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Social evolution and diminished olfactory function in larval honey bees.

Social evolution made larval honey bees dependent on adult colony members for feeding; they are confined to cells in waxen honeycombs and visited about 100 times per day by adult "nurse" bees. Based on organismal resource conservation theory, we predicted larvae have diminished olfactory capabilities at both the molecular and behavioral levels. Consistent with theory, larvae expressed very low levels of Orco, an essential gene for olfactory receptor (OR) function. By contrast, they showed higher expression of Ir25a, essential for other forms of sensory perception including gustation. Also consistent with theory, behavioral assays demonstrated that larvae cannot find food via olfaction, suggesting they use taste for feeding. By contrast, it is known that adult honey bees use OR-based olfaction extensively for a variety of behavioral functions, and the honey bee genome contains many OR-encoding genes. Comparative transcriptomic analyses of social and nonsocial insects suggest that this developmentally regulated suppression of olfactory function is related to social evolution, especially systems of offspring care.

Animals

Evolutionary Process Underlying Receptor Gene Expansion and Cellular Divergence of Olfactory Sensory Neurons in Honeybees.

Olfaction is crucial for animals' survival and adaptation. Unlike the strict singular expression of odorant receptor (OR) genes in vertebrate olfactory sensory neurons (OSNs), insects exhibit complex OR gene expression patterns. In honeybees (Apis mellifera), a significant expansion of OR genes implies a selection preference for the olfactory demands of social insects. However, the mechanisms underlying receptor expression specificity and their contribution to OSN divergence remain unclear. In this study, we used single-nucleus multiomics profiling to investigate the transcriptional regulation of OR genes and the cellular identity of OSNs in A. mellifera. We identified three distinct OR expression patterns, singular OR expression, co-expression of multiple OR genes with a single active promoter, and co-expression of multiple OR genes with multiple active promoters. Notably, ∼50% of OSNs co-expressed multiple OR genes, driven by polycistronic transcription of tandemly duplicated OR genes via a single active promoter. In these OSNs, their identity was determined by the first transcribed receptor. The divergent activation of the promoter for duplicated OR genes ensures the coordinated increased divergence of OSN population. By integrating multiomics data with genomic architecture, we illustrate how fundamental genetic mechanisms drive OR gene expansion and influence flanking regulatory elements, ultimately contributing to the cellular divergence of OSNs. Our findings highlight the interplay between gene duplication and regulatory evolution in shaping OSN diversity, providing new insights into the evolution and adaptation of olfaction in social insects. This study also sheds light on how genetic innovations contribute to the evolution of complex traits.

Animals

Transcriptional interference gates monogenic odorant receptor expression in ants.

Communication is crucial to social life, and in ants, it is mediated primarily through olfaction. Ants have more odorant receptor (OR) genes than any other group of insects, generated through tandem duplications that produce large genomic arrays of related genes. The mechanism by which olfactory sensory neurons (OSNs) produce a single functional OR from these arrays remains unclear. In ant OSNs, only mRNA from one OR in an array is exported into the cytoplasm, while upstream genes are silent and transcripts from downstream genes remain nuclear. Here, we show that readthrough transcription in the downstream direction generates non-translated transcripts. We also find that OR promoters are bidirectional, producing antisense long non-coding RNAs. We suspect that neither readthrough nor antisense transcription produces functional RNA but that bidirectional transcription alone is critical to suppressing the expression of all other OR genes in a tandem array. Finally, we present evidence that this regulatory architecture is conserved across ants and bees, suggesting that this mechanism for functionally monogenic OR expression is widespread in insects with expanded OR repertoires.

Animals

Comparative analyses of olfactory receptor repertoires in Schizothorax fish based on the chromosome-level genomes: Implications for regulatory roles of dietary differentiation and ploidy variation.

The olfactory receptor (OR) genes constitute the molecular basis of fish olfaction, mediating survival behaviors and environmental adaptation while coevolving with habitat-driven evolution. Schizothorax, a cyprinid genus endemic to the Qinghai-Tibetan Plateau, exhibits remarkable dietary divergence and ploidy variation in response to plateau environmental changes, which presumably facilitates the adaptive evolution of OR genes. However, the evolutionary patterns of OR genes associated with trophic divergence and ploidy variation in this genus remain unclear. In this study, three species were selected: the herbivorous diploid S. macropogon, the carnivorous diploid S. lantsangensis, and the herbivorous tetraploid S. curvilabiatus. S. macropogon possessed 142 OR genes (92.25% functional), primarily located on chromosomes 14 and 24, with the fewest sequence clusters. Such compact gene repertoire and highly overlapping chromosomal clusters indicated specialization for a herbivorous olfactory niche. S. lantsangensis contained 127 OR genes (93.70% functional), concentrated on chromosomes 4 and 5, with fewer sequence clusters and a scattered distribution, reflecting evolution of OR genes under carnivorous feeding habits. The herbivorous tetraploid S. curvilabiatus exhibited striking features: 316 OR genes (94.30% functional), the most subfamilies, unique ε and κ OR subfamilies, and species-specific motifs. These characteristics revealed that ploidy, rather than herbivory, dominated OR gene evolution. In conclusion, dietary differentiation and ploidy variation together drove olfactory adaptive evolution in Schizothorax, providing new insights into vertebrate OR gene ecological adaptation.

Animals

Antennal transcriptome analysis of chemosensory proteins in the raspberry weevil, Aegorhinus superciliosus (Coleoptera: Curculionidae).

Aegorhinus superciliosus (Coleoptera: Curculionidae) is a polyphagous pest of economic importance in southern Chile, the chemical ecology of which remains poorly characterized. Across insect species, chemosensory proteins, including odorant receptors (ORs), gustatory receptors (GRs), ionotropic receptors (IRs), odorant-binding proteins (OBPs), chemosensory proteins (CSPs), and sensory neuron membrane proteins (SNMPs), mediate the detection of chemical cues involved in host selection, reproduction, and other ecologically relevant behaviors. In this study, the antennal transcriptome of adult A. superciliosus was sequenced and analyzed using a de novo RNA-seq approach. Three independent biological replicates per sex were used for RNA-seq, and the same number of independent biological replicates was used for RT-qPCR validation; sequencing yielded 147,409,936 high-quality reads after quality filtering. A total of 112 candidate chemosensory genes were identified, comprising 43 ORs, 34 OBPs, 10 CSPs, 18 IRs, 5 GRs, and 2 SNMPs. Phylogenetic analyses assigned these candidate proteins to established clades, providing a comparative framework for functional inference for ORs and OBPs. Sex- and tissue-biased expression analyses revealed that several ORs, including AsupOR4, AsupOR19, and AsupOBP13, exhibit antennal enrichment and sex-specific expression patterns. Notably, AsupOR19 and AsupOBP13 displayed strong female-biased expression. In addition, transcripts of selected ORs and OBPs were detected in non-antennal tissues, such as the rostrum and legs, suggesting potential functional versatility beyond canonical olfaction. Together, these findings represent the first molecular identification of the chemosensory repertoire of A. superciliosus. This study establishes a foundation for reverse chemical ecology approaches aimed at identifying behaviorally active volatile organic compounds (VOCs) toward environmentally sustainable strategies for integrated pest management.

Animals

Signatures for viral infection and inflammation in the proximal olfactory system in familial Alzheimer's disease.

Alzheimer's disease (AD) is characterized by deficits in olfaction and olfactory pathology preceding diagnosis of dementia. Here we analyzed differential gene and protein expression in the olfactory bulb (OB) and tract (OT) of familial AD (FAD) individuals carrying the autosomal dominant presenilin 1 E280A mutation. Compared to control, FAD OT had increased immunostaining for β-amyloid (Aβ) and CD68 in high and low myelinated regions, as well as increased immunostaining for Iba1 in the high myelinated region. In FAD samples, RNA sequencing showed: (1) viral infection in the OB; (2) inflammation in the OT that carries information via entorhinal cortex from the OB to hippocampus, a brain region essential for learning and memory; and (3) decreased oligodendrocyte deconvolved transcripts. Interestingly, spatial proteomic analysis confirmed altered myelination in the OT of FAD individuals, implying dysfunction of communication between the OB and hippocampus. These findings raise the possibility that viral infection and associated inflammation and dysregulation of myelination of the olfactory system may disrupt hippocampal function, contributing to acceleration of FAD progression.

Humans

Illuminating the mystery of thylacine extinction: a role for relaxed selection and gene loss.

Gene loss shapes lineage-specific traits but is often overlooked in species survival. In this study, we investigate the role of ancestral gene loss using the extinction icon-thylacine (Thylacinus cynocephalus). While studies of neutral genetic variation indicate a population decline before extinction, the impact of thylacine-specific ancestral gene losses remains unexplored. The availability of a chromosomal-level genome of the extinct thylacine offers a unique opportunity for such comparative studies. Here, we leverage palaeogenomic data to compare gene presence/absence patterns between the Tasmanian devil and thylacine. We discovered ancestral (between 13-1 Ma) loss of SAMD9L, HSD17B13, CUZD1 and VWA7 due to multiple gene-inactivating mutations, corroborated by short-read sequencing. The timing of gene loss mirrors the thylacine's shift towards hypercarnivory and increased body size. Notably, the loss of SAMD9 correlates with a carnivorous diet. Our genome-wide analysis reveals olfactory receptor loss and relaxed selection, aligning with reduced olfactory lobes in the thylacine, indicating olfaction is not its primary hunting sense. By integrating palaeogenomic data with comparative genomics, our study reveals ancestral gene losses and their impact on species survival and resilience to environmental changes. Our approach can be extended to other extinct and endangered species, helping to identify genetic factors for conservation efforts.

Animals

Strong but diffuse genetic divergence underlies differentiation in an incipient species of marine stickleback.

Understanding how lineages proceed along the "speciation continuum" and how species boundaries are maintained over time remain central questions in evolutionary biology. Populations early in the speciation process can give us detailed insight into the reproductive barriers that first initiate speciation. In this study, we explore the nature of genomic divergence between two sympatric marine stickleback ecotypes from Atlantic Canada, "whites" and "commons". Males of each ecotype exhibit distinct nuptial colorations, nesting habits, and parental care strategies. Using population genomic analyses of SNPs and copy number variants (CNVs; deletions and duplications) we show that whites and commons consistently form distinct populations. We uncover genomic differentiation in the white ecotype characteristic of an incipient species, showing extremely low genome-wide differentiation (FST) and very recent divergence (~1 kya). Demographic analysis detected very low levels of ongoing gene flow between populations. Our results and prior genomic studies suggest that reproductive isolation is being maintained between ecotypes despite recent evidence that hybridization in nature does occur. Contrary to other systems, we found many small, but dispersed regions of high differentiation throughout the genome rather than explicitly within chromosomal inversions or the sex chromosomes. On chromosomes VII and XVI, we identified CNVs overlapping genes enriched for olfaction, which may play a role in differences in reproductive strategies between ecotypes. Ultimately, our results demonstrate that genome-wide rather than localized differences can underlie the early stages of divergence, and that this pattern is corroborated by both SNPs and CNVs.

Copy Number Variation

Electron microscopic studies of testes in Kallman syndrome.

A patient with Kallman syndrome is presented emphasizing the urologic aspects of this unusual disorder. Testes biopsy at the time of orchiopexy demonstrated infantile testes with interstitial fibrosis and a diminished Leydig and Sertoli cell population. The electron micrograph confirmed type B Sertoli cells. The implications of these findings are discussed and details of treatment given.

Adolescent

Ancestral complexity and constrained diversification of the ant olfactory system.

Communication is a cornerstone of social living, allowing the exchange of information to align goals and synchronize behaviour. Ants, a group of highly successful social insects, have heightened olfactory abilities that are integral to their evolutionary success. Essential for colony cohesion and cooperation, a female-specific olfactory subsystem processes information about nestmate recognition cues (cuticular hydrocarbons), including basiconic sensilla on the antenna and a cluster of specific glomeruli in the antennal lobe. While it has often been linked to ants' social lifestyle, the evolutionary origins and phylogenetic distribution of this system remain unknown. We conducted a comparative exploration of the ant olfactory system across eight major subfamilies, integrating neuroanatomical, chemical and behavioural analyses. Our findings reveal that sophistication of the ant olfactory system has deep evolutionary roots. Moreover, antennal lobe investment is not associated with social traits such as colony size, polygyny or foraging strategies, but correlates with cuticular hydrocarbon profile complexity. Despite neuroanatomical differences, different ant species consistently excel in nestmate discrimination, indicating adaptation to chemical diversity while maintaining reliable social recognition. This suggests that cuticular hydrocarbon profile and neuronal investment in olfactory neuropil have co-evolved to sustain discrimination performance.

Animals

Evaluation of the hypothalamic-pituitary function in a female with hypogonadotropic hypogonadism and anosmia.

A case of Kallmann's syndrome in a woman is presented to evaluate the hypothalamic-pituitary function and status of the genital organs. The diagnosis of Kallmann's syndrome was performed under the determination of low circulating level of estradiol-17 beta and gonadotropins and low sensitivity to an olfactometer. Pituitary response to LRH was observed. Plasma LH response to LRH was observed in a lesser degree compared with the less impaired response of FSH. Daily injection of LRH for 13 days increased pituitary response of gonadotropin secretion. Diminished prolactin secretion and the dissociation of response to TRH and chlorpromazine were shown. Laparoscopic findings revealed a hypoplastic uterus and nearly normal sized ovaries. Ovarian response to exogenous gonadotropins was affirmed by increased estradiol-17 beta level. These results indicated disturbed hypothalamic control of gonadotropins and prolactin, and a reserved pituitary function in this case. Low circulating level of estradiol-17 beta might affect the heterogenous response of the hypothalamic-pituitary axis.

Adrenocorticotropic Hormone