Martin Beye

Heinrich-Heine-Universität Düsseldorf | HHU · Department of Biology

Understanding of the neural bases for complex behaviors in Hymenoptera insect species has been limited by a lack of tools that allow measuring neuronal activity simultaneously in different brain regions. Here, we developed the first pan-neuronal genetic driver in a Hymenopteran model organism, the honey bee, and expressed the calcium indicator GCaM...

Animals develop sex-specific morphological structures that are diverse between organisms. However, understanding the developmental and evolutionary mechanisms governing these traits is still limited and largely restricted to DM domain genes, which are conserved, sex-specific developmental regulators identified in genetic models. Here, we report a s...

The honeybee is a haplodiploid organism in which sexual development is determined by the complementary sex determiner (csd) gene and realized by sex-specific splicing processes involving the feminizer (fem) gene. We used high throughput transcriptome sequencing (RNA-Seq) to characterize the transcriptional differences between the sexes caused by th...

Highly social insects are characterized by caste dimorphism, with distinct size differences of reproductive organs between fertile queens and the more or less sterile workers. An abundance of nutrition or instruction via diet-specific compounds has been proposed as explanations for the nutrition-driven queen and worker polyphenism. Here, we further...

Genotypes of dsx-mutated females of Fig 4 as obtained from NGS analyses. The dsx WT nucleotide sequences are represented as a reference sequence. NGS, next-generation sequencing; WT, wild type. (PDF)

Alignment of the amino acid sequence harboring the zink finger motifs (ZF I and ZF II) of the DM domain. The deleted conserved histidine at position 68 of the honeybee sequence (Am) is highlighted with an arrow. (PDF)

The worker bees reared in the colony and the genetic female bees reared manually on worker nutrition. (PDF)

Reproductive organ size of genetic females at larval stage 5 that were double mutant for fem and that were reared on worker nutrition. (PDF)

The intersex reproductive organs of Fig 4 at higher magnification. Scale bar, 1 mm. The genetic females were double mutant for dsx and reared on worker nutrition. For further details, see legend of Fig 4 in the main text. (PDF)

The phenotypes of worker nutrition-reared genetic females and genetic males at an early pupal stage. These females have the typical reduced reproductive organ of workers and the fully developed reproductive organs of males. Head and (a) and (c) and reproductive organ (b) and (d). Gonads were stained with aceto-orcein (reddish coloring) to facilitat...

The genetic male bees reared in colony and manually on worker nutrition. (PDF)

The numbers of mutated larvae and the numbers of length-modified (different to the WT) sequences. WT, wild type. (PDF)

Genes and targeted genomic sites. Genomic organization of the genes fru (a), loc552773 (b), dsx (c), and fem (d) with the designated sgRNA target sites (black arrows). Boxes indicate exons. If genes transcribe sexual splice variants, they are presented. Green boxes indicate common, red the female-specific, and blue the male specific ORF of the sexu...

Nucleotide sequences of the sgRNAs. Sequences complementary to the designated genomic target site are shown in bold letters. sgRNA, single guide RNA. (PDF)

The detected deletions and insertions mediated by CRISPR/Cas9 method in a sample (n = 25) of mutated nucleotide sequences. CRISPR/Cas9, clustered regularly interspaced short palindromic repeats/CRISPR-associated protein 9. (PDF)

Large gonads of the male type in genetic females double mutant for fem. (PDF)

The reared genetic females with intersex reproductive organ that were double mutant for dsx. (PDF)

The nucleotide sequences of the fem-mutated genetic females that were reared on worker nutrition and that have large-sized gonads of the male type. (a) Diagrams of the FL analysis for each of the 4 individuals and WT worker bee examples. (b) The nucleotide sequences. We conducted fragment and sequence analysis on amplicons of cDNA to ensure that th...

Nucleotide sequence changes detected in the mutated larvae at the designated target site. At least 10 clones for each larvae were sequenced. These nucleotide changes were consistently not observed in 7 nontreated (WT) larvae. The sequence complementary to the sgRNAs are underlined. sgRNA, single guide RNA; WT, wild type. (PDF)

The heterozygous, female genotype of the csd gene in the fem double nonsense mutants. (PDF)

Abstract Functional genetic studies in honeybees have been limited by transformation tools that lead to a high rate of transposon integration into the germline of the queens. A high transformation rate is required to reduce screening efforts because each treated queen needs to be maintained in a separate honeybee colony. Here, we report on further...

Short linear motifs (SLiMs) can play pivotal functional roles in proteins, such as targeting proteins to specific subcellular localizations, modulating the efficiency of translation and tagging proteins for degradation. Until recently we had little knowledge about SLiM evolution. Only a few amino acids in these motifs are functionally important, ma...

Honeybees form societies in which thousands of members integrate their behaviours to act as a single functional unit. We have little knowledge on how the collaborative features are regulated by workers' activities because we lack methods that enable collection of simultaneous and continuous behavioural information for each worker bee. In this study...

Background Hygienic behavior (HB) enables honeybees to tolerate parasites, including infection with the parasitic mite Varroa destructor, and it is a well-known example of a quantitative genetic trait. The understanding of the molecular processes underpinning the quantitative differences in this behavior remains limited. ResultsWe performed gene ex...

Honeybees live in complex societies whose capabilities far exceed those of the sum of their single members. This social synergism is achieved mainly by the worker bees, which form a female caste. The worker bees display diverse collaborative behaviors and engage in different behavioral tasks, which are controlled by the central nervous system (CNS)...

S1 Figure: Venn diagram of the number of differentially expressed (DEGs) and differentially spliced (DSGs) genes in the worker/male and worker/queen comparisons. S1 Table: Numbers of reads that were sequenced and the numbers and proportions of reads that were mapped to the honeybee genome. S2 Table: Number of differentially expressed genes in the b...

Pooled samples are frequently used in experiments measuring gene expression. In this method, RNA from different individuals sharing the same experimental conditions and explanatory variables is blended and their concentrations are jointly measured. As a matter of principle, individuals are represented in equal shares in each pool. However, some deg...

Abstract Background The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population...

The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some spe...

The shift from solitary to social behavior is one of the major evolutionary transitions. Primitively eusocial bumblebees are uniquely placed to illuminate the evolution of highly eusocial insect societies. Bumblebees are also invaluable natural and agricultural pollinators, and there is widespread concern over recent population declines in some spe...

Significance We report the first to our knowledge genetically engineered honeybees, which are important pollinators and interesting biological models for the study of social and complex behaviors as well as caste and sexual development. This genetic manipulation tool will enable systematic studies of biological processes in an organism building com...

The primary signal of sex determination in the honeybee, the complementary sex determiner (csd) gene, evolved from a gene duplication event from an ancestral copy of the fem gene. Recently, other paralogs of the fem gene have been identified in several ant and bumblebee genomes. This discovery and the close phylogenetic relationship of the paralogo...

The first generation of genome sequence assemblies and annotations have had a significant impact upon our understanding of the biology of the sequenced species, the phylogenetic relationships among species, the study of populations within and across species, and have informed the biology of humans. As only a few Metazoan genomes are approaching fin...

Recent studies in a representative selection of holometabolous insects suggest that, despite diversity at the instructive level, the signal-relaying part of the sex-determining pathway is remarkably well conserved. In principle, it is composed of the transformer gene (tra) , which acts as a common binary switch that transduces the selected sexual f...

Recent studies in a representative selection of holometabolous insects suggest that, despite diversity at the instructive level, the signal-relaying part of the sex-determining pathway is remarkably well conserved. In principle, it is composed of the transformer gene (tra), which acts as a common binary switch that transduces the selected sexual fa...

Some genes regulate phenotypes that are either present or absent. They are often important regulators of developmental switches and are involved in morphological evolution. We have little understanding of the molecular mechanisms by which these absence/presence gene functions have evolved, because the phenotype and fitness of molecular intermediate...

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The honey bee, Apis mellifera, displays a rich behavioural repertoire, social organization and caste differentiation, and has an interesting mode of sex determination, but we still know little about its underlying genetic programs. We lack stable transgenic tools in honey bees that would allow genetic control of gene activity in stable transgenic l...

Heteroallelic and homo- or hemiallelic Csd (Complementary sex determiner) proteins determine sexual fate in the honeybee (Apis mellifera) by controlling the alternative splicing of the downstream gene fem (feminizer). Thus far, we have little understanding of how heteroallelic Csd proteins mediate the splicing of female fem mRNAs or how Fem protein...

Division of labor in social insects has made the evolution of collective traits possible that cannot be achieved by individuals alone. Differences in behavioral responses produce variation in engagement in behavioral tasks, which as a consequence, generates a division of labor. We still have little understanding of the genetic components influencin...

The number of uncapping acts per L bee in mixed L/H and pure L bee cages. Distributions were compared with a Poisson process. If we exclude a single bee that showed exceptional performance (>9 uncapping acts) from each dataset (combined data from all cages), the distributions are consistent with a Poisson distribution (KS-test, P>0.05; L bees in mi...

Candidate genes associated with the interaction (BxC) of uncapping behavior (B) and genotypic mixing (C). A modified t-test was performed on the log-transformed expression ratios gained from 132 hybridizations between 76 L strain worker bees. Expression levels relate to non-active L bees from pure L bee colonies. Oligo Ids, Gene Ids, and Comments a...

The list of genes identified in the modules of highly correlated transcripts and their functions in Drosophila melanogaster orthologs. Modules of transcriptionally correlated genes inferred from 943 transcripts associated with the interaction of uncapping behavior and hygienic genotype composition (BxC). Pearson correlation analysis was performed o...

A network view of three highly co-regulated transcript sets after module formation. Correlated transcripts are shown in ovals with their gene names. The distances between genes in the plot correspond to their relative connectivity within the network, as calculated by a multiple scaling procedure. |r—| denotes the average correlation and connectivit...

The number of L bees that engaged in the uncapping task, but not also in the second hygienic task, removing, in mixed L/H and pure L bee groups (cumulated data). The observed numbers in mixed and pure L groups were compared with a χ2-test (df = 1; *P<0.025). (PDF)

Candidate genes associated with uncapping behavior (B). A modified t-test was performed on the log-transformed expression ratios gained from 132 hybridizations between 76 L strain worker bees. Expression levels relate to non-active L bees from pure L bee colonies. Oligo Ids, Gene Ids, and Comments are obtained from the UIUC Honey bee oligo 13K v1 a...

Candidate genes associated with genotypic mixing (C). A modified t-test was performed on the log-transformed expression ratios gained from 132 hybridizations between 76 L strain worker bees. Expression levels relate to non-active L bees from pure L bee colonies. Oligo Ids, Gene Ids, and Comments are obtained from the UIUC Honey bee oligo 13K v1 ann...

Box plots displaying the engagement and performance of removing activities by L bees (shown in blue boxes) and H bees (shown in red boxes) in mixed L/H and pure L or H bee groups. (A) The proportion (%) of L1/L2 or H1/H2 bees that engaged in removing tasks in the different cages. (B) The counts of removing acts per L1 or L2 and H1 or H2 worker bee...

Microarray experimental design. Each box indicates an RNA sample from a bee that exhibited uncapping behavior (square boxes) or a control bee that showed no hygienic behavior (oval boxes). Light blue and dark blue colored boxes were assigned to bees depending on whether they were derived from the mixed L/H bee colony or the pure L bee colony, respe...

The number of uncapped brood cells in mixed L/H bee groups (cumulative data from all cages). The expected numbers of uncapped cells (those that were treated) was estimated from the mean relative proportion of uncapped cells in pure L or H bee groups and the relative proportion of L and H bees in the mixed groups. The mean percentage of uncapped bro...

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