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Johnson, K. P.

Publications and source records attributed to Johnson, K. P..

At least 19 recordsLinked to original sources

A phylogenomic framework for avian feather lice (Phthiraptera: Ischnocera)

Comprehensive phylogenies serve as foundations for taxonomic, comparative, and coevolutionary studies. Avian feather lice comprise the most diverse Parvorder (Ischnocera) of parasitic lice (Phthiraptera). Convergence and reduction of morphological features in this group have made past attempts at understanding the evolutionary relationships of feather lice challenging. Several recent phylogenomic studies have begun shedding light on the broader scale evolutionary tree of this group. However, additional taxonomic sampling is needed for a more complete understanding of the phylogeny and for higher statistical power in comparative studies. Here we investigate the higher-level relationships of feather lice based on the most comprehensive taxon sample to date. We leverage genome sequences of 260 samples of feather lice and 25 outgroup taxa to reconstruct a phylogenomic tree based on 2,395 target nuclear ortholog genes, using both concatenated and coalescent methods. These trees provide high support across nearly all branches of the topology, resolving backbone relationships as well as more detailed relationships within major groups. These phylogenies provide a framework for future comparative studies of feather lice, including comparisons with avian phylogeny and investigating patterns of diversification.

evolutionary biology↗

The genomic landscape of asymmetric introgression tracks chromosomal characteristics in tinamous (Aves: Tinamidae)

We use single genomes from seven tinamou species (Palaeognathae: Tinamidae) and apply a genome-architecture-aware phylogenomic approach to (1) quantify the landscape of introgression, (2) discriminate among conflicting genealogical signals in the genome, and (3) reconstruct evolutionary history. Using summary statistics and full likelihood, we detect pervasive asymmetric introgression between two sympatric Amazonian species clouding phylogenetic relationships in this group. However, these introgression results are sensitive to the assumed species tree. When assuming the Z-chromosome phylogeny as the species tree, the landscape of introgression is non-random; introgression is negatively associated with chromosome length, elevated at macrochromosome ends, and near zero for the Z-chromosome (the avian sex chromosome). A pseudo-autosomal region on the Z-chromosome, which recombines homologously with that of the W-chromosome, shows elevated introgression comparable to that of autosomes. Our results resolve the species tree of tinamous and imply a history of linked selection purging migrant alleles that are deleterious in the hybrid genome. This selection is countered in regions of the genome expected to experience elevated recombination, allowing introgressed alleles to accumulate across >20% of the genome. This work demonstrates a genome-architecture-aware approach to resolving the species tree in the face of introgression. As chromosome-level reference genomes spanning the tree of life become increasingly available, phylogenomic studies would benefit from the adoption of genome-architecture-aware approaches like ours. This is because the genomic landscapes of introgression and genealogy are largely predicted by chromosomal characteristics.

genomics↗

Independent and repeated acquisition of endosymbiotic bacteria across the diversification of feather lice

Many parasitic insects, including lice, form close relationships with endosymbiotic bacteria that are crucial for their survival. In this study, we used genomic sequencing to investigate the distribution and evolutionary history of the bacterial genus Sodalis across a broad range of feather louse species spanning 156 genera. Phylogenomic analysis revealed significant diversity among Sodalis lineages in feather lice, and robust evidence for their independent and repeated acquisition by different louse clades throughout their radiation. Among the 1,020 louse genomes analyzed, at least 22% contained Sodalis, distributed across 57 louse genera. Cophylogenetic analyses between the Sodalis and feather louse phylogenies indicated considerable mismatch. This phylogenetic incongruence between lice and Sodalis, along with the presence of distantly related Sodalis lineages in otherwise closely related louse species, strongly indicates repeated independent acquisition of this endosymbiont. Additionally, evidence of cospeciation among a few closely related louse species, coupled with frequent acquisition of these endosymbionts from free-living bacteria, further highlights the diverse evolutionary processes shaping Sodalis endosymbiosis in feather lice.

evolutionary biology↗

Genomics of experimental adaptive radiation in the cryptic coloration of feather lice

1A major challenge faced by living organisms is adaptation to novel environments. This process is poorly understood because monitoring genetic changes in natural populations is difficult. One way to simplify the task is to focus on organisms that can be studied in captivity under conditions that remain largely natural. Feather lice (Insecta, Phthiraptera, Ischnocera) are host-specific parasites of birds that live, feed, and breed solely on feathers. Birds defend themselves against lice, which damage feathers, by killing them with their beaks during bouts of preening. In response, feather lice have evolved background-matching cryptic coloration to help them avoid preening. We experimentally manipulated the color backgrounds of host-specific pigeon lice (Columbicola columbae) by confining them to different colored breeds of rock pigeon (Columba livia) over a period of four years (ca. 60 louse generations). Over the course of the experiment, we sampled lice from pigeons every six months for genomic resequencing, and then calculated allele frequency differences and trajectories to identify putative genomic sites under selection. We documented many loci that changed in response to selection for color. Most loci putatively under selection were unshared among replicate populations of lice, indicating that independent adaptation of distinct lineages to the same novel environment resulted in similar phenotypes driven by different genotypes.

evolutionary biology↗

Whole-genome phylogenomics of the tinamous (Aves: Tinamidae): comparing gene tree estimation error between BUSCOs and UCEs illuminates rapid divergence with introgression

As an old group that has diversified in South America over millions of years, the tinamous (Palaeognathae: Tinamidae) are of high interest for understanding the evolution of birds and the assembly of the Neotropical biota. However, there are currently no complete species-level phylogenies of this group. Most prior work has been based on either morphological data or a small number of molecular markers, each of which has limited capability for reconstructing the tinamou phylogeny. Therefore, the interrelationships of most tinamou species are uncertain. We analyzed 80 whole-genomes from a mix of historical study skins and frozen tissues, including all 46 recognized species of tinamous to (1) reconstruct their interrelationships, (2) estimate the timeframe of tinamou evolution, and (3) examine for the effects of incomplete lineage sorting (ILS) and ancestral introgression on genome evolution. We compared results for coding (BUSCO) and ultraconserved element (UCE) loci, as well as sex-linked and autosomal markers, and used fossil-calibrated tip-dating to estimate divergence times. Tinamous diverged from their sister-group, the extinct Moas, 50-60 mya, and their crown divergence occurred roughly 30-40 mya, followed by constant diversification rates until the present. Phylogenetic reconstructions were largely robust across methods and datasets. Only one clade in the genus Crypturellus displayed substantial species-tree discordance across the different data sets. To investigate the impacts of introgression on this discordance, we quantified introgression for 100kb non-overlapping windows across the genome, and identified pervasive genome-wide introgression. The distribution of this introgression across the genome was dependent on the assumed phylogeny applied to the f-branch model. When assuming one of these topologies in the f-branch model, patterns of introgression matched theoretical predictions about genome architecture. Overall, we present the most complete phylogeny for tinamous to date, identify an unrecognized species, and provide a case study for species-level phylogenomic analysis using whole-genomes.

genomics↗

Origin and diversification of a globally distributed group of parasitic feather lice

Despite their extensive diversity and ecological importance, the history of diversification for most groups of parasitic organisms remains relatively understudied. Elucidating broad macroevolutionary patterns of parasites is challenging, often limited by the availability of samples, genetic resources, and knowledge about ecological relationships with their hosts. In this study, we explore the macroevolutionary history of parasites by focusing on parasitic body lice from doves. Building on extensive knowledge of ecological relationships and previous phylogenomic studies of their avian hosts, we tested specific questions about the evolutionary origins of the body lice of doves, leveraging whole genome data sets for phylogenomics. Specifically, we sequenced whole genomes from 68 samples of dove body lice, including representatives of all body louse genera from 51 host taxa. From these data, we assembled >2,300 nuclear genes to estimate dated phylogenetic relationships among body lice and several outgroup taxa. The resulting phylogeny of body lice was well supported, although some branches had conflicting signal across the genome. We then reconstructed ancestral biogeographic ranges of body lice and compared the body louse phylogeny to phylogeny of doves, and also to a previously published phylogeny of the wing lice of doves. Divergence estimates placed the origin of body lice in the late Oligocene. Body lice likely originated in Australasia and dispersed with their hosts during the early Miocene, with subsequent codivergence and host switching throughout the world. Notably, this evolutionary history is very similar to that of dove wing lice, despite the stronger dispersal capabilities of wing lice compared to body lice. Our results highlight the central role of hosts in driving macroevolutionary patterns of their parasites over long periods of time.

evolutionary biology↗

Phylogenomics and biogeography of the feather lice (Phthiraptera: Ischnocera) of parrots

Avian feather lice (Phthiraptera: Ischnocera) have undergone morphological diversification into ecomorphs based on the mechanism for escaping host preening defenses. Parrot lice are one prominent example of this phenomenon, with wing, body, or head louse ecomorphs occurring on various groups of parrots. Currently defined genera of parrot lice typically correspond to this ecomorphological variation. Here we explore the phylogenetic relationships among parrot feather lice by sequencing whole genomes and assembling a target set of 2,395 nuclear protein coding genes. Phylogenetic trees based on concatenated and coalescent analyses of these data reveal highly supported trees with strong agreement between methods of analysis. These trees reveal that parrot feather lice fall into two separate clades that form a grade with respect to the Brueelia-complex. All parrot louse genera sampled by more than one species were recovered as monophyletic. The evolutionary relationships among these lice showed evidence of strong biogeographic signal, which may also be related to the relationships among their hosts.

evolutionary biology↗

Mitogenome fragmentation evolves multiple times within a major group of parasitic lice

Animal mitochondrial genomes (mitogenomes) typically exhibit a highly conserved gene content and organisation, with genes encoded on a single circular chromosome. However, many species of parasitic lice (Insecta: Phthiraptera) are notable exceptions, having mitogenomes fragmented into multiple circular chromosomes. To understand the process of mitogenome fragmentation, we conducted a large-scale genomic study of a major group of lice, Amblycera, with extensive taxon sampling. Analyses of the evolution of mitogenome structure across a phylogenomic tree of 90 samples from 53 genera, revealed evidence for multiple independent origins of mitogenome fragmentation, some inferred to have occurred less than five million years ago. We leveraged these many independent origins of fragmentation to compare the rates of DNA substitution and gene rearrangement, specifically contrasting branches with fragmented and non-fragmented mitogenomes. We found that lineages with fragmented mitochondrial genomes had significantly higher rates of mitochondrial sequence evolution. In addition, lineages with fragmented mitochondrial genomes were more likely to have mitogenome gene rearrangements than those with single-chromosome mitochondrial genomes. By combining phylogenomics and mitochondrial genomics we provide a detailed portrait of mitogenome evolution across this group of insects with a remarkably unstable mitogenome structure, identifying processes of molecular evolution that are correlated with mitogenome fragmentation. Author SummaryMitochondria are organelles that play a key role in providing energy to cells essential for life. The structure of the mitochondrial genome is conserved across most animal groups, being a single circular chromosome containing 37 genes. Deviations from this structure are typically detrimental and associated with some human diseases. However, in very few animal groups, the mitochondrial genome is fragmented into multiple circular chromsomes. In one group of insects, parasitic lice, fragmentation varies among species, with some having a complete circular genome and others having their mitochondrial genome fragmented in two or more smaller chromosomes. Here, we use whole genome sequencing reads to analyze an unprecedented number of species from a diverse group of lice (Amblycera) that exhibits both single-chromosome and fragmented mitochondrial genomes to understand how this fragmentation evolved. We found that fragmentation evolved many times independently in this group and this fragmentation is correlated faster rates mitochondrial molecular evolution and with an increased frequency of gene rearrangement. We also provide evidence that the rate of mitochondrial genome fragmentation changes over time. Altogether, our combination of broad sampling and phylogenomic and comparative analyses provide new insights into the mechanisms and dynamics of mitochondrial genome fragmentation.

molecular biology↗

Chromosome-aware phylogenomics of Assassin Bugs (Hemiptera: Reduvioidea) elucidates ancient gene conflict

Though the phylogenetic signal of loci on sex chromosomes can differ from those on autosomes, chromosomal-level genome assemblies for non-vertebrates are still relatively scarce and conservation of chromosomal gene content across deep phylogenetic scales has therefore remained largely unexplored. We here assemble a uniquely large and diverse set of samples (17 Anchored Hybrid Enrichment [AHE], 24 RNA-Seq, and 70 whole-genome sequencing [WGS] samples of variable depth) for the medically important assassin bugs (Reduvioidea). We assess the performance of genes based on multiple features (e.g., nucleotide vs. amino acid, nuclear vs. mitochondrial, and autosomal vs. X chromosomal) and employ different methods (concatenation and coalescence analyses) to reconstruct the unresolved phylogeny of this diverse ([~]7,000 spp.) and old (>180 MYA) group. Our results show that genes on the X chromosome are more likely to have discordant phylogenies than those on autosomes. We find that the X chromosome conflict is driven by high gene substitution rates that impact accuracy of phylogenetic inference. However, gene tree clustering showed strong conflict even after discounting variable third codon positions. Alternative topologies were not particularly enriched for sex chromosome loci, but spread across the genome. We conclude that binning genes to autosomal or sex chromosomes may result in a more accurate picture of the complex evolutionary history of a clade.

genomics↗

Nano-computed tomography reveals repeated phenotypic divergence in parasites to escape host defense

Understanding how selective pressures drive morphological change is a central question in evolutionary biology. Feather lice have repeatedly diversified into convergent ecomorphs, based on how they escape from host defenses in different microhabitats. Here, we used nano-computed tomography scan data of 89 specimens of feather lice, belonging to four ecomorph groups to quantify variation of functional traits, including mandibular muscle volume, limb length, and three-dimensional head shape data in these tiny insects. The results suggest that the shape of the head, the proportional volume of the chewing muscles, and the length of the leg segments in feather lice are all strongly associated with specific host-habitats. Further, species that co-occur on hosts have increased rates of morphological evolution, suggesting competition for host space is one of the drivers of morphology. This supports previous work indicating that the phenotypic diversity of feather lice is the result of repeated convergence resulting from resource partitioning, microhabitat specialization, and selection pressures imposed by host defense.

evolutionary biology↗

Host body size, not host population size, predicts genome-wide effective population size of parasites

The effective population size (Ne) of an organism is expected to be generally proportional to the total number of individuals in a population. In parasites, we might expect the effective population size to be proportional to host population size and host body size, because both are expected to increase the number of parasite individuals. However, among other factors, parasite populations are sometimes so extremely subdivided that high levels of inbreeding may distort these predicted relationships. Here, we used whole-genome sequence data from dove parasites (71 feather louse species of the genus Columbicola) and phylogenetic comparative methods to study the relationship between parasite effective population size and host population size and body size.We found that parasite effective population size is largely explained by host body size but not host population size. These results suggest the potential local population size (infrapopulation or deme size) is more predictive of the long-term effective population size of parasites than is the total number of potential parasite infrapopulations (i.e., host individuals). Impact SummaryParasites, among Earths most diverse, threatened, and under-protected animals, play a central role in ecosystem function. The effective population size (Ne) of an organism has a profound impact on evolutionary processes, such as the relative contributions of selection and genetic drift to genomic change. Population size is also one of the most important parameters in conservation biology. For free-living organisms, it is expected that Ne is generally proportional to the total number of individuals in a population. However, for parasites, among other factors, populations are sometimes so extremely subdivided that high levels of inbreeding may distort these relationships. In this study, we used whole-genome sequence data from dove parasites and phylogenetic comparative methods to investigate the relationship between parasite effective population size (Ne) and host population size and body size. Our results revealed a positive relationship between parasite effective population size (Ne) and host body size, but not host population size. These results suggest that the size of parasite infrapopulations may be the most important factor when considering parasite effective population size, and have important implications for conservation.

evolutionary biology↗

Long-distance dispersal of pigeons and doves generated new ecological opportunities for host-switching and adaptive radiation by their parasites

Adaptive radiation is an important mechanism of organismal diversification, and can be triggered by new ecological opportunities. Although poorly studied in this regard, parasites present an ideal system to study adaptive radiations because of their close associations with host species. Both experimental and comparative studies suggest that the ectoparasitic wing lice of pigeons and doves have undergone an adaptive radiation, resulting in differences in both body size and overall coloration. Here we show that long-distance dispersal by dove hosts was important for parasite diversification, providing new ecological opportunities for parasites to speciate by host-switching. We further show that these new opportunities for host-switching decreased over time, and cospeciation became the more dominant mode of parasite speciation. Taken together, our results suggest that host dispersal, followed by host-switching, provided novel ecological opportunities that facilitated adaptive radiation by parasites.

evolutionary biology↗

Genome-resolved metagenomic analyses reveal the presence of a bacterial endosymbiont in an avian nasal mite (Rhinonyssidae; Mesostigmata)

Rhinonyssidae (Mesostigmata) is a family of nasal mites only found in birds. All species are hematophagous endoparasites, which may damage the nasal cavities of birds, and also could be potential reservoirs or vectors of other infections. However, the role of members of Rhinonyssidae as disease vectors in wild bird populations remains uninvestigated, with studies of the microbiomes of Rhinonyssidae being almost non-existent. In the nasal mite (Tinaminyssus melloi) from rock doves (Columba livia), a previous study found evidence of a highly abundant putatively endosymbiotic bacteria from Class Alphaproteobacteria. Here, we expanded the sample size of this species, incorporated contamination controls, and increased sequencing depth in shotgun sequencing and genome-resolved metagenomic analyses. Our goal was to increase the information regarding this mite species with its putative endosymbiont. Our results support the endosymbiotic nature of this bacterial taxon, which is the first described for birds nasal mites to date, and improve the overall understanding of the microbiota inhabiting these mites.

molecular biology↗

The interplay between host biogeography and phylogeny in structuring diversification of the feather louse genus Penenirmus

Parasite diversification is influenced by many of the same factors that affect speciation of free-living organisms, such as biogeographic barriers. However, the ecology and evolution of the host lineage also has a major impact on parasite speciation. Here we explore the interplay between biogeography and host-association on the pattern of diversification in a group of ectoparasitic lice (Insecta: Phthiraptera: Penenirmus) that feeds on the feathers of woodpeckers, barbets, and honeyguides (Piciformes) and some songbirds (Passeriformes). We use whole genome sequencing of 41 ingroup and 12 outgroup samples to develop a phylogenomic dataset of DNA sequences from a reference set of 2,395 single copy ortholog genes, for a total of nearly four million aligned base positions. The phylogenetic trees resulting from both concatenated and gene-tree/species-tree coalescent analyses were nearly identical and highly supported. These trees recovered the genus Penenirmus as monophyletic and identified several major clades, which tended to be associated with one major host group. However, cophylogenetic analysis revealed that host-switching was a prominent process in the diversification of this group. This host-switching generally occurred within single major biogeographic regions. We did, however, find one case in which it appears that a rare dispersal event by a woodpecker lineage from North America to Africa allowed its associated louse to colonize a woodpecker in Africa, even though the woodpecker lineage from North America never became established there.

evolutionary biology↗

The assembled and annotated genome of the pigeon louse Columbicola columbae, a model ectoparasite

The pigeon louse Columbicola columbae is a longstanding and important model for studies of ectoparasitism and host-parasite coevolution. However, a deeper understanding of its evolution and capacity for rapid adaptation is limited by a lack of genomic resources. Here, we present a high-quality draft assembly of the C. columbae genome, produced using a combination of Oxford Nanopore, Illumina, and Hi-C technologies. The final assembly is 208 Mb in length, with 12 chromosome-size scaffolds representing 98.1% of the assembly. For gene model prediction, we used a novel clustering method (wavy_choose) for Oxford Nanopore RNA-seq reads to feed into the MAKER annotation pipeline. High recovery of conserved single-copy orthologs (BUSCOs) suggests that our assembly and annotation are both highly complete and highly accurate. Consistent with the results of the only other assembled louse genome, Pediculus humanus, we find that C. columbae has a relatively low density of repetitive elements, the majority of which are DNA transposons. Also similar to P. humanus, we find a reduced number of genes encoding opsins, G protein-coupled receptors, odorant receptors, insulin signaling pathway components, and detoxification proteins in the C. columbae genome, relative to other insects. We propose that such losses might characterize the genomes of obligate, permanent ectoparasites with predictable habitats, limited foraging complexity, and simple dietary regimes. The sequencing and analysis for this genome were relatively low-cost, and took advantage of a new clustering technique for Oxford Nanopore RNAseq reads that will be useful to future genome projects.

genomics↗

Patterns of microbiome variation among infrapopulations of permanent bloodsucking parasites

While interspecific variation in microbiome composition can often be readily explained by factors such as host species identity, there is still limited knowledge of how microbiomes vary at scales lower than the species level (e.g., between individuals or populations). Here, we evaluated variation in microbiome composition of individual parasites among infrapopulations (i.e., populations of parasites of the same species living on a single host individual). To address this question, we used genome-resolved and shotgun metagenomic data of 17 infrapopulations (balanced design) of the permanent, bloodsucking seal louse Echinophthirius horridus sampled from individual Saimaa ringed seals Pusa hispida saimensis. Both genome-resolved and read-based metagenomic classification approaches consistently show that parasite infrapopulation identity is a significant factor that explains both qualitative and quantitative patterns of microbiome variation at the intraspecific level. This study contributes to the general understanding of the factors driving patterns of intraspecific variation in microbiome composition, especially of bloodsucking parasites, and has implications for understanding how well-known processes occurring at higher taxonomic levels, such as phylosymbiosis, might arise in these systems.

ecology↗

Mitochondrial genomes of Columbicola feather lice are highly fragmented, indicating repeated evolution of minicircle-type genomes in parasitic lice

Most animals have a conserved mitochondrial genome structure composed of a single chromosome. However, some organisms have their mitochondrial genes separated on several smaller circular or linear chromosomes. Highly fragmented circular chromosomes (\"minicircles\") are especially prevalent in parasitic lice (Insecta: Phthiraptera), with 16 species known to have between 9 and 20 mitochondrial minicircles per genome. All of these species belong to the same clade (mammalian lice), suggesting a single origin of drastic fragmentation. Nevertheless, other work indicates a lesser degree of fragmentation (2-3 chromosomes/genome) is present in some avian feather lice (Ischnocera: Philopteridae). In this study, we tested for minicircles in four species of the feather louse genus Columbicola (Philopteridae). Using whole genome shotgun sequence data, we applied three different bioinformatic approaches for assembling the Columbicola mitochondrial genome. We further confirmed these approaches by assembling the mitochondrial genome of Pediculus humanus from shotgun sequencing reads, a species known to have minicircles. All three methods indicated Columbicola spp. genomes are highly fragmented into 15-17 minicircles between 1,119 and 3,173 bp in length, with 1-4 genes per minicircle. Subsequent annotation of the minicircles indicated that tRNA arrangements of minicircles varied substantially between species. These mitochondrial minicircles for species of Columbicola represent the first feather lice (Philopteridae) for which minicircles have been found in a full mitochondrial genome assembly. Combined with recent phylogenetic studies of parasitic lice, our results provide strong evidence that highly fragmented mitochondrial genomes, which are otherwise rare across the Tree of Life, evolved multiple times within parasitic lice.

evolutionary biology↗

Experimental evolution of reproductive isolation from a single natural population

Ecological speciation occurs when local adaptation generates reproductive isolation as a by-product of natural selection1-3. Although ecological speciation is a fundamental source of diversification, the mechanistic link between natural selection and reproductive isolation remains poorly understood, especially in natural populations2-6. Here we show that experimental evolution of parasite body size over four years (ca. 60 generations) leads to reproductive isolation in natural populations of feather lice on birds. When lice are transferred to pigeons of different sizes they rapidly evolve differences in body size that are correlated with host size. These size differences trigger mechanical mating isolation between lice that are locally adapted to the different sized hosts. Size differences among lice also influence the outcome of competition between males for access to females. Thus, body size directly mediates reproductive isolation through its influence on both inter-sexual compatibility and intra-sexual competition. Our results confirm that divergent natural selection acting on a single phenotypic trait can cause reproductive isolation to emerge from a single natural population in real time.

evolutionary biology↗