Two distinct genomic regions, harbouring the period and fruitless genes, affect male courtship song in Drosophila montana

Lagisz, Malgorzata; Wen, Shuo‐Yang; Routtu, Jarkko; Klappert, Kirsten; Mazzi, Dominique; Morales‐Hojas, Ramiro; Ma, Schäfer; Vieira, Jorge; Hoikkala, Anneli; Ritchie, Michael G.; Butlin, Roger K.

doi:10.1038/hdy.2011.129

Cited by 11 publications

(14 citation statements)

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“…This has been further emphasised with the finding that RNAi-mediated knockdown of fru extinguishes male courtship in the cockroach Blattella germanica, suggesting that the large role fru has in the production of male sexual behaviours has been conserved for at least a large portion of insect evolution (Clynen et al, 2011). Despite this, many of the courtship behaviours influenced by fru are known to be species-specific, and fru has been implicated as a potential candidate gene for species-specific divergence in QTL (quantitative trait loci) studies (Gleason and Ritchie, 2004;Lagisz et al, 2012). Furthermore, a recent study of the fru connector region using three species of fruit fly (Genus: Anastrepha) found evidence of positive selection based on both sequence differences and population gene frequencies, suggesting that fru may contribute to species-specific differences in male courtship behaviour of Anastrepha species (Sobrinho and de Brito, 2010).…”

Section: Introductionmentioning

confidence: 99%

The evolution of novelty in conserved genes; evidence of positive selection in the Drosophila fruitless gene is localised to alternatively spliced exons

et al. 2013

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There has been much debate concerning whether cis-regulatory or coding changes are more likely to produce evolutionary innovation or adaptation in gene function, but an additional complication is that some genes can dramatically diverge through alternative splicing, increasing the diversity of gene function within a locus. The fruitless gene is a major transcription factor with a wide range of pleiotropic functions, including a fundamental conserved role in sexual differentiation, species-specific morphology and an important influence on male sexual behaviour. Here, we examine the structure of fruitless in multiple species of Drosophila, and determine the patterns of selective constraint acting across the coding region. We found that the pattern of selection, estimated from the ratio of non-synonymous to synonymous substitutions, varied considerably across the gene, with most regions of the gene evolutionarily conserved but with several regions showing evidence of divergence as a result of positive selection. The regions that showed evidence of positive selection were found to be localised to relatively consistent regions across multiple speciation events, and are associated with alternative splicing. Alternative splicing may thus provide a route to gene diversification in key regulatory loci.

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Section: Introductionmentioning

confidence: 99%

The evolution of novelty in conserved genes; evidence of positive selection in the Drosophila fruitless gene is localised to alternatively spliced exons

et al. 2013

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“…The simulated trait effect size was based on a QTL detected for song variation in crosses between North American and Finnish D. montana (Colorado and Oulanka, that is, a different population from North America) Schafer et al, 2010;Lagisz et al, 2012). We failed to detect QTL for the same traits and genomic positions as the between-population study.…”

Section: Discussionmentioning

confidence: 97%

“…We failed to detect QTL for the same traits and genomic positions as the between-population study. These were for IPI and pulse number on the X chromosome, and FRE, CN and IPI on chromosome 2 (Lagisz et al, 2012). We then attempted to implicate the same chromosomes using the chromosome-partitioning analysis.…”

Section: Discussionmentioning

confidence: 99%

“…We compare the within-population QTL analysis of song variation with previous work that identified QTL influencing courtship song by using between-population outbred crosses of D. montana (from Oulanka, Finland and Colorado, N. America). The detected QTL were on two chromosomes (X and 2) and one candidate gene was potentially associated with each QTL (per and fru, respectively) (Schafer et al, 2010;Lagisz et al, 2012), although it has not been confirmed whether these or other genes under the peaks are responsible for the phenotypic effects.…”

Section: Introductionmentioning

confidence: 99%

“…We performed simulations using custom scripts to estimate the probability of detecting, within the Vancouver pedigree, a QTL of similar magnitude to the one detected in the inter-population study (Lagisz et al, 2012). We used sexaveraged map distances and simulated a trait with heritability of 0.30, half the variance of which was caused by a single QTL in the middle of chromosome 2 (V a = 0.15, V qtl = 0.15, V residual = 0.70).…”

Section: Power Analysismentioning

confidence: 99%

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The genetic architecture of sexually selected traits in two natural populations of Drosophila montana

et al. 2015

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We investigated the genetic architecture of courtship song and cuticular hydrocarbon traits in two phygenetically distinct populations of Drosophila montana. To study natural variation in these two important traits, we analysed within-population crosses among individuals sampled from the wild. Hence, the genetic variation analysed should represent that available for natural and sexual selection to act upon. In contrast to previous between-population crosses in this species, no major quantitative trait loci (QTLs) were detected, perhaps because the between-population QTLs were due to fixed differences between the populations. Partitioning the trait variation to chromosomes suggested a broadly polygenic genetic architecture of within-population variation, although some chromosomes explained more variation in one population compared with the other. Studies of natural variation provide an important contrast to crosses between species or divergent lines, but our analysis highlights recent concerns that segregating variation within populations for important quantitative ecological traits may largely consist of small effect alleles, difficult to detect with studies of moderate power.

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Sexual selection on song and cuticular hydrocarbons in two distinct populations of Drosophila montana

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Wicker-Thomas

Butlin

et al. 2011

Ecology and Evolution

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Sexual selection has the potential to contribute to population divergence and speciation. Most studies of sexual selection in Drosophila have concentrated on a single signaling modality, usually either courtship song or cuticular hydrocarbons (CHCs), which can act as contact pheromones. We have examined the relationship between both signal types and reproductive success using F1–3 offspring of wild-collected flies, raised in the lab. We used two populations of the Holarctic species Drosophila montana that represent different phylogeographic clades that have been separate for ca. 0.5 million years (MY), and differ to some extent in both traits. Here, we characterize the nature and identify the targets of sexual selection on song, CHCs, and both traits combined within the populations. Three measures of courtship outcome were used as fitness proxies. They were the probability of mating, mating latency, and the production of rejection song by females, and showed patterns of association with different traits that included both linear and quadratic selection. Courtship song predicted courtship outcome better than CHCs and the signal modalities acted in an additive rather than synergistic manner. Selection was generally consistent in direction and strength between the two populations and favored males that sang more vigorously. Sexual selection differed in the extent, strength, and nature on some of the traits between populations. However, the differences in the directionality of selection detected were not a good predictor of population differences. In addition, a character previously shown to be important for species recognition, interpulse interval, was found to be under sexual selection. Our results highlight the complexity of understanding the relationship between within-population sexual selection and population differences. Sexual selection alone cannot predict differences between populations.

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Two distinct genomic regions, harbouring the period and fruitless genes, affect male courtship song in Drosophila montana

Cited by 11 publications

References 53 publications

The evolution of novelty in conserved genes; evidence of positive selection in the Drosophila fruitless gene is localised to alternatively spliced exons

The evolution of novelty in conserved genes; evidence of positive selection in the Drosophila fruitless gene is localised to alternatively spliced exons

The genetic architecture of sexually selected traits in two natural populations of Drosophila montana

Sexual selection on song and cuticular hydrocarbons in two distinct populations of Drosophila montana

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