Journal of experimental zoology. Part B, Molecular and developmental evolution最新文献

Trichoptera (caddisflies) is one of the most species-rich orders of aquatic insects. Species of caddisflies cover a broad ecological diversity as exemplified by various uses of underwater silk secretions. Diversity of silk use generally aligns with the evolution of major caddisfly lineages, specifically at the subordinal level: Annulipalpia (retreat makers) and Integripalpia (cocoon and tube-case makers). However, silk use within suborders differs for a few exceptional species in these clades. In this study, we provide the first whole genome assemblies and annotations for two unusual Integripalpia species: Limnocentropus insolitus, whose hard tube-case is anchored to boulders by a rigid, elongated silken stalk, and Phryganopsyche brunnea which builds a “floppy” cylindrical case that lacks the typical robustness of tube-cases. Its texture rather resembles that of the flexible retreats built by Annulipalpia. Using the two high-quality genome assemblies, we identified and annotated the major silk gene, h-fibroin, and compared its amino acid composition across various groups, including retreat, cocoon, and tube-case makers. Our phylogenetic analysis confirmed the phylogenetic position of the two species in the tube-case-making clade. The major silk gene of L. insolitus shows a similar amino acid composition to other tube-case-making species. In contrast, the amino acid composition of P. brunnea resembles that of retreat-making species, in particular with regard to the high content of proline. This is consistent with the hypothesis that proline could be linked to enhanced extensibility of silk fibers. Taken together, our results underscore the role of silk genes in shaping the evolutionary ecology of retreat- and tube-case-making in caddisflies.

Insects display exceptional phenotypic plasticity, which can be mediated by epigenetic modifications, including CpG methylation and histone modifications. In vertebrates, both are interlinked and CpG methylation is associated with gene repression. However, little is known about these regulatory systems in invertebrates, where CpG methylation is mainly restricted to gene bodies of transcriptionally active genes. A widely conserved mechanism involves the co-transcriptional deposition of H3K36 trimethylation and the targeted methylation of unmethylated CpGs by the de novo DNA methyltransferase DNMT3. However, DNMT3 has been lost multiple times in invertebrate lineages raising the question of how the links between CpG methylation, histone modifications and gene expression are affected by its loss. Here, we report the epigenetic landscape of Leptinotarsa decemlineata, a beetle species that has lost DNMT3 but retained CpG methylation. We combine RNA-seq, enzymatic methyl-seq and CUT&Tag to study gene expression, CpG methylation and patterns of H3K36me3 and H3K27ac histone modifications on a genome-wide scale. Despite the loss of DNMT3, H3K36me3 mirrors CpG methylation patterns. Together, they give rise to signature profiles for expressed and not expressed genes. H3K27ac patterns show a prominent peak at the transcription start site that is predictive of expressed genes irrespective of their methylation status. Our study provides new insights into the evolutionary flexibility of epigenetic modification systems that urge caution when generalizing across species.

Ants exhibit complex social organization, morphologically and functionally distinct castes, and the exploitation of diverse ecological niches. How these features have influenced embryonic development relative to other insects remains unclear. Insect embryogenesis has been classified into three modes: In long germ-band development, exemplified by the fruit fly Drosophila melanogaster, segments along the entire anterior–posterior axis of the embryonic primordium are established almost simultaneously, before gastrulation, with the initial embryonic primordium surrounding almost the entire volume of the egg. In short and intermediate germ-band modes, the embryonic primordium occupies a smaller proportion of the egg surface, with anterior segments initially specified, and remaining segments being added sequentially from a posterior growth zone. Here, we examine embryogenesis in three myrmicine ants, the fungus-gardening ants Atta texana and Mycocepurus smithii, and the red imported fire ant Solenopsis invicta. We find that these ant embryos combine features of short germ-band development with a newly characterized progressive pattern of segmentation that has been associated with some long germ-band-developing insects. Despite similarities in the size of ant and Drosophila eggs, embryogenesis in the three ant species is 10- to 20-fold longer than in Drosophila and is also significantly longer than in two other hymenopteran species that have been studied, the honeybee Apis mellifera and the jewel wasp Nasonia vitripennis. Moreover, the embryos produced by A. texana foundress queens develop to first instar larvae 25% faster than embryos produced by mature queens. We discuss these results in the context of the eusocial lifestyle of ants.

Over the course of hundreds of millions of years, biomineralization has evolved independently many times across all kingdoms of life. Among animals, the phylum Mollusca displays a remarkable diversity in biomineral structures, particularly the molluscan shell, which varies greatly in shape, size, pigmentation, and patterning. Shell matrix proteins (SMPs) are key components of these shells, and are thought to drive the precipitation of calcium carbonate minerals and influence shell morphology. However, this structure-function relationship has rarely been studied directly because tools for knocking out genes did not exist in molluscs until recently. In this study, we report the first successful use of CRISPR/Cas9 gene editing to target an SMP in gastropod molluscs. Using the emerging model gastropod Crepidula atrasolea, we generated knockouts of the SMP1 gene. Successful gene editing was confirmed by Sanger and MiSeq sequencing, and loss of SMP1 expression was validated through high-content imaging of crispant embryos. This study establishes C. atrasolea as a valuable model for investigating the genetic basis of shell formation and provides a framework for applying CRISPR/Cas9 technology in other molluscan species. Our approach will enable future studies to thoroughly test the role of SMPs in shaping the diverse array of molluscan shell structures.

In mammals, the increase in cranial suture complexity throughout postnatal ontogeny has been linked to mechanical forces that load on the skull, including compression forces from mastication and the presence and use of cranial appendages in ungulates. Suture complexity, or interdigitation, provides a large absorptive capacity for mechanical stress. Deer are unique among ungulates by the presence of antlers only in males. In particular, Neotropical species exhibit a great diversity in terms of morphology, weight, sexual size dimorphism (absence or presence), and ecology. To evaluate the relationship of suture interdigitation with the mechanical stress produced by antlers, we quantified the complexity of the interfrontal and coronal sutures using fractal dimension (D) in six Neotropical deer species. Utilizing the occlusal tooth area (OTA) of the first upper molar as a proxy of age, we analyze changes of D throughout postnatal ontogeny and test for sexual dimorphism. In all species, ontogenetic series indicate an increase of complexity of both sutures with OTA. Overall, the species with a significant sexual dimorphism in body size and antlers with more than one tine show the more complex sutures, with the presence of greater interdigitation in adult males than in females, regardless of the existence of intraspecific fights during the rut. This is the first study where sexual dimorphism in cranial suture complexity in relation to the presence of antlers in deer is reported, suggesting the role of the interfrontal and coronal sutures on the dissipation of mechanical stress forces produced by the presence of antlers.

De novo genes, which originate from noncoding DNA, are known to have a high rate of turnover over short evolutionary timescales, such as within a species. Thus, their expression is often lineage- or genetic background-specific. However, little is known about their levels and breadth of expression as populations of a species diverge. In this study, we utilized publicly available RNA-seq data to examine the expression of newly evolved open reading frames (neORFs) in comparison to non- and protein-coding genes in Drosophila melanogaster populations from the derived species range in Europe and the ancestral range in sub-Saharan Africa. Our datasets included two adult tissue types as well as whole bodies at two temperatures for both sexes and three larval/prepupal developmental stages in a single tissue and sex, which allowed us to examine neORF expression and divergence across multiple sample types as well as sex and population. We detected a relatively large proportion (approximately 50%) of annotated neORFs as expressed in the population samples, with neORFs often showing greater expression divergence between populations than non- or protein-coding genes. However, differential expression of neORFs between populations tended to occur in a sample type-specific manner. On the other hand, neORFs displayed less sex-biased expression than the other two gene classes, with the majority of sex-biased neORFs detected in whole bodies, which may be attributable to the presence of the gonads. We also found that neORFs shared among multiple lines in the original set of inbred lines in which they were first detected were more likely to be both expressed and differentially expressed in the new population samples, suggesting that neORFs at a higher frequency (i.e. present in more individuals) within a species are more likely to be functional.