Systematics and the Origin of Species On Ernst Mayr's 100th Anniversary (2005) / Chapter Skim
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16 Genetics and Genomics of Drosophila Mating Behavior--TRUDY F. C. MACKAY, STEFANIE L. HEINSOHN, RICHARD F. LYMAN, AMANDA J. MOEHRING, THEODORE J. MORGAN, AND STEPHANIE M. ROLLMANN
16 Genetics and Genomics of Drosophila Mating Behavior--TRUDY F. C. MACKAY, STEFANIE L. HEINSOHN, RICHARD F. LYMAN, AMANDA J. MOEHRING, THEODORE J. MORGAN, AND STEPHANIE M. ROLLMANN
Pages 307-331
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From page 307... ...
In contrast to recent progress in understanding the genetic basis of postzygotic isolat ing mechanisms, little is known about the genetic architecture of sexual isolation. Here, we have subjected Drosophila melano gaster to 29 generations of replicated divergent artificial selection for mating speed.
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Several species pairs are only partially reproductively isolated, producing fertile hybrids that can be backcrossed to one of the parental species to generate segregating backcross mapping populations. Furthermore, Drosophila melanogaster is a model organism with excellent genetic and genomic resources that are ideal for genetically dissecting complex traits, including the ability to clone chromosomes, replicate genotypes, and rear large numbers of individuals under uniform environmental conditions; publicly available mutations and deficiency stocks useful for mapping; abundant segregating variation in natural populations that can readily be selected in the laboratory to produce divergent phenotypes a complete well annotated genome sequence; and several platforms for whole-genome transcriptional profiling.
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. SEXUAL ISOLATION AMONG SPECIES Despite the wealth of knowledge regarding genetic mechanisms that affect Drosophila courtship behavior, we know virtually nothing of the
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In the first species pair, sexual isolation is attributable to female discrimination against males of the sibling species; males readily court females of either species. QTLs affecting male traits against which D
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. Recombination mapping of third-chromosome QTLs using visible morphological markers revealed at least four epistatic QTLs affecting Z male mating success and at least two QTLs affecting Z female mating preference (Ting et al., 2001)
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. Here, we describe the results of 29 generations of replicated selection for increased and decreased mating speed from a large heterogeneous base population and the analysis of the whole genome transcriptional response to artificial selection.
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Quantitative Genetic Analysis of Selection Response Realized heritability of copulation latency was computed for each replicate from the regression of cumulated response (as a deviation from the control) on cumulated selection differential (Falconer and Mackay, 1996)
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In the latter case, one would expect common alleles affecting variation in transcript abundance to have the same effect in both selection lines. Therefore, contrast statements were used to assess whether transcript abundance for probe sets with L and/or S × L terms at or below the Q = 0.001 threshold was significantly different between the two Fast lines and the two Slow lines, both pooled over sexes, and for each sex separately.
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Reduced mating speed could be attributable to reduced male copulation latency, reduced female receptivity, or both. At generations 18, 20, and 21, we assessed copulation latency when Fast females of each replicate were paired with Slow males and when Slow females of each replicate were paired with Fast males.
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316 , t on es 1 (E) mal lines; selection )
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Transcriptional Response to Selection for Copulation Latency We assessed transcript abundance at the time of selection for the Fast and Slow selection lines, using Affymetrix high-density oligonucleotide whole genome microarrays. Raw expression data are given in Table 4, which is published as supporting information on the PNAS web site.
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Thus, there was little evidence for nonrandom distribution of probe sets with significantly altered transcript abundance within each chromosome arm. The probe sets that were up-regulated in each comparison of Fast and Slow selection lines fell into all major biological process and molecular function Gene Ontology (GO)
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Drosophila Mating Behavior / 319 FIGURE 16.2 Relative log2 fold changes in transcript abundance in Fast vs. Slow selection lines.
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For example, more probe sets than expected that are up-regulated in Fast relative to Slow females fall into the physiological biological process and binding molecular function categories. On the other hand, there are fewer probe sets than expected in the regulation biological process and transcription regulator categories that exhibit significant changes in transcript abundance in multiple comparisons of selection lines (Tables 16.1 and 16.2)
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322 from )
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was also altered between these selection lines. Novel candidate genes affecting mating behavior implicated by changes in transcript abundance between selection lines include 15 of the 39 members of the predicted family of odorant binding proteins; genes involved in circadian rhythm, larval locomotion, learning and memory, and olfactory behavior; and genes involved in neurogenesis (Table 16.3)
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TABLE 16.3 Genes with Altered Transcript Abundance in Lines Selected for Increased and Decreased Copulation Latency Trait Genea Comparison Fold Olfactory-binding protein Obp8a F > S 1.37 Obp18a S > F 1.24 Obp19c S& > F& 1.51 Obp44a S& > F& 1.30 Obp50b F( > S( 1.39 Obp50c F( > S( 1.39 Obp51a F( > S( 1.28 Obp56a S& > F& 1.94 Obp56d S& > F&, F( > S( 1.13, 1.25 Obp57a S > F 1.37 Obp57b F > S 1.39 Obp57c S& > F& 1.18 Obp83c S& > F& 1.75 Obp99b S > F 2.07 Obp99c F > S 1.09 Circadian rhythm Pka-R2 F& > S& 1.10 Cry F( > S( 1.20 Clk F( > S( 1.19 sgg F( > S( 1.19 tim S > F 1.48 Pdf S > F 1.28 Larval locomotion sbb S > F 1.30 for S > F 1.07 Learning and memory Fas2 S& > F& 1.18 Pka-R1 S& > F& 1.11 pum F& > S& 1.14 Olfaction Van F& > S& 1.26 Neurogenesis pbl F& > S& 1.07 stc F& > S& 1.04 lola S& > F& 1.15 Ras85D F& > S& 1.11 robo S& > F& 1.35 Dl F& > S& 1.25 disco S& > F& 1.73 ab S > F 1.31 aay S > F 1.06 dlg1 S > F 1.17 sktl S > F 1.20 dally S > F 1.23 pnt F > S 1.51 elav S > F 1.35 numb S > F 1.43 cpo S > F 1.45 Catecholamine metabolism Dat S& > F& 1.10 Regulation of insulin receptor pathway foxo F( > S( 1.28 Hsp90 chaperone, stress response Hsp83 F( > S( 1.14 Protein folding, stress response Hsp27 F& > S& 1.14
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Because we did not observe inbreeding depression for mating speed, as would be expected if deleterious alleles were recessive, we infer that the most likely cause of asymmetry was the segregation of low-frequency alleles affecting increased female copulation latency in the base population. The transcriptional response to selection for mating speed was profound, with >3,700 probe sets (21% of the total number on the microarray)
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CONCLUSION In the future, functional studies will be required to test the extent to which transcript profiling of divergent selection lines accurately predicts genes that directly affect the selected trait. One such test is to assess whether mutations at candidate genes implicated by the analysis of differential transcript abundance affect the trait.
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Another functional test is to perform quantitative complementation tests of mutations at the candidate genes with the selection lines, to assess whether coregulation of transcription translates to epistasis at the level of trait phenotype. Mutations are not available for many of the genes with altered transcript abundance in response to selection (e.g., the odorant-binding proteins)
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(1995) Cost of mating in Drosophila melanogaster females is mediated by male accessory gland products.
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(1996) Polygenic mutation in Drosophila melanogaster: Genetic interactions between selection lines and candidate quantitative trait loci.
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(2000) Deficiency mapping of quantitative trait loci affecting longevity in Drosophila melanogaster.
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(1995) Sexual isolation in Drosophila melanogaster: A possible case for incipient speciation.
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