Oral venom systems evolved multiple times in numerous vertebrates enabling the exploitation of unique predatory niches. Yet how and when they evolved remains poorly understood. Up to now, most ...research on venom evolution has focused strictly on the toxins. However, using toxins present in modern day animals to trace the origin of the venom system is difficult, since they tend to evolve rapidly, show complex patterns of expression, and were incorporated into the venom arsenal relatively recently. Here we focus on gene regulatory networks associated with the production of toxins in snakes, rather than the toxins themselves. We found that overall venom gland gene expression was surprisingly well conserved when compared to salivary glands of other amniotes. We characterized the "metavenom network," a network of ∼3,000 nonsecreted housekeeping genes that are strongly coexpressed with the toxins, and are primarily involved in protein folding and modification. Conserved across amniotes, this network was coopted for venom evolution by exaptation of existing members and the recruitment of new toxin genes. For instance, starting from this common molecular foundation,
lizards, shrews, and solenodon, evolved venoms in parallel by overexpression of kallikreins, which were common in ancestral saliva and induce vasodilation when injected, causing circulatory shock. Derived venoms, such as those of snakes, incorporated novel toxins, though still rely on hypotension for prey immobilization. These similarities suggest repeated cooption of shared molecular machinery for the evolution of oral venom in mammals and reptiles, blurring the line between truly venomous animals and their ancestors.
Oxford Nanopore's third‐generation single‐molecule sequencing platform promises to decrease costs for reagents and instrumentation. After a 2‐year hiatus following the initial announcement, the first ...devices have been released as part of an early access program. We explore the performance of this platform by resequencing the lambda phage genome, and amplicons from a snake venom gland transcriptome. Although the handheld MinION sequencer can generate more than 150 megabases of raw data in one run, at most a quarter of the resulting reads map to the reference, with less than average 10% identity. Much of the sequence consists of insertion/deletion errors, or is seemingly without similarity to the template. Using the lambda phage data as an example, although the reads are long, averaging 5 kb, at best 890 ± 1932 bases per mapped read could be matched to the reference without soft clipping. In the course of a 36 h run on the MinION, it was possible to resequence the 48 kb lambda phage reference at 16× coverage. Currently, substantially larger projects would not be feasible using the MinION. Without increases in accuracy, which would be required for applications such as genome scaffolding and phasing, the current utility of the MinION appears limited. Library preparation requires access to a molecular laboratory, and is of similar complexity and cost to that of other next‐generation sequencing platforms. The MinION is an exciting step in a new direction for single‐molecule sequencing, though it will require dramatic decreases in error rates before it lives up to its promise.
Microbiomes provide a range of benefits to their hosts which can lead to the coevolution of a joint ecological niche. However, holometabolous insects, some of the most successful organisms on Earth, ...occupy different niches throughout development, with larvae and adults being physiologically and morphologically highly distinct. Furthermore, transition between the stages usually involves the loss of the gut microbiome since the gut is remodeled during pupation. Most eusocial organisms appear to have evolved a workaround to this problem by sharing their communal microbiome across generations. However, whether this vertical microbiome transmission can overcome perturbations of the larval microbiome remains untested. Honey bees have a relatively simple, conserved, coevolved adult microbiome which is socially transmitted and affects many aspects of their biology. In contrast, larval microbiomes are more variable, with less clear roles. Here, we manipulated the gut microbiome of
-reared larvae, and after pupation of the larvae, we inoculated the emerged bees with adult microbiome to test whether adult and larval microbiome stages may be coupled (e.g., through immune priming). Larval treatments differed in bacterial composition and abundance, depending on diet, which also drove larval gene expression. Nonetheless, adults converged on the typical core taxa and showed limited gene expression variation. This work demonstrates that honey bee adult and larval stages are effectively microbiologically decoupled, and the core adult microbiome is remarkably stable to early developmental perturbations. Combined with the transmission of the microbiome in early adulthood, this allows the formation of long-term host-microbiome associations.
This work investigated host-microbiome interactions during a crucial developmental stage-the transition from larvae to adults, which is a challenge to both, the insect host and its microbiome. Using the honey bee as a tractable model system, we showed that microbiome transfer after emergence overrides any variation in the larvae, indicating that larval and adult microbiome stages are effectively decoupled. Together with the reliable vertical transfer in the eusocial system, this decoupling ensures that the adults are colonized with a consistent and derived microbiome after eclosion. Taken all together, our data provide additional support that the evolution of sociality, at least in the honey bee system tested here, is linked with host-microbiome relationships.
Abstract
Gene expression changes contribute to complex trait variations in both individuals and populations. However, the evolution of gene expression underlying complex traits over macroevolutionary ...timescales remains poorly understood. Snake venoms are proteinaceous cocktails where the expression of each toxin can be quantified and mapped to a distinct genomic locus and traced for millions of years. Using a phylogenetic generalized linear mixed model, we analyzed expression data of toxin genes from 52 snake species spanning the 3 venomous snake families and estimated phylogenetic covariance, which acts as a measure of evolutionary constraint. We find that evolution of toxin combinations is not constrained. However, although all combinations are in principle possible, the actual dimensionality of phylomorphic space is low, with envenomation strategies focused around only four major toxin families: metalloproteases, three-finger toxins, serine proteases, and phospholipases A2. Although most extant snakes prioritize either a single or a combination of major toxin families, they are repeatedly recruited and lost. We find that over macroevolutionary timescales, the venom phenotypes were not shaped by phylogenetic constraints, which include important microevolutionary constraints such as epistasis and pleiotropy, but more likely by ecological filtering that permits a small number of optimal solutions. As a result, phenotypic optima were repeatedly attained by distantly related species. These results indicate that venoms evolve by selection on biochemistry of prey envenomation, which permit diversity through parallelism, and impose strong limits, since only a few of the theoretically possible strategies seem to work well and are observed in extant snakes.
The ability to generate long sequencing reads and access long-range linkage information is revolutionizing the quality and completeness of genome assemblies. Here we use a hybrid approach that ...combines data from four genome sequencing and mapping technologies to generate a new genome assembly of the honeybee Apis mellifera. We first generated contigs based on PacBio sequencing libraries, which were then merged with linked-read 10x Chromium data followed by scaffolding using a BioNano optical genome map and a Hi-C chromatin interaction map, complemented by a genetic linkage map.
Each of the assembly steps reduced the number of gaps and incorporated a substantial amount of additional sequence into scaffolds. The new assembly (Amel_HAv3) is significantly more contiguous and complete than the previous one (Amel_4.5), based mainly on Sanger sequencing reads. N50 of contigs is 120-fold higher (5.381 Mbp compared to 0.053 Mbp) and we anchor > 98% of the sequence to chromosomes. All of the 16 chromosomes are represented as single scaffolds with an average of three sequence gaps per chromosome. The improvements are largely due to the inclusion of repetitive sequence that was unplaced in previous assemblies. In particular, our assembly is highly contiguous across centromeres and telomeres and includes hundreds of AvaI and AluI repeats associated with these features.
The improved assembly will be of utility for refining gene models, studying genome function, mapping functional genetic variation, identification of structural variants, and comparative genomics.
Eusociality has convergently evolved multiple times, but the genomic basis of caste-based division of labor and degree to which independent origins of eusociality have utilized common genes remain ...largely unknown. Here we characterize caste-specific transcriptomic profiles across development and adult body segments from pharaoh ants (Monomorium pharaonis) and honey bees (Apis mellifera), representing two independent origins of eusociality. We identify a substantial shared core of genes upregulated in the abdomens of queen ants and honey bees that also tends to be upregulated in mated female flies, suggesting that these genes are part of a conserved insect reproductive groundplan. Outside of this shared groundplan, few genes are differentially expressed in common. Instead, the majority of the thousands of caste-associated genes are plastically expressed, rapidly evolving, and relatively evolutionarily young. These results emphasize that the recruitment of both highly conserved and lineage-specific genes underlie the convergent evolution of novel traits such as eusociality.
Key innovations provide ecological opportunity by enabling access to new resources, colonization of new environments, and are associated with adaptive radiation. The most well-known pattern ...associated with adaptive radiation is an early burst of phenotypic diversification. Venoms facilitate prey capture and are widely believed to be key innovations leading to adaptive radiation. However, few studies have estimated their evolutionary rate dynamics. Here, we test for patterns of adaptive evolution in venom gene expression data from 52 venomous snake species. By identifying shifts in tempo and mode of evolution along with models of phenotypic evolution, we show that snake venom exhibits the macroevolutionary dynamics expected of key innovations. Namely, all toxin families undergo shifts in their rates of evolution, likely in response to changes in adaptive optima. Furthermore, we show that rapid-pulsed evolution modelled as a Lévy process better fits snake venom evolution than conventional early burst or Ornstein-Uhlenbeck models. While our results support the idea of snake venom being a key innovation, the innovation of venom chemistry lacks clear mechanisms that would lead to reproductive isolation and thus adaptive radiation. Therefore, the extent to which venom directly influences the diversification process is still a matter of contention.
Evolutionary innovations underlie the rise of diversity and complexity-the 2 long-term trends in the history of life. How does natural selection redesign multiple interacting parts to achieve a new ...emergent function? We investigated the evolution of a biomechanical innovation, the latch-spring mechanism of trap-jaw ants, to address 2 outstanding evolutionary problems: how form and function change in a system during the evolution of new complex traits, and whether such innovations and the diversity they beget are repeatable in time and space. Using a new phylogenetic reconstruction of 470 species, and X-ray microtomography and high-speed videography of representative taxa, we found the trap-jaw mechanism evolved independently 7 to 10 times in a single ant genus (Strumigenys), resulting in the repeated evolution of diverse forms on different continents. The trap mechanism facilitates a 6 to 7 order of magnitude greater mandible acceleration relative to simpler ancestors, currently the fastest recorded acceleration of a resettable animal movement. We found that most morphological diversification occurred after evolution of latch-spring mechanisms, which evolved via minor realignments of mouthpart structures. This finding, whereby incremental changes in form lead to a change of function, followed by large morphological reorganization around the new function, provides a model for understanding the evolution of complex biomechanical traits, as well as insights into why such innovations often happen repeatedly.
Vector-borne viral diseases threaten human and wildlife worldwide. Vectors are often viewed as a passive syringe injecting the virus. However, to survive, replicate and spread, viruses must ...manipulate vector biology. While most vector-borne viral research focuses on vectors transmitting a single virus, in reality, vectors often carry diverse viruses. Yet how viruses affect the vectors remains poorly understood. Here, we focused on the varroa mite (Varroa destructor), an emergent parasite that can carry over 20 honey bee viruses, and has been responsible for colony collapses worldwide, as well as changes in global viral populations. Co-evolution of the varroa and the viral community makes it possible to investigate whether viruses affect vector gene expression and whether these interactions affect viral epidemiology.
Using a large set of available varroa transcriptomes, we identified how abundances of individual viruses affect the vector's transcriptional network. We found no evidence of competition between viruses, but rather that some virus abundances are positively correlated. Furthermore, viruses that are found together interact with the vector's gene co-expression modules in similar ways, suggesting that interactions with the vector affect viral epidemiology. We experimentally validated this observation by silencing candidate genes using RNAi and found that the reduction in varroa gene expression was accompanied by a change in viral load.
Combined, the meta-transcriptomic analysis and experimental results shed light on the mechanism by which viruses interact with each other and with their vector to shape the disease course.
Parent-of-origin effects, whereby specific phenotypes are differentially inherited paternally or maternally, provide useful clues to better understand transgenerational effect transmission. Ancestral ...diet influences offspring phenotypes, including body composition and fitness. However, the specific role that mothers and fathers play in the transmission of altered phenotypes to male and female offspring remains unclear. We investigated the influence of the parent-of-origin's diet on adult progeny phenotypes and reproductive output for three generations in fruit flies ( Drosophila melanogaster). Males and females reared on a control diet were exposed to the control diet or one of two altered (no- or high-) sugar treatment diets for a single generation. Flies from one of the two altered diet treatments were then mated to control flies in a full-factorial design to produce F
offspring and kept on control media for each following generation. We found parent-of-origin (triglyceride) and non-parent-of-origin (sugar) body composition effects, which were transgenerational and sex-specific. Additionally, we observed a negative correlation between intergenerational maternal reproductive output and triglyceride levels, suggesting that ancestral diet may affect fitness. This work demonstrates that ancestral diet can transmit altered phenotypes in a parent-of-origin and sex-specific manner and highlights that mechanisms regulating such transmission have been greatly overlooked. This article is part of the theme issue 'The role of plasticity in phenotypic adaptation to rapid environmental change'.
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