The Interactive Fly

Zygotically transcribed genes

Olfaction in Drosophila

Olfactory receptors Olfactory neurons of the antenna and maxillary palp Olfactory glomeruli in the antennal lobe Mushroom body and olfactory learning

  • Odorant Receptors
  • Mushroom Bodies - A site for formation and retrieval of olfactory memories
  • The structural biology of olfactory organs
  • Molecular, anatomical, and functional organization of the Drosophila olfactory system

  • Characterization of Drosophila odorant receptors
  • Functional analysis of odorant receptors
  • Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet

    Goldman-Huertas, B., Mitchell, R. F., Lapoint, R. T., Faucher, C. P., Hildebrand, J. G. and Whiteman, N. K. (2015). Evolution of herbivory in Drosophilidae linked to loss of behaviors, antennal responses, odorant receptors, and ancestral diet. Proc Natl Acad Sci U S A 112(10): 3026-3031. PubMed ID: 25624509

    Herbivory is a key innovation in insects, yet has only evolved in one-third of living orders. The evolution of herbivory likely involves major behavioral changes mediated by remodeling of canonical chemosensory modules. Herbivorous flies in the genus Scaptomyza (Drosophilidae) are compelling species in which to study the genomic architecture linked to the transition to herbivory because they recently evolved from microbe-feeding ancestors and are closely related to Drosophila melanogaster. This study found that Scaptomyza flava, a leaf-mining specialist on plants in the family (Brassicaceae), was not attracted to yeast volatiles in a four-field olfactometer assay, whereas D. melanogaster was strongly attracted to these volatiles. Yeast-associated volatiles, especially short-chain aliphatic esters, elicited strong antennal responses in D. melanogaster, but weak antennal responses in electroantennographic recordings from S. flava. The genome of S. flava was sequenced, and this species' odorant receptor repertoire was characterized. Orthologs of odorant receptors, which detect yeast volatiles in D. melanogaster and mediate critical host-choice behavior, were deleted or pseudogenized in the genome of S. flava. These genes were lost step-wise during the evolution of Scaptomyza. Additionally, Scaptomyza has experienced gene duplication and likely positive selection in paralogs of Or67b in D. melanogaster. Olfactory sensory neurons expressing Or67b are sensitive to green-leaf volatiles. Major trophic shifts in insects are associated with chemoreceptor gene loss as recently evolved ecologies shape sensory repertoires (Goldman-Huertas, 2005).

    Understanding the origins and consequences of trophic shifts, especially the transition to herbivory, has been a central problem in evolutionary biology. The paleontological record suggests that evolutionary transitions to herbivory have been rare in insects, and the first transitions to herbivory in vertebrates occurred long after the colonization of land. However, species radiations result from herbivorous transitions in insects and vertebrates, suggesting that herbivory is a key innovation. Identifying functional genomic changes associated with the evolutionary transition to herbivory could yield insight into the mechanisms that have driven their success. However, the origins of the most diverse clades of herbivorous insects are ancient and date to the Jurassic or earlier, limiting meaningful genomic comparisons. In contrast, herbivory has evolved more times in Diptera than in any other order. The Drosophilidae is an excellent system to study the evolution of herbivory from a functional genomic perspective because it includes several transitions to herbivory, and the genomic model Drosophila melanogaster (Goldman-Huertas, 2005).

    The transition to herbivory involves adaptations in physiology, morphology, and behavior. The evolution of sensory repertoires could reinforce or even precipitate these adaptations through adaptive loss or relaxation of functional constraint subsequent to a trophic shift. Adaptive loss of chemoreceptors has been rarely shown but occurs in nematodes, although their olfactory systems are distinct from insects. Families of mammalian olfactory receptor proteins have been remodeled during transitions to flight, aquatic lifestyles, and frugivory. Similarly, the evolution of diet specialization in Drosophila species correlates with chemoreceptor gene losses, and hematophagous flies have lost gustatory receptors that detect sweet compounds. More profound changes such as the evolution of new protein families are associated with major evolutionary transitions such as the evolution of flight in insects. Although gene loss is unlikely to be a driving force of innovation, loss-of-function mutations may be exeptations that allow novel behaviors to evolve by disrupting ancestral attractions. If detection of different chemical cues becomes selected in a novel niche, then loss through relaxed constraint may indicate which chemical cues have changed during a trophic shift (Goldman-Huertas, 2005).

    The chemosensory repertoires of many drosophilid species have been functionally annotated. The genus Drosophila includes 23 species with published genome sequences, and D. melanogaster presents the most fully characterized insect olfactory system, allowing potential linkage of receptor remodeling to a mechanistic understanding of behavioral change (Goldman-Huertas, 2005).

    Most drosophilids feed on yeast and other microbes growing on decaying plant tissues. Adult female D. melanogaster and distantly related species innately prefer yeast chemical cues to those produced by the fruit on which they oviposit. D. melanogaster detects volatiles with chemoreceptors of several different protein families, but especially receptors from the odorant receptor (OR) gene family, some of which, such as Or42b, are highly conserved across species. Or42b is necessary for attraction and orientation to vinegar and aliphatic esters. Similar compounds activate Or42b across many Drosophila species, suggesting that volatile cues for yeast, and the associated receptors, are conserved across the Drosophilidae (Goldman-Huertas, 2005).

    The ancestral feeding niche for the genus Scaptomyza (Drosophilidae) is microbe-feeding, but Scaptomyza use decaying leaves and stems rather than the fermenting fruit used by D. melanogaster and other members of the subgenus Sophophora. The close association of Scaptomyza with decaying plant tissues may have precipitated the evolution of herbivory <20 MyBP. Adult females of the species S. flava feed and oviposit on living leaves of many cruciferous plants (Brassicales) including Arabidopsis thaliana. Females puncture leaves with serrated ovipositors to create feeding and oviposition sites, and larvae mine and pupate within the living leaves (Goldman-Huertas, 2005).

    This study used Scaptomyza as a model to test the hypothesis that functional loss of chemosensory genes has played a role in a major ecological transition to herbivory in insects. It was hypothesized that the conserved detection of yeast volatiles would be lost in the herbivorous Scaptomyza lineage. This loss was tested by comparing D. melanogaster and S. flava at behavioral, physiological, and genetic levels. First, it was hypothesized that gravid ovipositing S. flava females would not be attracted to yeast volatiles. Second, it was hypothesized that the olfactory sensory organs of S. flava would have a decreased ability to detect individual yeast volatiles and volatile mixtures. Third, chemoreceptor genes from the OR gene family implicated in detection of yeast volatiles would be lost in the S. flava genome. Finally, it was predicted that chemoreceptor genes potentially mediating detection of plant volatiles would show evidence of positive selection and possibly, neofunctionalization (Goldman-Huertas, 2005).

    Olfaction is used by insects to find resources, mates, and oviposition substrates. This study tested the hypothesis that S. flava is not attracted to yeast volatiles, whereas D. melanogaster is attracted to yeast volatiles. A four-field olfactometer assay was used in which filtered air blown through four corners of a diamond-shaped arena establishes four independent airfields. Two of the four fields were exposed to yeast volatiles from Saccharomyces cerevisiae cultures. The presence of gravid adult females of both species in either yeast or control fields was recorded every 6 s for 10 min. D. melanogaster flies spent 82.4 ± 18.2% SD of the assay time in yeast-volatile fields and more time in yeast-volatile fields than S. flava. S. flava did not spend more time in yeast-volatile fields and divided residence time evenly between yeast and control fields, consistent with a loss of attraction to yeast volatiles in S. flava flies (Goldman-Huertas, 2005).

    Because S. flava flies failed to increase their residence time in olfactometer quadrants exposed to yeast volatiles, it was hypothesized that S. flava antennal olfactory sensory neurons (OSNs) were deficient in their ability to detect yeast volatiles. This hypothesis was tested by conducting electroantennogram (EAG) measurements in adult D. melanogaster and S. flava flies of both sexes 4-20 d after eclosion, exposed to the same yeast volatiles used in the olfactometer assays and to crushed rosette leaves of the host plant of S. flava flies in laboratory colonies (Arabidopsis thaliana accession Col-0). EAG responses are driven by the aggregate depolarization of OSNs in the antennae and scale with the concentration and identity of stimulants. No difference were found between sexes and data for male and female flies were combined. Consistently lower EAG signals were recorded in S. flava flies compared with D. melanogaster, preventing interspecific comparisons of signal amplitude, possibly due to differences in electrical properties of antennae (Goldman-Huertas, 2005).

    The antennae of S. flava were more strongly stimulated by Arabidopsis volatiles than by yeast, whereas the antennae of D. melanogaster were more responsive to volatiles from yeast than those from Arabidopsis. Responses were recorded to a small panel of three volatiles associated with A. thaliana [(Z)-3-hexenol, myrcene, phenethyl isothiocyanate] and two with S. cerevisiae (2-phenylethanol, ethyl acetate). Antennae of both species detected all volatiles compared with a negative control. The antennae of S. flava were most responsive to (Z)-3-hexenol, a volatile produced by damaged leaves of many plant species, and were also highly attuned to phenethyl isothiocyanate, a hydrolyzed product of glucosinolates, which are the major defensive compound in host plants of S. flava. Responses to myrcene and 2-phenylethanol were not in the expected direction, although 2-phenylethanol, as a widespread floral volatile, may remain an important chemical cue for Scaptomyza adults (Goldman-Huertas, 2005).

    Antennae of S. flava were less responsive to yeast and the yeast-associated volatile ethyl acetate than to plant-related volatiles, but these relative comparisons were insufficient to prove that the detection threshold for yeast volatiles had decreased in Scaptomyza. Therefore the sensitivity of S. flava and D. melanogaster flies to this and other short-chain aliphatic esters was tested by exposing females to half-log dilution series of ethyl acetate, ethyl propionate, and isobutyl acetate. Sensitivity was defined as the first concentration increase that generated an increased antennal response. S. flava was insensitive to ethyl acetate at the concentrations tested. S. flava was also less responsive to ethyl propionate and isobutyl acetate compared with D. melanogaster. Scaptomyza is considerably less sensitive to short aliphatic esters, which may account for differences in signal strength in response to plant and yeast volatile mixtures and the lack of attraction to yeast volatiles by S. flava. This unresponsiveness is consistent with the fact that deficits in the production of aliphatic esters in a yeast strain decreased attractiveness to D. melanogaster flies (Goldman-Huertas, 2005).

    The lack of attraction and minimal EAG response to yeast volatiles in S. flava suggested that chemosensory genes have been lost or changed in herbivorous Scaptomyza species. ORs are expressed in the dendrites of OSNs in the antennae and maxillary palps and are the primary receptors by which most neopteran insects detect odors in their environments. The OR family has been functionally annotated in D. melanogaster, and members of subfamily H OR genes in particular are highly conserved and enriched in receptors for aliphatic esters, a group of compounds S. flava detected poorly (Goldman-Huertas, 2005).

    To characterize changes in the OR gene repertoire in S. flava associated with the olfactory phenotypes, the genome of S. flava and annotated OR genes were annotated by using reciprocal tBLASTn searches of previously annotated Drosophila OR protein sequences against this de novo S. flava genome assembly. 65 full-length ORFs for OR genes were found in S. flava. Consistent with previous OR gene-naming conventions, ORs were named after the D. melanogaster ortholog or the most closely related gene, with the exception of OrN1 and OrN2 orthologs, which are not present in D. melanogaster (Goldman-Huertas, 2005).

    Protein translations of S. flava genes were included in a phylogeny of D. melanogaster, Drosophila virilis, Drosophila mojavensis, and Drosophila grimshawi OR protein sequences to assess homology. The latter three species are the closest relatives of Scaptomyza with fully sequenced genomes (Goldman-Huertas, 2005).

    S. flava retains duplicates of Or42a, Or67a, Or74a, Or83c, Or98a, and OrN2 found in other sequenced Drosophila species. Scaptomyza also has duplications not shared with close relatives, although nine of these genes are pseudogenized. The majority of paralogs (56%) were found on the same scaffold in tandem arrays. The functional significance of these gene duplications is not yet clear, but it is suggestive that Or67b, with three copies in S. flava, is in single copy in nearly all sequenced Drosophila. In D. melanogaster, neurons expressing Or67b respond to green leaf volatiles such as (Z)-3-hexenol, to which S. flava also has a robust antennal response (Goldman-Huertas, 2005).

    Only four widely conserved ORs were uniquely lost (Or22a and Or85d) or pseudogenized (Or9a, Or42b) in the Scaptomyza lineage. Syntenic regions flanking OR losses were recovered in the genome assembly. Orthologs of Or9a, Or22a, and Or42b are intact in 23 Drosophila species with genome sequences, and Or85d is missing only in the Drosophila albomicans and Drosophila rhopaloa genome assemblies. As predicted, orthologs of ORs that persist in microbe-feeding Drosophila species and are lost in S. flava, function in yeast-volatile detection. Or42b is highly conserved in sequence among Drosophila species, and the receptor is highly attuned to aliphatic esters at low concentrations. Knockouts of Or42b in adult D. melanogaster result in failure to orient in flight toward aliphatic ester odor plumes , and rescuing these neurons restores attraction to yeast volatiles. Similarly, no sequences similar to Or22a were present in the S. flava assembly, although conserved intergenic regions were found in S. flava that flank Or22a in other Drosophila species. Or22a also detects aliphatic esters and in the specialist species Drosophila erecta and Drosophila sechellia, Or22a detects volatiles produced by host fruit. Both Or22a and Or42b are activated by floral volatiles of Arum palestinum, which mimics yeast fermentation volatiles and attracts a diversity of drosophilids. Finally, Or85d orthologs were not detected in the S. flava genome by BLAST or by inspection of genome regions flanking Or85d in other species. Or85d is expressed in the maxillary palps and in D. melanogaster is responsive to the yeast metabolites 2-heptanol, ethyl acetate, and isoamyl acetate. Or85d is highly sensitive to phenethyl acetate, a common volatile of many yeast species. In D. melanogaster, Or9a is activated by a broad range of ketone-, alcohol-, and carboxylic acid-containing ligands. Some of these ligands, such as acetoin, are common yeast volatiles and strong attractants. The consequences of Or9a pseudogenization will require further study (Goldman-Huertas, 2005).

    A time-calibrated phylogeny of the family Drosophilidae suggests that herbivory evolved in Scaptomyza ca.13.5 million years ago (95% highest posterior density 10.02–17.48 million years ago), overlapping with age ranges inferred from previous analyses. Ancestral state reconstructions were performed in the APE package by using an equal rates model. This analysis indicated that microbe feeding is ancestral in Drosophila and Scaptomyza (99.7% probability) and that herbivory evolved once within the genus Scaptomyza (Goldman-Huertas, 2005).

    It was hypothesized that OR gene losses would coincide with the evolution of herbivory. Degenerate PCR primers were developed from genomes of multiple Scaptomyza and Drosophila species that targeted exonic sequences of Or22a and Or9a, and conserved, flanking, intergenic sequences of Or42b and Or85d (Goldman-Huertas, 2005).

    Gene losses in S. flava were confirmed by PCR screen in three natural populations, with the exception of SflaOr9a-1, which appeared to be present in a functional copy in a population from Arizona. A preliminary genome assembly of Scaptomyza pallida was consistent with PCR screening results for OR loss patterns in this species. The presence/absence of S. flava gene losses was reconstructed along ancestral nodes and found that three of the four OR gene losses in S. flava (Or22a, Or85d, Or42b) coincided with or preceded the evolution of herbivory in Scaptomyza. Losses were shared by herbivorous congeners. Or22a, while lost in S. flava, is intact in the microbe-feeding species Scaptomyza apicata and S. pallida and is also lost in two other herbivorous species, Scaptomyza nigrita and Scaptomyza graminum (Goldman-Huertas, 2005).

    Specialist, microbe-feeding Drosophila species, such as D. sechellia and D. erecta have an accelerated rate of chemoreceptor gene loss, but this pattern could also be due to nearly neutral processes. S. flava feeds almost exclusively on plants within the Brassicales, and it was hypothesized that this species has experienced an accelerated rate of chemosensory gene loss compared with other microbe-feeding Drosophila species. This hypothesis was tested by coding homologous groups of ORs as present or absent in S. flava, D. virilis, D. mojavensis and D. grimshawi (the closest Drosophila relatives of Scaptomyza), and two models of gene loss were inferred in the Brownie software package. No evidence was found for the alternative model of increased rate of loss in Scaptomyza, but it cannot be ruled out that there were insufficient loss events to parameterize the more complex model or that other chemoreceptor gene families have undergone accelerated loss in S. flava. Also, S. flava is oligophagous, feeding on many plant species in the Brassicales, and it is less specialized than D. sechellia and D. erecta (Goldman-Huertas, 2005).

    Because the shift to herbivory in Scaptomyza likely involved many changes in olfactory cues, it was hypothesized that some S. flava OR genes should bear signatures of episodic positive selection, as flies adapted to a novel environment. To test this hypothesis, null and alternative (branch-site) models were inferred in PAML 4.7a where subsets of codons in extant S. flava ORs could evolve under (i) purifying or neutral selection or (ii) purifying, neutral, or positive selection, relative to 12 Drosophila species. A phylogeny-aware alignment program, PRANK, was used to identify regions where indels were probable while minimizing sensitivity to alignment errors. Alignments where more than one taxon had an inferred indel in greater than two regions were trimmed by using Gblocks to remove columns with ambiguous homology(Goldman-Huertas, 2005).

    After correcting for false discovery, two ORs were found in which the branch-site model consistent with episodic positive selection was more likely than the null model. Or88a had the strongest statistical support for the branch-site model. In D. melanogaster, Or88a functions in recognition of male and virgin female conspecifics . Two other branches among the S. flava Or67b paralogs also supported the branch-site model: an ancestral branch preceding a Scaptomyza-specific duplication event and a branch leading to Or67b-3. Homologs of this gene in D. melanogaster encode ORs that respond to the green-leaf volatile (Z)-3-hexenol, one of the most salient ligands found in EAG studies of S. flava. Experimental, functional, and population-based tests are needed to verify whether positive selection has fixed amino acid changes in the Scaptomyza lineage (Goldman-Huertas, 2005).

    It is concluded that trophic transitions in the history of animal life, such as herbivory, may be mediated by genetic changes in chemosensory repertoires. The majority of Drosophilidae feed on microbes, and distantly related drosophilid lineages are attracted by the same yeast-mimicking floral scent produced by A. palestinum. A subset of the ORs stimulated by this scent are highly conserved in other drosophilids, which may be part of a homologous and conserved olfactory circuit used to find fermenting host substrates across the family. It was hypothesized that mutations disrupting the function of OR homologs in this conserved olfactory circuit could mediate the evolution of herbivory or other novel food preferences (Goldman-Huertas, 2005).

    S. flava, an herbivorous drosophilid, has lost orthologs of ORs involved in this generalized yeast olfactory circuit. Consistent with these findings, S. flava did not respond to yeast volatiles in a behavioral assay. Antennae of S. flava were weakly activated by active yeast cultures and short-chain aliphatic esters, key compounds found in yeast volatile blends and known ligands of ORs in D. melanogaster lost in S. flava. However, retention of some ORs implicated in yeast-volatile detection, such as Or92a and Or59b, implies that S. flava may retain the ability to detect some untested yeast compounds (Goldman-Huertas, 2005).

    It is hypothesized that OR genes would be intact in nonherbivorous Scaptomyza and gene losses would coincide with the transition to herbivory. Or22a loss did coincide with the evolution of herbivory, but losses of Or42b and Or85d likely predate the evolution of plant feeding. These more ancient losses of conserved yeast-volatile receptors suggest ancestral Scaptomyza may have already evolved novel olfactory pathways that were later co-opted by herbivorous lineages, and in fact, many Scaptomyza species feed on microbes living within decaying leaves or in leaf mines produced by other insects. Sister groups of many major herbivorous insect lineages also feed on detritus and fungi, suggesting that the transition from microbe feeding to herbivory may be common. The genetic changes that underlie host-finding remain to be identified, but recently duplicated ORs, such as the unique triplication of Or67b in Scaptomyza, are likely candidates for further functional study. Subtle, targeted remodeling of chemoreceptor repertoires may be a general mechanism driving changes in behavior, facilitating trophic shifts and ultimately diversification in animals (Goldman-Huertas, 2005).

  • Molecular determinants of odorant receptor function in insects
  • Insect olfactory receptors are heteromeric ligand-gated ion channels
  • Receptors for mate recognition in Drosophila
  • Insect odorant response sensitivity is tuned by metabotropically autoregulated olfactory receptors
  • Variant ionotropic glutamate receptors as chemosensory receptors in Drosophila
  • Metabolite exchange between microbiome members produces compounds that influence Drosophila behavior
  • Transcriptional regulation of odorant receptors; Mechanisms of odor receptor gene choice in Drosophila
  • An RNA-seq screen of the Drosophila antenna identifies a transporter necessary for ammonia detection
  • Requirement for Drosophila SNMP1 for rapid activation and termination of pheromone-induced activity
  • The corepressor Atrophin specifies odorant receptor expression in Drosophila
  • Vibrational detection of odorant functional groups by Drosophila melanogaster

  • Odorant receptors

    # Symbol Name Map Location Entrez Gene
    1 Or1a Odorant receptor 1a 1A7--8 Entrez Gene
    2 Or2a Odorant receptor 2a 2E3--F1 Entrez Gene
    3 Or7a Odorant receptor 7a 7D14--16 Entrez Gene
    4 Or10a Odorant receptor 10a 10B12--13 Entrez Gene
    5 Or13a Odorant receptor 13a 13F16--18 Entrez Gene
    6 Or19a Odorant receptor 19a 19B3--C Entrez Gene
    7 Or22a Odorant receptor 22a 22A3--4 Entrez Gene
    8 Or22b Odorant receptor 22b 22A3--4 Entrez Gene
    9 Or22c Odorant receptor 22c 22C1 Entrez Gene
    10 Or23a Odorant receptor 23a 23A2--3 Entrez Gene
    11 Or24a Odorant receptor 24a 24D5--6 Entrez Gene
    12 Or30a Odorant receptor 30a 30A2 Entrez Gene
    13 Or33a Odorant receptor 33a 33B5 Entrez Gene
    14 Or33b Odorant receptor 33b 33B5 Entrez Gene
    15 Or33c Odorant receptor 33c 33B5--6 Entrez Gene
    16 Or35a Odorant receptor 35a 35D4 Entrez Gene
    17 Or42a Odorant receptor 42a 41F11 Entrez Gene
    18 Or42b Odorant receptor 42b 41F11 Entrez Gene
    19 Or43a Odorant receptor 43a 43A1 Entrez Gene
    20 Or43b Odorant receptor 43b 43F5--6 Entrez Gene
    21 Or45a Odorant receptor 45a 45C7--D1 Entrez Gene
    22 Or45b Odorant receptor 45b 45F1--3 Entrez Gene
    23 Or46a Odorant receptor 46a 46E6--9 Entrez Gene
    24 Or47a Odorant receptor 47a 47E1 Entrez Gene
    25 Or47b Odorant receptor 47b 47E6--F1 Entrez Gene
    26 Or49a Odorant receptor 49a 49A2--3 Entrez Gene
    27 Or49b Odorant receptor 49b 49D1--2 Entrez Gene
    28 Or56a Odorant receptor 56a 56E4--5 Entrez Gene
    29 Or59a Odorant receptor 59a 59D11--E1 Entrez Gene
    30 Or59b Odorant receptor 59b 59E1 Entrez Gene
    31 Or59c Odorant receptor 59c 59E1 Entrez Gene
    32 Or63a Odorant receptor 63a 63B1 Entrez Gene
    33 Or65a Odorant receptor 65a 65A7--11 Entrez Gene
    34 Or65b Odorant receptor 65b 65A7--11 Entrez Gene
    35 Or65c Odorant receptor 65c 65A7--11 Entrez Gene
    36 Or67a Odorant receptor 67a 67B6--7 Entrez Gene
    37 Or67b Odorant receptor 67b 67B10 Entrez Gene
    38 Or67c Odorant receptor 67c 67D3--5 Entrez Gene
    39 Or67d Odorant receptor 67d 67D3--5 Entrez Gene
    40 Or69a Odorant receptor 69a 69E8--F1 Entrez Gene
    41 Or69b Odorant receptor 69b 69E8--F1 Entrez Gene
    42 Or71a Odorant receptor 71a 71B1 Entrez Gene
    43 Or74a Odorant receptor 74a 74A5--B1 Entrez Gene
    44 Or82a Odorant receptor 82a 82A3--4 Entrez Gene
    45 Or83a Odorant receptor 83a 83A2--3 Entrez Gene
    46 Orco (Or83b) Odorant receptor co-receptor 83A2--3 Entrez Gene
    47 Or83c Odorant receptor 83c 83D2--4 Entrez Gene
    48 Or85a Odorant receptor 85a 84F6--9 Entrez Gene
    49 Or85b Odorant receptor 85b 85A2--3 Entrez Gene
    50 Or85c Odorant receptor 85c 85A2--3 Entrez Gene
    51 Or85d Odorant receptor 85d 85A3--4 Entrez Gene
    52 Or85e Odorant receptor 85e 85A5 Entrez Gene
    53 Or85f Odorant receptor 85f 85D14--16 Entrez Gene
    54 Or88a Odorant receptor 88a 88A10 Entrez Gene
    55 Or92a Odorant receptor 92a 92E7--8 Entrez Gene
    56 Or94a Odorant receptor 94a 94D8--10 Entrez Gene
    57 Or94b Odorant receptor 94b 94D9--10 Entrez Gene
    58 Or98a Odorant receptor 98a 98A15--B1 Entrez Gene
    59 Or98b Odorant receptor 98b 98C3--4 Entrez Gene
    60 Or1a Odorant receptor 1a 1A1--2 Entrez Gene
    61 Or19b Odorant receptor 19b 19B1 Entrez Gene

    Zygotically transcribed genes

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