01994nas a2200181 4500008004100000022001400041245008700055210006900142260001600211300001000227490000600237520142100243653002301664100002201687700002301709700002501732856005501757 2022 eng d a2399-364200aIndependent evolution of highly variable, fragmented mitogenomes of parasitic lice0 aIndependent evolution of highly variable fragmented mitogenomes  cJul-08-2022 a10 pp0 v53 a

The mitochondrial genomes (mitogenomes) of bilaterian animals are highly conserved structures that usually consist of a single circular chromosome. However, several species of parasitic lice (Insecta: Phthiraptera) possess fragmented mitogenomes, where the mitochondrial genes are present on separate, circular chromosomes. Nevertheless, the extent, causes, and consequences of this structural variation remain poorly understood. Here, we combined new and existing data to better understand the evolution of mitogenome fragmentation in major groups of parasitic lice. We found strong evidence that fragmented mitogenomes evolved many times within parasitic lice and that the level of fragmentation is highly variable, including examples of heteroplasmic arrangements. We also found a significant association between mitochondrial fragmentation and signatures of relaxed selection. Mitochondrial fragmentation was also associated with changes to a lower AT%, possibly due to differences in mutation biases. Together, our results provide a significant advance in understanding the process of mitogenome fragmentation and provide an important perspective on mitochondrial evolution in eukaryotes.

Supplementary data files please visit the publisher's website, Under supplementary information https://www.nature.com/articles/s42003-022-03625-0. There are 6 supplementary data files

10aPessoaiella absita1 aSweet, Andrew, D.1 aJohnson, Kevin, P.1 aCameron, Stephen, L. uhttps://www.nature.com/articles/s42003-022-03625-002040nas a2200301 4500008004100000022001400041245011200055210006900167260001600236300000900252490000800261520110000269653001201369653001901381653001401400653002901414653002301443653001401466100002201480700002301502700001701525700002401542700002401566700001601590700003101606700002501637856007601662 2021 eng d a0378-111900aStructure, gene order, and nucleotide composition of mitochondrial genomes in parasitic lice from Amblycera0 aStructure gene order and nucleotide composition of mitochondrial cFeb-01-2021 a7 pp0 v7683 a

Parasitic lice have unique mitochondrial (mt) genomes characterized by rearranged gene orders, variable genome structures, and less AT content compared to most other insects. However, relatively little is known about the mt genomes of Amblycera, the suborder sister to all other parasitic lice. Comparing among nine different genera (including representative of all seven families), we show that Amblycera have variable and highly rearranged mt genomes. Some genera have fragmented genomes that vary considerably in length, whereas others have a single mt chromosome. Notably, these genomes are more AT-biased than most other lice. We also recover genus-level phylogenetic relationships among Amblycera that are consistent with those reported from large nuclear datasets, indicating that mt sequences are reliable for reconstructing evolutionary relationships in Amblycera. However, gene order data cannot reliably recover these same relationships. Overall, our results suggest that the mt genomes of lice, already know to be distinctive, are even more variable than previously thought.

10aAT-bias10aCrotophaga ani10aEvolution10aMyiothylpis luteoviridis10aOrganelle genomics10aPhylogeny1 aSweet, Andrew, D.1 aJohnson, Kevin, P.1 aCao, Yanghui1 ade_Moya, Robert, S.1 aSkinner, Rachel, K.1 aTan, Milton1 aVirrueta-Herrera, Stephany1 aCameron, Stephen, L. uhttps://www.sciencedirect.com/science/article/abs/pii/S037811192030981101974nas a2200169 4500008004100000022001400041245013900055210006900194260001600263300001100279490000800290520134500298100002801643700002501671700003201696856007601728 2021 eng d a0378-111900aHow are the mitochondrial genomes reorganized in Hexapoda? Differential evolution and the first report of convergences within Hexapoda0 aHow are the mitochondrial genomes reorganized in Hexapoda Differ cJul-01-2021 a1457190 v7913 a

The evolution of the Hexapoda mitochondrial genome has been the focus of several genetic and evolutionary studies over the last decades. However, they have concentrated on certain taxonomic orders of economic or health importance. The recent increase of mitochondrial genomes sequencing of diverse taxonomic orders generates an important opportunity to clarify the evolution of this group of organisms. However, there is no comparative study that investigates the evolution of the Hexapoda mitochondrial genome. In order to verify the level of rearrangement and the mitochondrial genome evolution, we performed a comparative genomic analysis of the Hexapoda mitochondrial genome available in the NCBI database. Using a combination of bioinformatics methods to carefully examine the mitochondrial gene rearrangements in 1198 Hexapoda species belonging to 32 taxonomic orders, we determined that there is a great variation in the rate of rearrangement by gene and by taxonomic order. A higher rate of genetic reassortment is observed in Phthiraptera, Thysanoptera, Protura, and Hymenoptera; compared to other taxonomic orders. Twenty-four events of convergence in the genetic order between different taxonomic orders were determined, most of them not previously reported; which proves the great evolutionary dynamics within Hexapoda.

1 aMoreno-Carmona, Manuela1 aCameron, Stephen, L.1 aQuiroga, Carlos, Fernando P uhttps://www.sciencedirect.com/science/article/abs/pii/S037811192100313902478nas a2200253 4500008004100000022001400041245014600055210006900201260001600270300001000286520160200296653001701898653001701915653004101932653001501973653001101988653001301999100002202012700002302034700002602057700002302083700002502106856009302131 2023 eng d a2160-183600aDraft genome assemblies of the avian louse Brueelia nebulosa and its associates using long-read sequencing from an individual specimen0 aDraft genome assemblies of the avian louse iBrueelia nebulosai a cFeb-03-2023 a13 pp3 a

 Sequencing high molecular weight (HMW) DNA with long-read and linked-read technologies has promoted a major increase in more complete genome sequences for nonmodel organisms. Sequencing approaches that rely on HMW DNA have been limited to larger organisms or pools of multiple individuals, but recent advances have allowed for sequencing from individuals of small-bodied organisms. Here, we use HMW DNA sequencing with PacBio long reads and TELL-Seq linked reads to assemble and annotate the genome from a single individual feather louse (Brueelia nebulosa) from a European Starling (Sturnus vulgaris). We assembled a genome with a relatively high scaffold N50 (637 kb) and with BUSCO scores (96.1%) comparable to louse genomes assembled from pooled individuals. We annotated a number of genes (10,938) similar to the human louse (Pediculus humanus) genome. Additionally, calling phased variants revealed that the Brueelia genome is more heterozygous (∼1%) then expected for a highly obligate and dispersal-limited parasite. We also assembled and annotated the mitochondrial genome and primary endosymbiont (Sodalis) genome from the individual louse, which showed evidence for heteroplasmy in the mitogenome and a reduced genome size in the endosymbiont compared to its free-living relative. Our study is a valuable demonstration of the capability to obtain high-quality genomes from individual small, nonmodel organisms. Applying this approach to other organisms could greatly increase our understanding of the diversity and evolution of individual genomes.

10aectoparasite10aEndosymbiont10ahistorical effective population size10amitogenome10aPacBio10aTELL-Seq1 aSweet, Andrew, D.1 aBrowne, Daniel, R.1 aHernandez, Alvaro, G.1 aJohnson, Kevin, P.1 aCameron, Stephen, L. uhttps://academic.oup.com/g3journal/advance-article/doi/10.1093/g3journal/jkad030/702574102689nas a2200205 4500008004100000022001400041245015900055210006900214260001600283300001000299490000600309520199700315653001902312653002502331653002002356100002202376700002302398700002502421856003702446 2020 eng d a2167-835900aMitochondrial genomes of Columbicola feather lice are highly fragmented, indicating repeated evolution of minicircle-type genomes in parasitic lice0 aMitochondrial genomes of iColumbicolai feather lice are highly f cMar-23-2020 a27 pp0 v83 a

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 nine 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 genusColumbicola(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 ofPediculus humanusfrom shotgun sequencing reads, a species known to have minicircles.Columbicola spp. genomes are highly fragmented into 15–17 minicircles between ∼1,100 and ∼3,100 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.

10aBioinformatics10aConvergent evolution10agenome assembly1 aSweet, Andrew, D.1 aJohnson, Kevin, P.1 aCameron, Stephen, L. uhttps://peerj.com/articles/8759/02669nas a2200145 4500008004100000245009300041210006900134520212400203100002502327700002402352700002302376700002502399700002302424856007602447 2011 eng d00aMitochondrial genome deletions and minicirclesare common in lice (Insecta: Phthiraptera)0 aMitochondrial genome deletions and minicirclesare common in lice3 a

Background:The gene composition, gene order and structure of the mitochondrial genome are remarkably stableacross bilaterian animals. Lice (Insecta: Phthiraptera) are a major exception to this genomic stability in that thecanonical single chromosome with 37 genes found in almost all other bilaterians has been lost in multiple lineagesin favour of multiple, minicircular chromosomes with less than 37 genes on each chromosome.

Results:Minicircular mt genomes are found in six of the ten louse species examined to date and three types ofminicircles were identified: heteroplasmic minicircles which coexist with full sized mt genomes (type 1); multigenechromosomes with short, simple control regions, we infer that the genome consists of several such chromosomes(type 2); and multiple, single to three gene chromosomes with large, complex control regions (type 3). Mappingminicircle types onto a phylogenetic tree of lice fails to show a pattern of their occurrence consistent with anevolutionary series of minicircle types. Analysis of the nuclear-encoded, mitochondrially-targetted genes inferredfrom the body louse,Pediculus, suggests that the loss of mitochondrial single-stranded binding protein (mtSSB)may be responsible for the presence of minicircles in at least species with the most derived type 3 minicircles(Pediculus, Damalinia).

Conclusions:Minicircular mt genomes are common in lice and appear to have arisen multiple times within thegroup. Life history adaptive explanations which attribute minicircular mt genomes in lice to the adoption of blood-feeding in the Anoplura are not supported by this expanded data set as minicircles are found in multiple non-blood feeding louse groups but are not found in the blood-feeding genusHeterodoxus. In contrast, a mechanistexplanation based on the loss of mtSSB suggests that minicircles may be selectively favoured due to the incapacityof the mt replisome to synthesize long replicative products without mtSSB and thus the loss of this gene lead tothe formation of minicircles in lice.

1 aCameron, Stephen, L.1 aYoshizawa, Kazunori1 aMizukoshi, Atsushi1 aWhiting, Michael, F.1 aJohnson, Kevin, P. uhttps://bmcgenomics.biomedcentral.com/articles/10.1186/1471-2164-12-39402193nas a2200301 4500008004100000245010800041210006900149260001200218300000900230490000600239520126200245653001701507653001701524653001201541653001801553100002401571700002101595700002201616700002801638700002301666700002701689700002501716700002501741700002401766700002501790700002301815856005301838 2019 eng d00aExtensive host-switching of avian feather lice following the Cretaceous-Paleogene mass extinction event0 aExtensive hostswitching of avian feather lice following the Cret c11-2019 a6 pp0 v23 a

Nearly all lineages of birds host parasitic feather lice. Based on recent phylogenomic studies, the three major lineages of modern birds diverged from each other before the Cretaceous- Paleogene (K-Pg) mass extinction event. In contrast, studies of the phylogeny of feather lice on birds, indicate that these parasites diversified largely after this event. However, these studies were unable to reconstruct the ancestral avian host lineage for feather lice. Here we use genome sequences of a broad diversity of lice to reconstruct a phylogeny based on 1,075 genes. By comparing this louse evolutionary tree to the avian host tree, we show that feather lice began diversifying on the common ancestor of waterfowl and landfowl, then radiated onto other avian lineages by extensive host-switching. Dating analyses and cophylogenetic comparisons revealed that two of three lineages of birds that diverged before the K-Pg boundary acquired their feather lice after this event via host-switching.

Data availability

Data generated during this study are available through the Illinois Databank (https://doi.org/10.13012/B2IDB-0440388_V1)39. Raw read sequences are available in the NCBI SRA database (Supplementary Table 3).

10aFeather lice10aGalloanserae10aNeoaves10aPalaeognathae1 ade_Moya, Robert, S.1 aAllen, Julie, M.1 aSweet, Andrew, D.1 aWalden, Kimberly, K. O.1 aPalma, Ricardo, L.1 aSmith, Vincent, Stuart1 aCameron, Stephen, L.1 aValim, Michel, Paiva1 aGalloway, Terry, D.1 aWeckstein, Jason, D.1 aJohnson, Kevin, P. uhttp://www.nature.com/articles/s42003-019-0689-703003nas a2200517 4500008004100000022001400041245005900055210005900114260001600173300001800189490000800207520154000215653001401755653001401769653001301783653001601796653001901812100002301831700003001854700002101884700002101905700002201926700002201948700002101970700002001991700002202011700002802033700002302061700002402084700002102108700002102129700003102150700002702181700002502208700002502233700002402258700002102282700002002303700001702323700001702340700001402357700002002371700002402391700002402415856004602439 2018 eng d a0027-842400aPhylogenomics and the evolution of hemipteroid insects0 aPhylogenomics and the evolution of hemipteroid insects cNov-12-2018 a12775 - 127800 v1153 a

Hemipteroid insects (Paraneoptera), with over 10% of all known insect diversity, are a major component of terrestrial and aquatic ecosystems. Previous phylogenetic analyses have not consistently resolved the relationships among major hemipteroid lineages. We provide maximum likelihood-based phylogenomic analyses of a taxonomically comprehensive dataset comprising sequences of 2,395 single-copy, protein-coding genes for 193 samples of hemipteroid insects and outgroups. These analyses yield a well-supported phylogeny for hemipteroid insects. Monophyly of each of the three hemipteroid orders (Psocodea, Thysanoptera, and Hemiptera) is strongly supported, as are most relationships among suborders and families. Thysanoptera (thrips) is strongly supported as sister to Hemiptera. However, as in a recent large-scale analysis sampling all insect orders, trees from our data matrices support Psocodea (bark lice and parasitic lice) as the sister group to the holometabolous insects (those with complete metamorphosis). In contrast, four-cluster likelihood mapping of these data does not support this result. A molecular dating analysis using 23 fossil calibration points suggests hemipteroid insects began diversifying before the Carboniferous, over 365 million years ago. We also explore implications for understanding the timing of diversification, the evolution of morphological traits, and the evolution of mitochondrial genome organization. These results provide a phylogenetic framework for future studies of the group.

10aHemiptera10aPhylogeny10aPsocodea10asystematics10atranscriptomes1 aJohnson, Kevin, P.1 aDietrich, Christopher, H.1 aFriedrich, Frank1 aBeutel, Rolf, G.1 aWipfler, Benjamin1 aPeters, Ralph, S.1 aAllen, Julie, M.1 aPetersen, Malte1 aDonath, Alexander1 aWalden, Kimberly, K. O.1 aKozlov, Alexey, M.1 aPodsiadlowski, Lars1 aMayer, Christoph1 aMeusemann, Karen1 aVasilikopoulos, Alexandros1 aWaterhouse, Robert, M.1 aCameron, Stephen, L.1 aWeirauch, Christiane1 aSwanson, Daniel, R.1 aPercy, Diana, M.1 aHardy, Nate, B.1 aTerry, Irene1 aLiu, Shanlin1 aZhou, Xin1 aMisof, Bernhard1 aRobertson, Hugh, M.1 aYoshizawa, Kazunori uhttps://www.pnas.org/content/115/50/1277502328nas a2200157 4500008004100000245016500041210006900206260000900275300001400284490000700298520172700305100002502032700002302057700002502080856006502105 2007 eng d00aThe Mitochondrial Genome of the Screamer Louse Bothriometopus (Phthiraptera: Ischnocera): Effects of ExtensiveGene Rearrangements on the Evolution of the Genome0 aMitochondrial Genome of the Screamer Louse Bothriometopus Phthir c2007 a589 - 6040 v653 a

Mitochondrial (mt) genome rearrangement has generally been studied with respect to the phenomenon itself, focusing on their phylogenetic distribution and causal mechanisms. Rearrangements have additional significance through effects on substitution, transcription, and mRNA processing. Lice are an ideal group in which to study the interactions between rearrangements and these factors due to the heightened rearrangement rate within this group. The entire mt genome of the screamer louse Bothriometopus was sequenced and compared to previously sequenced louse genomes. The mt genome is 15,564 bp, circular, and all genes are encoded on the same strand. The gene arrangement differs radically from both other louse species and the ancestral insect. Nucleotide composition is A+T biased, but there is no skew which may be due to reversal of replication direction or a transcriptional effect. Bothriometopus has both tRNA duplication and concerted evolution which has not been observed previously. Eleven of the 13 protein-coding genes have 3' end stem-loop structures which may allow mRNA processing without flanking tRNAs and so facilitate gene rearrangements. There are five candidate control regions capable of forming stem-loop structures. Two are structurally more similar to the control regions of other insect species than those of other lice. Analyses of Bothriometopus demonstrate that louse mt genomes, in addition to being extensively rearranged, differ significantly from most insect species in nucleotide composition biases, tRNA evolution, protein-coding gene structures and putative signaling sites such as the control region. These may be either a cause or a consequence of gene rearrangements.

1 aCameron, Stephen, L.1 aJohnson, Kevin, P.1 aWhiting, Michael, F. uhttp://link.springer.com/article/10.1007%2Fs00239-007-9042-801715nas a2200241 4500008004100000245008200041210006900123260000900192300001200201490000700213520091700220653002401137653001301161653001201174653003101186653001701217653001801234100002501252700002301277700001701300700002501317856013101342 2006 eng d00aEvidence from mitochondrial genomics on interordinal relationships in insects0 aEvidence from mitochondrial genomics on interordinal relationshi c2006 a27 - 340 v643 a

Mitochondrial (mt) genomes are the largest molecular data source for deep level insect phylogenetics that is also obtainable in a reasonable timeframe and for a reasonable cost. Over 100 insect mt genomes have been sequenced, representing 29 of the 30 orders, multiple suborders for a third of the orders, and many representatives of the mega-diverse orders. Genome rearrangements have been found in a third of the insect orders however these rearrangements diagnose groups of ordinal or lower rank. Sequence based phylogenetic hypotheses utilizing mt genomic data are a promising source of data on interordinal relationships however these studies are hampered by base compositional biases, unequal rates of nucleotide substitution across groups and other long-branch effects. Available data from the field of insect mitogenomic phylogenetics is reviewed and future directions in this research outlined.

10agene rearrangements10agenomics10aInsecta10ainterordinal relationships10amitochondria10aPhylogenetics1 aCameron, Stephen, L.1 aBeckenbach, Andrew1 aDowton, Mark1 aWhiting, Michael, F. uhttp://www.senckenberg.de/files/content/forschung/publikationen/arthropodsystematics/asp_64_1/asp_64_1_cameron_et_al_27-34.pdf00430nas a2200121 4500008004100000245005100041210005100092260000900143100002500152700002300177700002300200856008500223 2006 eng d00aEvolution of the mitochondrial genomes of lice0 aEvolution of the mitochondrial genomes of lice c20061 aCameron, Stephen, L.1 aCovacin, Catherine1 aJohnson, Kevin, P. uhttps://phthiraptera.myspecies.info/content/evolution-mitochondrial-genomes-lice01362nas a2200217 4500008004100000245010900041210006900150260003100219300001200250490000700262520066700269653001400936653001300950653001700963653001000980100001600990700001601006700002501022700002401047856007301071 2006 eng d00aExtraordinary number of gene rearrangements in the mitochondrial genomes of lice (Phthiraptera: Insecta)0 aExtraordinary number of gene rearrangements in the mitochondrial bBlackwell Publishingc2006 a63 - 680 v153 a

The arrangement of genes in the mitochondrial (mt) genomes of most insects is the same, or near-identical, to that inferred to be ancestral for insects. We sequenced the entire mt genome of the small pigeon louse, Campanulotes bidentatus compar, and part of the mt genomes of nine other species of lice. These species were from six families and the three main suborders of the order Phthiraptera. There was no variation in gene arrangement among species within a family but there was much variation in gene arrangement among the three suborders of lice. There has been an extraordinary number of gene rearrangements in the mitochondrial genomes of lice!

10aAmblycera10aAnoplura10aCampanulotes10amtDNA1 aCovacin, C.1 aShao, Renfu1 aCameron, Stephen, L.1 aBarker, Stephen, C. uhttp://www.phthiraptera.info/sites/phthiraptera.info/files/46197.pdf