Ant cuticular hydrocarbons are heritable and associated with variation in colony productivity

Abstract

In social insects, cuticular hydrocarbons function in nest-mate recognition and also provide a waxy barrier against desiccation, but basic evolutionary features, including the heritability of hydrocarbon profiles and how they are shaped by natural selection are largely unknown. We used a new pharaoh ant ( Monomorium pharaonis ) laboratory mapping population to estimate the heritability of individual cuticular hydrocarbons, genetic correlations between hydrocarbons, and fitness consequences of phenotypic variation in the hydrocarbons. Individual hydrocarbons had low to moderate estimated heritability, indicating that some compounds provide more information about genetic relatedness and can also better respond to natural selection. Strong genetic correlations between compounds are likely to constrain independent evolutionary trajectories, which is expected, given that many hydrocarbons share biosynthetic pathways. Variation in cuticular hydrocarbons was associated with variation in colony productivity, with some hydrocarbons experiencing strong directional selection. Altogether, this study builds on our knowledge of the genetic architecture of the social insect hydrocarbon profile and indicates that hydrocarbon variation is shaped by natural selection.

Candidate genes involved in cuticular hydrocarbon differentiation between cryptic, parabiotic ant species

“…Although the profiles of the lab-acclimated ants differed from those sampled at natural conditions, we could show that the species-specific CHC profiles were relatively stable. These results are thus consistent with CHC profiles of the ants being heritable and species-specific ( van Zweden et al 2009 ; Walsh et al 2020 ), instead of resulting from phenotypic plasticity induced by environmental factors in the natural habitat. The differences between acclimation and natural profile may be the result of various differences between natural and lab conditions such as climate ( Menzel et al 2018 ; Sprenger et al 2018 ), different food ( Liang and Silverman 2000 ; Sorvari et al 2008 ), different nest materials ( Crosland 1989 ; Heinze et al 1996 ) or isolation from either their parabiotic partners ( Sprenger et al 2019 ) or their queen and subsequent changes in fertility ( Liebig et al 2000 ; Dietemann et al 2003 ).…”

Advances in deciphering the genetic basis of insect cuticular hydrocarbon biosynthesis and variation

“…To the best of our knowledge, however, the influence of particularly epigenetic factors on CHC profiles has not been investigated at all so far. Furthermore, quantitative genetic studies hint at additive effects of many genes with the potential to cumulatively impact CHC variation, complementing studies on heritability and genetic correlations between individual CHC compounds (Foley and Telonis-Scott 2011;Berson et al 2019b;Walsh et al 2020). This would limit the significance of the candidate gene approach for resolving the genetic basis of CHC biosynthesis.…”

Social Behavior, Ovary Size, and Population of Origin Influence Cuticular Hydrocarbons in the Orchid Bee Euglossa dilemma

“…The complete set of CHCs expressed on an insect, the CHC profile, may consist of multiple classes of linear and branched alkanes and alkenes, and their qualitative and quantitative variation can be highly dynamic and sensitive to a range of environmental, genetic, or physiological factors (Walsh et al, 2020;Bonduriansky et al, 2015). The expression of some CHC compounds is directly linked to pathways that regulate reproduction in insects therefore enabling CHCs to potentially reflect honest information about individual physiological condition (Kuo et al, 2012;Makki et al, 2014).…”