Desiccation Resistance and Micro-Climate Adaptation: Cuticular Hydrocarbon Signatures of Different Argentine Ant Supercolonies Across California

Abstract

Cuticular hydrocarbons (CHCs), the dominant fraction of the insects' epicuticle and the primary barrier to desiccation, form the basis for a wide range of chemical signaling systems. In eusocial insects, CHCs are key mediators of nestmate recognition, and colony identity appears to be maintained through a uniform CHC profile. In the unicolonial Argentine ant Linepithema humile, an unparalleled invasive expansion has led to vast supercolonies whose nestmates can still recognize each other across thousands of miles. CHC profiles are expected to display considerable variation as they adapt to fundamentally differing environmental conditions across the Argentine ant's expanded range, yet this variation would largely conflict with the vastly extended nestmate recognition based on CHC uniformity. To shed light on these seemingly contradictory selective pressures, we attempt to decipher which CHC classes enable adaptation to such a wide array of environmental conditions and contrast them with the overall CHC profile uniformity postulated to maintain nestmate recognition. n-Alkanes and n-alkenes showed the largest adaptability to environmental conditions most closely associated with desiccation, pointing at their function for water-proofing. Trimethyl alkanes, on the other hand, were reduced in environments associated with higher desiccation stress. However, CHC patterns correlated with environmental conditions were largely overriden when taking overall CHC variation across the expanded range of L. humile into account, resulting in conserved colony-specific CHC signatures. This delivers intriguing insights into the hierarchy of CHC functionality integrating both adaptation to a wide array of different climatic conditions and the maintenance of a universally accepted chemical profile.

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

“…Our study is the first social insect study to link variation in cuticular hydrocarbons with variation in colony productivity, although previous social insect studies have linked variation in cuticular hydrocarbons to worker survival (Sprenger et al 2018) or to climatic or biotic variation (Menzel et al 2017;Buellesbach et al 2018;Sprenger et al 2018 Interestingly, we found similar linear selection patterns using both definitions, as all significant linear estimates were in the same direction between the two definitions (Figure 3, Supplement table 2). This suggests that the hydrocarbon profile optima are largely aligned for the production of both reproductives and workers in our study population.…”

“…), diet, and environmental conditions experienced by the colonies. Such control in particular is valuable given the complexity of social insect colonies (Linksvayer 2006;Kronauer & Libbrecht 2018) and the sensitivity of the hydrocarbon profile to changes in the environment or diet (Francis et al 1989;vander Meer et al 1989;Liang & Silverman 2000;Tissot et al 2001;Buczkowski et al 2005;van Zweden et al 2009;Pavković-Lučić et al 2016;Menzel et al 2017;Buellesbach et al 2018). Although future field studies would be beneficial, in particular to identify how variation in cuticular hydrocarbons affects colony productivity in a natural setting, a field study on a similar scale as our study is likely not feasible.…”

“…Knowledge of the fitness consequences of trait variation is necessary to characterize the type (e.g., directional, stabilizing, or disruptive) and strength of natural selection acting on a trait (Lande & Arnold 1983;Arnold & Wade 1984;Janzen & Stern 1998;Morrissey & Sakrejda 2013). Variation in the social insect hydrocarbon profile may affect individual survival and colony productivity by affecting desiccation resistance (Gordon 2013;Buellesbach et al 2018;Sprenger et al 2018;Friedman et al 2019) or by influencing chemical communication among nestmates and the collective behavior of the colony (Lahav et al 2001;Green & Gordon 2003;Martin & Drijfhout 2009a;Liebig 2010;Buellesbach et al 2018).…”

Cuticle Hydrocarbons Show Plastic Variation under Desiccation in Saline Aquatic Beetles

“…Therefore, these changes may reflect a physical response of the CHC blend to dryness rather than a physiological mechanism to control water loss. Indeed, these CHC changes would reduce overall waterproofing, although some authors found that alkenes also increase with temperature [22,52].…”

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

“…Nongenetic factors contributing to CHC diversity could potentially overshadow the detectable impact of individual biosynthesis genes, hampering attempts to fully resolve the explicit contributions of each individual gene. Several studies have revealed a remarkable adaptability of CHC profiles to diverse biotic and abiotic conditions in different insect taxa (e.g., Rajpurohit et al 2017;Buellesbach et al 2018b;Menzel et al 2018). Also, since CHC biosynthesis is linked to the uptake of amino acids (Dillwith et al 1982;Chase et al 1990) and has been shown to be influenced by several metabolic pathways, such as the citric acid cycle and fatty acid synthesis (Barber et al 2005;Blomquist and Bagnères 2010), diet can contribute to variations in CHC profiles as well (e.g., Fedina et al 2012).…”