Behavioural elements and sensory cues involved in sexual isolation between<i>Drosophila melanogaster</i>strains

Grillet, Micheline; Ferveur, Jean‐François; Everaerts, Claude

doi:10.1098/rsos.172060

“…Courtship of Drosophila melanogaster Meigen is one of the best studied behavioural repertoires and is multimodal and complex (Grillet, Ferveur, & Everaerts, ; Pavlou & Goodwin, ). The courtship repertoire within the genus Drosophila Fallén is more variable than is widely appreciated.…”

Section: Introductionmentioning

confidence: 99%

Evolution and diversity of the courtship repertoire in the Drosophila montium species group (Diptera: Drosophilidae)

Chen

¹

,

Chen

²

,

Katoh

³

et al. 2019

J of Evolutionary Biology

View full text Add to dashboard Cite

Changes in elements of courtship behaviour can influence sexual isolation between species. Large‐scale analyses of changes, including loss and gain of courtship elements, across a relatively complete phylogenetic group are rare but needed to understand the significance of such changes, for example whether the gain and loss of courtship elements are essentially arbitrary or equally reversible. In most species of Drosophila, courtship, including singing, mainly occurs before mounting as premounting courtship. The Drosophila montium species group is unusual because loss of premounting courtship and gain of post‐mounting one has been detected in this group. Here, we provide an extensive analysis on the courtship repertoire and songs of 42 species in this group. Synchronously captured video and audio recordings were analysed to describe courtship patterns and male courtship songs, and changes were analysed in a phylogenetic context. Ancestral state reconstruction suggests that a gain of post‐mounting courtship singing at the ancestor of this species group has been accompanied by a concurrent decrease in the incidence of premounting courtship singing and has led to subsequent further decrease and eventually complete loss of premounting courtship song in several lineages. Alongside this evolutionary trend towards post‐mounting courtship, sine song and a special type of “high pulse repetition song” have become more widely used for courtship during species diversification in the montium group. It is likely that the elaboration of post‐mounting courtship behaviours is associated with changes in the relative importance of pre‐ and post‐mounting components of mating systems, such as sperm competition or cryptic female choice.

show abstract

“…Based on this, we believe that the origin of assortative mating between Z-and M-type females is linked to their divergent perception and/or integration of male cues. Indeed, while Z females only respond to a precise and complete multisensory set of signal provided by homotypic males (GRILLET et al 2012;GRILLET et al 2018), M-type females only need part of these cues to be sexually receptive (COLEGRAVE et al 2000;GRILLET 2009;MA et al 2010;GRILLET et al 2012;GRILLET et al 2018).…”

Section: Discussionmentioning

confidence: 99%

“…Moreover, the experimental variation of the male tricosene ratio (7T/5T) only partly affects mating preference in Z females (GRILLET et al 2012). This suggests that the asymmetrical sexual isolation between Z and M populations involves female perception of other male-non acoustic-sensory cues (COLEGRAVE et al 2000;GRILLET et al 2012;GRILLET et al 2018).The hypothesis of sexual isolation based on multiple sensory signals and/or systems is somewhat supported by the finding that the divergence of mating preference between Z and M populations depend on a highly polygenic control (HOLLOCHER et al 1997;TING et al 2001; KAUER AND SCHLÖTTERER 2004). Also, among several genes showing matingdependent variation of expression, desat2 is up-regulated in Z flies, but down-regulated in M flies, after mating (MICHALAK et al 2007).…”

mentioning

confidence: 99%

See 1 more Smart Citation

Experimental introgression to evaluate the impact of sex specific traits onDrosophila melanogasterincipient speciation

Cortot

¹

,

Farine

²

,

Houot

³

et al. 2019

Preprint

Self Cite

0

View full text Add to dashboard Cite

Sex specific traits are involved in speciation but it is difficult to determine whether their variation initiates or reinforces sexual isolation. In some insects, speciation depends of the rapid change of expression in desaturase genes coding for sex pheromones. Two closely related desaturase genes are involved in Drosophila melanogaster pheromonal communication: desat1 affects both the production and the reception of sex pheromones while desat2 is involved in their production in flies of Zimbabwe populations. There is a strong asymmetric sexual isolation between Zimbabwe populations and all other "Cosmopolitan" populations: Zimbabwe females rarely copulate with Cosmopolitan males whereas Zimbabwe males readily copulate with all females. All populations express desat1 but only Zimbabwe strains show high desat2 expression. To evaluate the impact of sex pheromones, female receptivity and desat expression on the incipient speciation process between Zimbabwe and Cosmopolitan populations, we introgressed the Zimbabwe genome into a Cosmopolitan genome labelled with the white mutation, using a multi-generation procedure. The association between these sex-specific traits was determined during the procedure. The production of pheromones was largely dissociated between the sexes. The copulation frequency (but not latency) was highly correlated with the female-but not with the male-principal pheromones. We finally obtained two stable white lines showing Zimbabwe-like sex pheromones, copulation discrimination and desat expression. Our study indicates that the variation of sex pheromones and of mating discrimination depend of distinct-yet overlapping-sets of genes in each sex suggesting that their cumulated effects participate to reinforce the speciation process. FANG et al. 2002). However, the expression of desat2 is not totally abolished in M strains, but seems to be "only" strongly repressed (MICHALAK et al. 2007). While the desat2 gene is largely involved in the production of a variant female cuticular hydrocarbon (CH): 5,9-heptacosadiene (5,9HD; (COYNE et al. 1999; DALLERAC et al. 2000), its effect in the increased production of 5-tricosene (5T) in Z males remains unknown (GRILLET et al. 2012).While both Z females and males show high levels of C5-desaturated CHs, in several west-African strains only females-but not males-produce high levels of C5-desaturated CHs (5,9HD in Tai strain; (PECHINE et al. 1988;SUREAU AND FERVEUR 1999). The desat1 gene, flanking desat2, is expressed in all D. melanogaster strains (Z and M) and codes for the production of C7-desaturated CHs in males (7-tricosene = 7T) and in females (7,11heptacosadiene = 7,11HD; (JALLON 1984; WICKER-THOMAS et al. 1997; MARCILLAC et al. 2005a). Surprisingly, desat1 is also involved in the discrimination of sex pheromones and in the emission of other yet unidentified mating cues (MARCILLAC et al. 2005b; BOUSQUET et al. 2012; BOUSQUET et al. 2016). 6The variation of the female heptacosadiene ratio (7,11HD/5,9HD) has apparently no or very little effect on male ...

show abstract

“…Moreover, the experimental variation of the male tricosene ratio (7T/5T) only partly affects mating preference in Z females (Grillet et al 2012). This suggests that the asymmetrical sexual isolation between Z and M populations involves female perception of other male—non acoustic—sensory cues (Colegrave et al 2000; Grillet et al 2012; Grillet et al 2018). The hypothesis of sexual isolation based on multiple sensory signals and/or systems is somewhat supported by the finding that the divergence of mating preference between Z and M populations depends on a highly polygenic control (Hollocher et al 1997; Ting et al 2001; Kauer and Schlötterer 2004).…”

mentioning

confidence: 99%

Experimental Introgression To Evaluate the Impact of Sex Specific Traits onDrosophila melanogasterIncipient Speciation

Cortot

¹

,

Farine

²

,

Houot³

et al. 2019

G3 Genes|Genomes|Genetics

Self Cite

View full text Add to dashboard Cite

Sex specific traits are involved in speciation but it is difficult to determine whether their variation initiates or reinforces sexual isolation. In some insects, speciation depends of the rapid change of expression in desaturase genes coding for sex pheromones. Two closely related desaturase genes are involved in Drosophila melanogaster pheromonal communication: desat1 affects both the production and the reception of sex pheromones while desat2 is involved in their production in flies of Zimbabwe populations. There is a strong asymmetric sexual isolation between Zimbabwe populations and all other “Cosmopolitan” populations: Zimbabwe females rarely copulate with Cosmopolitan males whereas Zimbabwe males readily copulate with all females. All populations express desat1 but only Zimbabwe strains show high desat2 expression. To evaluate the impact of sex pheromones, female receptivity and desat expression on the incipient speciation process between Zimbabwe and Cosmopolitan populations, we introgressed the Zimbabwe genome into a Cosmopolitan genome labeled with the white mutation, using a multi-generation procedure. The association between these sex-specific traits was determined during the procedure. The production of pheromones was largely dissociated between the sexes. The copulation frequency (but not latency) was highly correlated with the female—but not with the male—principal pheromones. We finally obtained two stable white lines showing Zimbabwe-like sex pheromones, copulation discrimination and desat expression. Our study indicates that the variation of sex pheromones and mating discrimination depend of distinct—yet overlapping—sets of genes in each sex suggesting that their cumulated effects participate to reinforce the speciation process.

show abstract

Behavioural elements and sensory cues involved in sexual isolation betweenDrosophila melanogasterstrains

Cited by 13 publications

References 77 publications

Evolution and diversity of the courtship repertoire in the Drosophila montium species group (Diptera: Drosophilidae)

Evolution and diversity of the courtship repertoire in the Drosophila montium species group (Diptera: Drosophilidae)

Experimental introgression to evaluate the impact of sex specific traits onDrosophila melanogasterincipient speciation

Experimental Introgression To Evaluate the Impact of Sex Specific Traits onDrosophila melanogasterIncipient Speciation

Contact Info

Product

Resources

About