The Genetics of Male Pheromone Preference Difference Between Drosophila melanogaster and Drosophila simulans

Species of flies in the genus Drosophila differ dramatically in their preferences for mates, but little is known about the genetic or neurological underpinnings of this evolution. Recent advances have been made to our understanding of one case: pheromone preference evolution between the species D. melanogaster and D. simulans. Males of both species are very sensitive to the pheromone 7,11-HD that is present only on the cuticle of female D. melanogaster. In one species this cue activates courtship, and in the other it represses it. This change in valence was recently shown to result from the modification of central processing neurons, rather than changes in peripherally expressed receptors, but nothing is known about the genetic changes that are responsible. In the current study, we show that a 1.35 Mb locus on the X chromosome has a major effect on male 7,11-HD preference. Unfortunately, when this locus is divided, the effect is largely lost. We instead attempt to filter the 159 genes within this region using our newfound understanding of the neuronal underpinnings of this phenotype to identify and test candidate genes. We present the results of these tests, and discuss the difficulty of identifying the genetic architecture of behavioral traits and the potential of connecting these genetic changes to the neuronal modifications that elicit different behaviors.

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The genetics of male pheromone preference difference between Drosophila melanogaster and D. simulans

10.1101/793315 ◽

2019 ◽

Author(s):

Michael P. Shahandeh ◽

Alison Pischedda ◽

Jason M. Rodriguez ◽

Thomas L. Turner

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

Genetic Architecture ◽

Major Effect ◽

The Other ◽

Male Pheromone ◽

Genetic Changes ◽

Behavioral Traits ◽

Central Processing ◽

Preference Evolution

AbstractSpecies of flies in the genus Drosophila differ dramatically in their preferences for mates, but little is known about the genetic or neurological underpinnings of this evolution. Recent advances have been made to our understanding of one case: pheromone preference evolution between the species D. melanogaster and D. simulans. Males of both species are very sensitive to the pheromone 7,11-HD that is present only on the cuticle of female D. melanogaster. In one species this cue activates courtship, and in the other it represses it. This change in valence was recently shown to result from the modification of central processing neurons, rather than changes in peripherally expressed receptors, but nothing is known about the genetic changes that are responsible. In the current study, we show that a 1.35 Mb locus on the X chromosome has a major effect on male 7,11-HD preference. Unfortunately, when this locus is divided, the effect is largely lost. We instead attempt to filter the 159 genes within this region using our newfound understanding of the neuronal underpinnings of this phenotype to identify and test candidate genes. We present the results of these tests, and discuss the difficulty of identifying the genetic architecture of behavioral traits and the potential of connecting these genetic changes to the neuronal modifications that elicit different behaviors.

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Spontaneous formation of compound X chromosomes in Drosophila melanogaster.

Genetics ◽

10.1093/genetics/119.1.95 ◽

1988 ◽

Vol 119 (1) ◽

pp. 95-103

Author(s):

R J Morrison ◽

J D Raymond ◽

J R Zunt ◽

J K Lim ◽

M J Simmons

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

The Other ◽

X Chromosomes ◽

Multiple Factors ◽

Spontaneous Formation ◽

Chromosome Attachment ◽

Recombination Experiments ◽

Attachment Process

Abstract Males carrying different X chromosomes were tested for the ability to produce daughters with attached-X chromosomes. This ability is characteristic of males carrying an X chromosome derived from 59b-z, a multiply marked X chromosome, and is especially pronounced in males carrying the unstable 59b-z chromosomes Uc and Uc-lr. Recombination experiments with one of the Uc-lr chromosomes showed that the formation of compound chromosomes depends on two widely separated segments. One of these is proximal to the forked locus and is probably proximal to the carnation locus. This segment may contain the actual site of chromosome attachment. The other essential segment lies between the crossveinless and vermilion loci and may contain multiple factors that influence the attachment process.

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MATERNALLY INFLUENCED EMBRYONIC LETHALITY: ALLELE SPECIFIC GENETIC RESCUE AT A FEMALE FERTILITY LOCUS IN DROSOPHILA MELANOGASTER

Canadian Journal of Genetics and Cytology ◽

10.1139/g76-092 ◽

1976 ◽

Vol 18 (4) ◽

pp. 773-781 ◽

Cited By ~ 6

Author(s):

Patricia Romans ◽

R. B. Hodgetts ◽

D. Nash

Keyword(s):

Drosophila Melanogaster ◽

Embryonic Development ◽

X Chromosome ◽

Maternal Effect ◽

Female Offspring ◽

The Other ◽

Genetic Rescue ◽

Homozygous Mutant ◽

Allele Specific ◽

Normal Males

A new locus, mel(l)R1, with a maternal effect on embryonic development, has been mapped at about 0.5 on the X chromosome of Drosophila melanogaster and localized cytologically between bands 2D6 and 3A1. Genotypically mutant embryos die if produced by homozygous mutant females but survive if produced by heterozygous females. Two mutant alleles have been isolated. One of these is genetically rescuable: when homozygous mutant females are mated to mutant males, all the embryos die, but when these females are mated to normal males, female offspring are produced. The other allele is not rescuable. Genetic rescue is dominant at this locus since females heterozygous for the two mutant alleles produce female offspring in crosses to normal males.

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X-LINKED FEMALE-STERILE LOCI IN DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/113.3.695 ◽

1986 ◽

Vol 113 (3) ◽

pp. 695-712

Author(s):

Norbert Perrimon ◽

Dawson Mohler ◽

Lee Engstrom ◽

A P Mahowald

Keyword(s):

Drosophila Melanogaster ◽

Embryonic Development ◽

X Chromosome ◽

Maternal Effect ◽

The Other ◽

Drosophila Genome ◽

Relative Contribution ◽

Clone Analysis ◽

Single Allele ◽

Lethal Genes

ABSTRACT We have examined the number of X-linked loci specifically required only during oogenesis. Complementation analyses among female-sterile (fs) mutations obtained in two mutagenesis screens—Gans' and Mohler's—indicate that any fs locus represented by two or more mutant alleles in Gans' collection are usually present in Mohler's collection. However, when a locus is represented by a single allele in one collection, it is generally not present in the other collection. We propose that this discrepancy is due to the fact that most "fs loci" represented by less than two mutant alleles are, in fact, vital (zygotic lethal) genes, and that the fs alleles are hypomorphic mutations of such genes. In support of this hypothesis we have identified lethal alleles at 12 of these "fs loci." The present analysis has possibly identified all maternal-effect lethal loci detectable by mutations on the X chromosome and has allowed us to reevaluate the number of "ovary-specific fs" loci in the Drosophila genome. Finally, germline clone analysis of a large number of fs mutations was performed in order to estimate the relative contribution of germline and somatic cell derivatives to oogenesis and to embryonic development. All the maternal-effect lethal loci tested are germline-dependent.

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VERMILION-DEFICIENCY

The Journal of General Physiology ◽

10.1085/jgp.1.6.645 ◽

1919 ◽

Vol 1 (6) ◽

pp. 645-656 ◽

Cited By ~ 9

Author(s):

Calvin B. Bridges

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

The Other ◽

Crossing Over ◽

Actual Length ◽

Eye Color ◽

Lethal Action ◽

Recessive Mutations ◽

Slight Rise ◽

The Individual

In May, 1916, a culture of Drosophila melanogaster showed that a new sex-linked lethal had arisen. The linkage relations indicated that the position of the lethal was in the neighborhood of the sex-linked recessive "vermilion," whose locus in the X chromosome is at 33.0. When females heterozygous for the lethal were outcrossed to vermilion males, all the daughters that received the lethal-bearing chromosome showed vermilion eye-color, though, from the pedigree, vermilion was known to be absent from the ancestry of the mother. The lethal action and the unexpected appearance of vermilion both suggested that this was another instance of the phenomenon called "deficiency;" that is, the loss or "inactivation" of the genes of a section of the X chromosome. The lethal action would then be due to the deficient region including one or more genes necessary for the life of the individual. The appearance of vermilion in females carrying only one vermilion gene would be explainable on the ground that the deficient-bearing females are virtually haploid for the region including the vermilion locus. Linkage tests showed that the amount of crossing over in the neighborhood of the deficiency was cut down by about five units. Part of this may be attributed to the actual length of the "deficient" region, within which it is probable that no crossing over occurs, and part (probably most) to an alteration in the synaptic relations in the regions immediately adjacent. In more remote regions there was no disturbance or perhaps a slight rise in the frequency of crossing over. Both the local fall and the possible rise in more distant regions would seem to argue that a "pucker" at synapsis had been caused by an actual shortening of the deficient chromosome. That the deficient region extends to the left of the locus of vermilion was indicated by a test in which it was observed that the presence of an extra piece of chromosome including the loci for vermilion and sable ("vermilion-sable duplication") did not neutralize the lethal action of the deficiency. Haploid tests with the other recessive mutations in the neighborhood of vermilion showed that the deficiency was not extensive enough to include their loci. Cytological preparations were made but were unsatisfactory. The stock was finally lost, apparently as the result of injurious action upon viability, fertility, and productivity by the deficiency.

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A COMPARISON OF HEAT AND INTERCHROMOSOMAL EFFECTS ON RECOMBINATION AND INTERFERENCE IN DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/89.1.65 ◽

1978 ◽

Vol 89 (1) ◽

pp. 65-77

Author(s):

R F Grell

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

Thermal Dissociation ◽

Temporal Sequence ◽

The Other ◽

Centromeric Heterochromatin ◽

Drosophila Genome ◽

Chromosome 2 ◽

Independent Control ◽

Order Of Magnitude

ABSTRACT Heat and interchromosomal effects on recombination have been compared for 23 regions comprising the predominantly euchromatic portions of the five arms of the Drosophila genome. Patterns of response are strikingly similar, with both modifiers causing proximal and distal increases and minimal effects in the middle of the arms. Changes in interference for the same regions in the presence of the two modifiers reveal little similarity, except for the X chromosome. The question of independent control of interference and recombination, as well as alternatives for their temporal sequence, is discussed. Recombination response to the two modifiers in the centric heterochromatin of chromosoaime 2 is markedly different from that found in euchromatin. The interchromosomal effect is absent here, whereas heat induces an increase roughly an order of magnitude greater than that found in euchromatin and totally unlike the lack of response in the proximal heterochromatin of the X chromosome. It is proposed that the sequestering of DNA satellite I (thermal dissociation 9-20° lower than that of the other major satellites) in the centromeric heterochromatin of chromosome 2 (but not in X or 3) may account for the increase.

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THE RELATION OF EXCHANGE TO NONDISJUNCTION IN HETEROLOGOUS CHROMOSOME PAIRS IN THE DROSOPHILA FEMALE

Genetics ◽

10.1093/genetics/88.3.499 ◽

1978 ◽

Vol 88 (3) ◽

pp. 499-503

Author(s):

E Novitski

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

Independent Set ◽

The Other ◽

Crossing Over

ABSTRACT An analysis of the relationships in Drosophila melanogaster between one set of homologues (third chromosome) undergoing crossing over and a second, independent set (X chromosome) undergoing nondisjunction shows that the nondisjunctional set almost invariably segregates from one of the members of the crossover set and not the other. The results seem contradictory to the expectations based on the "distributive pairing hypothesis" according to which nondisjunctional (i.e., noncrossover) elements form a "distributive pool" whose members behave independently of those which have been involved in exchange.

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A COMPARISON OF MUTATION RATES FOR SPECIFIC LOCI AND CHROMOSOME REGIONS IN DYSGENIC HYBRID MALES OF DROSOPHILA MELANOGASTER

Genetics ◽

10.1093/genetics/106.1.85 ◽

1984 ◽

Vol 106 (1) ◽

pp. 85-94

Author(s):

Michael J Simmons ◽

John D Raymond ◽

Nancy A Johnson ◽

Thomas M Fahey

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

The Other ◽

Hybrid Dysgenesis ◽

P Element ◽

Mutation Rates ◽

P Elements ◽

White Locus ◽

Insertion Mutations ◽

Chromosome Regions

ABSTRACT The mutation rates of specific loci and chromosome regions were estimated for two types of dysgenic hybrid males. These came from crosses between P or Q males and M females in the P-M system of hybrid dysgenesis. The M × P hybrids were the more mutable for each of the loci and chromosome regions tested. The Beadex locus was highly mutable in these hybrids but did not mutate at all in the sample of gametes from the M × Q hybrids. The singed locus had 75% of the mutability of Beadex in the M × P hybrids; it was also mutable in the M × Q hybrids. The white locus was only slightly mutable in the M × P hybrids and not at all mutable in the M × Q hybrids. The mutations in singed and white probably arose from the insertion of P elements into these loci; the mutations at Beadex probably involved the action of a P element located near this locus on the X chromosome of the P strain that was used in the experiments. Mutations in two chromosome regions, one including the zeste-white loci and the other near the miniature locus, were much more frequent in the M × P hybrids than in the M × Q hybrids. These mutations also probably arose from P element insertions. The implication is that insertion mutations occur infrequently in the M × Q hybrids, possibly because most of the P elements they carry are defective. In M × P hybrids, there is variation among loci with respect to P elements mutagenesis, indicating that P elements possess a degree of insertional specificity.

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COM, a Heterochromatic Locus Governing the Control of Independent Endogenous Retroviruses From Drosophila melanogaster

Genetics ◽

10.1093/genetics/164.2.501 ◽

2003 ◽

Vol 164 (2) ◽

pp. 501-509 ◽

Cited By ~ 2

Author(s):

Sophie Desset ◽

Carine Meignin ◽

Bernard Dastugue ◽

Chantal Vaury

Keyword(s):

Drosophila Melanogaster ◽

X Chromosome ◽

Somatic Cells ◽

Endogenous Retrovirus ◽

Endogenous Retroviruses ◽

The Other ◽

Genetic Determinant ◽

Genetic Determinants

Abstract ZAM and Idefix are two endogenous retroviruses whose expression is tightly controlled in Drosophila melanogaster. However, a line exists in which this control has been perturbed, resulting in a high mobilization rate for both retroviruses. This line is called the U (unstable) line as opposed to the other S (stable) lines. In the process of analyzing this control and tracing the genetic determinant involved, we found that ZAM and Idefix expression responded to two types of controls: one restricting their expression to specific somatic cells in the ovaries and the other silencing their expression in S lines but permitting it in U lines. While studying this second control in the U or S backgrounds, we found that the heterochromatic locus 20A2-3 on the X chromosome, previously implicated in the regulation of a third retroelement, gypsy, also controlled both ZAM and Idefix. We report here that genetic determinants necessary for endogenous retrovirus silencing occur at the 20A2-3 locus, which we call COM, for centre organisateur de mobilisation. We propose that if this point of control becomes mutated during the life of the fly, it may trigger processes reactivating dormant endogenous retroviruses and thus bring about sudden bursts of mobilization.

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Epistatic Control of Non-Mendelian Inheritance in Mouse Interspecific Crosses

Genetics ◽

10.1093/genetics/143.4.1739 ◽

1996 ◽

Vol 143 (4) ◽

pp. 1739-1752 ◽

Cited By ~ 2

Author(s):

Xavier Montagutelli ◽

Rowena Turner ◽

Joseph H Nadeau

Keyword(s):

X Chromosome ◽

Genetic Basis ◽

Mendelian Inheritance ◽

The Other ◽

Interspecific Crosses ◽

Chromosome 2 ◽

Mus Spretus ◽

F1 Hybrid ◽

Strong Deviation ◽

Marker Loci

Abstract Strong deviation of allele frequencies from Mendelian inheritance favoring Mus spretus-derived alleles has been described previously for X-linked loci in four mouse interspecific crosses. We reanalyzed data for three of these crosses focusing on the location of the gene(s) controlling deviation on the X chromosome and the genetic basis for incomplete deviation. At least two loci control deviation on the X chromosome, one near Xist (the candidate gene controlling X inactivation) and the other more centromerically located. In all three crosses, strong epistasis was found between loci near Xist and marker loci on the central portion of chromosome 2. The mechanism for this deviation from Mendelian expectations is not yet known but it is probably based on lethality of embryos carrying particular combinations of alleles rather than true segregation distortion during oogenesis in F1 hybrid females.

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