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There are calls for research into the historical evolutionary relationships between humans and their commensals, as it would greatly inform models that predict the spread of pests and diseases under urban population expansion. The earliest civilizations emerged approximately 10 000 years ago and created conditions ideal for the establishment and spread of commensal urban pests. Commensal relations between humans and pests likely emerged with these early civilizations; however, for most species (e.g. German cockroach and black rat), these relationships have formed relatively recently—within the last 5000 years—raising the question of whether others could have emerged earlier. Following comparative whole genome analysis of bed bugs,Cimex lectularius, belonging to two genetically distinct lineages, one associated with bats and the other with humans, coupled with demographic modelling, our findings suggests that while their association with humans dates back potentially hundreds of thousands of years, a dramatic change in the effective population size of the human-associated lineage occurred approximately 13 000 years ago; a pattern not found in the bat-associated lineage. The timing and magnitude of the demographic patterns provide compelling evidence that the human-associated lineage closely tracked the demographic history of modern humans and their movement into the first cities. As such, bed bugs may represent the firsttrueurban pest insect species. 

Neoclytus acuminatus acuminatus, the red-headed ash borer, is a wood-boring longhorn beetle (Cerambycidae: Cerambycinae) native to North America and introduced in Eurasia and South America. Its larvae develop in dying or recently dead hardwood trees, including ecologically and economically significant species of ash, hickory, and oak. We sequenced, assembled, and annotated the genome of a female N. acuminatus and compared it to the publicly available genomes of other cerambycid species. The 508 Mb N. acuminatus genome assembly spanned 20 contigs (19 nuclear + 1 mitochondrial), with an N50 of 52.59 Mb and largest contig of 61.20 Mb. A moderately high fraction of the genome (62.63%) comprised repetitive sequences, with nearly all (99.4%) expected single-copy orthologous genes (BUSCOs) present and fully assembled. We identified 2 contigs as fragments of the N. acuminatus sex chromosome. Genome annotation identified 12,899 genes, including 109 putative horizontally transferred loci. Synteny analysis identified well-conserved blocks of collinearity between the N. acuminatus genome and other Cerambycidae. The genome contains a similar number of genes encoding putative plant cell wall degrading enzymes as other Cerambycidae. The N. acuminatus genome provides new insights into genome evolution in the family Cerambycidae, known for its rich diversity of xylophagous species, and provides a new viewpoint from which to study the evolution and genomic basis of traits such as wood-feeding and olfaction in beetles and other insects. 

Abstract Just exactly which tree(s) should we assume when testing evolutionary hypotheses? This question has plagued comparative biologists for decades. Though all phylogenetic comparative methods require input trees, we seldom know with certainty whether even a perfectly estimated tree (if this is possible in practice) is appropriate for our studied traits. Yet, we also know that phylogenetic conflict is ubiquitous in modern comparative biology, and we are still learning about its dangers when testing evolutionary hypotheses. Here, we investigate the consequences of tree-trait mismatch for phylogenetic regression in the presence of gene tree–species tree conflict. Our simulation experiments reveal excessively high false positive rates for mismatched models with both small and large trees, simple and complex traits, and known and estimated phylogenies. In some cases, we find evidence of a directionality of error: assuming a species tree for traits that evolved according to a gene tree sometimes fares worse than the opposite. We also explored the impacts of tree choice using an expansive, cross-species gene expression dataset as an arguably “best-case” scenario in which one may have a better chance of matching tree with trait. Offering a potential path forward, we found promise in the application of a robust estimator as a potential, albeit imperfect, solution to some issues raised by tree mismatch. Collectively, our results emphasize the importance of careful study design for comparative methods, highlighting the need to fully appreciate the role of accurate and thoughtful phylogenetic modeling. 

Abstract The common bed bug, Cimex lectularius, is a globally distributed pest insect of medical, veterinary, and economic importance. Previous reference genome assemblies for this species were generated from short read sequencing data, resulting in a ~650 Mb composed of thousands of contigs. Here, we present a haplotype-resolved, chromosome-level reference genome, generated from an adult Harlen strain female specimen. Using PacBio long read and Omni-C proximity sequencing, we generated a 540 Mb genome with 15 chromosomes (13 autosomes and 2 sex chromosomes - X1X2) with an N50 > 30 Mb and BUSCO > 90%. Previous karyotyping efforts indicate an XY sex chromosome system, with 2n=26 and X1X1X2X2 females and X1X2Y males; however significant fragmentation of the X chromosome has also been reported. We further use whole genome resequencing data from males and females to identify the X1 and X2 chromosomes based on sex biases in coverage. This highly contiguous reference genome assembly provides a much-improved resource for identifying chromosomal genome architecture, and for interpreting patterns of urban outbreaks and signatures of selection linked to insecticide resistance. 

Abstract MotivationThe scale and scope of comparative trait data are expanding at unprecedented rates, and recent advances in evolutionary modeling and simulation sometimes struggle to match this pace. Well-organized and flexible applications for conducting large-scale simulations of evolution hold promise in this context for understanding models and more so our ability to confidently estimate them with real trait data sampled from nature. ResultsWe introduce TraitTrainR, an R package designed to facilitate efficient, large-scale simulations under complex models of continuous trait evolution. TraitTrainR employs several output formats, supports popular trait data transformations, accommodates multi-trait evolution, and exhibits flexibility in defining input parameter space and model stacking. Moreover, TraitTrainR permits measurement error, allowing for investigation of its potential impacts on evolutionary inference. We envision a wealth of applications of TraitTrainR, and we demonstrate one such example by examining the problem of evolutionary model selection in three empirical phylogenetic case studies. Collectively, these demonstrations of applying TraitTrainR to explore problems in model selection underscores its utility and broader promise for addressing key questions, including those related to experimental design and statistical power, in comparative biology. Availability and implementationTraitTrainR is developed in R 4.4.0 and is freely available at https://github.com/radamsRHA/TraitTrainR/, which includes detailed documentation, quick-start guides, and a step-by-step tutorial. 

Abstract Tetraopes are aposematic longhorn beetles (Cerambycidae) that feed primarily on toxic plants in the genus Asclepias (milkweeds). Studies of Tetraopes and their host plants have revealed compelling evidence for insect–plant coevolution and cospeciation. We sequenced, assembled, and annotated the genome of the common red milkweed beetle, Tetraopes tetrophthalmus, and explored gene content and evolution, focusing on annotated genes putatively involved in chemosensation, allelochemical detoxification, and phytophagy. Comparisons were made to the Asian longhorned beetle (Anoplophora glabripennis) genome. The genome assembly comprised 779 Mb distributed across 1,057 contigs, with an N50 of 2.21 Mb and 13,089 putative genes, including 97.3% of expected single-copy orthologs. Manual curation identified 122 putative odorant receptors (OR) and 162 gustatory receptors (GR), the former number similar to A. glabripennis but the latter only 69% of the A. glabripennis suite. We also documented a greater percentage of pseudogenic GRs and ORs compared to A. glabripennis, suggesting an ongoing reduction in chemosensory function, perhaps related to host specialization. We found lower diversity within certain well-studied gene families predicted to encode putative plant cell wall degrading enzymes in the T. tetrophthalmus genome, perhaps also due to host specialization. Exploring genes relevant to stress and allelochemical detoxification revealed evidence of an abundance of ABC-family genes in the T. tetrophthalmus genome, which may be related to sequestering toxic cardiac glycosides. Our studies further illuminate the genomic basis and evolution of chemosensation in longhorn beetles and provide a new vantage point from which to explore the ecology and evolution of specialized plant-feeding in Tetraopes and other phytophagous beetles. 

Abstract Modern comparative biology owes much to phylogenetic regression. At its conception, this technique sparked a revolution that armed biologists with phylogenetic comparative methods (PCMs) for disentangling evolutionary correlations from those arising from hierarchical phylogenetic relationships. Over the past few decades, the phylogenetic regression framework has become a paradigm of modern comparative biology that has been widely embraced as a remedy for shared ancestry. However, recent evidence has shown doubt over the efficacy of phylogenetic regression, and PCMs more generally, with the suggestion that many of these methods fail to provide an adequate defense against unreplicated evolution—the primary justification for using them in the first place. Importantly, some of the most compelling examples of biological innovation in nature result from abrupt lineage-specific evolutionary shifts, which current regression models are largely ill equipped to deal with. Here we explore a solution to this problem by applying robust linear regression to comparative trait data. We formally introduce robust phylogenetic regression to the PCM toolkit with linear estimators that are less sensitive to model violations than the standard least-squares estimator, while still retaining high power to detect true trait associations. Our analyses also highlight an ingenuity of the original algorithm for phylogenetic regression based on independent contrasts, whereby robust estimators are particularly effective. Collectively, we find that robust estimators hold promise for improving tests of trait associations and offer a path forward in scenarios where classical approaches may fail. Our study joins recent arguments for increased vigilance against unreplicated evolution and a better understanding of evolutionary model performance in challenging—yet biologically important—settings. 

Abstract Likelihood-based tests of phylogenetic trees are a foundation of modern systematics. Over the past decade, an enormous wealth and diversity of model-based approaches have been developed for phylogenetic inference of both gene trees and species trees. However, while many techniques exist for conducting formal likelihood-based tests of gene trees, such frameworks are comparatively underdeveloped and underutilized for testing species tree hypotheses. To date, widely used tests of tree topology are designed to assess the fit of classical models of molecular sequence data and individual gene trees and thus are not readily applicable to the problem of species tree inference. To address this issue, we derive several analogous likelihood-based approaches for testing topologies using modern species tree models and heuristic algorithms that use gene tree topologies as input for maximum likelihood estimation under the multispecies coalescent. For the purpose of comparing support for species trees, these tests leverage the statistical procedures of their original gene tree-based counterparts that have an extended history for testing phylogenetic hypotheses at a single locus. We discuss and demonstrate a number of applications, limitations, and important considerations of these tests using simulated and empirical phylogenomic data sets that include both bifurcating topologies and reticulate network models of species relationships. Finally, we introduce the open-source R package SpeciesTopoTestR (SpeciesTopology Tests in R) that includes a suite of functions for conducting formal likelihood-based tests of species topologies given a set of input gene tree topologies.