceptionally, oral venoms are a tractable model of trait evolution, being largely composed of proteinaceous toxins that have evolved in many tetrapods, ranging from reptiles to mammals. Given the diversity of venomous lineages, they are believed to have evolved convergently, even though biochemically similar toxins occur in all taxa. Results Here, we investigate whether ancestral genes harbouring similar biochemical activity may have primed venom evolution, focusing on the origins of kallikrein-like serine proteases that form the core of most vertebrate oral venoms. Using syntenic relationships between genes flanking known toxins, we traced the origin of kallikreins to a single locus containing one or more nearby paralogous kallikrein-like clusters. Additionally, phylogenetic analysis of vertebrate serine proteases revealed that kallikrein-like toxins in mammals and reptiles are genetically distinct from non-toxin ones. Conclusions Given the shared regulatory and genetic machinery, these findings suggest that tetrapod venoms evolved by co-option of proteins that were likely already present in saliva. We term such genes ‘toxipotent’—in the case of salivary kallikreins they already had potent vasodilatory activity that was weaponized by venomous lineages. Furthermore, the ubiquitous distribution of kallikreins across vertebrates suggests that the evolution of envenomation may be more common than previously recognized, blurring the line between venomous and non-venomous animals.

The evolutionary history of human spindle genes includes back-and-forth gene flow with Neandertals

Proteins associated with the spindle apparatus, a cytoskeletal structure that ensures the proper segregation of chromosomes during cell division, experienced an unusual number of amino acid substitutions in modern humans after the split from the ancestors of Neandertals and Denisovans. Here, we analyze the history of these substitutions and show that some of the genes in which they occur may have been targets of positive selection. We also find that the two changes in the kinetochore scaffold 1 (KNL1) protein, previously believed to be specific to modern humans, were present in some Neandertals. We show that the KNL1 gene of these Neandertals shared a common ancestor with present-day Africans about 200,000 years ago due to gene flow from the ancestors (or relatives) of modern humans into Neandertals. Subsequently, some non-Africans inherited this modern human-like gene variant from Neandertals, but none inherited the ancestral gene variants. These results add to the growing evidence of early contacts between modern humans and archaic groups in Eurasia and illustrate the intricate relationships among these groups.

Sequence Diversity, Locus Structure, and Evolutionary History of the SpTransformer Genes in the Sea Urchin Genome

The generation of large immune gene families is often driven by evolutionary pressure exerted on host genomes by their pathogens, which has been described as the immunological arms race. The SpTransformer (SpTrf) gene family from the California purple sea urchin, Strongylocentrotus purpuratus, is upregulated upon immune challenge and encodes the SpTrf proteins that interact with pathogens during an immune response. Native SpTrf proteins bind both bacteria and yeast, and augment phagocytosis of a marine Vibrio, while a recombinant SpTrf protein (rSpTrf-E1) binds a subset of pathogens and a range of pathogen associated molecular patterns. In the sequenced sea urchin genome, there are four SpTrf gene clusters for a total of 17 genes. Here, we report an in-depth analysis of these genes to understand the sequence complexities of this family, its genomic structure, and to derive a putative evolutionary history for the formation of the gene clusters. We report a detailed characterization of gene structure including the intron type and UTRs with conserved transcriptional start sites, the start codon and multiple stop codons, and locations of polyadenylation signals. Phylogenetic and percent mismatch analyses of the genes and the intergenic regions allowed us to predict the last common ancestral SpTrf gene and a theoretical evolutionary history of the gene family. The appearance of the gene clusters from the theoretical ancestral gene may have been driven by multiple duplication and deletion events of regions containing SpTrf genes. Duplications and ectopic insertion events, indels, and point mutations in the exons likely resulted in the extant genes and family structure. This theoretical evolutionary history is consistent with the involvement of these genes in the arms race in responses to pathogens and suggests that the diversification of these genes and their encoded proteins have been selected for based on the survival benefits of pathogen binding and host protection.

BOPAL 2.0 and a study of tRNA and rRNA gene evolution in Clostridium

We present BOPAL 2.0, an improved version of the BOPAL algorithm for the evolutionary history inference of tRNA and rRNA genes in bacterial genomes. Our approach can infer complete evolutionary scenarios and ancestral gene orders on a phylogeny and considers a wide range of events such as duplications, deletions, substitutions, inversions and transpositions. It is based on the fact that tRNA and rRNA genes are often organized in operons/clusters in bacteria, and this information is used to help identify orthologous genes for each genome comparison. BOPAL 2.0 introduces new features, such as a triple-wise alignment step, context-aware singleton matching and a second pass of the algorithm. Evaluation on simulated datasets shows that BOPAL 2.0 outperforms the original BOPAL in terms of the accuracy of inferred events and ancestral genomes. We also present a study of the tRNA/rRNA gene evolution in the Clostridium genus, in which the organization of these genes is very divergent. Our results indicate that tRNA and rRNA genes in Clostridium have evolved through numerous duplications, losses, transpositions and substitutions, but very few inversions were inferred.

Recurrent Duplication and Diversification of Acrosomal Fertilization Proteins in Abalone

Reproductive proteins mediating fertilization commonly exhibit rapid sequence diversification driven by positive selection. This pattern has been observed among nearly all taxonomic groups, including mammals, invertebrates, and plants, and is remarkable given the essential nature of the molecular interactions mediating fertilization. Gene duplication is another important mechanism that facilitates the generation of molecular novelty. Following duplication, paralogs may parse ancestral gene function (subfunctionalization) or acquire new roles (neofunctionalization). However, the contributions of duplication followed by sequence diversification to the molecular diversity of gamete recognition genes has been understudied in many models of fertilization. The marine gastropod mollusk abalone is a classic model for fertilization. Its two acrosomal proteins (lysin and sp18) are ancient gene duplicates with unique gamete recognition functions. Through detailed genomic and bioinformatic analyses we show how duplication events followed by sequence diversification has played an ongoing role in the evolution of abalone acrosomal proteins. The common ancestor of abalone had four members of its acrosomal protein family in a tandem gene array that repeatedly experienced positive selection. We find that both sp18 paralogs contain positively selected sites located in different regions of the paralogs, consistent with a subfunctionalization model where selection acted upon distinct binding interfaces in each paralog. Further, a more recent species-specific duplication of both lysin and sp18 in the European abalone H. tuberculata is described. Despite clade-specific acrosomal protein paralogs, there are no concomitant duplications of egg coat proteins in H. tuberculata, indicating that duplication of egg proteins per se is not responsible for retention of duplicated acrosomal proteins. We hypothesize that, in a manner analogous to host/pathogen evolution, sperm proteins are selected for increased diversity through extensive sequence divergence and recurrent duplication driven by conflict mechanisms.

Genome Comparisons of the Fission Yeasts Reveal Ancient Collinear Loci Maintained by Natural Selection

Fission yeasts have a unique life history and exhibit distinct evolutionary patterns from other yeasts. Besides, the species demonstrate stable genome structures despite the relatively fast evolution of their genomic sequences. To reveal what could be the reason for that, comparative genomic analyses were carried out. Our results provided evidence that the structural and sequence evolution of the fission yeasts were correlated. Moreover, we revealed ancestral locally collinear blocks (aLCBs), which could have been inherited from their last common ancestor. These aLCBs proved to be the most conserved regions of the genomes as the aLCBs contain almost eight genes/blocks on average in the same orientation and order across the species. Gene order of the aLCBs is mainly fission-yeast-specific but supports the idea of filamentous ancestors. Nevertheless, the sequences and gene structures within the aLCBs are as mutable as any sequences in other parts of the genomes. Although genes of certain Gene Ontology (GO) categories tend to cluster at the aLCBs, those GO enrichments are not related to biological functions or high co-expression rates, they are, rather, determined by the density of essential genes and Rec12 cleavage sites. These data and our simulations indicated that aLCBs might not only be remnants of ancestral gene order but are also maintained by natural selection.

Fungus-originated glucanase and monooxygenase genes in creeping bent grass (Agrostis stolonifera L.)

Recent studies have revealed presence of fungus-originated genes in genomes of cool-season grasses, suggesting occurrence of multiple ancestral gene transfer events between the two distant lineages. The current article describes identification of glucanase-like and monooxygenase-like genes from creeping bent grass, as lateral gene transfer candidates. An in silico analysis suggested presence of the glucanase-like gene in Agrostis, Deyeuxia, and Polypogon genera, but not in other species belonging to the clade 1 of the Poeae tribe. Similarly, the monooxygenase-like gene was confined to Agrostis and Deyeuxia genera. A consistent result was obtained from PCR-based screening. The glucanase-like gene was revealed to be ubiquitously expressed in young seedlings of creeping bent grass. Although expression of the monooxygenase-like gene was suggested in plant tissues, the levels were considerably lower than those of the glucanase-like gene. A phylogenetic analysis revealed close relationships of the two genes between the corresponding genes in fungal endophyte species of the Epichloë genus, suggesting that the genes originated from the Epichloë lineage.

The whale shark genome reveals patterns of vertebrate gene family evolution

Chondrichthyes (cartilaginous fishes) are fundamental for understanding vertebrate evolution, yet their genomes are understudied. We report long-read sequencing of the whale shark genome to generate the best gapless chondrichthyan genome assembly yet with higher contig contiguity than all other cartilaginous fish genomes, and studied vertebrate genomic evolution of ancestral gene families, immunity, and gigantism. We found a major increase in gene families at the origin of gnathostomes (jawed vertebrates) independent of their genome duplication. We studied vertebrate pathogen recognition receptors (PRRs), which are key in initiating innate immune defense, and found diverse patterns of gene family evolution, demonstrating that adaptive immunity in gnathostomes did not fully displace germline-encoded PRR innovation. We also discovered a new Toll-like receptor (TLR29) and three NOD1 copies in the whale shark. We found chondrichthyan and giant vertebrate genomes had decreased substitution rates compared to other vertebrates, but gene family expansion rates varied among vertebrate giants, suggesting substitution and expansion rates of gene families are decoupled in vertebrate genomes. Finally, we found gene families that shifted in expansion rate in vertebrate giants were enriched for human cancer-related genes, consistent with gigantism requiring adaptations to suppress cancer.

RADseq data reveal a lack of admixture in a mouse lemur contact zone contrary to previous microsatellite results

Despite being one of the most fundamental biological processes, the process of speciation remains poorly understood in many groups of organisms. Mouse lemurs are a species-rich genus of small primates endemic to Madagascar, whose diversity has only recently been uncovered using genetic data and is primarily found among morphologically cryptic, allopatric populations. To assess to what extent described species represent reproductively isolated entities, studies are needed in areas where mouse lemur taxa come into contact. Hybridization has previously been reported in a contact zone between two closely related mouse lemur species (Microcebus murinus and M. griseorufus) based on microsatellite data. Here, we revisit this system using RADseq data for populations in, near, and far from the contact zone, including many of the individuals that had previously been identified as hybrids. Surprisingly, we find no evidence for admixed nuclear ancestry in any of the individuals. Re-analyses of microsatellite data and simulations suggest that previously inferred hybrids were false positives and that the program NewHybrids can be particularly sensitive to erroneously inferring hybrid ancestry. Using coalescent-bases analyses, we also show an overall lack of recent gene flow between the two species, and low levels of ancestral gene flow. Combined with evidence for local syntopic occurrence, these data indicate that M. murinus and M. griseorufus are reproductively isolated. Finally, we estimate that they diverged less than a million years ago, suggesting that completion of speciation is relatively rapid in mouse lemurs. Future work should focus on the underpinnings of reproductive isolation in this cryptic primate radiation, which are mostly unknown. Our study also provides a cautionary tale for the inference of hybridization with microsatellite data.