Divergent selection on behavioural and chemical traits between reproductively isolated populations of Drosophila melanogaster

Abstract

Speciation is driven by traits that can act to prevent mating between nascent lineages, including male courtship and female preference for male traits. Mating barriers involving these traits evolve quickly because there is strong selection on males and females to maximize reproductive success, and the tight co‐evolution of mating interactions can lead to rapid diversification of sexual behaviour. Populations of Drosophila melanogaster show strong asymmetrical reproductive isolation that is correlated with geographic origin. Using strains that capture natural variation in mating traits, we ask two key questions: which specific male traits are females selecting, and are these traits under divergent sexual selection? These questions have proven extremely challenging to answer, because even in closely related lineages males often differ in multiple traits related to mating behaviour. We address these questions by estimating selection gradients for male courtship and cuticular hydrocarbons for two different female genotypes. We identify specific behaviours and particular cuticular hydrocarbons that are under divergent sexual selection and could potentially contribute to premating reproductive isolation. Additionally, we report that a subset of these traits are plastic; males adjust these traits based on the identity of the female genotype they interact with. These results suggest that even when male courtship is not fixed between lineages, ongoing selection can act on traits that are important for reproductive isolation.

The neurodevelopmental genesalan shepardandNeurogliancontribute to female mate preference in AfricanDrosophila melanogaster

“…Both shep and Nrg regulate neurological development, specifically neural remodeling during metamorphosis, contributing heavily to the formation of higher learning centers, specifically those responsible for processing olfactory signals (Carhan et al, 2005; Chen et al, 2014). This complements a gene ontology analysis of outliers for female mate preference by Coughlan et al (2021) that found significant outliers involved in sensory perception, including three olfactory receptors, as well as genes important for learning and memory, cognition, and neurological development.Both of these analyses are consistent with previous work in these populations of D. melanogaster has suggested a large role for olfaction in female mate preference (Grillet et al, 2012; Moran, 2006; Jin et al, 2022). Given these complementary observations it will be important to understand how differences in Nrg and shep alleles potentially correlation with structural and/or functional changes in the neural networks of females that show high or low mate discrimination preference and whether this is correlelated with the olfactory cues used in mate preference.…”

“…The two male strains used in the experiment are phenotypically indistinguishable, so to be able to tell them apart we placed them on food containing blue food coloring 48 hours prior to the bheavioral assay. This is a non-invasive, robust identification method that does not affect male courtship behavior or female preference (Wu et al, 1995; Hollocher et al, 1997; Coughlan et al, 2021; Serrato-Capuchina et al, 2021; Jin et al, 2022). All behavioral assays were performed in a room held at a constant 20C degrees Celsius and 50% humidity within two hours of the incubator lights turning on to maximize the number of copulations we could observe.…”

“…For our representative African strain we chose Z53 because its behavior profile is well documented and has been consistent across studies (Wu et al, 1995;Hollocher et al, 1997;Moran, 2006;Jin et al, 2022). For our representative non-African strain we chose DGRP882.…”

“…Males were housed individually because group housing can potentially change courtship vigor (Dixon et al 2003). All individuals were allowed to age 7-10 days, before experiments because this is the timeframe that produces the maximum number of matings for the African strains (Jin et al 2022). The two male strains used in the experiment are phenotypically indistinguishable, so to be able to tell them apart we placed them on food containing blue food coloring 48 hours prior to the bheavioral assay.…”

“…This experimental procedure involves crossing strains with divergent behavior to a common mutant background. We chose to use the non-African strain DGRP882, and the African strain, Z53, as our representative strains because the behavior of males and females from both strains has been previously documented (Jin et al, 2022).…”