Kin recognition in Drosophila: rearing environment and relatedness can modulate gut microbiota and cuticular hydrocarbon odour profiles

Abstract

From inbreeding avoidance to kin‐selected cooperation, social behaviours are frequently reliant on kin recognition. However, kin recognition mechanisms are costly to evolve and currently not very well understood. Recent evidence suggests that, by altering their host's odour, gut and other host‐associated microorganisms may provide a promising avenue for understanding kin recognition. In Drosophila melanogaster, kin recognition can mediate mate choice, sexual conflict and larval competition/cooperation, underscoring its important functional role. As is commonly the case, kin recognition in this species depends on both familiarity (i.e. shared rearing environment) and relatedness, and seems to rely mainly on body odours determined by cuticular hydrocarbons. Here, we investigated the degree to which larval rearing environment and relatedness (full‐sibs versus unrelated) determine co‐variation between gut microbiota and cuticular hydrocarbons in D. melanogaster. We found that rearing environment strongly determined microbiota composition and cuticular hydrocarbon profiles, but that these effects were independent from each other. In contrast, relatedness did not influence microbiota composition, but had a strong influence on microbiota diversity, which in turn covaried significantly with cuticular hydrocarbon profiles. Our results show that, in D. melanogaster, odours may convey information about both familiarity and relatedness via an interaction between: 1) direct effects of the rearing environment on cuticular hydrocarbons and 2) indirect effects of relatedness on cuticular hydrocarbons via gut microbiota diversity.

Between‐partner concordance of vertically transmitted gut microbiota diminishes reproductive output in the dung beetle Onthophagus taurus

“…Instead, our results are consistent with the possibility that the gut microbiome may mediate familiarity/kin recognition (Lizé et al, 2013(Lizé et al, , 2014, to the extent that mating avoidance between individuals with similar microbial profiles may promote outcrossing. Interestingly, in Drosophila, the gut microbiota appears to influence kin recognition via modifications of cuticular hydrocarbons, thereby shaping the scent profiles used in mate choice (García-Roa et al, 2022;Lewis et al, 2014). Bacterial symbionts support cuticle synthesis and have the potential to interfere with the host's cuticular hydrocarbon profile in several insects, including beetles (Engl & Kaltenpoth, 2018).…”

“…For example, Lizé et al (2014) provided evidence for a role of gut bacteria in kin recognition in Drosophila. Here, the microbiome appears to affect copulation preference as a function of familiarity (D. bifasciata) and diet (D. melanogaster), potentially via changes in the composition of the hosts' cuticular hydrocarbon compounds (García-Roa et al, 2022;Lewis et al, 2014). Intriguingly, Sharon et al (2010Sharon et al ( , 2011 also showed that some components of the gut microbiome of two D. melanogaster lines reared on different food sources were responsible for assortative mating-an observation that hints at a potential role for microbial symbionts in reproductive isolation and ecological speciation.…”

No evidence that relatedness or familiarity modulates male harm in Drosophila melanogaster flies from a wild population

“…It is already a model system in sexual conflict studies, exhibiting intense sexual conflict that includes both precopulatory (i.e., male harassment; Teseo et al, 2016) and post‐copulatory (i.e., toxic ejaculates (Wigby & Chapman, 2004, 2005)) harm to females. It is also capable of kin recognition in both its larval (Khodaei & Long, 2019) and adult stages (García‐Roa et al, 2022; Lize et al, 2013; Tan et al, 2013). Moreover, previous evidence has shown evidence of cooperation among kin (Khodaei & Long, 2019, 2020), and it is the first species in which males were shown to decrease male harm when competing against related males (Carazo et al, 2014).…”

“…In addition, gut microbiota has been shown to play an important role in kin recognition in D. melanogaster (García-Roa et al, 2022;Heys et al, 2018;Lize et al, 2013). Gut microbiota is transferred into the medium by females during oviposition, and is heavily influenced by environmental factors, including the food regime flies are kept in (Broderick & Lemaitre, 2012;García-Roa et al, 2022). Consequently, the gut microbiome of laboratory flies kept under the same food is bound to exhibit considerably less inter-individual variation than in nature.…”

“…Furthermore, such variability was detected even though fruits were carefully controlled for ripeness and external damage (inducing differences in yeast content), which is unlikely to be the case in nature (Dweck et al, 2013). In addition, gut microbiota has been shown to play an important role in kin recognition in D. melanogaster (García-Roa et al, 2022;Heys et al, 2018;Lize et al, 2013). Gut microbiota is transferred into the medium by females during oviposition, and is heavily influenced by environmental factors, including the food regime flies are kept in (Broderick & Lemaitre, 2012;García-Roa et al, 2022).…”