Early-exposure to new sex pheromone blend alters mate preference in female butterflies and in their offspring

Abstract

Insects use species-specific sex pheromone blends to attract members of the opposite sex which express the corresponding molecular receptors. Given this lock and key mechanism used for species identification and mate choice, it is currently not well understood how pheromone blends or receptor systems evolve. One possibility is that insects develop preferences for new sex pheromone blends via the process of learning, and that these learned preferences may be passed on to the next generation. We tested these hypotheses by exposing newly emerged Bicyclus anynana female butterflies to either wild type or to modified male sex pheromone blends. A few days later, we scored female mating outcome in a choice trial involving both male types. We also assessed the mating outcome of naïve offspring of females that underwent distinct odor learning trials to test for a potential inheritance of learned odor preferences. Naïve (parental) females mated preferentially with Wt-blend males, but females pre-exposed to new blends either shifted their preference to new-blend males, or mated equally with males of either blend type; the response depending on the new blend they were introduced to. Naïve daughters of females who were exposed to new-blend males behaved similarly to their experienced mothers. We demonstrate that females are able to learn preferences for novel pheromone blends in response to a short social experience, and pass that learned preference down to the next generation. This suggests that learning can be a key factor in the evolution of sex pheromone blend recognition and in chemosensory speciation.Significance statementWhile the diversity of sex pheromone communication systems across insects is well documented, the mechanisms that lead to such diversity are not well understood. Sex pheromones constitute a species-specific system of sexual communication that reinforces interspecific reproductive isolation. When odor blends evolve, the efficacy of male-female communication becomes compromised, unless preference for novel blends also evolves. We explore odor learning as a possible mechanism leading to changes in sex pheromone preferences. We show that preferences for new blends can develop following a short learning experience, and that these novel preferences can be transmitted to the next generation. To our knowledge, this is the first investigation of sex pheromone blend preference learning impacting mate choice and being inherited in an insect.

The Role of Learning on Insect and Spider Sexual Behaviors, Sexual Trait Evolution, and Speciation

“…This is the first study that shows inheritance of a learned response to a pheromone blend. Dion et al, 2017 African cotton leafworm moth Spodoptera littoralis Exposure Olfactory. Females exposed to a 0.1 female equivalent of the sex pheromone extract for 4 min, within 2 min from the beginning of scotophase or 3 h before the onset of the expected scotophase on the first 2 days after emergence.…”

Transgenerational inheritance of learned preferences for novel host plant odors inBicyclus anynanabutterflies

“…, ; Westerman and Monteiro ) as well as pheromone odors (Dion et al. ). In addition, these latter learned pheromone preferences have been transmitted to the next generation to affect naïve pheromone preferences (Dion et al.…”

“…In addition, these latter learned pheromone preferences have been transmitted to the next generation to affect naïve pheromone preferences (Dion et al. ). Experiments on larval food preference learning and inheritance, however, have never been conducted in this species.…”

“…Bicyclus anynana is also a species where adults have previously been shown to learn a variety of different wing patterns (Westerman et al 2012(Westerman et al , 2014Westerman and Monteiro 2013) as well as pheromone odors (Dion et al 2017). In addition, these latter learned pheromone preferences have been transmitted to the next generation to affect naïve pheromone preferences (Dion et al 2017). Experiments on larval food preference learning and inheritance, however, have never been conducted in this species.…”

Common Practice Solvent Extraction Does not Reflect Actual Emission of a Sex Pheromone During Butterfly Courtship

“…While MSP3 amount did increase in some (but not all; van Bergen et al, 2013) studies with mating success, this may simply be due to the fact that MSP3 amount correlates to MSP1 amount (Nieberding et al, 2012;this study). This study further suggests that the most important MSP component for mating success, MSP2 (Nieberding et al, 2012;Dion et al, 2017), may be under active control for emission by males and the environment in which males are tested may matter for MSP2 emission. We may thus underestimate the role of chemical communication in mating success and sexual selection, and particularly of MSP2 amounts in B. anynana, by using unnatural, laboratory-based, environmental conditions (Miller and Svensson, 2014;Holveck, 2017, 2018).…”