Many insects release chemical signals, known as sex pheromones, to attract mates over long distances. The pheromones of male bumble bees, for example, contain chemicals called fatty alcohols. Each species of bumble bee releases a different blend of these chemicals, and even species that are closely related may produce very different ‘cocktails’ of pheromones.

The enzymes that make fatty alcohols are called fatty acyl reductases (or FARs for short). Any change to a gene that encodes one of these enzymes could change the final mix of pheromones produced. This in turn could have far-reaching effects for the insect, and in particular its mating success. Over time, these changes could even result in new species. Yet no one has previously looked into how the genes for FAR enzymes have evolved in bumble bees, or how these genes might have shaped the evolution of this important group of insects.

Tupec, Buček et al. set out to learn what genetic changes led the males of three common species of bumble bees to make dramatically different mixes of pheromones. Comparing the genetic information of bumble bees with that of other insects showed that the bumble bees and their close relatives, stingless bees, often had extra copies of genes for certain FAR enzymes. Inserting some of these genes into yeast cells caused the yeast to make the correct blend of bumble bee pheromones, confirming that these genes did indeed produce the mixture of chemicals in these signals.

Further, detailed analysis of the bumble bees’ genetic information revealed many genetic sequences, called transposable elements, close to the genes for the FAR enzymes. Transposable elements make the genetic material less stable; they can be ‘cut’ or ‘copied and pasted’ in multiple locations and often cause other genes to be duplicated or lost. Tupec et al. concluded that these transposable elements led to a dramatic increase in the number of genes for FAR enzymes in a common ancestor of bumble bees and stingless bees, ultimately allowing a new pheromone ‘language’ to evolve in these insects.

These results add to our understanding of the chemical and genetic events that influence what chemicals insects use to communicate with each other. Tupec, Buček et al. also hope that a better knowledge of the enzymes that insects use to make pheromones could have wide applications. Other insects – including pest moths – use a similar mixture of fatty alcohols as pheromones. Artificially produced enzymes, such as FAR enzymes, could thus be used to mass-produce pheromones that may control insect pests.

Accumulation of DNA sequencing data is greatly outpacing our ability to experimentally assess the function of the sequenced genes, and most of these genes are expected to never be functionally characterized (Koonin, 2005). Important insights into the evolutionary processes shaping the genomes of individual species or lineages can be gathered from predictions of gene families, gene ortholog groups and gene function. However, direct experimental evidence of the function of gene family members is often unavailable or limited (Lespinet et al., 2002; Demuth et al., 2006; Rispe et al., 2008; Cortesi et al., 2015; Niimura and Nei, 2006). Gene duplication is hypothesized to be among the major genetic mechanisms of evolution (Ohno, 1970; Zhang, 2003). Although the most probable evolutionary fate of duplicated genes is the loss of one copy, the temporary redundancy accelerates gene sequence divergence and can result in gene subfunctionalization or neofunctionalization—acquisition of slightly different or completely novel functions in one copy of the gene (Innan and Kondrashov, 2010; Lynch and Conery, 2000).

The alcohol-forming fatty acyl-CoA reductases (FARs, EC 1.2.1.84) belong to a multigene family that underwent a series of gene duplications and subsequent gene losses, pseudogenizations and possibly functional diversification of some of the maintained copies, following the birth-and-death model of gene family evolution (Eirín-López et al., 2012). FARs exhibit notable trends in gene numbers across organism lineages; there are very few FAR genes in fungi, vertebrates and non-insect invertebrates such as Caenorhabditis elegans, whereas plant and insect genomes typically harbor an extensive number of FAR gene family members (Eirín-López et al., 2012). FARs are critical for production of primary fatty alcohols, which are naturally abundant fatty acid (FA) derivatives with a wide variety of biological roles. Fatty alcohols are precursors of waxes and other lipids that serve as surface-protective or hydrophobic coatings in plants, insects and other animals (Wang et al., 2017; Cheng and Russell, 2004; Jaspers et al., 2014); precursors of energy-storing waxes (Metz et al., 2000; Teerawanichpan and Qiu, 2010a; Teerawanichpan and Qiu, 2012); and components of ether lipids abundant in the cell membranes of cardiac, nervous and immunological tissues (Nagan and Zoeller, 2001).

Additionally, in some insect lineages, FARs were recruited for yet another task—biosynthesis of fatty alcohols that serve as pheromones or pheromone precursors. Moths (Lepidoptera) are the most well-studied model of insect pheromone biosynthesis and have been the subject of substantial research effort related to FARs. Variation in FAR enzymatic specificities is a source of sex pheromone signal diversity among moths in the genus Ostrinia (Lassance et al., 2013) and is also responsible for the distinct pheromone composition in two reproductively isolated races of the European corn borer Ostrinia nubilalis (Lassance et al., 2010). Divergence in pheromone biosynthesis can potentially install or strengthen reproductive barriers, ultimately leading to speciation (Smadja and Butlin, 2009). However, the biological significance of a large number of insect FAR paralogs remains unclear, as all FARs implicated in moth and butterfly sex pheromone biosynthesis are restricted to a single clade, indicating that one FAR group was exclusively recruited for pheromone biosynthesis (Lassance et al., 2010; Liénard et al., 2010; Liénard et al., 2014; Antony et al., 2009). While more than 20 FARs have been experimentally characterized from 23 moth and butterfly (Lepidoptera) species (Tupec et al., 2017), FARs from other insect orders have received far less attention. Single FAR genes have been isolated and experimentally characterized from Drosophila (Diptera) (Jaspers et al., 2014), the European honey bee (Hymenoptera) (Teerawanichpan et al., 2010b) and the scale insect Ericeus pela (Hemiptera) (Hu et al., 2018). Our limited knowledge of FAR function prevents us from drawing inferences about the biological significance of the FAR gene family expansion in insects.

Bumble bees (Hymenoptera: Apidae) are a convenient experimental model to study insect FAR evolution because the majority of bumble bee species produces fatty alcohols as species-specific components of male marking pheromones (MMPs) (Ayasse and Jarau, 2014), which are presumed to be biosynthesized by some of the numerous bumble bee FAR gene family members (Buček et al., 2016). Bumble bee males employ MMPs to attract conspecific virgin queens (Goulson, 2010). In addition to fatty alcohols, MMPs generally contain other FA derivatives and terpenoid compounds. MMP fatty alcohols consist predominantly of saturated, mono-unsaturated and poly-unsaturated fatty alcohols with 16–18 carbon atoms (Ayasse and Jarau, 2014). Pheromone mixtures from three common European bumble bee species, B. terrestris, B. lucorum and B. lapidarius, are representative of the known MMP chemical diversity. Fatty alcohols are the major compounds in MMPs of B. lapidarius (hexadecanol and Z9-hexadecenol) and accompany electroantennogram-active compounds in B. terrestris (hexadecanol, octadecatrienol, octadecenol) and B. lucorum (hexadecanol, Z9,Z12-octadecadienol, Z9,Z12,Z15-octadecatrienol, octadecanol) (Bergström et al., 1973; Kullenberg et al., 1973; Kullenberg et al., 1970; Urbanová et al., 2001; Sobotník et al., 2008; Luxová et al., 2003; Zácek et al., 2009).

In our previous investigation of the molecular basis of pheromone diversity in bumble bees, we found that the substrate specificities of fatty acyl desaturases (FADs), enzymes presumably acting upstream of FARs in pheromone biosynthesis (Tillman et al., 1999), are conserved across species despite differences in the compositions of their unsaturated FA-derived pheromone components (Buček et al., 2013). These findings suggest that the substrate specificity of FADs contributes only partially to the species-specific composition of FA-derived MMPs (Buček et al., 2013). The fatty alcohol content in bumble bee MMPs is therefore presumably co-determined by the enzymatic specificity of other pheromone biosynthetic steps, such as FA biosynthesis/transport or FA reduction. Analysis of the B. terrestris male labial gland (LG) transcriptome uncovered a remarkably high number of putative FAR paralogs, including apparently expressed pseudogenes, strongly indicating dynamic evolution of the FAR gene family and the contribution of FARs to the LG-localized MMP biosynthesis (Buček et al., 2016).

Here, we aimed to determine how the members of the large FAR gene family in the bumble bee lineage contribute to MMP biosynthesis. We sequenced B. lapidarius male LG and fat body (FB) transcriptomes and functionally characterized the FAR enzymes, along with FAR candidates from B. terrestris and B. lucorum, in a yeast expression system. We combined experimental information about FAR enzymatic specificities with quantitative information about bumble bee FAR expression patterns, as well as comprehensive gas chromatography (GC) analysis of MMPs and their FA precursors in the bumble bee male LG, with inference of the hymenopteran FAR gene tree. In addition, we investigated the content of transposable elements (TEs) in the genomic environment of FAR genes in genomes of two bumble bee species, B. terrestris and B. impatiens. We conclude that a dramatic TE-mediated expansion of the FAR gene family started in the common ancestor of the bumble bee (Bombini: Bombus) and stingless bee (Meliponini) lineages, which presumably shaped the pheromone communication in these lineages.

Since the first genome-scale surveys of gene families, gene duplications and lineage-specific gene family expansions have been considered major mechanisms of diversification and adaptation in eukaryotes (Lespinet et al., 2002) and prokaryotes (Jordan et al., 2001). Tracing the evolution of gene families and correlating them with the evolution of phenotypic traits has been facilitated by the growing number of next-generation genomes and transcriptomes from organisms spanning the entire tree of life. However, obtaining experimental evidence of the function of numerous gene family members across multiple species or lineages is laborious. Thus, such data are scarce, and researchers have mostly relied on computational inference of gene function (Radivojac et al., 2013). Here, we aimed to combine computational inference with experimental characterization of gene function to understand the evolution of the FAR family, for which we predicted a substantial gene number expansion in our initial transcriptome analysis of the buff-tailed bumble bee B. terrestris (Buček et al., 2016). We specifically sought to determine whether the FARs that emerged through expansion of the FAR gene family substantially contribute to MMP biosynthesis in bumble bees.

We found that the FAR-A group underwent massive expansion in all analyzed species of bumble bee and stingless bee lineages but not in any other Hymenoptera species, with the exceptions of the ant Camponotus floridanus and the mining bee Andrena vaga (Figure 1, Figure 2). The phylogenetic sister group relationship of bumble bees and stingless bees (Peters et al., 2017; Branstetter et al., 2017) indicates that the FAR duplication process occurred or started in their ancestor, while the increased number of predicted FAR-A genes in A. vaga and C. floridanus suggests that the FAR-A genes independently underwent duplication in other hymenopteran lineages. According to estimated lineage divergence times, FAR duplication events in bumble bees and stingless bees started after their divergence from Apis 54 million years ago (40–69 million years 95% confidence interval) (Peters et al., 2017). The number of inferred FAR-A orthologs is inflated by predicted pseudogenes—FARs with fragmented coding sequences that lack some of the catalytically essential domains and motifs (Figure 1—figure supplement 2). These predicted catalytically inactive yet highly expressed FAR-A pseudogenes might play a role in regulating the FAR-catalyzed reduction (Pils and Schultz, 2004). The number of predicted FAR-A pseudogenes indicate that the FAR-A ortholog group expansion in this lineage was a highly dynamic process (Figure 1, Figure 1—figure supplement 2). The high number of species-specific FAR-A duplications or losses between the closely related species B. lucorum and B. terrestris, which diverged approximately 5 million years ago (Hines, 2008), further indicates the dynamic evolutionary processes acting on the FAR genes. Notably, gene family expansion inference based on mixed transcriptome and genome data is limited by (1) the uncertainty of distinguishing genuine genes from alternative splice variants and non-overlapping transcript fragments and (2) potential errors in genome assemblies or annotations. The pattern of lineage-specific FAR-A gene expansion in stingless bees and bumble bees is, to the best of our knowledge, corroborated by all genomic and transcriptomic datasets currently available for this group. Confirming many of the other potential lineage-specific FAR gene expansions in Hymenoptera will, however, require analysis of additional genomic resources.

Strikingly, both stingless bees and bumble bees share a life strategy of scent marking using LG secretion (Jarau et al., 2004). In worker stingless bees, LG secretion is used as a trail pheromone to recruit nestmates to food resources and generally contains fatty alcohols such as hexanol, octanol, and decanol in the form of their fatty acyl esters (Jarau et al., 2006; Jarau et al., 2010). The correlation between FAR-A ortholog group expansion and use of LG-produced fatty alcohols as marking pheromones or their precursors suggests a critical role for FAR-A gene group expansion in the evolution of scent marking. In the future, identification and characterization of FAR candidates involved in production of stingless bee worker LG-secretion could corroborate this hypothesis.

Bumble bee orthologs (FAR-G) of B. mori pheromone-biosynthetic FAR (Moto et al., 2003) are not abundantly or specifically expressed in male bumble bee LGs, as evidenced by RNA-Seq RPKM values (Figure 1—figure supplement 1). MMP-biosynthetic FARs in bumble bees and female sex pheromone-biosynthetic FARs in moths (Lepidoptera) were therefore most likely recruited independently for the tasks of pheromone biosynthesis.

Various models have attempted to describe the evolutionary mechanisms leading to the emergence and maintenance of gene duplicates (Innan and Kondrashov, 2010). The fragmented state of the B. terrestris genome and its limited synteny with the A. mellifera genome restricts our ability to reconstruct the genetic events accompanying the FAR duplications resulting in the FAR-A ortholog group expansion. Notably, the MMP quantities in bumble bees are substantially higher than quantities of pheromones in other insects of comparable size. For example, B. terrestris, B. lucorum and B. lapidarius bumble bee males can produce several milligrams of MMPs (Kindl, personal communication, Figure 5), while the sphingid moth Manduca sexta produces tens of nanograms of sex pheromone (Tumlinson et al., 1989). Taking into consideration the large quantities of MMPs in bumble bee males, we speculate that gene dosage benefits could substantially contribute to the duplications and duplicate fixation of MMP-biosynthetic FARs. Under this model, sexual selection favoring bumble bee males capable of producing large quantities of MMPs could fix the duplicated FARs in a population (Lespinet et al., 2002; Innan and Kondrashov, 2010).

Mechanistically, gene duplications can be facilitated by associated TEs (Reams and Roth, 2015; Schrader and Schmitz, 2018). The content of repetitive DNA in the B. terrestris and B. impatiens genome assemblies is 14.8% and 17.9%, respectively (Sadd et al., 2015), which is lower than in other insects such as the beetle Tribolium castaneum (30%), Drosophila (more than 20%) or the parasitoid wasp Nasonia vitripenis (more than 30%), but substantially higher than in the honey bee Apis mellifera (9.5%) (Elsik et al., 2014; Weinstock and Honeybee Genome Sequencing Consortium, 2006). Our finding that TEs are enriched in the vicinity of FAR-A genes in the B. terrestris and B. impatiens genomes indicates that TEs presumably contributed to the massive expansion of the FAR-A ortholog group (Figure 3). Expansions of another pheromone biosynthetic gene family, FADs, in the fly Drosophila and in corn borer moths (Ostrinia) also have been found to be mediated by TEs. It was proposed that up to seven FAD loci in these species originated by repeated retrotransposition or DNA-mediated transposition (Fang et al., 2009; Xue et al., 2007).

One notable feature of FAR-A expansion in bumble bees and stingless bees is the extent of gene expansion, often generating 10 or more predicted FAR genes (Figure 2). One scenario for FAR-A expansion is that TEs provided substrates for non-homologous recombination that led to the initial duplication (Reams and Roth, 2015; Bourque, 2009). Redundant copies of the ancestral FAR-A gene that arose as a result of the duplication were not under strong purifying selection and might have tolerated accumulation of TEs in their vicinity. The higher abundance of TEs subsequently made the region vulnerable to structural rearrangements, which facilitated expansion of the FAR-A genes. Janoušek et al. presented a model in which TEs facilitate gene family expansions in mammalian genomes (Janoušek et al., 2013; Janoušek et al., 2016). Their model describes gradual accumulation of TEs along with expansions of gene families, which under some model parameters can lead to a runaway process characterized by rapid and accelerating gene family expansion (Janoušek et al., 2016). In bumble bees, this runaway process could have been facilitated by fixation of duplicated FAR-A genes due to sexual selection for increased FAR expression. However, alternative scenarios are possible. For example, initial duplication of the FAR-A ancestral gene might have been unrelated to TEs, and TEs may have accumulated after the initial duplication. Alternatively, translocation of the FAR-A ancestral copy to a TE-rich region in the common ancestor of bumble bees and stingless bees might have facilitated expansion of this ortholog group. Further research is needed to confirm which of these scenarios is most likely.

The spectrum of fatty alcohols in B. terrestris and B. lucorum male LG differs substantially from that of B. lapidarius. In both B. terrestris and B. lucorum, the male LG extract contains a rich blend of C14–C26 fatty alcohols with zero to three double bonds (Figure 5). In B. lapidarius, the male LG extract is less diverse and dominated by Z9-16:OH and 16:OH (Figure 5, Figure 5—source data 1). To uncover how the distinct repertoire of FAR orthologs contributes to the biosynthesis of species-specific MMPs, we functionally characterized LG-expressed FARs. We previously found that the transcript levels of biosynthetic genes generally reflect the biosynthetic pathways most active in bumble bee LG (Buček et al., 2016; Buček et al., 2013). For further experimental characterization, we therefore selected the FAR-A and FAR-J gene candidates, which exhibited high and preferential expression in male LG (Figure 1—figure supplement 1). Notably, the abundant expression of BlapFAR-A1 and BterFAR-J in both virgin queen and male LG (Figure 4—figure supplement 1) suggests that these FARs might also have been recruited for production of queen-specific signals (Amsalem et al., 2014). We found that the highly similar BlucFAR-A1/BterFAR-A1 and BlapFAR-A1 orthologs exhibit distinct substrate preferences for longer fatty acyl chains (C18–C26) and shorter monounsaturated fatty acyl chains (Z9-16: and Z9-18:), respectively. This substrate preference correlates with the abundance of Z9-16:OH in B. lapidarius MMP and the almost complete absence of Z9-16:OH in B. lucorum and B. terrestris (Figure 5—source data 1). BlapFAR-A4 and to some extent BlapFAR-A5 likely further contribute to the biosynthesis of Z9-16:OH in B. lapidarius. The ability of BlucFAR-A1 and BterFAR-A1 (and not of BlapFAR-A1) to reduce long monounsaturated fatty acyls (Z15-20:) also correlates with the absence of detectable amounts of Z15-20:OH in B. lapidarius MMP.

Our comprehensive GC analysis of bumble bee male LGs, however, indicates that the composition of LG fatty acyls is another factor that contributes substantially to the final MMP composition. For example, the very low quantities of Z9-16:OH in B. terrestris and B. lucorum and of Z15-20:OH in B. lapidarius (Figure 5) can be ascribed to the absence of a FAR with the corresponding substrate specificity, but the availability of potential substrates, that is very low amount of Z9-16: acyl in B. lucorum and B. terrestris male LG and the absence of detectable Z15-20: acyl in B. lapidarius LG also likely contribute.

We detected several fatty alcohols in FBs of B. terrestris and B. lucorum, 16:OH, Z9,Z12-18:OH and Z9,Z12,Z15-18:OH being the most abundant (Figure 5—source data 1, Figure 5—figure supplement 1). Fatty alcohols are not expected to be transported from FB across haemolymph to LG (Buček et al., 2016). However, the presence of Z9,Z12-18: and Z9,Z12,Z15-18: fatty alcohols in FB provides an explanation for why we did not find a FAR reducing Z9,Z12-18: and Z9,Z12,Z15-18: among the functionally characterized candidates from B. terrestris and B. lucorum. Our candidate selection criteria were based on the LG-specific FAR transcript abundance, and we might have disregarded a FAR that is capable of polyunsaturated fatty acyl reduction and is expressed at comparable levels in both LG and FB.

We noted several discrepancies between the FAR specificity in the yeast expression system and the apparent FAR specificity in vivo (i.e. the apparent specificity of fatty acyl reduction in bumble bee LG calculated from the fatty acyl and fatty alcohol content, Figure 5—figure supplement 1). We found that BlapFAR-A1 is capable of producing substantial amounts of Z9-16:OH and Z9-18:OH (Figure 6—figure supplement 8A) in the yeast system, while in B. lapidarius LG, only Z9-16: acyl is converted to Z9-16:OH, as evidenced by the absence of detectable amounts of Z9-18:OH (Figure 5). Additionally, BlapFAR-A1 and BlapFAR-A4 produce in the yeast expression system polyunsaturated fatty alcohols (Figure 6) that are not present in B. lapidarius male LG, despite the presence of corresponding fatty acyls in the LG (Figure 5). A possible explanation for the differences between FAR specificities in the bumble bee LG and the yeast expression system is that the pool of LG fatty acyls that we assessed and used to evaluate the apparent FAR specificities has a different composition than the LG pool of fatty acyl-CoAs, which are the form of fatty acyls accepted by FARs as substrates. The presumably low concentrations of Z9,Z12-18:CoA, Z9,Z12,Z15-18:CoA, and Z9-18:CoA in the LG of male B. lapidarius compared to the concentrations of the respective fatty acyls could prevent detectable accumulation of the corresponding fatty alcohols. We therefore propose that the selectivity of enzymes and binding proteins that convert fatty acyls to fatty acyl-CoAs (Oba et al., 2004) and protect fatty acyl-CoAs from hydrolysis (Matsumoto et al., 2001) represents an additional mechanism shaping the species-specific fatty alcohol composition in bumble bee male LGs.

In sum, the functional characterization of bumble bee FARs indicates that the combined action of FARs from the expanded FAR-A ortholog group has the capability to biosynthesize the majority of bumble bee MMP fatty alcohols. The substrate specificity of FARs apparently contributes to the species-specific MMP composition, but other biosynthetic steps, namely the process of fatty acyl and fatty acyl-CoA accumulation, likely also contribute to the final fatty alcohol composition of bumble bee MMPs.

Complete short read (Illumina HiSeq2500) data from B. lucorum and B. lapidarius were deposited in the Sequence Read Archive (https://www.ncbi.nlm.nih.gov/sra) with BioSample accession numbers SAMN08625119, SAMN08625120, SAMN08625121, and SAMN08625122 under BioProject ID PRJNA436452.

1. 1. Tupec M
   2. Buček A

   (2018) BioProject

   ID PRJNA436452. Complete short read (Illumina HiSeq2500) data from B. lucorum and B. lapidarius.

   https://www.ncbi.nlm.nih.gov/bioproject/PRJNA436452

1. 1. Peters RS
   2. Krogmann L
   3. Mayer C
   4. Donath A
   5. Gunkel S
   6. Meusemann K
   7. Kozlov A
   8. Podsiadlowski L
   9. Petersen M
   10. Lanfear R
   11. Diez PA
   12. Heraty J
   13. Kjer KM
   14. Klopfstein S
   15. Meier R
   16. Polidori C
   17. Schmitt T
   18. Liu S
   19. Zhou X
   20. Wappler T
   21. Rust J
   22. Misof B
   23. Niehuis O

   (2017) BioProject

   ID PRJNA252240. Tetragonula carbonaria transcriptomes.

   https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA252240
2. 1. Sadd BM
   2. Barribeau SM
   3. Bloch G
   4. de Graaf DC
   5. Dearden P
   6. Elsik CG
   7. Gadau J
   8. Grimmelikhuijzen CJ
   9. Hasselmann M
   10. Lozier JD
   11. Robertson HM
   12. Smagghe G
   13. Stolle E
   14. Van Vaerenbergh M
   15. Waterhouse RM
   16. Bornberg-Bauer E
   17. Klasberg S
   18. Bennett AK
   19. Câmara F
   20. Guigó R
   21. Hoff K
   22. Mariotti M
   23. Munoz-Torres M
   24. Murphy T
   25. Santesmasses D
   26. Amdam GV
   27. Beckers M
   28. Beye M
   29. Biewer M
   30. Bitondi MM
   31. Blaxter ML
   32. Bourke AF
   33. Brown MJ
   34. Buechel SD
   35. Cameron R
   36. Cappelle K
   37. Carolan JC
   38. Christiaens O
   39. Ciborowski KL
   40. Clarke DF
   41. Colgan TJ
   42. Collins DH
   43. Cridge AG
   44. Dalmay T
   45. Dreier S
   46. du Plessis L
   47. Duncan E
   48. Erler S
   49. Evans J
   50. Falcon T
   51. Flores K
   52. Freitas FC
   53. Fuchikawa T
   54. Gempe T
   55. Hartfelder K
   56. Hauser F

   (2015) BioProject

   ID PRJNA45869. Bombus terrestris genome.

   https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA45869
3. 1. Honeybee Genome Sequencing Consortium

   (2006) BioProject

   ID PRJNA13343. Apis mellifera genome.

   https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA13343
4. 1. Honeybee Genome Sequencing Consortium

   (2010) BioProject

   ID PRJNA274144. Camponotus floridanus genome.

   https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA274144
5. 1. Nygaard S
   2. Zhang G
   3. Schiøtt M
   4. Li C
   5. Wurm Y
   6. Hu H
   7. Zhou J
   8. Ji L
   9. Qiu F
   10. Rasmussen M
   11. Pan H
   12. Hauser F
   13. Krogh A
   14. Grimmelikhuijzen CJ
   15. Wang J
   16. Boomsma JJ

   (2011) BioProject

   ID PRJNA271903. Acromyrmex echinatior genome.

   https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA271903
6. 1. Werren JH
   2. Richards S
   3. Desjardins CA
   4. Niehuis O
   5. Gadau J
   6. Colbourne JK; Nasonia Genome Working Group
   7. Werren JH
   8. Colbourne JK

   (2011) BioProject

   ID PRJNA20073. Nasonia vitripennis genome.

   https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA20073
7. 1. Patalano S
   2. Vlasova A
   3. Wyatt C
   4. Ewels P
   5. Camara F
   6. Ferreira PG
   7. Asher CL
   8. Jurkowski TP
   9. Segonds-Pichon A
   10. Bachman M
   11. González-Navarrete I
   12. Minoche AE
   13. Krueger F
   14. Lowy E
   15. Marcet-Houben M
   16. Rodriguez-Ales JL
   17. Nascimento FS
   18. Balasubramanian S
   19. Gabaldon T
   20. Tarver JE
   21. Andrews S
   22. Himmelbauer H
   23. Hughes WO
   24. Guigó R
   25. Reik W
   26. Sumner S

   (2015) BioProject

   ID PRJNA301748. Polistes canadensis genome.

   https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA301748
8. 1. Woodard SH
   2. Fischman BJ
   3. Venkat A
   4. Hudson ME
   5. Varala K
   6. Cameron SA
   7. Clark AG
   8. Robinson GE

   (2011) BioProject

   ID PRJNA62691. Melipona quadrifasciatatranscriptome.

   https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA62691
9. 1. Peters RS
   2. Krogmann L
   3. Mayer C
   4. Donath A
   5. Gunkel S
   6. Meusemann K
   7. Kozlov A
   8. Podsiadlowski L
   9. Petersen M
   10. Lanfear R
   11. Diez PA
   12. Heraty J
   13. Kjer KM
   14. Klopfstein S
   15. Meier R
   16. Polidori C
   17. Schmitt T
   18. Liu S
   19. Zhou X
   20. Wappler T
   21. Rust J
   22. Misof B
   23. Niehuis O

   (2017) BioProject

   ID PRJNA252285. Bombus rupestris transcriptomes.

   https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA252285
10. 1. Sadd BM
    2. Barribeau SM
    3. Bloch G
    4. de Graaf DC
    5. Dearden P
    6. Elsik CG
    7. Gadau J
    8. Grimmelikhuijzen CJ
    9. Hasselmann M
    10. Lozier JD
    11. Robertson HM
    12. Smagghe G
    13. Stolle E
    14. Van Vaerenbergh M
    15. Waterhouse RM
    16. Bornberg-Bauer E
    17. Klasberg S
    18. Bennett AK
    19. Câmara F
    20. Guigó R
    21. Hoff K
    22. Mariotti M
    23. Munoz-Torres M
    24. Murphy T
    25. Santesmasses D
    26. Amdam GV
    27. Beckers M
    28. Beye M
    29. Biewer M
    30. Bitondi MM
    31. Blaxter ML
    32. Bourke AF
    33. Brown MJ
    34. Buechel SD
    35. Cameron R
    36. Cappelle K
    37. Carolan JC
    38. Christiaens O
    39. Ciborowski KL
    40. Clarke DF

    (2015) BioProject

    ID PRJNA61101. Bombus impatiens genome.

    https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA61101
11. 1. Bonasio R
    2. Zhang G
    3. Ye C
    4. Mutti NS
    5. Fang X
    6. Qin N
    7. Donahue G
    8. Yang P
    9. Li Q
    10. Li C
    11. Zhang P
    12. Huang Z
    13. Berger SL
    14. Reinberg D
    15. Wang J
    16. Liebig J

    (2010) BioProject

    ID PRJNA273397. Harpegnathos saltator genomes.

    https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA273397
12. 1. Woodard SH
    2. Fischman BJ
    3. Venkat A
    4. Hudson ME
    5. Varala K
    6. Cameron SA
    7. Clark AG
    8. Robinson GE

    (2011) BioProject

    ID PRJNA87021. Megachile rotundata transcriptome.

    https://www.ncbi.nlm.nih.gov/bioproject/?term=PRJNA87021

1. 1. Altschul SF
   2. Gish W
   3. Miller W
   4. Myers EW
   5. Lipman DJ

   (1990) Basic local alignment search tool

   Journal of Molecular Biology 215:403–410.

   https://doi.org/10.1016/S0022-2836(05)80360-2

   • PubMed
   • Google Scholar
2. 1. Amsalem E
   2. Kiefer J
   3. Schulz S
   4. Hefetz A

   (2014) The effect of caste and reproductive state on the chemistry of the cephalic labial glands secretion of bombus terrestris

   Journal of Chemical Ecology 40:900–912.

   https://doi.org/10.1007/s10886-014-0484-3

   • PubMed
   • Google Scholar
3. 1. Anders S
   2. Pyl PT
   3. Huber W

   (2015) HTSeq--a Python framework to work with high-throughput sequencing data

   Bioinformatics 31:166–169.

   https://doi.org/10.1093/bioinformatics/btu638

   • PubMed
   • Google Scholar
4. 1. Angov E

   (2011) Codon usage: nature's roadmap to expression and folding of proteins

   Biotechnology Journal 6:650–659.

   https://doi.org/10.1002/biot.201000332

   • PubMed
   • Google Scholar
5. 1. Antony B
   2. Fujii T
   3. Moto K
   4. Matsumoto S
   5. Fukuzawa M
   6. Nakano R
   7. Tatsuki S
   8. Ishikawa Y

   (2009) Pheromone-gland-specific fatty-acyl reductase in the adzuki bean borer, ostrinia scapulalis (Lepidoptera: Crambidae)

   Insect Biochemistry and Molecular Biology 39:90–95.

   https://doi.org/10.1016/j.ibmb.2008.10.008

   • PubMed
   • Google Scholar
6. 1. Ayasse M
   2. Jarau S

   (2014) Chemical ecology of bumble bees

   Annual Review of Entomology 59:299–319.

   https://doi.org/10.1146/annurev-ento-011613-161949

   • Google Scholar
7. 1. Bergström G
   2. Kullberg BJ
   3. Ställberg-Stenhagen S

   (1973)

   Studies on natural odoriferous compounds: vii. recognition of two forms of Bombus lucorum L. (Hymenoptera, Apidae) by analysis of the volatile marking secretion from individual males

   Zoon 1:31–42.

   • Google Scholar
8. 1. Bonasio R
   2. Zhang G
   3. Ye C
   4. Mutti NS
   5. Fang X
   6. Qin N
   7. Donahue G
   8. Yang P
   9. Li Q
   10. Li C
   11. Zhang P
   12. Huang Z
   13. Berger SL
   14. Reinberg D
   15. Wang J
   16. Liebig J

   (2010) Genomic comparison of the ants camponotus floridanus and harpegnathos saltator

   Science 329:1068–1071.

   https://doi.org/10.1126/science.1192428

   • PubMed
   • Google Scholar
9. 1. Bourque G

   (2009) Transposable elements in gene regulation and in the evolution of vertebrate genomes

   Current Opinion in Genetics & Development 19:607–612.

   https://doi.org/10.1016/j.gde.2009.10.013

   • PubMed
   • Google Scholar
10. 1. Brachmann CB
    2. Davies A
    3. Cost GJ
    4. Caputo E
    5. Li J
    6. Hieter P
    7. Boeke JD

    (1998) Designer deletion strains derived from saccharomyces cerevisiae S288C: a useful set of strains and plasmids for PCR-mediated gene disruption and other applications

    Yeast 14:115–132.

    https://doi.org/10.1002/(SICI)1097-0061(19980130)14:2<115::AID-YEA204>3.0.CO;2-2

    • PubMed
    • Google Scholar
11. 1. Branstetter MG
    2. Danforth BN
    3. Pitts JP
    4. Faircloth BC
    5. Ward PS
    6. Buffington ML
    7. Gates MW
    8. Kula RR
    9. Brady SG

    (2017) Phylogenomic insights into the evolution of stinging wasps and the origins of ants and bees

    Current Biology 27:1019–1025.

    https://doi.org/10.1016/j.cub.2017.03.027

    • PubMed
    • Google Scholar
12. 1. Buček A
    2. Vogel H
    3. Matoušková P
    4. Prchalová D
    5. Záček P
    6. Vrkoslav V
    7. Šebesta P
    8. Svatoš A
    9. Jahn U
    10. Valterová I
    11. Pichová I

    (2013) The role of desaturases in the biosynthesis of marking pheromones in bumblebee males

    Insect Biochemistry and Molecular Biology 43:724–731.

    https://doi.org/10.1016/j.ibmb.2013.05.003

    • PubMed
    • Google Scholar
13. 1. Buček A
    2. Brabcová J
    3. Vogel H
    4. Prchalová D
    5. Kindl J
    6. Valterová I
    7. Pichová I

    (2016) Exploring complex pheromone biosynthetic processes in the bumblebee male labial gland by RNA sequencing

    Insect Molecular Biology 25:295–314.

    https://doi.org/10.1111/imb.12221

    • PubMed
    • Google Scholar
14. 1. Carlson DA
    2. Roan CS
    3. Yost RA
    4. Hector J

    (1989) Dimethyl disulfide derivatives of long chain alkenes, alkadienes, and alkatrienes for gas chromatography/mass spectrometry

    Analytical Chemistry 61:1564–1571.

    https://doi.org/10.1021/ac00189a019

    • Google Scholar
15. 1. Cheng JB
    2. Russell DW

    (2004) Mammalian wax biosynthesis. I. identification of two fatty acyl-Coenzyme A reductases with different substrate specificities and tissue distributions

    The Journal of Biological Chemistry 279:37789–37797.

    https://doi.org/10.1074/jbc.M406225200

    • PubMed
    • Google Scholar
16. Software

    1. Core Team R

    (2016)

    R: A Language and Environment for Statistical Computing

    GBIF.
17. 1. Cortesi F
    2. Musilová Z
    3. Stieb SM
    4. Hart NS
    5. Siebeck UE
    6. Malmstrøm M
    7. Tørresen OK
    8. Jentoft S
    9. Cheney KL
    10. Marshall NJ
    11. Carleton KL
    12. Salzburger W

    (2015) Ancestral duplications and highly dynamic opsin gene evolution in percomorph fishes

    PNAS 112:1493–1498.

    https://doi.org/10.1073/pnas.1417803112

    • PubMed
    • Google Scholar
18. 1. Darling AC
    2. Mau B
    3. Blattner FR
    4. Perna NT

    (2004) Mauve: multiple alignment of conserved genomic sequence with rearrangements

    Genome Research 14:1394–1403.

    https://doi.org/10.1101/gr.2289704

    • PubMed
    • Google Scholar
19. 1. Demuth JP
    2. De Bie T
    3. Stajich JE
    4. Cristianini N
    5. Hahn MW

    (2006) The evolution of mammalian gene families

    PLOS ONE 1:e85.

    https://doi.org/10.1371/journal.pone.0000085

    • PubMed
    • Google Scholar
20. 1. Eirín-López JM
    2. Rebordinos L
    3. Rooney AP
    4. Rozas J

    (2012) The birth-and-death evolution of multigene families revisited

    Genome Dynamics 7:170–196.

    https://doi.org/10.1159/000337119

    • PubMed
    • Google Scholar
21. 1. Elsik CG
    2. Worley KC
    3. Bennett AK
    4. Beye M
    5. Camara F
    6. Childers CP
    7. de Graaf DC
    8. Debyser G
    9. Deng J
    10. Devreese B
    11. Elhaik E
    12. Evans JD
    13. Foster LJ
    14. Graur D
    15. Guigo R
    16. Hoff KJ
    17. Holder ME
    18. Hudson ME
    19. Hunt GJ
    20. Jiang H
    21. Joshi V
    22. Khetani RS
    23. Kosarev P
    24. Kovar CL
    25. Ma J
    26. Maleszka R
    27. Moritz RF
    28. Munoz-Torres MC
    29. Murphy TD
    30. Muzny DM
    31. Newsham IF
    32. Reese JT
    33. Robertson HM
    34. Robinson GE
    35. Rueppell O
    36. Solovyev V
    37. Stanke M
    38. Stolle E
    39. Tsuruda JM
    40. Vaerenbergh MV
    41. Waterhouse RM
    42. Weaver DB
    43. Whitfield CW
    44. Wu Y
    45. Zdobnov EM
    46. Zhang L
    47. Zhu D
    48. Gibbs RA
    49. HGSC production teams
    50. Honey Bee Genome Sequencing Consortium

    (2014) Finding the missing honey bee genes: lessons learned from a genome upgrade

    BMC Genomics 15:86.

    https://doi.org/10.1186/1471-2164-15-86

    • PubMed
    • Google Scholar
22. 1. Fang S
    2. Ting CT
    3. Lee CR
    4. Chu KH
    5. Wang CC
    6. Tsaur SC

    (2009) Molecular evolution and functional diversification of fatty acid desaturases after recurrent gene duplication in Drosophila

    Molecular Biology and Evolution 26:1447–1456.

    https://doi.org/10.1093/molbev/msp057

    • PubMed
    • Google Scholar
23. Book

    1. Goulson D

    (2010)

    Bumblebees - Behaviour, Ecology and Conservation

    Oxford: Oxford University Press.

    • Google Scholar
24. 1. Hines HM

    (2008) Historical biogeography, divergence times, and diversification patterns of bumble bees (Hymenoptera: apidae: bombus)

    Systematic Biology 57:58–75.

    https://doi.org/10.1080/10635150801898912

    • PubMed
    • Google Scholar
25. 1. Holz C
    2. Hesse O
    3. Bolotina N
    4. Stahl U
    5. Lang C

    (2002) A micro-scale process for high-throughput expression of cDNAs in the yeast saccharomyces cerevisiae

    Protein Expression and Purification 25:372–378.

    https://doi.org/10.1016/S1046-5928(02)00029-3

    • PubMed
    • Google Scholar
26. 1. Hornáková D
    2. Matousková P
    3. Kindl J
    4. Valterová I
    5. Pichová I

    (2010) Selection of reference genes for real-time polymerase chain reaction analysis in tissues from bombus terrestris and Bombus lucorum of different ages

    Analytical Biochemistry 397:118–120.

    https://doi.org/10.1016/j.ab.2009.09.019

    • PubMed
    • Google Scholar
27. 1. Hu Y-H
    2. Chen X-M
    3. Yang P
    4. Ding W-F

    (2018) Characterization and functional assay of a fatty acyl-CoA reductase gene in the scale insect, ericerus pela chavannes (Hemiptera: coccoidae)

    Archives of Insect Biochemistry and Physiology 97:e21445.

    https://doi.org/10.1002/arch.21445

    • Google Scholar
28. 1. Innan H
    2. Kondrashov F

    (2010) The evolution of gene duplications: classifying and distinguishing between models

    Nature Reviews Genetics 11:97–108.

    https://doi.org/10.1038/nrg2689

    • PubMed
    • Google Scholar
29. 1. Janoušek V
    2. Karn RC
    3. Laukaitis CM

    (2013) The role of retrotransposons in gene family expansions: insights from the mouse abp gene family

    BMC Evolutionary Biology 13:107.

    https://doi.org/10.1186/1471-2148-13-107

    • PubMed
    • Google Scholar
30. 1. Janoušek V
    2. Laukaitis CM
    3. Yanchukov A
    4. Karn RC

    (2016) The role of retrotransposons in gene family expansions in the human and mouse genomes

    Genome Biology and Evolution 8:2632–2650.

    https://doi.org/10.1093/gbe/evw192

    • PubMed
    • Google Scholar
31. 1. Jarau S
    2. Hrncir M
    3. Zucchi R
    4. Barth FG

    (2004) A stingless bee uses labial gland secretions for scent trail communication ( Trigona recursa smith 1863)

    Journal of Comparative Physiology A: Sensory, Neural, and Behavioral Physiology 190:233–239.

    https://doi.org/10.1007/s00359-003-0489-9

    • Google Scholar
32. 1. Jarau S
    2. Schulz CM
    3. Hrncir M
    4. Francke W
    5. Zucchi R
    6. Barth FG
    7. Ayasse M

    (2006) Hexyl decanoate, the first trail pheromone compound identified in a stingless bee, trigona recursa

    Journal of Chemical Ecology 32:1555–1564.

    https://doi.org/10.1007/s10886-006-9069-0

    • PubMed
    • Google Scholar
33. 1. Jarau S
    2. Dambacher J
    3. Twele R
    4. Aguilar I
    5. Francke W
    6. Ayasse M

    (2010) The trail pheromone of a stingless bee, trigona corvina (Hymenoptera, apidae, meliponini), varies between populations

    Chemical Senses 35:593–601.

    https://doi.org/10.1093/chemse/bjq057

    • PubMed
    • Google Scholar
34. 1. Jaspers MH
    2. Pflanz R
    3. Riedel D
    4. Kawelke S
    5. Feussner I
    6. Schuh R

    (2014) The fatty acyl-CoA reductase waterproof mediates airway clearance in Drosophila

    Developmental Biology 385:23–31.

    https://doi.org/10.1016/j.ydbio.2013.10.022

    • PubMed
    • Google Scholar
35. 1. Jordan IK
    2. Makarova KS
    3. Spouge JL
    4. Wolf YI
    5. Koonin EV

    (2001) Lineage-specific gene expansions in bacterial and archaeal genomes

    Genome Research 11:555–565.

    https://doi.org/10.1101/gr.GR-1660R

    • PubMed
    • Google Scholar
36. 1. Kalyaanamoorthy S
    2. Minh BQ
    3. Wong TKF
    4. von Haeseler A
    5. Jermiin LS

    (2017) ModelFinder: fast model selection for accurate phylogenetic estimates

    Nature Methods 14:587–589.

    https://doi.org/10.1038/nmeth.4285

    • PubMed
    • Google Scholar
37. 1. Kapheim KM
    2. Pan H
    3. Li C
    4. Salzberg SL
    5. Puiu D
    6. Magoc T
    7. Robertson HM
    8. Hudson ME
    9. Venkat A
    10. Fischman BJ
    11. Hernandez A
    12. Yandell M
    13. Ence D
    14. Holt C
    15. Yocum GD
    16. Kemp WP
    17. Bosch J
    18. Waterhouse RM
    19. Zdobnov EM
    20. Stolle E
    21. Kraus FB
    22. Helbing S
    23. Moritz RF
    24. Glastad KM
    25. Hunt BG
    26. Goodisman MA
    27. Hauser F
    28. Grimmelikhuijzen CJ
    29. Pinheiro DG
    30. Nunes FM
    31. Soares MP
    32. Tanaka ÉD
    33. Simões ZL
    34. Hartfelder K
    35. Evans JD
    36. Barribeau SM
    37. Johnson RM
    38. Massey JH
    39. Southey BR
    40. Hasselmann M
    41. Hamacher D
    42. Biewer M
    43. Kent CF
    44. Zayed A
    45. Blatti C
    46. Sinha S
    47. Johnston JS
    48. Hanrahan SJ
    49. Kocher SD
    50. Wang J
    51. Robinson GE
    52. Zhang G

    (2015) Genomic signatures of evolutionary transitions from solitary to group living

    Science 348:1139–1143.

    https://doi.org/10.1126/science.aaa4788

    • PubMed
    • Google Scholar
38. 1. Koonin EV

    (2005) Orthologs, paralogs, and evolutionary genomics

    Annual Review of Genetics 39:309–338.

    https://doi.org/10.1146/annurev.genet.39.073003.114725

    • PubMed
    • Google Scholar
39. 1. Kullenberg B
    2. Bergström G
    3. Ställberg-Stenhagen S

    (1970) Volatile components of the cephalic marking secretion of male bumble bees

    Acta Chemica Scandinavica 24:1481–1483.

    https://doi.org/10.3891/acta.chem.scand.24-1481

    • PubMed
    • Google Scholar
40. 1. Kullenberg B
    2. Bergstrom G
    3. Bringer B
    4. Carlberg B
    5. Cederberg B

    (1973)

    Observations on scent marking by bombus Latr. and Psithyrus Lep. males (Hym. Apidae) and localization of site of production of the secretion

    Zoon 1:23–30.

    • Google Scholar
41. 1. Langmead B
    2. Salzberg SL

    (2012) Fast gapped-read alignment with bowtie 2

    Nature Methods 9:357–359.

    https://doi.org/10.1038/nmeth.1923

    • PubMed
    • Google Scholar
42. 1. Lassance JM
    2. Groot AT
    3. Liénard MA
    4. Antony B
    5. Borgwardt C
    6. Andersson F
    7. Hedenström E
    8. Heckel DG
    9. Löfstedt C

    (2010) Allelic variation in a fatty-acyl reductase gene causes divergence in moth sex pheromones

    Nature 466:486–489.

    https://doi.org/10.1038/nature09058

    • PubMed
    • Google Scholar
43. 1. Lassance JM
    2. Liénard MA
    3. Antony B
    4. Qian S
    5. Fujii T
    6. Tabata J
    7. Ishikawa Y
    8. Löfstedt C

    (2013) Functional consequences of sequence variation in the pheromone biosynthetic gene pgFAR for ostrinia moths

    PNAS 110:3967–3972.

    https://doi.org/10.1073/pnas.1208706110

    • PubMed
    • Google Scholar
44. 1. Lespinet O
    2. Wolf YI
    3. Koonin EV
    4. Aravind L

    (2002) The role of lineage-specific gene family expansion in the evolution of eukaryotes

    Genome Research 12:1048–1059.

    https://doi.org/10.1101/gr.174302

    • PubMed
    • Google Scholar
45. 1. Liénard MA
    2. Hagström AK
    3. Lassance JM
    4. Löfstedt C

    (2010) Evolution of multicomponent pheromone signals in small ermine moths involves a single fatty-acyl reductase gene

    PNAS 107:10955–10960.

    https://doi.org/10.1073/pnas.1000823107

    • PubMed
    • Google Scholar
46. 1. Liénard MA
    2. Wang HL
    3. Lassance JM
    4. Löfstedt C

    (2014) Sex pheromone biosynthetic pathways are conserved between moths and the butterfly bicyclus anynana

    Nature Communications 5:3957.

    https://doi.org/10.1038/ncomms4957

    • PubMed
    • Google Scholar
47. 1. Luxová A
    2. Valterová I
    3. Stránský K
    4. Hovorka O
    5. Svatoš A

    (2003) Biosynthetic studies on marking pheromones of bumblebee males

    Chemoecology 13:81–87.

    https://doi.org/10.1007/s00049-003-0230-8

    • Google Scholar
48. 1. Lynch M
    2. Conery JS

    (2000) The evolutionary fate and consequences of duplicate genes

    Science 290:1151–1155.

    https://doi.org/10.1126/science.290.5494.1151

    • PubMed
    • Google Scholar
49. 1. Marchler-Bauer A
    2. Derbyshire MK
    3. Gonzales NR
    4. Lu S
    5. Chitsaz F
    6. Geer LY
    7. Geer RC
    8. He J
    9. Gwadz M
    10. Hurwitz DI
    11. Lanczycki CJ
    12. Lu F
    13. Marchler GH
    14. Song JS
    15. Thanki N
    16. Wang Z
    17. Yamashita RA
    18. Zhang D
    19. Zheng C
    20. Bryant SH

    (2015) CDD: ncbi's conserved domain database

    Nucleic Acids Research 43:D222–D226.

    https://doi.org/10.1093/nar/gku1221

    • PubMed
    • Google Scholar
50. 1. Matousková P
    2. Luxová A
    3. Matousková J
    4. Jiros P
    5. Svatos A
    6. Valterová I
    7. Pichová I

    (2008) A delta9 desaturase from bombus lucorum males: investigation of the biosynthetic pathway of marking pheromones

    Chembiochem : A European Journal of Chemical Biology 9:2534–2541.

    https://doi.org/10.1002/cbic.200800374

    • PubMed
    • Google Scholar
51. 1. Matsumoto S
    2. Yoshiga T
    3. Yokoyama N
    4. Iwanaga M
    5. Koshiba S
    6. Kigawa T
    7. Hirota H
    8. Yokoyama S
    9. Okano K
    10. Mita K
    11. Shimada T
    12. Tatsuki S

    (2001) Characterization of acyl-CoA-binding protein (ACBP) in the pheromone gland of the silkworm, bombyx mori

    Insect Biochemistry and Molecular Biology 31:603–609.

    https://doi.org/10.1016/S0965-1748(00)00165-X

    • PubMed
    • Google Scholar
52. 1. Metz JG
    2. Pollard MR
    3. Anderson L
    4. Hayes TR
    5. Lassner MW

    (2000) Purification of a jojoba embryo fatty acyl-coenzyme A reductase and expression of its cDNA in high erucic acid rapeseed

    Plant Physiology 122:635–644.

    https://doi.org/10.1104/pp.122.3.635

    • PubMed
    • Google Scholar
53. 1. Minh BQ
    2. Nguyen MA
    3. von Haeseler A

    (2013) Ultrafast approximation for phylogenetic bootstrap

    Molecular Biology and Evolution 30:1188–1195.

    https://doi.org/10.1093/molbev/mst024

    • PubMed
    • Google Scholar
54. 1. Mortazavi A
    2. Williams BA
    3. McCue K
    4. Schaeffer L
    5. Wold B

    (2008) Mapping and quantifying mammalian transcriptomes by RNA-Seq

    Nature Methods 5:621–628.

    https://doi.org/10.1038/nmeth.1226

    • PubMed
    • Google Scholar
55. 1. Moto K
    2. Yoshiga T
    3. Yamamoto M
    4. Takahashi S
    5. Okano K
    6. Ando T
    7. Nakata T
    8. Matsumoto S

    (2003) Pheromone gland-specific fatty-acyl reductase of the silkmoth, bombyx mori

    PNAS 100:9156–9161.

    https://doi.org/10.1073/pnas.1531993100

    • PubMed
    • Google Scholar
56. 1. Nagan N
    2. Zoeller RA

    (2001) Plasmalogens: biosynthesis and functions

    Progress in Lipid Research 40:199–229.

    https://doi.org/10.1016/S0163-7827(01)00003-0

    • PubMed
    • Google Scholar
57. 1. Niimura Y
    2. Nei M

    (2006) Evolutionary dynamics of olfactory and other chemosensory receptor genes in vertebrates

    Journal of Human Genetics 51:505–517.

    https://doi.org/10.1007/s10038-006-0391-8

    • PubMed
    • Google Scholar
58. 1. Nygaard S
    2. Zhang G
    3. Schiøtt M
    4. Li C
    5. Wurm Y
    6. Hu H
    7. Zhou J
    8. Ji L
    9. Qiu F
    10. Rasmussen M
    11. Pan H
    12. Hauser F
    13. Krogh A
    14. Grimmelikhuijzen CJ
    15. Wang J
    16. Boomsma JJ

    (2011) The genome of the leaf-cutting ant acromyrmex echinatior suggests key adaptations to advanced social life and fungus farming

    Genome Research 21:1339–1348.

    https://doi.org/10.1101/gr.121392.111

    • PubMed
    • Google Scholar
59. 1. Oba Y
    2. Ojika M
    3. Inouye S

    (2004) Characterization of CG6178 gene product with high sequence similarity to firefly luciferase in Drosophila melanogaster

    Gene 329:137–145.

    https://doi.org/10.1016/j.gene.2003.12.026

    • PubMed
    • Google Scholar
60. Book

    1. Ohno S

    (1970) Evolution by Gene Duplication

    Springer.

    https://doi.org/10.1007/978-3-642-86659-3

    • Google Scholar
61. 1. Patalano S
    2. Vlasova A
    3. Wyatt C
    4. Ewels P
    5. Camara F
    6. Ferreira PG
    7. Asher CL
    8. Jurkowski TP
    9. Segonds-Pichon A
    10. Bachman M
    11. González-Navarrete I
    12. Minoche AE
    13. Krueger F
    14. Lowy E
    15. Marcet-Houben M
    16. Rodriguez-Ales JL
    17. Nascimento FS
    18. Balasubramanian S
    19. Gabaldon T
    20. Tarver JE
    21. Andrews S
    22. Himmelbauer H
    23. Hughes WO
    24. Guigó R
    25. Reik W
    26. Sumner S

    (2015) Molecular signatures of plastic phenotypes in two eusocial insect species with simple societies

    PNAS 112:13970–13975.

    https://doi.org/10.1073/pnas.1515937112

    • PubMed
    • Google Scholar
62. 1. Peters RS
    2. Krogmann L
    3. Mayer C
    4. Donath A
    5. Gunkel S
    6. Meusemann K
    7. Kozlov A
    8. Podsiadlowski L
    9. Petersen M
    10. Lanfear R
    11. Diez PA
    12. Heraty J
    13. Kjer KM
    14. Klopfstein S
    15. Meier R
    16. Polidori C
    17. Schmitt T
    18. Liu S
    19. Zhou X
    20. Wappler T
    21. Rust J
    22. Misof B
    23. Niehuis O

    (2017) Evolutionary history of the hymenoptera

    Current Biology 27:1013–1018.

    https://doi.org/10.1016/j.cub.2017.01.027

    • PubMed
    • Google Scholar
63. 1. Pils B
    2. Schultz J

    (2004) Inactive enzyme-homologues find new function in regulatory processes

    Journal of Molecular Biology 340:399–404.

    https://doi.org/10.1016/j.jmb.2004.04.063

    • PubMed
    • Google Scholar
64. 1. Prasad VP
    2. Wagner S
    3. Keul P
    4. Hermann S
    5. Levkau B
    6. Schäfers M
    7. Haufe G

    (2014) Synthesis of fluorinated analogues of sphingosine-1-phosphate antagonists as potential radiotracers for molecular imaging using positron emission tomography

    Bioorganic & Medicinal Chemistry 22:5168–5181.

    https://doi.org/10.1016/j.bmc.2014.08.009

    • PubMed
    • Google Scholar
65. 1. Prchalová D
    2. Buček A
    3. Brabcová J
    4. Žáček P
    5. Kindl J
    6. Valterová I
    7. Pichová I

    (2016) Regulation of isoprenoid pheromone biosynthesis in bumblebee males

    ChemBioChem 17:260–267.

    https://doi.org/10.1002/cbic.201500415

    • PubMed
    • Google Scholar
66. 1. Quinlan AR
    2. Hall IM

    (2010) BEDTools: a flexible suite of utilities for comparing genomic features

    Bioinformatics 26:841–842.

    https://doi.org/10.1093/bioinformatics/btq033

    • PubMed
    • Google Scholar
67. 1. Radivojac P
    2. Clark WT
    3. Oron TR
    4. Schnoes AM
    5. Wittkop T
    6. Sokolov A
    7. Graim K
    8. Funk C
    9. Verspoor K
    10. Ben-Hur A
    11. Pandey G
    12. Yunes JM
    13. Talwalkar AS
    14. Repo S
    15. Souza ML
    16. Piovesan D
    17. Casadio R
    18. Wang Z
    19. Cheng J
    20. Fang H
    21. Gough J
    22. Koskinen P
    23. Törönen P
    24. Nokso-Koivisto J
    25. Holm L
    26. Cozzetto D
    27. Buchan DW
    28. Bryson K
    29. Jones DT
    30. Limaye B
    31. Inamdar H
    32. Datta A
    33. Manjari SK
    34. Joshi R
    35. Chitale M
    36. Kihara D
    37. Lisewski AM
    38. Erdin S
    39. Venner E
    40. Lichtarge O
    41. Rentzsch R
    42. Yang H
    43. Romero AE
    44. Bhat P
    45. Paccanaro A
    46. Hamp T
    47. Kaßner R
    48. Seemayer S
    49. Vicedo E
    50. Schaefer C
    51. Achten D
    52. Auer F
    53. Boehm A
    54. Braun T
    55. Hecht M
    56. Heron M
    57. Hönigschmid P
    58. Hopf TA
    59. Kaufmann S
    60. Kiening M
    61. Krompass D
    62. Landerer C
    63. Mahlich Y
    64. Roos M
    65. Björne J
    66. Salakoski T
    67. Wong A
    68. Shatkay H
    69. Gatzmann F
    70. Sommer I
    71. Wass MN
    72. Sternberg MJ
    73. Škunca N
    74. Supek F
    75. Bošnjak M
    76. Panov P
    77. Džeroski S
    78. Šmuc T
    79. Kourmpetis YA
    80. van Dijk AD
    81. ter Braak CJ
    82. Zhou Y
    83. Gong Q
    84. Dong X
    85. Tian W
    86. Falda M
    87. Fontana P
    88. Lavezzo E
    89. Di Camillo B
    90. Toppo S
    91. Lan L
    92. Djuric N
    93. Guo Y
    94. Vucetic S
    95. Bairoch A
    96. Linial M
    97. Babbitt PC
    98. Brenner SE
    99. Orengo C
    100. Rost B
    101. Mooney SD
    102. Friedberg I

    (2013) A large-scale evaluation of computational protein function prediction

    Nature Methods 10:221–227.

    https://doi.org/10.1038/nmeth.2340

    • PubMed
    • Google Scholar
68. 1. Reams AB
    2. Roth JR

    (2015) Mechanisms of gene duplication and amplification

    Cold Spring Harbor Perspectives in Biology 7:a016592.

    https://doi.org/10.1101/cshperspect.a016592

    • PubMed
    • Google Scholar
69. 1. Rehan SM
    2. Glastad KM
    3. Lawson SP
    4. Hunt BG

    (2016) The genome and methylome of a subsocial small carpenter bee, ceratina calcarata

    Genome Biology and Evolution 8:1401–1410.

    https://doi.org/10.1093/gbe/evw079

    • PubMed
    • Google Scholar
70. 1. Rispe C
    2. Kutsukake M
    3. Doublet V
    4. Hudaverdian S
    5. Legeai F
    6. Simon JC
    7. Tagu D
    8. Fukatsu T

    (2008) Large gene family expansion and variable selective pressures for cathepsin B in aphids

    Molecular Biology and Evolution 25:5–17.

    https://doi.org/10.1093/molbev/msm222

    • PubMed
    • Google Scholar
71. 1. Rossmann MG
    2. Moras D
    3. Olsen KW

    (1974) Chemical and biological evolution of nucleotide-binding protein

    Nature 250:194–199.

    https://doi.org/10.1038/250194a0

    • PubMed
    • Google Scholar
72. 1. Sadd BM
    2. Barribeau SM
    3. Bloch G
    4. de Graaf DC
    5. Dearden P
    6. Elsik CG
    7. Gadau J
    8. Grimmelikhuijzen CJ
    9. Hasselmann M
    10. Lozier JD
    11. Robertson HM
    12. Smagghe G
    13. Stolle E
    14. Van Vaerenbergh M
    15. Waterhouse RM
    16. Bornberg-Bauer E
    17. Klasberg S
    18. Bennett AK
    19. Câmara F
    20. Guigó R
    21. Hoff K
    22. Mariotti M
    23. Munoz-Torres M
    24. Murphy T
    25. Santesmasses D
    26. Amdam GV
    27. Beckers M
    28. Beye M
    29. Biewer M
    30. Bitondi MM
    31. Blaxter ML
    32. Bourke AF
    33. Brown MJ
    34. Buechel SD
    35. Cameron R
    36. Cappelle K
    37. Carolan JC
    38. Christiaens O
    39. Ciborowski KL
    40. Clarke DF
    41. Colgan TJ
    42. Collins DH
    43. Cridge AG
    44. Dalmay T
    45. Dreier S
    46. du Plessis L
    47. Duncan E
    48. Erler S
    49. Evans J
    50. Falcon T
    51. Flores K
    52. Freitas FC
    53. Fuchikawa T
    54. Gempe T
    55. Hartfelder K
    56. Hauser F
    57. Helbing S
    58. Humann FC
    59. Irvine F
    60. Jermiin LS
    61. Johnson CE
    62. Johnson RM
    63. Jones AK
    64. Kadowaki T
    65. Kidner JH
    66. Koch V
    67. Köhler A
    68. Kraus FB
    69. Lattorff HM
    70. Leask M
    71. Lockett GA
    72. Mallon EB
    73. Antonio DS
    74. Marxer M
    75. Meeus I
    76. Moritz RF
    77. Nair A
    78. Näpflin K
    79. Nissen I
    80. Niu J
    81. Nunes FM
    82. Oakeshott JG
    83. Osborne A
    84. Otte M
    85. Pinheiro DG
    86. Rossié N
    87. Rueppell O
    88. Santos CG
    89. Schmid-Hempel R
    90. Schmitt BD
    91. Schulte C
    92. Simões ZL
    93. Soares MP
    94. Swevers L
    95. Winnebeck EC
    96. Wolschin F
    97. Yu N
    98. Zdobnov EM
    99. Aqrawi PK
    100. Blankenburg KP
    101. Coyle M
    102. Francisco L
    103. Hernandez AG
    104. Holder M
    105. Hudson ME
    106. Jackson L
    107. Jayaseelan J
    108. Joshi V
    109. Kovar C
    110. Lee SL
    111. Mata R
    112. Mathew T
    113. Newsham IF
    114. Ngo R
    115. Okwuonu G
    116. Pham C
    117. Pu LL
    118. Saada N
    119. Santibanez J
    120. Simmons D
    121. Thornton R
    122. Venkat A
    123. Walden KK
    124. Wu YQ
    125. Debyser G
    126. Devreese B
    127. Asher C
    128. Blommaert J
    129. Chipman AD
    130. Chittka L
    131. Fouks B
    132. Liu J
    133. O'Neill MP
    134. Sumner S
    135. Puiu D
    136. Qu J
    137. Salzberg SL
    138. Scherer SE
    139. Muzny DM
    140. Richards S
    141. Robinson GE
    142. Gibbs RA
    143. Schmid-Hempel P
    144. Worley KC

    (2015) The genomes of two key bumblebee species with primitive eusocial organization

    Genome Biology 16:76.

    https://doi.org/10.1186/s13059-015-0623-3

    • PubMed
    • Google Scholar
73. 1. Schrader L
    2. Schmitz J

    (2018) The impact of transposable elements in adaptive evolution

    Molecular Ecology.

    https://doi.org/10.1111/mec.14794

    • PubMed
    • Google Scholar
74. 1. Smadja C
    2. Butlin RK

    (2009) On the scent of speciation: the chemosensory system and its role in premating isolation

    Heredity 102:77–97.

    https://doi.org/10.1038/hdy.2008.55

    • PubMed
    • Google Scholar
75. 1. Sobotník J
    2. Kalinová B
    3. Cahlíková L
    4. Weyda F
    5. Ptácek V
    6. Valterová I

    (2008) Age-dependent changes in structure and function of the male labial gland in Bombus terrestris

    Journal of Insect Physiology 54:204–214.

    https://doi.org/10.1016/j.jinsphys.2007.09.003

    • PubMed
    • Google Scholar
76. 1. Stolle E
    2. Wilfert L
    3. Schmid-Hempel R
    4. Schmid-Hempel P
    5. Kube M
    6. Reinhardt R
    7. Moritz RF

    (2011) A second generation genetic map of the bumblebee bombus terrestris (Linnaeus, 1758) reveals slow genome and chromosome evolution in the Apidae

    BMC Genomics 12:48.

    https://doi.org/10.1186/1471-2164-12-48

    • PubMed
    • Google Scholar
77. 1. Teerawanichpan P
    2. Qiu X

    (2010a) Fatty acyl-CoA reductase and wax synthase from Euglena gracilis in the biosynthesis of medium-chain wax esters

    Lipids 45:263–273.

    https://doi.org/10.1007/s11745-010-3395-2

    • PubMed
    • Google Scholar
78. 1. Teerawanichpan P
    2. Robertson AJ
    3. Qiu X

    (2010b) A fatty acyl-CoA reductase highly expressed in the head of honey bee (apis mellifera) involves biosynthesis of a wide range of aliphatic fatty alcohols

    Insect Biochemistry and Molecular Biology 40:641–649.

    https://doi.org/10.1016/j.ibmb.2010.06.004

    • PubMed
    • Google Scholar
79. 1. Teerawanichpan P
    2. Qiu X

    (2012) Molecular and functional analysis of three fatty acyl-CoA reductases with distinct substrate specificities in copepod calanus finmarchicus

    Marine Biotechnology 14:227–236.

    https://doi.org/10.1007/s10126-011-9406-3

    • PubMed
    • Google Scholar
80. 1. Tillman JA
    2. Seybold SJ
    3. Jurenka RA
    4. Blomquist GJ

    (1999) Insect pheromones--an overview of biosynthesis and endocrine regulation

    Insect Biochemistry and Molecular Biology 29:481–514.

    https://doi.org/10.1016/S0965-1748(99)00016-8

    • PubMed
    • Google Scholar
81. 1. Tumlinson JH
    2. Brennan MM
    3. Doolittle RE
    4. Mitchell ER
    5. Brabham A
    6. Mazomenos BE
    7. Baumhover AH
    8. Jackson DM

    (1989) Identification of a pheromone blend attractive toManduca sexta (L.) males in a wind tunnel

    Archives of Insect Biochemistry and Physiology 10:255–271.

    https://doi.org/10.1002/arch.940100402

    • Google Scholar
82. 1. Tupec M
    2. Buček A
    3. Valterová I
    4. Pichová I

    (2017) Biotechnological potential of insect fatty acid-modifying enzymes

    Zeitschrift Für Naturforschung C 72:387–403.

    https://doi.org/10.1515/znc-2017-0031

    • PubMed
    • Google Scholar
83. 1. Urbanová K
    2. Valterová I
    3. Hovorka O
    4. Kindl J

    (2001) Chemotaxonomical characterisation of males bombus lucorum (Hymenptera: apidae) collected in czech republic

    European Journal of Entomology 127:111–115.

    https://doi.org/10.14411/eje.2001.017

    • Google Scholar
84. 1. Wang M
    2. Wu H
    3. Xu J
    4. Li C
    5. Wang Y
    6. Wang Z

    (2017) Five fatty Acyl-Coenzyme A reductases are involved in the biosynthesis of primary alcohols in Aegilops tauschii Leaves

    Frontiers in Plant Science 8:.

    https://doi.org/10.3389/fpls.2017.01012

    • Google Scholar
85. 1. Weinstock GM
    2. Honeybee Genome Sequencing Consortium

    (2006) Insights into social insects from the genome of the honeybee apis mellifera

    Nature 443:931–949.

    https://doi.org/10.1038/nature05260

    • PubMed
    • Google Scholar
86. 1. Werren JH
    2. Richards S
    3. Desjardins CA
    4. Niehuis O
    5. Gadau J
    6. Colbourne JK
    7. Werren JH
    8. Richards S
    9. Desjardins CA
    10. Niehuis O
    11. Gadau J
    12. Colbourne JK
    13. Beukeboom LW
    14. Desplan C
    15. Elsik CG
    16. Grimmelikhuijzen CJ
    17. Kitts P
    18. Lynch JA
    19. Murphy T
    20. Oliveira DC
    21. Smith CD
    22. van de Zande L
    23. Worley KC
    24. Zdobnov EM
    25. Aerts M
    26. Albert S
    27. Anaya VH
    28. Anzola JM
    29. Barchuk AR
    30. Behura SK
    31. Bera AN
    32. Berenbaum MR
    33. Bertossa RC
    34. Bitondi MM
    35. Bordenstein SR
    36. Bork P
    37. Bornberg-Bauer E
    38. Brunain M
    39. Cazzamali G
    40. Chaboub L
    41. Chacko J
    42. Chavez D
    43. Childers CP
    44. Choi JH
    45. Clark ME
    46. Claudianos C
    47. Clinton RA
    48. Cree AG
    49. Cristino AS
    50. Dang PM
    51. Darby AC
    52. de Graaf DC
    53. Devreese B
    54. Dinh HH
    55. Edwards R
    56. Elango N
    57. Elhaik E
    58. Ermolaeva O
    59. Evans JD
    60. Foret S
    61. Fowler GR
    62. Gerlach D
    63. Gibson JD
    64. Gilbert DG
    65. Graur D
    66. Gründer S
    67. Hagen DE
    68. Han Y
    69. Hauser F
    70. Hultmark D
    71. Hunter HC
    72. Hurst GD
    73. Jhangian SN
    74. Jiang H
    75. Johnson RM
    76. Jones AK
    77. Junier T
    78. Kadowaki T
    79. Kamping A
    80. Kapustin Y
    81. Kechavarzi B
    82. Kim J
    83. Kim J
    84. Kiryutin B
    85. Koevoets T
    86. Kovar CL
    87. Kriventseva EV
    88. Kucharski R
    89. Lee H
    90. Lee SL
    91. Lees K
    92. Lewis LR
    93. Loehlin DW
    94. Logsdon JM
    95. Lopez JA
    96. Lozado RJ
    97. Maglott D
    98. Maleszka R
    99. Mayampurath A
    100. Mazur DJ
    101. McClure MA
    102. Moore AD
    103. Morgan MB
    104. Muller J
    105. Munoz-Torres MC
    106. Muzny DM
    107. Nazareth LV
    108. Neupert S
    109. Nguyen NB
    110. Nunes FM
    111. Oakeshott JG
    112. Okwuonu GO
    113. Pannebakker BA
    114. Pejaver VR
    115. Peng Z
    116. Pratt SC
    117. Predel R
    118. Pu LL
    119. Ranson H
    120. Raychoudhury R
    121. Rechtsteiner A
    122. Reese JT
    123. Reid JG
    124. Riddle M
    125. Robertson HM
    126. Romero-Severson J
    127. Rosenberg M
    128. Sackton TB
    129. Sattelle DB
    130. Schlüns H
    131. Schmitt T
    132. Schneider M
    133. Schüler A
    134. Schurko AM
    135. Shuker DM
    136. Simões ZL
    137. Sinha S
    138. Smith Z
    139. Solovyev V
    140. Souvorov A
    141. Springauf A
    142. Stafflinger E
    143. Stage DE
    144. Stanke M
    145. Tanaka Y
    146. Telschow A
    147. Trent C
    148. Vattathil S
    149. Verhulst EC
    150. Viljakainen L
    151. Wanner KW
    152. Waterhouse RM
    153. Whitfield JB
    154. Wilkes TE
    155. Williamson M
    156. Willis JH
    157. Wolschin F
    158. Wyder S
    159. Yamada T
    160. Yi SV
    161. Zecher CN
    162. Zhang L
    163. Gibbs RA
    164. Nasonia Genome Working Group

    (2010) Functional and evolutionary insights from the genomes of three parasitoid Nasonia species

    Science 327:343–348.

    https://doi.org/10.1126/science.1178028

    • PubMed
    • Google Scholar
87. 1. Woodard SH
    2. Fischman BJ
    3. Venkat A
    4. Hudson ME
    5. Varala K
    6. Cameron SA
    7. Clark AG
    8. Robinson GE

    (2011) Genes involved in convergent evolution of eusociality in bees

    PNAS 108:7472–7477.

    https://doi.org/10.1073/pnas.1103457108

    • PubMed
    • Google Scholar
88. 1. Xue B
    2. Rooney AP
    3. Kajikawa M
    4. Okada N
    5. Roelofs WL

    (2007) Novel sex pheromone desaturases in the genomes of corn borers generated through gene duplication and retroposon fusion

    PNAS 104:4467–4472.

    https://doi.org/10.1073/pnas.0700422104

    • PubMed
    • Google Scholar
89. 1. Ye J
    2. Coulouris G
    3. Zaretskaya I
    4. Cutcutache I
    5. Rozen S
    6. Madden TL

    (2012) Primer-BLAST: a tool to design target-specific primers for polymerase chain reaction

    BMC Bioinformatics 13:134.

    https://doi.org/10.1186/1471-2105-13-134

    • PubMed
    • Google Scholar
90. 1. Yu G
    2. Smith DK
    3. Zhu H
    4. Guan Y
    5. Lam TT-Y

    (2016) GGTREE: an R package for visualization and annotation of phylogenetic trees with their covariates and other associated data

    Methods in Ecology and Evolution.

    https://doi.org/10.1111/2041-210X.12628

    • Google Scholar
91. 1. Zácek P
    2. Kalinová B
    3. Sobotník J
    4. Hovorka O
    5. Ptácek V
    6. Coppée A
    7. Verheggen F
    8. Valterová I

    (2009) Comparison of age-dependent quantitative changes in the male labial gland secretion of bombus terrestris and Bombus lucorum

    Journal of Chemical Ecology 35:698–705.

    https://doi.org/10.1007/s10886-009-9650-4

    • PubMed
    • Google Scholar
92. 1. Zhang J

    (2003) Evolution by gene duplication: an update

    Trends in Ecology & Evolution 18:292–298.

    https://doi.org/10.1016/S0169-5347(03)00033-8

    • Google Scholar
93. 1. Žáček P
    2. Kindl J
    3. Frišonsová K
    4. Průchová M
    5. Votavová A
    6. Hovorka O
    7. Kovalczuk T
    8. Valterová I

    (2015) Biosynthetic studies of the male marking pheromone in bumblebees by using labelled fatty acids and Two-Dimensional gas chromatography with mass detection

    ChemPlusChem 80:839–850.

    https://doi.org/10.1002/cplu.201402420

    • Google Scholar

Author details

1. Michal Tupec

   1. Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic
   2. Department of Biochemistry, Faculty of Science, Charles University, Prague, Czech Republic

   Contribution

   Validation, Investigation, Visualization, Writing—original draft

   Contributed equally with

   Aleš Buček

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0003-2371-4850

2. Aleš Buček

   1. Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic
   2. Okinawa Institute of Science and Technology Graduate University, Okinawa, Japan

   Contribution

   Conceptualization, Validation, Investigation, Visualization, Methodology, Writing—original draft

   Contributed equally with

   Michal Tupec

   For correspondence

   ales.bucek@oist.jp

   Competing interests

   No competing interests declared

3. Václav Janoušek

   Department of Zoology, Faculty of Science, Charles University, Prague, Czech Republic

   Contribution

   Validation, Investigation, Methodology, Writing—original draft

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0002-6894-6826

4. Heiko Vogel

   Department of Entomology, Max Planck Institute for Chemical Ecology, Jena, Germany

   Contribution

   Formal analysis, Validation, Investigation

   Competing interests

   No competing interests declared

   "This ORCID iD identifies the author of this article:" 0000-0001-9821-7731

5. Darina Prchalová

   Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

6. Jiří Kindl

   Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic

   Contribution

   Investigation, Methodology

   Competing interests

   No competing interests declared

7. Tereza Pavlíčková

   Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic

   Contribution

   Formal analysis, Investigation, Methodology

   Competing interests

   No competing interests declared

8. Petra Wenzelová

   Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic

   Contribution

   Formal analysis, Supervision, Investigation, Writing—original draft

   Competing interests

   No competing interests declared

9. Ullrich Jahn

   Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic

   Contribution

   Data curation, Supervision, Validation, Methodology, Writing—original draft

   Competing interests

   No competing interests declared

10. Irena Valterová

    Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic

    Contribution

    Conceptualization, Data curation, Supervision, Funding acquisition, Validation, Methodology, Writing—original draft

    Competing interests

    No competing interests declared

11. Iva Pichová

    Institute of Organic Chemistry and Biochemistry of the Czech Academy of Sciences, Prague, Czech Republic

    Contribution

    Conceptualization, Supervision, Funding acquisition, Validation, Methodology, Writing—original draft

    For correspondence

    iva.pichova@uochb.cas.cz

    Competing interests

    No competing interests declared

    "This ORCID iD identifies the author of this article:" 0000-0002-2178-9819

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