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Sex chromosomes play an outsized role in adaptation and speciation, and thus deserve particular attention in evolutionary genomics. In particular, fusions between sex chromosomes and autosomes can produce neo‐sex chromosomes, which offer important insights into the evolutionary dynamics of sex chromosomes. Here, we investigate the evolutionary origin of the previously reportedDanausneo‐sex chromosome within the tribe Danaini. We assembled and annotated genomes ofTirumala septentrionis(subtribe Danaina),Ideopsis similis(Amaurina),Idea leuconoe(Euploeina) andLycorea halia(Itunina) and identified their Z‐linked scaffolds. We found that theDanausneo‐sex chromosome resulting from the fusion between a Z chromosome and an autosome corresponding to theMelitaea cinxiachromosome (McChr) 21 arose in a common ancestor of Danaina, Amaurina and Euploina. We also identified two additional fusions as the W chromosome further fused with the synteny block McChr31 inI. similisand independent fusion occurred between ancestral Z chromosome and McChr12 inL. halia. We further tested a possible role of sexually antagonistic selection in sex chromosome turnover by analysing the genomic distribution of sex‐biased genes inI. leuconoeandL. halia. The autosomes corresponding to McChr21 and McChr31 involved in the fusions are significantly enriched in female‐ and male‐biased genes, respectively, which could have hypothetically facilitated fixation of the neo‐sex chromosomes. This suggests a role of sexual antagonism in sex chromosome turnover in Lepidoptera. The neo‐Z chromosomes of bothI. leuconoeandL. haliaappear fully compensated in somatic tissues, but the extent of dosage compensation for the ancestral Z varies across tissues and species.

 

Comparative studies of aging are a promising approach to identifying general properties of and processes leading to aging. While to date, many comparative studies of aging in animals have focused on relatively narrow species groups, methodological innovations now allow for studies that include evolutionary distant species. However, comparative studies of aging across a wide range of species that have distinct life histories introduce additional challenges in experimental design. Here, we discuss these challenges, highlight the most pressing problems that need to be solved, and provide suggestions based on current approaches to successfully carry out comparative aging studies across the animal kingdom.

 

Apicomplexa are ancient and diverse organisms which have been poorly characterized by modern genomics. To better understand the evolution and diversity of these single-celled eukaryotes, we sequenced the genome ofOphryocystis elektroscirrha, a parasite of monarch butterflies,Danaus plexippus. We contextualize our newly generated resources within apicomplexan genomics before answering longstanding questions specific to this host-parasite system. To start, the genome is miniscule, totaling only 9 million bases and containing fewer than 3,000 genes, half the gene content of two other sequenced invertebrate-infecting apicomplexans,Porospora giganteaandGregarina niphandrodes. We found thatO. elektroscirrhashares different orthologs with each sequenced relative, suggesting the true set of universally conserved apicomplexan genes is very small indeed. Next, we show that sequencing data from other potential host butterflies can be used to diagnose infection status as well as to study diversity of parasite sequences. We recovered a similarly sized parasite genome from another butterfly,Danaus chrysippus, that was highly diverged from theO. elektroscirrhareference, possibly representing a distinct species. Using these two new genomes, we investigated potential evolutionary response by parasites to toxic phytochemicals their hosts ingest and sequester. Monarch butterflies are well-known to tolerate toxic cardenolides thanks to changes in the sequence of their Type II ATPase sodium pumps. We show thatOphryocystiscompletely lacks Type II or Type 4 sodium pumps, and related proteins PMCA calcium pumps show extreme sequence divergence compared to other Apicomplexa, demonstrating new avenues of research opened by genome sequencing of non-model Apicomplexa.

 

Meiosis is usually described as 4 essential and sequential processes: (1) homolog pairing; (2) synapsis, mediated by the synaptonemal complex; (3) crossing over; and (4) segregation. In this canonical model, the maturation of crossovers into chiasmata plays a vital role in holding homologs together and ensuring their segregation at the first meiotic division. However, Lepidoptera (moths and butterflies) undergo 3 distinct meiotic processes, only one of which is canonical. Lepidoptera males utilize 2 meiotic processes: canonical meiosis that produces nucleated fertile sperm, and a noncanonical meiosis that produces anucleated nonfertile sperm which are nonetheless essential for reproduction. Lepidoptera females, which carry heteromorphic sex chromosomes, undergo a completely achiasmate (lacking crossovers) meiosis, thereby requiring an alternative mechanism to ensure proper homolog segregation. Here, we report that the development of a molecular cell biology toolkit designed to properly analyze features of meiosis, including the synaptonemal complex structure and function, in the silkworm Bombyx mori. In addition to standard homology searches to identify Bombyx orthologs of known synaptonemal complex encoding genes, we developed an ortholog discovery app (Shinyapp) to identify Bombyx orthologs of proteins involved in several meiotic processes. We used this information to clone genes expressed in the testes and then created antibodies against their protein products. We used the antibodies to confirm the localization of these proteins in normal male spermatocytes, as well as using in vitro assays to confirm orthologous interactions. The development of this toolkit will facilitate further study of the unique meiotic processes that characterize meiosis in Lepidoptera.

 

The rate of 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, though 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. 

Abstract 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. 

Humoral and cellular immune responses provide animals with major defences against harmful pathogens. While it is often assumed that immune genes undergo rapid diversifying selection, this assumption has not been tested in many species. Moreover, it is likely that different classes of immune genes experience different levels of evolutionary constraint, resulting in varying selection patterns. We examined the evolutionary patterns for a set of 91 canonical immune genes of North American monarch butterflies (Danaus plexippus), using as an outgroup the closely related soldier butterfly (Danaus eresimus). As a comparison to these immune genes, we selected a set of control genes that were paired with each immune for approximate size and genomic location. As a whole, these immune genes had a significant but modest reduction in Tajima'sDrelative to paired‐control genes, but otherwise did not show distinct patterns of population genetic variation or evolutionary rates. When further partitioning these immune genes into four functional classes (recognition, signalling, modulation, and effector), we found distinct differences among these groups. Relative to control genes, recognition genes exhibit increased nonsynonymous diversity and divergence, suggesting reduced constraints on evolution, and supporting the notion that coevolution with pathogens results in diversifying selection. In contrast, signalling genes showed an opposite pattern of reduced diversity and divergence, suggesting evolutionary constraints and conservation. Modulator and effector genes showed no statistical differences from controls. These results are consistent with patterns found in immune genes in fruit flies andPierisbutterflies, suggesting that consistent selective pressures on different classes of immune genes broadly govern the evolution of innate immunity among insects.