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bioRxiv2018

High-density linkage map and QTLs for growth in snapper (Chrysophrys auratus)

Characterizing the genetic variation underlying phenotypic traits is a central objective in biological research. This research has been hampered in the past by the limited genomic resources available for most non-model species. However, recent advances in sequencing technology and related genotyping methods are rapidly changing this. Here we report the use of genome-wide SNP data from the ecologically and commercially important marine fish species Chrysophrys auratus (snapper) to 1) construct the first linkage map for this species, 2) scan for growth QTLs, and 3) search for candidate genes in the surrounding QTL regions. The newly constructed linkage map contained ~11K SNP markers and is the densest map to date in the fish family Sparidae. Comparisons with available genome scaffolds indicated that overall marker placement was strongly correlated between the scaffolds and linkage map (R = 0.7), but at fine scales (< 5 cM) there were some precision limitations. Of the 24 linkage groups, which reflect the 24 chromosomes of this species, three were found to contain QTLs with genome-wide significance for growth-related traits. A scan for 13 known candidate growth genes located the genes for growth hormone, parvalbumin, and myogenin within 13.2, 2.6, and 5.0 cM of these genome-wide significant QTLs, respectively. The linkage map and QTLs found in this study will advance the investigation of genome structure and selective breeding in snapper.

evolutionary biology↗

bioRxiv2018

Extreme genetic structure and dynamic range evolution in a montane passerine bird: implications for tropical diversification

AimEmploy phylogeographic analyses of a widespread species complex to examine the role of historical and evolutionary processes in the origin and maintenance of high species diversity in the Neotropical montane region.\n\nLocationNeotropical highlands.\n\nTaxonHenicorhina wood-wrens (Aves, Troglodytidae).\n\nMethodsWe collected mtDNA sequence data for 288 individuals thoroughly covering the range of the Henicorhina leucophrys complex from Mexico to Bolivia. Sequences were employed to characterize population structure, infer phylogenetic relationships among populations and their divergence times, examine lineage accumulation through time, and identify presumptive species using coalescent methods. We also explored the origin of elevational and latitudinal replacements involved in spatial changes in species assemblages in the Andes.\n\nResultsWe found remarkable genetic structure within the complex, which consists of numerous lineages reaching >12% sequence divergence; most divergent populations occur in areas separated by topographic barriers but several of them, typically not sister to each other, co-occur with elevational segregation on mountain slopes or replace each other with latitude along the Andes. Some close relatives occur in areas separated by thousands of kilometers, with more distant relatives occupying intervening areas. The complex likely originated in the Mexican highlands and expanded extensively in South America while diverging rapidly at a constant rate into many different lineages which have persisted for millions of years. Coalescent analyses consistently revealed that the complex may comprise more than 30 species; while we do not suggest these presumptive species should be recognized by taxonomists in the absence of additional data, H. leucophrys is a distant outlier among New World birds in terms of high lineage diversity within a single recognized species.\n\nMain ConclusionsOur study captured wood-wren lineages in the act of building up diversity via divergence and persistence in allopatry, achievement of secondary sympatry, and coexistence at the landscape scale mediated by ecological and evolutionary divergence. Although dispersal by wood-wrens is restricted at present and this likely accounts for strong population structure across topographic barriers, their ranges have been dynamic, managing to disperse over much of the montane Neotropics. Phases of expansion and contraction of ranges and localized extinctions of populations likely account for phylogeographic patterns which are precursors to the origin of new species and the accumulation of diversity in tropical mountains.

evolutionary biology↗

bioRxiv2018

Sexual behavior of the desert locust during intra- and inter-phase interactions

Mating and reproduction behaviors and strategies are fundamental aspects of an organisms evolutionary and ecological success. In locusts, intra- as well as inter-phase reproductive interactions among gregarious and solitarious locust populations have a major impact on the locust population dynamics. However, practically all previous work on locust sexual behavior has been limited to the gregarious phase. Here we provide a first detailed description of pre-copulatory behavior of solitarious desert locusts. We compare our findings with those of previous reports of pre-copulatory behavior of gregarious locusts, focusing on the behavioral elements that serve in inter-sex signaling and communication. We also studied inter-phase (mixed pairs) reproductive interactions. Solitarious males were found to invest more in pre-copulatory courtship and signaling compared to their gregarious counterparts; and the solitarious females played a comparatively more dominant role in the inter-sex communication. The solitarious females were also less prone to demonstrate the typical rejection-related behavioral patterns displayed by the gregarious females. As a consequence of the particular characteristic behavior of each phase, the most successful among intra- and inter-phase pairs were gregarious males with solitary females. Least successful were solitary males encountered with gregarious females, indicating a strong asymmetry in inter-phase reproductive interactions. We discuss these results in the context of non-random or assortative mating in locust mixed or sympatric solitarious-gregarious populations.

animal behavior and cognition↗

bioRxiv2018

Short-term insurance versus long-term bet-hedging strategies as adaptations to variable environments

Understanding how organisms adapt to environmental variation is a key challenge of biology. Central to this are bet-hedging strategies that maximize geometric mean fitness across generations, either by being conservative or diversifying phenotypes. Theoretical models of bet-hedging and the multiplicative fitness effects of environmental variation across generations have traditionally assumed that environmental conditions are constant within lifetimes. However, behavioral ecology has revealed adaptive responses to additive fitness effects of environmental variation within lifetimes, either through insurance or risk-sensitive strategies. Here we explore whether the effects of adaptive insurance interact with the evolution of bet-hedging by varying the position and skew of fitness functions within and between lifetimes. When insurance causes the optimal phenotype to shift from the peak to down the less steeply decreasing side of the fitness function, then conservative bet-hedging does not generally evolve on top of this, even if diversifying bet-hedging can. Canalization to reduce phenotypic variation within a lifetime is almost always favored, except when the tails of the fitness function are steeply convex and produce a novel risk-sensitive increase in phenotypic variance akin to diversifying bet-hedging. Importantly, using skewed fitness functions, we provide the first example of how conservative and diversifying bet-hedging strategies might coexist.

evolutionary biology↗

bioRxiv2018

Out of Africa by spontaneous migration waves

Hominin evolution is characterized by progressive regional differentiation, as well as migration waves, leading to anatomically modern humans that are assumed to have emerged in Africa and spread over the whole world. Why or whether Africa was the source region of modern humans and what caused their spread remains subject of ongoing debate. We present a spatially explicit, stochastic numerical model that includes ongoing mutations, demic diffusion, assortative mating and migration waves. Diffusion and assortative mating alone result in a structured population with relatively homogeneous regions bound by sharp clines. The addition of migration waves results in a power-law distribution of wave areas: for every large wave, many more small waves are expected to occur. This suggests that one or more out-of-Africa migrations would probably have been accompanied by numerous smaller migration waves across the world. The migration waves are considered \"spontaneous\", as the current model excludes environmental or other factors. Large waves preferentially emanate from the central areas of large, compact inhabited areas. During the Pleistocene, Africa was the largest such area most of the time, making Africa the statistically most likely origin of anatomically modern humans, without a need to invoke additional environmental or ecological drivers.

evolutionary biology↗

bioRxiv2018

Stress response, behavior, and development are shaped by transposable element-induced mutations in Drosophila

Mapping genotype to phenotype is challenging because of the difficulties in identifying both the traits under selection and the specific genetic variants underlying these traits. Most of the current knowledge of the genetic basis of adaptive evolution is based on the analysis of single nucleotide polymorphisms (SNPs). Despite increasing evidence for their causal role, the contribution of structural variants to adaptive evolution remains largely unexplored. In this work, we analyzed the population frequencies of 1,615 Transposable Element (TE) insertions in 91 samples from 60 worldwide natural populations of Drosophila melanogaster. We identified a set of 300 TEs that are present at high population frequencies, and located in genomic regions with high recombination rate, where the efficiency of natural selection is high. The age and the length of these 300 TEs are consistent with relatively young and long insertions reaching high frequencies due to the action of positive selection. Indeed, we, and others, found evidence of selective sweeps and/or population differentiation for 65 of them. The analysis of the genes located nearby these 65 candidate adaptive insertions suggested that the functional response to selection is related with the GO categories of response to stimulus, behavior, and development. We further showed that a subset of the candidate adaptive TEs affect expression of nearby genes, and five of them have already been linked to an ecologically relevant phenotypic effect. Our results provide a more complete understanding of the genetic variation and the fitness-related traits relevant for adaptive evolution. Similar studies should help uncover the importance of TE-induced adaptive mutations in other species as well.

evolutionary biology↗

bioRxiv2018

Genome sequence of the wheat stem sawfly, Cephus cinctus, a primitive hymenopteran and wheat pest, illuminates evolution of hymenopteran chemoreceptors

The wheat stem sawfly, Cephus cinctus, is a major pest of wheat and key ecological player in the grasslands of western North America. It also represents a distinctive lineage of sawflies that appeared early during the hymenopteran radiation, but after the clade of Eusymphyta sawflies that is the sister lineage of all other Hymenoptera. We present a high-quality draft genome assembly of 162 Mbp in 1,976 scaffolds with a scaffold N50 of 622 kbp. Automated gene annotation identified 11,210 protein-coding gene models and 1,307 non-coding RNA models. Thirteen percent of the assembly consists of ~58,000 transposable elements partitioned equally between Class-I and Class-II elements. Orthology analysis reveals that 86% of Cephus proteins have identifiable orthologs in other insects. Phylogenomic analysis of conserved subsets of these proteins supports the placement of the Cephidae between the Eusymphyta and the parasitic woodwasp superfamily Orussoidea. Manual annotation and phylogenetic analysis of families of odorant, gustatory, and ionotropic receptors, plus odorant binding proteins, shows that Cephus has representatives for most conserved and expanded gene lineages in the Apocrita (wasps, ants, and bees). Cephus has also maintained several insect gene lineages that have been lost from the Apocrita, most prominently the carbon dioxide receptor subfamily. Furthermore, Cephus encodes a few small lineage-specific chemoreceptor gene family expansions that might be involved in adaptations to new grasses including wheat. These comparative analyses identify gene family members likely to have been present in the hymenopteran ancestor and provide a new perspective on the evolution of the chemosensory gene repertoire.

genomics↗

bioRxiv2018

High-resolution 4D spatiotemporal analysis reveals the contributions of local growth dynamics to contrasting maize root system architectures

Root systems are branched networks that develop from simple growth properties of their individual roots. Yet a mature maize root system has many thousands of roots that each interact with soil structures, water and nutrient patches, and microbial ecologies in the micro-environments surrounding each root tip. Although the plasticity of root growth to these and other environmental factors is well known, how the many local processes contribute over time to global features of root system architecture is hardly understood. We employ an automated 3D root imaging pipeline to capture the growth of maize roots every four hours throughout seven days of seedling development. We model the contrasting architectures of two maize inbred genotypes and their hybrid to derive key parameters that distinguish complex growth patterns as a function of time. The statistical characteristics of local root growth defined the global system properties despite a large range of trait values. \"Computational dissection\" of a single root from each root system identified differences in the size of the root branching zone and lateral branching densities, but not radial patterns, that drove the contrasting root architectures from seedling to maturity. X-ray imaging of mature field-grown root crowns showed that seedling growth trajectories persisted throughout development and could predict eventual architectures, suggesting a strong genetic basis. The work connects individual and systemwide scales of root growth dynamics, providing the means for a function-valued approach to understanding the genetic and genetic x environment conditioning of root growth that will enable breeding for enhanced root traits.\n\nSIGNIFICANCE STATEMENTWhen and where roots grow determines their ability to capture short-lived and patchy water and nutrient resources to support the aboveground organs of the plant. Roots have no known long-distance external sensing mechanisms, but form branched networks that blindly explore the soil and respond to encountered local stimuli. How global architectures form from the many thousands of these local responses, and how they are controlled genetically are major open questions. Here we quantify differences in local root growth patterns of two inbred genotypes of maize that control contrasting systemwide properties. Measurements at the seedling stage were highly correlated with the complex architectures of mature root systems, paving the way for the development of crops with greater resource uptake capacity.

plant biology↗

bioRxiv2018

An Ishihara-style test of animal colour vision

O_LIColour vision mediates ecologically relevant tasks for many animals, such as mate choice, foraging and predator avoidance. However, our understanding of animal colour perception is largely derived from human psychophysics, even though animal visual systems differ from our own. Behavioural tests of non-human animals are required to understand how colour signals are perceived by them.\nC_LIO_LIHere we introduce a novel test of colour vision in animals inspired by the Ishihara colour charts, which are widely used to identify human colour deficiencies. These charts consist of dots that vary in colour, brightness and size, and are designed so that a numeral or letter is distinguishable from distractor dots for humans with normal colour vision. In our method, distractor dots have a fixed chromaticity (hue and saturation) but vary in luminance. Animals can be trained to find single target dots that differ from distractor dots in chromaticity. We provide Matlab code for creating these stimuli, which can be modified for use with different animals.\nC_LIO_LIWe demonstrate the success of this method with triggerfish, Rhinecanthus aculeatus, and highlight behavioural parameters that can be measured, including success of finding the target dot, time to detect dot and error rate. Triggerfish quickly learnt to select target dots that differed from distractors dots regardless of the particular hue or saturation, and proved to use acute colour vision. We measured discrimination thresholds by testing the detection of target colours that were of increasing colour distances ({Delta}S) from distractor dots in different directions of colour space. At least for some colours, thresholds indicated better discrimination than expected from the Receptor Noise Limited (RNL) model assuming 5% Weber fraction for the long-wavelength cone.\nC_LIO_LIThis methodology seems to be highly effective because it resembles natural foraging behavior for the triggerfish and may well be adaptable to a range of other animals, including mammals, birds, bees and freshwater fish. Other questions may be addressed using this methodology, including luminance thresholds, sensory bias, effects of sensory noise in detection tasks, colour categorization and saliency.\nC_LI

animal behavior and cognition↗

bioRxiv2018

The fitness consequences of genetic variation in wild populations of mice

Adaptive evolution can occur when genetic change affects traits subject to natural selection. Although selection is a deterministic process, adaptation can be difficult to predict in finite populations because the functional connections between genotype, phenotype, and fitness are complex. Here, we make these connections using a combination of field and laboratory experiments. We conduct a large-scale manipulative field experiment with wild populations of deer mice in distinct habitats to directly estimate natural selection on pigmentation traits and next test whether this selection drives changes in allele frequency at an underlying pigment locus. We find that divergent cryptic phenotypes are repeatedly favoured in each habitat, leaving footprints of selection in the Agouti gene. Next, using transgenic experiments in Mus, we functionally test one of the Agouti mutations associated with survival, a Serine deletion in exon 2, and find that it causes lighter coat colour via changes in its protein binding properties. Finally, we show significant change in the frequency of this mutation in our field experiment. Together, our findings demonstrate how a sequence variant alters phenotype and show the ensuing ecological consequences that drive changes in population allele frequency, thereby revealing the full process of evolution by natural selection.

evolutionary biology↗

bioRxiv2018

Antiviral genes are not rapidly evolving in Drosophila innubila

Viruses make up a considerable proportion of the pathogens infecting animals. They can spread rapidly between hosts, and sicken or even kill their hosts to promote their own proliferation. Due to this strong selective pressure, antiviral immune genes are some of the fastest evolving genes across metazoans, as highlighted in mammals and insects. While Drosophila melanogaster are frequently exposed to pathogenic RNA viruses, little is known about D. melanogasters ecology in terms of viral exposure, or if they are representative of other Drosophila species. Here, we sequence and assemble the genome of a highly diverged, mushroom-feeding Drosophila species, Drosophila innubila, a species frequently exposed to a highly pathogenic DNA virus. We investigate the evolution of the immune system and find little evidence for rapid evolution of the antiviral RNAi genes, though we do find rapid evolution of several other pathways, suggesting alternate means of viral resistance. This contrasts with D. melanogaster, and suggests that evolution of resistance to DNA viruses differs greatly from that of RNA viruses.

genomics↗

bioRxiv2018

Emergence of trait variability through the lens of nitrogen assimilation in Prochlorococcus

Intraspecific trait variability has important consequences for the function and stability of marine ecosystems. The marine cyanobacterium Prochlorococcus is a useful model system for understanding how trait variability emerges within microbial species: Its functional diversity is overlaid on measurable environmental gradients, providing a powerful lens into large-scale evolutionary processes. Here we examine variation in the ability to use nitrate across hundreds of Prochlorococcus genomes to better understand the modes of evolution influencing the allocation of ecologically important functions within microbial species. We find that nitrate assimilation genes are absent in basal lineages of Prochlorococcus but occur at an intermediate frequency that is randomly distributed within recently emerged clades. The distribution of nitrate assimilation genes within clades appears largely governed by vertical inheritance, stochastic gene loss, and homologous recombination among closely related cells. By mapping this process onto a model of Prochlorococcus macroevolution, we propose that niche-constructing adaptive radiations and subsequent niche partitioning set the stage for loss of nitrate assimilation genes from basal lineages as they specialized to lower light levels. Retention of these genes in recently emerged lineages has likely been facilitated by selection as they sequentially partitioned into niches where nitrate assimilation conferred a fitness benefit.

evolutionary biology↗

bioRxiv2018

Sex overrides mutation in Escherichia coli colonizing the gut

Bacteria evolve by mutation accumulation in laboratory experiments, but the tempo and mode of evolution in natural environments are largely unknown. Here we show, by experimental evolution of E. coli in the mouse gut, that the ecology of the gut controls bacterial evolution. If a resident E. coli strain is present in the gut, an invading strain evolves by rapid horizontal gene transfer; this mode precedes and outweighs evolution by point mutations. An epidemic infection by two phages drives gene uptake and produces multiple co-existing lineages of phage-carrying (lysogenic) bacteria. A minimal dynamical model explains the temporal pattern of phage epidemics and their complex evolutionary outcome as generic effects of phage-mediated selection. We conclude that phages are an important eco-evolutionary driving force - they accelerate evolution and promote genetic diversity of bacteria.\n\nOne Sentence SummaryBacteriophages drive rapid evolution in the gut.

evolutionary biology↗

bioRxiv2018

Familiarity increases aggressiveness among clonal fish.

Understanding how animal groups form and function is a major goal in behavioural ecology. Both genetic relatedness and familiarity among group mates have been shown to be key mediators of group composition. However, disentangling the two in most species is challenging as the most familiar individuals are often the most related, and vice versa. In order to gain a complete understanding of how individual interactions shape group behaviour it is crucial to understand the role each of this social relationship factors plays individually. To this end, we manipulated the level of familiarity among groups of the naturally clonal, and genetically identical fish, the Amazon molly (Poecilia formosa) and monitored group behaviour in an open-field and when given the opportunity to forage. Contrary to our predictions, fish that were the most familiar with each other showed the highest levels of aggression. Additionally, fish that were less familiar with each other exhibited the highest group cohesion and took the longest to begin feeding, compared to the more familiar fish. These results suggest that familiarity may socially buffer individuals from the perception of risk in novel environments, such as is common in most behavioural tests designed to test group behaviour. Increases in aggression that are associated with increasing familiarity as shown here might be a mechanism by which fish maintain a fission-fusion society with important consequences for the patterns of associations in group living animals.

animal behavior and cognition↗

bioRxiv2018

Bacterial and fungal contributions to delignification and lignocellulose degradation in forest soils with metagenomic and quantitative stable isotope probing

Delignification, or lignin-modification, facilitates the decomposition of lignocellulose in woody plant biomass. The extant diversity of lignin-degrading bacteria and fungi is underestimated by culture-dependent methods, limiting our understanding of the functional and ecological traits of decomposers populations. Here, we describe the use of stable isotope probing (SIP) coupled with amplicon and shotgun metagenomics to identify and characterize the functional attributes of lignin-, cellulose-and hemicellulose-degrading fungi and bacteria in coniferous forest soils from across North America. We tested the extent to which catabolic genes partitioned among different decomposer taxa; the relative roles of bacteria and fungi, and whether taxa or catabolic genes correlated with variation in lignocellulolytic activity, measured as the total assimilation of 13C-label into DNA and phospholipid fatty acids. We found high overall bacterial degradation of our model lignin substrate, particularly by gram-negative bacteria (Comamonadaceae and Caulobacteraceae), while fungi were more prominent in cellulose-degradation. Very few taxa incorporated 13C-label from more than one lignocellulosic polymer, suggesting specialization among decomposers. Collectively, members of Caulobacteraceae could degrade all three lignocellulosic polymers, providing new evidence for their importance in lignocellulose degradation. Variation in lignin-degrading activity was better explained by microbial community properties, such as catabolic gene content and community structure, than cellulose-degrading activity. SIP significantly improved shotgun metagenome assembly resulting in the recovery of several high-quality draft metagenome-assembled genomes and over 7,500 contigs containing unique clusters of carbohydrate-active genes. These results improve understanding of which organisms, conditions and corresponding functional genes contribute to lignocellulose decomposition.

molecular biology↗

bioRxiv2018

A Swiftian Voyage from Brobdingnag to Lilliput: Freshwater Planctomycetes drifting towards the poles of the genome size spectrum

Freshwater environments teem with microbes. Currently, our apprehension of evolutionary ecology of freshwater bacteria is hampered by the difficulty to establish organism models for the most representative clades. To circumvent the bottlenecks inherent to the cultivation-based techniques, we applied ecogenomics approaches in order to unravel the evolutionary history and the processes that drive genome architecture in hallmark freshwater lineages from Planctomycetes phylum. The evolutionary history inferences showed that sediment/soil Planctomycetes transitioned to aquatic environments were, through processes mostly associated with reductive genome evolution, gave rise to new freshwater-specific clades. The most successful lineage was found to simultaneously have the most specialized lifestyle (increased regulatory genetic circuits; metabolism tuned for mineralization of proteinaceous sinking aggregates; psychrotrophic behavior) and to harbor the smallest genomes, highlighting a genomic architecture shaped by niche-directed evolution.

microbiology↗

bioRxiv2018

Resistant potato starch fuels beneficial host-microbe interactions in the gut

Interactions between diet, the microbiota, and the host set the ecological conditions in the gut and have broad implications for health. Prebiotics are dietary compounds that may shift these conditions towards health by promoting the growth of beneficial microbes. Pigs fed a diet amended with 5% resistant potato starch (RPS) exhibited alterations associated with gut health relative to swine fed an unamended diet (CON). RPS intake increased abundances of anaerobic Clostridia in feces and several tissues, as well as intestinal concentrations of butyrate. Functional gene amplicons suggested bacteria similar to Anaerostipes hadrus were stimulated by RPS intake. The CON treatment exhibited increased abundances of several genera of Proteobacteria (which utilize respiratory metabolisms) in several location. RPS intake increased the abundance of regulatory T cells in the cecum, but not periphery, and cecal immune status alterations were indicative of enhanced mucosal defenses. A network analysis of host and microbial changes in the cecum revealed that regulatory T cells positively correlated with butyrate concentration, luminal IgA concentration, expression of IL-6 and DEF1B, and several mucosa-associated bacterial taxa. Thus, the administration of RPS modulated the microbiota and host response, improved cecal barrier function, promoted immunological tolerance, and reduced the niche for bacterial respiration.\n\nImportanceThe gut microbiota is central to host health. Many disease states and disorders appear to arise from interactions between the gut microbial community and host immune system. As a result, methods and interventions to support the growth and activity of beneficial gut microbes are being actively pursued. Feeding the gut microbiota with dietary compounds, known as prebiotics, is one of the most promising ways to support gut health. Here we describe a successful prebiotic intervention in weaning swine, a relevant translational model for human health. This work unites microbial and immunological data and demonstrates one way a prebiotic intervention can play out for the benefit of the host.

systems biology↗

bioRxiv2018

Mitochondrial DNA and their nuclear copies in parasitic wasp Pteromalus puparum: A comparative analysis in Chalcidoidea

Chalcidoidea (chalcidoid wasps) are an abundant and megadiverse insect group with both ecological and economical importance. Here we report a complete mitochondrial genome in Chalcidoidea from Pteromalus puparum (Pteromalidae). Eight tandem repeats followed by 6 reversed repeats were detected in its 3,308 bp control region. This long and complex control region may explain failures of amplifying and sequencing of complete mitochondrial genomes in some chalcidoids. In addition to 37 typical mitochondrial genes, an extra identical isoleucine tRNA (trnI) was detected. We speculate this recent mitochondrial gene duplication indicates that gene arrangements in chalcidoids are ongoing. A comparison among available chalcidoid mitochondrial genomes, reveals rapid gene order rearrangements overall, and high substitution rate in P. puparum. In addition, we identified 24 nuclear sequences of mitochondrial origin (NUMTs) in P. puparum, summing up to 9,989 bp, with 3,617 bp of these NUMTs originating from mitochondrial coding regions. NUMTs abundance in P. puparum is only one-twelfth of that in its relative, Nasonia vitripennis. Based on phylogenetic analysis, we provide evidence that a faster nuclear degradation rate contributes to the reduced NUMT numbers in P. puparum. Overall, our study shows unusually high rates of mitochondrial evolution and considerable variation in NUMT accumulation in Chalcidoidea.

genomics↗