Support for faster and more adaptive Z chromosome evolution in two divergent lepidopteran lineages^*

The rateof divergence for Z or X chromosomes is usually observed to be greater than autosomes, but the proposed evolutionary causes for this pattern vary, as do empirical results from diverse taxa. Even among moths and butterflies (Lepidoptera), which generally share a single‐origin Z chromosome, the handful of available studies give mixed support for faster or more adaptive evolution of the Z chromosome, depending on the species assayed. Here, we examine the molecular evolution of Z chromosomes in two additional lepidopteran species: the Carolina sphinx moth and the monarch butterfly, the latter of which possesses a recent chromosomal fusion yielding a segment of newly Z‐linked DNA. We find evidence for both faster and more adaptive Z chromosome evolution in both species, although this effect is strongest in the neo‐Z portion of the monarch sex chromosome. The neo‐Z is less male‐biased than expected of a Z chromosome, and unbiased and female‐biased genes drive the signal for adaptive evolution here. Together these results suggest that male‐biased gene accumulation and haploid selection have opposing effects on long‐term rates of adaptation and may help explain the discrepancies in previous findings as well as the repeated evolution of neo‐sex chromosomes in Lepidoptera

Neo-sex Chromosomes in the Monarch Butterfly, Danaus plexippus

We report the discovery of a neo-sex chromosome in the monarch butterfly, Danaus plexippus, and several of its close relatives. Z-linked scaffolds in the D. plexippus genome assembly were identified via sex-specific differences in Illumina sequencing coverage. Additionally, a majority of the D. plexippus genome assembly was assigned to chromosomes based on counts of one-to-one orthologs relative to the butterfly Melitaea cinxia (with replication using two other lepidopteran species), in which genome scaffolds have been mapped to linkage groups. Sequencing coverage-based assessments of Z linkage combined with homology-based chromosomal assignments provided strong evidence for a Z-autosome fusion in the Danaus lineage, involving the autosome homologous to chromosome 21 in M. cinxia. Coverage analysis also identified three notable assembly errors resulting in chimeric Z-autosome scaffolds. Cytogenetic analysis further revealed a large W chromosome that is partially euchromatic, consistent with being a neo-W chromosome. The discovery of a neo-Z and the provisional assignment of chromosome linkage for >90% of D. plexippus genes lays the foundation for novel insights concerning sex chromosome evolution in this female-heterogametic model species for functional and evolutionary genomics

Evolutionary Proteomics Reveals Distinct Patterns of Complexity and Divergence between Lepidopteran Sperm Morphs

This article has been accepted for publication in Genome Biology and Evolution Published by Oxford University Press. This work is licensed under a Creative Commons Attribution-NonCommercial 4.0 International License.Spermatozoa are one of the most strikingly diverse animal cell types. One poorly understood example of this diversity is sperm heteromorphism, where males produce multiple distinct morphs of sperm in a single ejaculate. Typically, only one morph is capable of fertilization and the function of the nonfertilizing morph, called parasperm, remains to be elucidated. Sperm heteromorphism has multiple independent origins, including Lepidoptera (moths and butterflies), where males produce a fertilizing eupyrene sperm and an apyrene parasperm, which lacks a nucleus and nuclear DNA. Here we report a comparative proteomic analysis of eupyrene and apyrene sperm between two distantly related lepidopteran species, the monarch butterfly (Danaus plexippus) and Carolina sphinx moth (Manduca sexta). In both species, we identified ∼700 sperm proteins, with half present in both morphs and the majority of the remainder observed only in eupyrene sperm. Apyrene sperm thus have a distinctly less complex proteome. Gene ontology (GO) analysis revealed proteins shared between morphs tend to be associated with canonical sperm cell structures (e.g., flagellum) and metabolism (e.g., ATP production). GO terms for morph-specific proteins broadly reflect known structural differences, but also suggest a role for apyrene sperm in modulating female neurobiology. Comparative analysis indicates that proteins shared between morphs are most conserved between species as components of sperm, whereas morph-specific proteins turn over more quickly, especially in apyrene sperm. The rapid divergence of apyrene sperm content is consistent with a relaxation of selective constraints associated with fertilization and karyogamy. On the other hand, parasperm generally exhibit greater evolutionary lability, and our observations may therefore reflect adaptive responses to shifting regimes of sexual selection.National Science Foundation award OAC-1541396/ACI-1541396NSF award OAC-1541396/ACI-1541396Syracuse UniversityUniversity of KansasKU Gould Fellowship and National Science Foundation award DEB-1701931Syracuse University FellowshipMarilyn Kerr Fellowshi

Sex, males, and hermaphrodites in the scale insect Icerya purchasi

Funding: This work was supported by a number of fellowships, namely a University Research Fellowship from Royal Society of London (to AG) and a Junior Research Fellowship from Balliol College, Oxford to AG. Funding came from Independent Research Fellowships from Natural Environment Research Council (grant no. NE/K009524/1 to AG and NE/K009516/1 to LR), a Consolidator Grant from European Research Council (grant no. 771387 to AG), a European Research Countil Starting Grant (PGErepro to LR), and a Royal Society Newton fellowship (to LR).Androdioecy (the coexistence of males and hermaphrodites) is a rare mating system for which the evolutionary dynamics are poorly understood. Here we study the only presumed case of androdioecy in insects, found in the cottony cushion scale, Icerya purchasi . In this species, female-like hermaphrodites have been shown to produce sperm and self-fertilize. However, rare males are sometimes observed too. In a large population-genetic analysis, we show for the first time that although self-fertilization appears to be the primary mode of reproduction, rare outbreeding events between males and hermaphrodites do occur, and we thereby confirm androdioecy as the mating system of I. purchasi . Thus, this insect appears to have the colonization advantages of a selfing organism while also benefitting from periodic reintroduction of genetic variation through outbreeding with males.Publisher PDFPeer reviewe

The Z chromosome is enriched for sperm proteins in two divergent species of Lepidoptera

Genes that promote sexual conflict, such as those with a sex-limited fitness benefit, are expected to accumulate differentially on sex chromosomes relative to autosomes. Few tests of this hypothesis exist for male homogametic (ZZ) taxa, however, and most use RNA expression data to identify such genes. Here, we employ a different identification method by using proteomic analysis of sperm cells to identify genes with a sex-limited benefit. We tested for a bias in genomic location of sperm protein genes in two species of Lepidoptera. An excess of sperm protein genes was identified on the Z chromosomes of both the Carolina sphinx moth (Manduca sexta) and the monarch butterfly (Danaus plexippus). Taking into consideration a Z-autosome fusion in monarchs, we discover that the ancestrally sex-linked portion of the genome is the source of this enrichment while the newly sex-linked portion still appears similar to autosomes in relative abundance of sperm protein genes. Together, these results point to an enrichment of male-beneficial genes on the Z chromosome and demonstrate the usefulness of proteomic datasets in sexual conflict research.The accepted manuscript in pdf format is listed with the files at the bottom of this page. The presentation of the authors' names and (or) special characters in the title of the manuscript may differ slightly between what is listed on this page and what is listed in the pdf file of the accepted manuscript; that in the pdf file of the accepted manuscript is what was submitted by the author

Population differentiation and structural variation in the Manduca sexta genome across the United States

Many species that are extensively studied in the laboratory are less well characterized in their natural habitat, and laboratory strains represent only a small fraction of the variation in a species’ genome. Here we investigate genomic variation in 3 natural North American populations of an agricultural pest and a model insect for many scientific disciplines, the tobacco hornworm (Manduca sexta). We show that hornworms from Arizona, Kansas, and North Carolina are genetically distinct, with Arizona being particularly differentiated from the other 2 populations using Illumina whole-genome resequencing. Peaks of differentiation exist across the genome, but here, we focus in on the most striking regions. In particular, we identify 2 likely segregating inversions found in the Arizona population. One inversion on the Z chromosome may enhance adaptive evolution of the sex chromosome. The larger, 8 Mb inversion on chromosome 12 contains a pseudogene which may be involved in the exploitation of a novel hostplant in Arizona, but functional genetic assays will be required to support this hypothesis. Nevertheless, our results reveal undiscovered natural variation and provide useful genomic data for both pest management and evolutionary genetics of this insect species

Population differentiation and structural variation in the Manduca sexta genome across the United States

Many species that are extensively studied in the laboratory are less well characterized in their natural habitat, and laboratory strains represent only a small fraction of the variation in a species’ genome. Here we investigate genomic variation in 3 natural North American populations of an agricultural pest and a model insect for many scientific disciplines, the tobacco hornworm (Manduca sexta). We show that hornworms from Arizona, Kansas, and North Carolina are genetically distinct, with Arizona being particularly differentiated from the other 2 populations using Illumina whole-genome resequencing. Peaks of differentiation exist across the genome, but here, we focus in on the most striking regions. In particular, we identify 2 likely segregating inversions found in the Arizona population. One inversion on the Z chromosome may enhance adaptive evolution of the sex chromosome. The larger, 8 Mb inversion on chromosome 12 contains a pseudogene which may be involved in the exploitation of a novel hostplant in Arizona, but functional genetic assays will be required to support this hypothesis. Nevertheless, our results reveal undiscovered natural variation and provide useful genomic data for both pest management and evolutionary genetics of this insect species