INCIPIENT SPECIATION BY SEXUAL ISOLATION IN<i>DROSOPHILA MELANOGASTER</i>: VARIATION IN MATING PREFERENCE AND CORRELATION BETWEEN SEXES

Hollocher, Hope; Ting, Chau‐Ti; Pollack, Francine; Wu, Chung‐I

doi:10.1111/j.1558-5646.1997.tb03965.x

Cited by 88 publications

(165 citation statements)

References 28 publications

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“…A suggestion may be that the divergence in the transcription factors (TFs) or trans-acting components on chromosome II is less than that of TFs on chromosome III, because the Z and M races separated. Hollocher et al (11) and Ting et al (14) have reported similar chromosome-wide differences. Between the Z and M races, the contribution to behavioral differentiation is substantially larger for chromosome III than for chromosome II.…”

Section: Discussionsupporting

confidence: 55%

“…The Zimbabwe race of D. melanogaster vis-à-vis the cosmopolitan populations are thus well suited to such a purpose. Females from Z lines (for Zimbabwe) do not readily mate with males from M lines (for melanogaster of the cosmopolitan type), whereas the reciprocal crosses experience much weaker or no discrimination (11).…”

mentioning

confidence: 99%

“…These two lines have been extensively analyzed for their behavioral, physiological, and molecular divergence (11)(12)(13)(14)(15)(16)(17)(18). The purpose of this study is to dissect the genetic architecture of transcription regulation.…”

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confidence: 99%

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Complex genetic interactions underlying expression differences between Drosophila races: Analysis of chromosome substitutions

Wang

McPeek³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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Regulation of gene expression is usually separated into cis and trans components. The separation may become artificial if much of the variation in expression is under multigenic and epistatic (e.g., cis-bytrans) control. There is hence a need to quantify the relative contribution of cis, trans, and cis-by-trans effects on expression divergence at different levels of evolution. To do so across the whole genome, we analyzed the full set of chromosome-substitution lines between the two behavioral races of Drosophila melanogaster. Our observations: (i) Only Ϸ3% of the genes with an expression difference are purely cis regulated. In fact, relatively few genes are governed by simple genetics because nearly 80% of expression differences are controlled by at least two chromosomes. (ii) For 14% of the genes, cis regulation does play a role but usually in conjunction with trans regulation. This joint action of cis and trans effects, either additive or epistatic, is referred to as inclusive cis effect. (iii) The percentage of genes with inclusive cis effect increases to 32% among genes that are strongly differentiated between the two races. (iv) We observed a nonrandom distribution of trans-acting factors, with a substantial deficit on the second chromosome. Between Drosophila racial groups, trans regulation of expression difference is extensive, and cis regulation often evolves in conjunction with trans effects.K nowledge of the genetics of complex traits is fundamental to modern medicine, agriculture, and evolutionary biology. Among all complex traits, gene expression as phenotype may be most amenable to genetic analysis. The first question about expression regulation naturally is whether there is a cis component and how strong the cis component is. (cis regulation refers to the control of expression by the gene itself whereas trans regulation refers to the influence of the genetic background.) Many studies have addressed this question at various levels of divergence (1-9). For example, one may measure the expressions of two alleles at the locus of interest in a common genetic background (usually F 1 s) (1, 2, 5). Because the collection of trans-acting factors in the same cellular environment is assumed to affect the two alleles equally, asymmetric allelic expression implies differences due to cis-regulatory divergence. Similarly, expression quantitative trait loci (eQTL) mapping permits inference of cis regulation if the eQTL is mapped closely to the expressed gene itself (6-10).A second question is how strong cis regulation is relative to trans regulation. In the extreme case where most expression variation is controlled by cis-trans interactions (e.g., joint actions of cis elements and transcription factors), the question would not be very meaningful because cis and trans components are both indispensable. It is desirable to explicitly model expression regulation to include cis, trans, and cis-by-trans control. Many kinds of data allow such explicit modeling. The use of large numbers of recombinant strains for express...

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Section: Discussionsupporting

confidence: 55%

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confidence: 99%

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Complex genetic interactions underlying expression differences between Drosophila races: Analysis of chromosome substitutions

Wang

McPeek³

et al. 2008

Proc. Natl. Acad. Sci. U.S.A.

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“…The former race occurs throughout the world, whereas the latter has been described from Zimbabwe, Zambia, and Botswana. In some parts of Africa, such as Zimbabwe, individuals of both races appear to be sympatric (Hollocher et al, 1997b;Fang et al, 2002;Takahashi and Ting, 2004). These races show marked but asymmetric sexual isolation: Zimbabwe-type females discriminate strongly against cosmopolitan males, whereas the reciprocal mating occurs readily (Wu et al, 1995;Hollocher et al, 1997a).…”

Section: Modalities Of Chemosensory Isolationmentioning

confidence: 99%

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

2008

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Chemosensory speciation is characterized by the evolution of barriers to genetic exchange that involve chemosensory systems and chemical signals. Here, we review some representative studies documenting chemosensory speciation in an attempt to evaluate the importance and the different aspects of the process in nature and to gain insights into the genetic basis and the evolutionary mechanisms of chemosensory trait divergence. Although most studies of chemosensory speciation concern sexual isolation mediated by pheromone divergence, especially in Drosophila and moth species, other chemically based behaviours (habitat choice, pollinator attraction) can also play an important role in speciation and are likely to do so in a wide range of invertebrate and vertebrate species. Adaptive divergence of chemosensory traits in response to factors such as pollinators, hosts and conspecifics commonly drives the evolution of chemical prezygotic barriers. Although the genetic basis of chemosensory speciation remains largely unknown, genomic approaches to chemosensory gene families and to enzymes involved in biosynthetic pathways of signal compounds now provide new opportunities to dissect the genetic basis of these complex traits and of their divergence among taxa.

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“…Subsequent studies revealed strong sexual isolation between these strains (Wu et al, 1995;Hollocher et al, 1997a, b) but little postzygotic isolation (Alipaz et al, 2005), indicating an early stage of speciation. Genetic analyses revealed that both male and female traits involved in assortative mating were most strongly influenced by chromosome 3 and least of all by the X chromosome (for example, Wu et al, 1995;Hollocher et al, 1997b;Ting et al, 2001;Michalak et al, 2007).…”

Section: Speciation and Sex-linked Genesmentioning

confidence: 99%

Speciation through evolution of sex-linked genes

2008

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Identification of genes involved in reproductive isolation opens novel ways to investigate links between stages of the speciation process. Are the genes coding for ecological adaptations and sexual isolation the same that eventually lead to hybrid sterility and inviability? We review the role of sex-linked genes at different stages of speciation based on four main differences between sex chromosomes and autosomes; (1) relative speed of evolution, (2) non-random accumulation of genes, (3) exposure of incompatible recessive genes in hybrids and (4) recombination rate. At early stages of population divergence ecological differences appear mainly determined by autosomal genes, but fastevolving sex-linked genes are likely to play an important role for the evolution of sexual isolation by coding for traits with sex-specific fitness effects (for example, primary and secondary sexual traits). Empirical evidence supports this expectation but mainly in female-heterogametic taxa. By contrast, there is clear evidence for both strong X-and Z-linkage of hybrid sterility and inviability at later stages of speciation. Hence genes coding for sexual isolation traits are more likely to eventually cause hybrid sterility when they are sex-linked. We conclude that the link between sexual isolation and evolution of hybrid sterility is more intuitive in male-heterogametic taxa because recessive sexually antagonistic genes are expected to quickly accumulate on the X-chromosome. However, the broader range of sexual traits that are expected to accumulate on the Z-chromosome may facilitate adaptive speciation in female-heterogametic species by allowing male signals and female preferences to remain in linkage disequilibrium despite periods of gene flow.

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INCIPIENT SPECIATION BY SEXUAL ISOLATION INDROSOPHILA MELANOGASTER: VARIATION IN MATING PREFERENCE AND CORRELATION BETWEEN SEXES

Cited by 88 publications

References 28 publications

Complex genetic interactions underlying expression differences between Drosophila races: Analysis of chromosome substitutions

Complex genetic interactions underlying expression differences between Drosophila races: Analysis of chromosome substitutions

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

Speciation through evolution of sex-linked genes

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