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1.
Genome Res ; 34(6): 863-876, 2024 Jul 23.
Article in English | MEDLINE | ID: mdl-38839375

ABSTRACT

Eusocial Hymenoptera have the highest recombination rates among all multicellular animals studied so far, but it is unclear why this is and how this affects the biology of individual species. A high-resolution linkage map for the ant Cardiocondyla obscurior corroborates genome-wide high recombination rates reported for ants (8.1 cM/Mb). However, recombination is locally suppressed in regions that are enriched with TEs, that have strong haplotype divergence, or that show signatures of epistatic selection in C. obscurior The results do not support the hypotheses that high recombination rates are linked to phenotypic plasticity or to modulating selection efficiency. Instead, genetic diversity and the frequency of structural variants correlate positively with local recombination rates, potentially compensating for the low levels of genetic variation expected in haplodiploid social Hymenoptera with low effective population size. Ultimately, the data show that recombination contributes to within-population polymorphism and to the divergence of the lineages within C. obscurior.


Subject(s)
Ants , Recombination, Genetic , Animals , Ants/genetics , Chromosome Mapping , Haplotypes , Genetic Variation , Genome, Insect , Selection, Genetic , Evolution, Molecular
2.
Chromosome Res ; 32(3): 10, 2024 Jul 22.
Article in English | MEDLINE | ID: mdl-39034331

ABSTRACT

The number of chromosomes varies tremendously across species. It is not clear whether having more or fewer chromosomes could be advantageous. The probability of non-disjunction should theoretically decrease with smaller karyotypes, but too long chromosomes should enforce spatial constraint for their segregation during the mitotic anaphase. Here, we propose a new experimental cell system to acquire novel insights into the mechanisms underlying chromosome segregation. We collected the endemic Australian ant Myrmecia croslandi, the only known species with the simplest possible karyotype of a single chromosome in the haploid males (and one pair of chromosomes in the diploid females), since males are typically haploid in hymenopteran insects. Five colonies, each with a queen and a few hundreds of workers, were collected in the Canberra district (Australia), underwent karyotype analysis to confirm the presence of a single pair of chromosomes in worker pupae, and were subsequently maintained in the laboratory in Paris (France). Starting from dissociated male embryos, we successfully conducted primary cell cultures comprised of single-chromosome cells. This could be developed into a unique model that will be of great interest for future genomic and cell biology studies related to mitosis.


Subject(s)
Ants , Chromosomes, Insect , Animals , Ants/genetics , Male , Female , Primary Cell Culture , Karyotyping , Karyotype , Haploidy , Chromosome Segregation
3.
BMC Biol ; 22(1): 109, 2024 May 13.
Article in English | MEDLINE | ID: mdl-38735942

ABSTRACT

BACKGROUND: Social insects vary considerably in their social organization both between and within species. In the California harvester ant, Pogonomyrmex californicus (Buckley 1867), colonies are commonly founded and headed by a single queen (haplometrosis, primary monogyny). However, in some populations in California (USA), unrelated queens cooperate not only during founding (pleometrosis) but also throughout the life of the colony (primary polygyny). The genetic architecture and evolutionary dynamics of this complex social niche polymorphism (haplometrosis vs pleometrosis) have remained unknown. RESULTS: We provide a first analysis of its genomic basis and evolutionary history using population genomics comparing individuals from a haplometrotic population to those from a pleometrotic population. We discovered a recently evolved (< 200 k years), 8-Mb non-recombining region segregating with the observed social niche polymorphism. This region shares several characteristics with supergenes underlying social polymorphisms in other socially polymorphic ant species. However, we also find remarkable differences from previously described social supergenes. Particularly, four additional genomic regions not in linkage with the supergene show signatures of a selective sweep in the pleometrotic population. Within these regions, we find for example genes crucial for epigenetic regulation via histone modification (chameau) and DNA methylation (Dnmt1). CONCLUSIONS: Altogether, our results suggest that social morph in this species is a polygenic trait involving a potential young supergene. Further studies targeting haplo- and pleometrotic individuals from a single population are however required to conclusively resolve whether these genetic differences underlie the alternative social phenotypes or have emerged through genetic drift.


Subject(s)
Ants , Animals , Ants/genetics , Social Behavior , Genomics , Genome, Insect , Polymorphism, Genetic , Biological Evolution , Female , California , Evolution, Molecular
4.
BMC Bioinformatics ; 25(1): 254, 2024 Aug 01.
Article in English | MEDLINE | ID: mdl-39090538

ABSTRACT

BACKGROUND: High-throughput experimental technologies can provide deeper insights into pathway perturbations in biomedical studies. Accordingly, their usage is central to the identification of molecular targets and the subsequent development of suitable treatments for various diseases. Classical interpretations of generated data, such as differential gene expression and pathway analyses, disregard interconnections between studied genes when looking for gene-disease associations. Given that these interconnections are central to cellular processes, there has been a recent interest in incorporating them in such studies. The latter allows the detection of gene modules that underlie complex phenotypes in gene interaction networks. Existing methods either impose radius-based restrictions or freely grow modules at the expense of a statistical bias towards large modules. We propose a heuristic method, inspired by Ant Colony Optimization, to apply gene-level scoring and module identification with distance-based search constraints and penalties, rather than radius-based constraints. RESULTS: We test and compare our results to other approaches using three datasets of different neurodegenerative diseases, namely Alzheimer's, Parkinson's, and Huntington's, over three independent experiments. We report the outcomes of enrichment analyses and concordance of gene-level scores for each disease. Results indicate that the proposed approach generally shows superior stability in comparison to existing methods. It produces stable and meaningful enrichment results in all three datasets which have different case to control proportions and sample sizes. CONCLUSION: The presented network-based gene expression analysis approach successfully identifies dysregulated gene modules associated with a certain disease. Using a heuristic based on Ant Colony Optimization, we perform a distance-based search with no radius constraints. Experimental results support the effectiveness and stability of our method in prioritizing modules of high relevance. Our tool is publicly available at github.com/GhadiElHasbani/ACOxGS.git.


Subject(s)
Gene Regulatory Networks , Gene Regulatory Networks/genetics , Humans , Algorithms , Neurodegenerative Diseases/genetics , Gene Expression Profiling/methods , Computational Biology/methods , Animals , Ants/genetics , Databases, Genetic
5.
BMC Genomics ; 25(1): 84, 2024 Jan 20.
Article in English | MEDLINE | ID: mdl-38245722

ABSTRACT

BACKGROUND: Venoms have evolved independently over a hundred times in the animal kingdom to deter predators and/or subdue prey. Venoms are cocktails of various secreted toxins, whose origin and diversification provide an appealing system for evolutionary researchers. Previous studies of the ant venom of Tetramorium bicarinatum revealed several Myrmicitoxin (MYRTX) peptides that gathered into seven precursor families suggesting different evolutionary origins. Analysis of the T. bicarinatum genome enabling further genomic approaches was necessary to understand the processes underlying the evolution of these myrmicitoxins. RESULTS: Here, we sequenced the genome of Tetramorium bicarinatum and reported the organisation of 44 venom peptide genes (vpg). Of the eleven chromosomes that make up the genome of T. bicarinatum, four carry the vpg which are organized in tandem repeats. This organisation together with the ML evolutionary analysis of vpg sequences, is consistent with evolution by local duplication of ancestral genes for each precursor family. The structure of the vpg into two or three exons is conserved after duplication events while the promoter regions are the least conserved parts of the vpg even for genes with highly identical sequences. This suggests that enhancer sequences were not involved in duplication events, but were recruited from surrounding regions. Expression level analysis revealed that most vpg are highly expressed in venom glands, although one gene or group of genes is much more highly expressed in each family. Finally, the examination of the genomic data revealed that several genes encoding transcription factors (TFs) are highly expressed in the venom glands. The search for binding sites (BS) of these TFs in the vpg promoters revealed hot spots of GATA sites in several vpg families. CONCLUSION: In this pioneering investigation on ant venom genes, we provide a high-quality assembly genome and the annotation of venom peptide genes that we think can fosters further genomic research to understand the evolutionary history of ant venom biochemistry.


Subject(s)
Ant Venoms , Ants , Humans , Animals , Venoms/genetics , Ant Venoms/chemistry , Ant Venoms/genetics , Ant Venoms/metabolism , Peptides/metabolism , Genome , Ants/genetics , Evolution, Molecular
6.
Mol Genet Genomics ; 299(1): 16, 2024 Feb 27.
Article in English | MEDLINE | ID: mdl-38411741

ABSTRACT

Mitochondria play a key role in cell biology and have their own genome, residing in a highly oxidative environment that induces faster changes than the nuclear genome. Because of this, mitochondrial markers have been exploited to reconstruct phylogenetic and phylogeographic relationships in studies of adaptation and molecular evolution. In this study, we determined the complete mitogenome of the fungus-farming ant Mycetophylax simplex (Hymenoptera, Formicidae) and conducted a comparative analysis among 29 myrmicine ant mitogenomes. Mycetophylax simplex is an endemic ant that inhabits sand dunes along the southern Atlantic coast. Specifically, the species occur in the ecosystem known as "restinga", within the Atlantic Forest biome. Due to habitat degradation, land use and decline of restinga habitats, the species is considered locally extinct in extremely urban beaches and is listed as vulnerable on the Brazilian Red List (ICMBio). We employed a mitochondrion-targeting approach to obtain the complete mitogenome through high-throughput DNA sequencing technology. This method allowed us to determine the mitogenome with high performance, coverage and low cost. The circular mitogenome has a length of 16,367 base pairs enclosing 37 genes (13 protein-coding genes, 22 tRNAs and 2 rRNAs) along with one control region (CR). All the protein-coding genes begin with a typical ATN codon and end with the canonical stop codons. All tRNAs formed the fully paired acceptor stems and fold into the typical cloverleaf-shaped secondary structures. The gene order is consistent with the shared Myrmicinae structure, and the A + T content of the majority strand is 81.51%. Long intergenic spacers were not found but some gene are slightly shorter. The phylogenetic relationships based on concatenated nucleotide and amino acid sequences of the 13 protein-coding genes, using Maximum Likelihood and Bayesian Inference methods, indicated that mitogenome sequences were useful in resolving higher-level relationship within Formicidae.


Subject(s)
Ants , Genome, Mitochondrial , Animals , Genome, Mitochondrial/genetics , Ecosystem , Bayes Theorem , Phylogeny , Mitochondria/genetics , Ants/genetics
7.
Proc Biol Sci ; 291(2026): 20241214, 2024 Jul.
Article in English | MEDLINE | ID: mdl-38981524

ABSTRACT

Obligatory ant-plant symbioses often appear to be single evolutionary shifts within particular ant lineages; however, convergence can be revealed once natural history observations are complemented with molecular phylogenetics. Here, we describe a remarkable example of convergent evolution in an ant-plant symbiotic system. Exclusively arboreal, Myrmelachista species can be generalized opportunists nesting in several plant species or obligately symbiotic, live-stem nesters of a narrow set of plant species. Instances of specialization within Myrmelachista are known from northern South America and throughout Middle America. In Middle America, a diverse radiation of specialists occupies understory treelets of lowland rainforests. The morphological and behavioural uniformity of specialists suggests that they form a monophyletic assemblage, diversifying after a single origin of specialization. Using ultraconserved element phylogenomics and ancestral state reconstructions, we show that shifts from opportunistic to obligately symbiotic evolved independently in South and Middle America. Furthermore, our analyses support a remarkable case of convergence within the Middle American radiation, with two independently evolved specialist clades, arising nearly simultaneously from putative opportunistic ancestors during the late Pliocene. This repeated evolution of a complex phenotype suggests similar mechanisms behind trait shifts from opportunists to specialists, generating further questions about the selective forces driving specialization.


Subject(s)
Ants , Biological Evolution , Phylogeny , Symbiosis , Ants/physiology , Ants/genetics , Animals , South America , Central America , Myrmecophytes
8.
Proc Biol Sci ; 291(2024): 20240494, 2024 Jun.
Article in English | MEDLINE | ID: mdl-38864332

ABSTRACT

Social organization, dispersal and fecundity coevolve, but whether they are genetically linked remains little known. Supergenes are prime candidates for coupling adaptive traits and mediating sex-specific trade-offs. Here, we test whether a supergene that controls social structure in Formica selysi also influences dispersal-related traits and fecundity within each sex. In this ant species, single-queen colonies contain only the ancestral supergene haplotype M and produce MM queens and M males, while multi-queen colonies contain the derived haplotype P and produce MP queens, PP queens and P males. By combining multiple experiments, we show that the M haplotype induces phenotypes with higher dispersal potential and higher fecundity in both sexes. Specifically, MM queens, MP queens and M males are more aerodynamic and more fecund than PP queens and P males, respectively. Differences between MP and PP queens from the same colonies reveal a direct genetic effect of the supergene on dispersal-related traits and fecundity. The derived haplotype P, associated with multi-queen colonies, produces queens and males with reduced dispersal abilities and lower fecundity. More broadly, similarities between the Formica and Solenopsis systems reveal that supergenes play a major role in linking behavioural, morphological and physiological traits associated with intraspecific social polymorphisms.


Subject(s)
Animal Distribution , Ants , Fertility , Social Behavior , Animals , Ants/physiology , Ants/genetics , Male , Female , Haplotypes
9.
Mol Ecol ; 33(8): e17322, 2024 Apr.
Article in English | MEDLINE | ID: mdl-38501589

ABSTRACT

The N6-methyladenosine (m6A) modification of RNA has been reported to remodel gene expression in response to environmental conditions; however, the biological role of m6A in social insects remains largely unknown. In this study, we explored the role of m6A in the division of labour by worker ants (Solenopsis invicta). We first determined the presence of m6A in RNAs from the brains of worker ants and found that m6A methylation dynamics differed between foragers and nurses. Depletion of m6A methyltransferase or chemical suppression of m6A methylation in foragers resulted in a shift to 'nurse-like' behaviours. Specifically, mRNAs of dopamine receptor 1 (Dop1) and dopamine transporter (DAT) were modified by m6A, and their expression increased dopamine levels to promote the behavioural transition from foragers to nurses. The abundance of Dop1 and DAT mRNAs and their stability were reduced by the inhibition of m6A modification caused by the silencing of Mettl3, suggesting that m6A modification in worker ants modulates dopamine synthesis, which regulates labour division. Collectively, our results provide the first example of the epitranscriptomic regulation of labour division in social insects and implicate m6A regulatory mechanism as a potential novel target for controlling red imported fire ants.


Subject(s)
Adenosine/analogs & derivatives , Ants , RNA , Humans , Animals , Dopamine/genetics , Dopamine/metabolism , Ants/genetics , RNA, Messenger/metabolism
10.
Mol Ecol ; 33(13): e17417, 2024 Jul.
Article in English | MEDLINE | ID: mdl-38808556

ABSTRACT

A co-evolutionary arms race ensues when parasites exhibit exploitative behaviour, which prompts adaptations in their hosts, in turn triggering counter-adaptations by the parasites. To unravel the genomic basis of this coevolution from the host's perspective, we collected ants of the host species Temnothorax longispinosus, parasitized by the social parasite Temnothorax americanus, from 10 populations in the northeastern United States exhibiting varying levels of parasite prevalence and living under different climatic conditions. We conducted a genome-wide association study (GWAS) to identify single nucleotide polymorphisms (SNPs) associated with both prevalence and climate. Our investigation highlighted a multitude of candidate SNPs associated with parasite prevalence, particularly in genes responsible for sensory perception of smell including odorant receptor genes. We further focused on population-specific compositions of cuticular hydrocarbons, a complex trait important for signalling, communication and protection against desiccation. The relative abundances of n-alkanes were correlated with climate, while there was only a trend between parasite prevalence and the relative abundances of known recognition cues. Furthermore, we identified candidate genes likely involved in the synthesis and recognition of specific hydrocarbons. In addition, we analysed the population-level gene expression in the antennae, the primary organ for odorant reception, and established a strong correlation with parasite prevalence. Our comprehensive study highlights the intricate genomic patterns forged by the interplay of diverse selection factors and how these are manifested in the expression of various phenotypes.


Subject(s)
Ants , Genome-Wide Association Study , Polymorphism, Single Nucleotide , Receptors, Odorant , Animals , Ants/genetics , Ants/parasitology , Receptors, Odorant/genetics , Climate , Host-Parasite Interactions/genetics , Adaptation, Physiological/genetics , Odorants , Hydrocarbons/metabolism
11.
Mol Ecol ; 33(15): e17454, 2024 Aug.
Article in English | MEDLINE | ID: mdl-39005142

ABSTRACT

The evolution of animals and their gut symbionts is a complex phenomenon, obscured by lability and diversity. In social organisms, transmission of symbionts among relatives may yield systems with more stable associations. Here, we study the history of a social insect symbiosis involving cephalotine ants and their extracellular gut bacteria, which come predominantly from host-specialized lineages. We perform multi-locus phylogenetics for symbionts from nine bacterial orders, and map prior amplicon sequence data to lineage-assigned symbiont genomes, studying distributions of rigorously defined symbionts across 20 host species. Based on monophyly and additional hypothesis testing, we estimate that these specialized gut bacteria belong to 18 distinct lineages, of which 15 have been successfully isolated and cultured. Several symbiont lineages showed evidence for domestication events that occurred later in cephalotine evolutionary history, and only one lineage was ubiquitously detected in all 20 host species and 48 colonies sampled with amplicon 16S rRNA sequencing. We found evidence for phylogenetically constrained distributions in four symbionts, suggesting historical or genetic impacts on community composition. Two lineages showed evidence for frequent intra-lineage co-infections, highlighting the potential for niche divergence after initial domestication. Nearly all symbionts showed evidence for occasional host switching, but four may, more often, co-diversify with their hosts. Through our further assessment of symbiont localization and genomic functional profiles, we demonstrate distinct niches for symbionts with shared evolutionary histories, prompting further questions on the forces underlying the evolution of hosts and their gut microbiomes.


Subject(s)
Ants , Domestication , Phylogeny , RNA, Ribosomal, 16S , Symbiosis , Animals , Symbiosis/genetics , Ants/microbiology , Ants/genetics , RNA, Ribosomal, 16S/genetics , Gastrointestinal Microbiome/genetics , Bacteria/genetics , Bacteria/classification , Biological Evolution
12.
Mol Phylogenet Evol ; 194: 108028, 2024 May.
Article in English | MEDLINE | ID: mdl-38342161

ABSTRACT

Myrmecophytic plants utilise defensive services offered by obligate ant partners nesting in their domatia in a novel means of survival in tropical habitats. Although much is known about the ecology of myrmecophytism, there aren't enough empirical examples to demonstrate whether it substantially influences evolutionary patterns in host plant lineages. In this study, we make use of the species-rich Macaranga (Euphorbiaceae) ant-plant symbiosis distributed in the Southeast Asian Sundaland to delve into the evolutionary dynamics of myrmecophytism in host plants. We generated the most comprehensive dated phylogeny of myrmecophytic Macaranga till date using genotyping-by-sequencing (GBS). With this in hand, we traced the evolutionary history of myrmecophytism in Macaranga using parametric biogeography and ancestral state reconstruction. Diversification rate analysis methods were employed to determine if myrmecophytism enhanced diversification rates in the genus. Our results demonstrate that myrmecophytism is labile and easily lost. Ancestral state reconstruction supported a single origin of myrmecophytism in Macaranga âˆ¼18 mya on Borneo followed by multiple losses. Diversification rate analysis methods did not yield sufficient evidence to support the hypothesis that myrmecophytism enhanced diversification rates in Macaranga; we found that topographical features on Borneo may have played a more direct role in the divergence of clades instead. Our study provides evidence that while the acquisition of domatia clearly functions as a key innovation that has enabled host plants to exploit the environment in novel ways, it may not necessarily enhance diversification rates. In fact, we hypothesise that overly specialised cases of myrmecophytism may even be an evolutionary dead end.


Subject(s)
Ants , Euphorbiaceae , Animals , Ants/genetics , Myrmecophytes , Phylogeny , Plants , Symbiosis/genetics
13.
Mol Phylogenet Evol ; 198: 108142, 2024 Sep.
Article in English | MEDLINE | ID: mdl-38964594

ABSTRACT

Assigning a query individual animal or plant to its derived population is a prime task in diverse applications related to organismal genealogy. Such endeavors have conventionally relied on short DNA sequences under a phylogenetic framework. These methods naturally show constraints when the inferred population sources are ambiguously phylogenetically structured, a scenario demanding substantially more informative genetic signals. Recent advances in cost-effective production of whole-genome sequences and artificial intelligence have created an unprecedented opportunity to trace the population origin for essentially any given individual, as long as the genome reference data are comprehensive and standardized. Here, we developed a convolutional neural network method to identify population origins using genomic SNPs. Three empirical datasets (an Asian honeybee, a red fire ant, and a chicken datasets) and two simulated populations are used for the proof of concepts. The performance tests indicate that our method can accurately identify the genealogy origin of query individuals, with success rates ranging from  93 % to 100 %. We further showed that the accuracy of the model can be significantly increased by refining the informative sites through FST filtering. Our method is robust to configurations related to batch sizes and epochs, whereas model learning benefits from the setting of a proper preset learning rate. Moreover, we explained the importance score of key sites for algorithm interpretability and credibility, which has been largely ignored. We anticipate that by coupling genomics and deep learning, our method will see broad potential in conservation and management applications that involve natural resources, invasive pests and weeds, and illegal trades of wildlife products.


Subject(s)
Deep Learning , Animals , Bees/genetics , Bees/classification , Ants/genetics , Ants/classification , Genetics, Population , Chickens/genetics , Chickens/classification , Polymorphism, Single Nucleotide , Genomics , Phylogeny
14.
J Evol Biol ; 37(2): 131-140, 2024 Feb 14.
Article in English | MEDLINE | ID: mdl-38366252

ABSTRACT

The highly invasive Argentine ant (Linepithema humile) started its colonisation from the species' native range in South America approximately 150 years ago and has since become one of the major pests in the world. We investigated how the shifts into new ranges have affected the evolution of Argentine ants' immune genes. To the best of our knowledge, this is the first broadscale population genetic study focusing on ants' immune genes. We analysed comprehensive targeted-seq data of immune and non-immune genes containing 174 genes from 18 Argentine ant supercolonies covering the species' native and introduced ranges. We predicted that the immune gene evolution of introduced supercolonies differs from that of the native supercolonies and proposed two different, non-mutually exclusive hypotheses for this: 1) the enemy release hypothesis and 2) the higher pathogen pressure hypothesis - both of which seem to explain the observed evolutionary patterns on their behalf. Our results show that the introduced supercolonies were targeted by weaker selection than natives, but positive selection was evident among supercolonies of both ranges. Moreover, in some cases, such as the antiviral RNAi genes, introduced range supercolonies harboured a higher proportion of positively selected genes than natives. This observation was striking, knowing the recent demographic history and the detected generally lower selection efficacy of introduced supercolonies. In conclusion, it is evident that pathogen pressure is ubiquitous and strongly affects the immune gene evolution in Argentine ants.


Subject(s)
Ants , Animals , Ants/genetics , Evolution, Molecular , South America , Introduced Species
15.
Naturwissenschaften ; 111(4): 39, 2024 Jul 15.
Article in English | MEDLINE | ID: mdl-39008082

ABSTRACT

Coastal dunes are unique habitats, threatened by human activities. In biogeographical terms, coastal dunes are habitat islands, being discrete and distinct patches of similar habitat among themselves, separated from each other by a different type of habitat. Furthermore, coastal dunes harbor endemic species, adapted to living solely in the habitats found on specific dune systems. For example, the honeypot ant Myrmecocystus baja is endemic and restricted to coastal dunes of Mexico's Baja California Pacific coast. This ecological and biogeographical scenario led to the questions whether their geographical isolation is reflected in their genetic diversity and structuring, and how their demographic history is related with the formation of the dune system habitats. To answer these questions, population genetic, isolation-with-migration, and phylogeographical analyses were carried out, based on mitochondrial and five nuclear intronic markers. Minimal gene flow was detected only between two of the dune systems sampled; otherwise, the M. baja populations were found to be isolated and genetically structured, and their divergence generally pre-dated the modern-day dune systems. It is therefore highly likely that these ants were already present in paleodunes and that each of the populations was established from founder populations as the dunes formed. These findings highlight the importance of coastal dunes for species such as the honeypot ant from Baja California, in promoting genetic differentiation.


Subject(s)
Ants , Ecosystem , Genetic Variation , Animals , Ants/genetics , Ants/classification , Mexico , DNA, Mitochondrial/genetics , Gene Flow , Phylogeography
16.
Int J Mol Sci ; 24(24)2023 Dec 05.
Article in English | MEDLINE | ID: mdl-38138959

ABSTRACT

The red imported fire ant (Solenopsis invicta Buren) is a social pest species with a robust reproductive ability that causes extensive damage. Identification of the genes involved in queen fertility is critical in order to better understand the reproductive biology and screening for the potential molecular targets in S. invicta. Here, we used the mRNA deep sequencing (RNA-seq) approach to identify differentially expressed genes (DEGs) in the transcriptomes of three reproductive caste types of S. invicta, including queen (QA) and winged female (FA) and male (MA) ants. The genes that were specific to and highly expressed in the queens were then screened, and the Vg2 and Vg3 genes were chosen as targets to explore their functions in oogenesis and fertility. A minimum of 6.08 giga bases (Gb) of clean reads was obtained from all samples, with a mapping rate > 89.78%. There were 7524, 7133, and 977 DEGs identified in the MA vs. QA, MA vs. FA, and FA vs. QA comparisons, respectively. qRT-PCR was used to validate 10 randomly selected DEGs, including vitellogenin 2 (Vg2) and 3 (Vg3), and their expression patterns were mostly consistent with the RNA-seq data. The S. invicta Vgs included conserved domains and motifs that are commonly found in most insect Vgs. SiVg2 and SiVg3 were highly expressed in queens and winged females and were most highly expressed in the thorax, followed by the fat body, head, and epidermis. Evaluation based on a loss-of-function-based knockdown analysis showed that the downregulation of either or both of these genes resulted in smaller ovaries, less oogenesis, and less egg production. The results of transcriptional sequencing provide a foundation for clarifying the regulators of queen fertility in S. invicta. The functions of SiVg2 and SiVg3 as regulators of oogenesis highlight their importance in queen fecundity and their potential as targets of reproductive disruption in S. invicta control.


Subject(s)
Ants , Vitellogenins , Animals , Female , Male , Vitellogenins/genetics , Vitellogenins/metabolism , Fire Ants , Reproduction/genetics , Fertility/genetics , Ants/genetics
17.
Sci Adv ; 10(22): eadp1532, 2024 May 31.
Article in English | MEDLINE | ID: mdl-38820161

ABSTRACT

Animals have evolved various sex determination systems. Here, we describe a newly found mechanism. A long noncoding RNA (lncRNA) transduces complementary sex determination (CSD) signal in the invasive Argentine ant. In this haplodiploid species, we identified a 5-kilobase hyper-polymorphic region underlying CSD: Heterozygous embryos become females, while homozygous and hemizygous embryos become males. Heterozygosity at the CSD locus correlates with higher expression of ANTSR, a gene that overlaps with the CSD locus and specifies an lncRNA transcript. ANTSR knockdown in CSD heterozygotes leads to male development. Comparative analyses indicated that, in Hymenoptera, ANTSR is an ancient yet rapidly evolving gene. This study reveals an lncRNA involved in genetic sex determination, alongside a previously unknown regulatory mechanism underlying sex determination based on complementarity among noncoding alleles.


Subject(s)
Ants , RNA, Long Noncoding , Sex Determination Processes , Animals , Ants/genetics , Sex Determination Processes/genetics , RNA, Long Noncoding/genetics , Female , Male , Alleles
18.
Commun Biol ; 7(1): 106, 2024 01 17.
Article in English | MEDLINE | ID: mdl-38233456

ABSTRACT

Ants are the most ubiquitous and ecologically dominant arthropods on Earth, and understanding their phylogeny is crucial for deciphering their character evolution, species diversification, and biogeography. Although recent genomic data have shown promise in clarifying intrafamilial relationships across the tree of ants, inconsistencies between molecular datasets have also emerged. Here I re-examine the most comprehensive published Sanger-sequencing and genome-scale datasets of ants using model comparison methods that model among-site compositional heterogeneity to understand the sources of conflict in phylogenetic studies. My results under the best-fitting model, selected on the basis of Bayesian cross-validation and posterior predictive model checking, identify contentious nodes in ant phylogeny whose resolution is modelling-dependent. I show that the Bayesian infinite mixture CAT model outperforms empirical finite mixture models (C20, C40 and C60) and that, under the best-fitting CAT-GTR + G4 model, the enigmatic Martialis heureka is sister to all ants except Leptanillinae, rejecting the more popular hypothesis supported under worse-fitting models, that place it as sister to Leptanillinae. These analyses resolve a lasting controversy in ant phylogeny and highlight the significance of model comparison and adequate modelling of among-site compositional heterogeneity in reconstructing the deep phylogeny of insects.


Subject(s)
Ants , Animals , Phylogeny , Ants/genetics , Bayes Theorem , Genomics , Genome
19.
BMC Genom Data ; 25(1): 70, 2024 Jul 15.
Article in English | MEDLINE | ID: mdl-39009995

ABSTRACT

OBJECTIVES: Ants are ecologically dominant insects in most terrestrial ecosystems, with more than 14,000 extant species in about 340 genera recorded to date. However, genomic resources are still scarce for most species, especially for species endemic in East or Southeast Asia, limiting the study of phylogeny, speciation and adaptation of this evolutionarily successful animal lineage. Here, we assemble and annotate the genomes of Odontoponera transversa and Camponotus friedae, two ant species with a natural distribution in China, to facilitate future study of ant evolution. DATA DESCRIPTION: We obtained a total of 16 Gb and 51 Gb PacBio HiFi data for O. transversa and C. friedae, respectively, which were assembled into the draft genomes of 339 Mb for O. transversa and 233 Mb for C. friedae. Genome assessments by multiple metrics showed good completeness and high accuracy of the two assemblies. Gene annotations assisted by RNA-seq data yielded a comparable number of protein-coding genes in the two genomes (10,892 for O. transversa and 11,296 for C. friedae), while repeat annotations revealed a remarkable difference of repeat content between these two ant species (149.4 Mb for O. transversa versus 49.7 Mb for C. friedae). Besides, complete mitochondrial genomes for the two species were assembled and annotated.


Subject(s)
Ants , Genome, Insect , Animals , Ants/genetics , Ants/classification , Genome, Insect/genetics , Molecular Sequence Annotation , Phylogeny , Genomics/methods
20.
PLoS One ; 19(6): e0302371, 2024.
Article in English | MEDLINE | ID: mdl-38857223

ABSTRACT

Formica is a large genus in the family Formicidae with high diversity in its distribution, morphology, and physiology. To better understand evolutionary characteristics of Formica, the complete mitochondrial genomes (mitogenomes) of two Formica species were determined and a comparative mitogenomic analysis for this genus was performed. The two newly sequenced Formica mitogenomes each included 37 typical mitochondrial genes and a large non-coding region (putative control region), as observed in other Formica mitogenomes. Base composition, gene order, codon usage, and tRNA secondary structure were well conserved among Formica species, whereas diversity in sequence size and structural characteristics was observed in control regions. We also observed several conserved motifs in the intergenic spacer regions. These conserved genomic features may be related to mitochondrial function and their highly conserved physiological constraints, while the diversity of the control regions may be associated with adaptive evolution among heterogenous habitats. A negative AT-skew value on the majority chain was presented in each of Formica mitogenomes, indicating a reversal of strand asymmetry in base composition. Strong codon usage bias was observed in Formica mitogenomes, which was predominantly determined by nucleotide composition. All 13 mitochondrial protein-coding genes of Formica species exhibited molecular signatures of purifying selection, as indicated by the ratio of non-synonymous substitutions to synonymous substitutions being less than 1 for each protein-coding gene. Phylogenetic analyses based on mitogenomic data obtained fairly consistent phylogenetic relationships, except for two Formica species that had unstable phylogenetic positions, indicating mitogenomic data are useful for constructing phylogenies of ants. Beyond characterizing two additional Formica mitogenomes, this study also provided some key evolutionary insights into Formica.


Subject(s)
Ants , Evolution, Molecular , Genome, Mitochondrial , Phylogeny , Animals , Ants/genetics , Codon Usage , RNA, Transfer/genetics , Base Composition
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