Sexual selection contributes to partial restoration of phenotypic robustness in a butterfly

Abstract

Phenotypic variation is the raw material for selection that is ubiquitous for most traits in natural populations, yet the processes underlying phenotypic evolution or stasis often remain unclear. Here, we report phenotypic evolution in a mutant line of the butterfly Bicyclus anynana after outcrossing with the genetically polymorphic wild type population. The comet mutation modifies two phenotypic traits known to be under sexual selection in this butterfly: the dorsal forewing eyespots and the pheromone-producing structures. The original comet mutant line was inbred and remained phenotypically stable for at least seven years, but when outcrossed to the wild type population the outcrossed comet line surprisingly recovered the wild type phenotype within 8 generations at high (27 °C), but not at low (20 °C), developmental temperatures. Male mating success experiments then revealed that outcrossed comet males with the typical comet phenotype suffered from lower mating success, while mating success of outcrossed comet males resembling wild types was partially restored. We document a fortuitous case where the addition of genetic polymorphism around a spontaneous mutation could have allowed partial restoration of phenotypic robustness. We further argue that sexual selection through mate choice is likely the driving force leading to phenotypic robustness in our system.

Polyphenism of visual and chemical secondary sexually-selected wing traits in the butterfly Bicyclus anynana: How different is the intermediate phenotype?

“…In the second experiment (experiment B), we re-used already published data from Nieberding et al . [45] to quantify lifetime changes in MSP production across WS and DS forms. Here the larvae were reared either in the standard rearing environment (27°C) or at 20°C in an incubator (SANYO MLR351H), and the pupae and adults after emergence were kept at the same temperature as the one experienced during development (27°C: WS-27/27; 20°C: DS-20/20).…”

“…Regarding our third objective, several studies analysed age-related changes in MSP composition in the WS phenotype [35,44], but only Nieberding et al . [45] quantified MSP components in both WS and DS phenotypes at different ages, without focusing on this aspect. Hence, we re-analysed data from published literature [45].…”

“…[45] quantified MSP components in both WS and DS phenotypes at different ages, without focusing on this aspect. Hence, we re-analysed data from published literature [45]. Here we assessed potential differences in developmental reaction norms of MSP production with increasing age for these two seasonal forms.…”

Mosaic evolution of molecular pathways for sex pheromone communication in a butterfly

“…MSP concentrations were determined as previously described (Nieberding et al 2008(Nieberding et al , 2018. In short, one forewing and hindwing of each male was soaked in 600ul of hexane during 5 minutes.…”

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

“…We hypothesized that common practice solvent extraction could blur sex pheromone quantification and as such limit our understanding of how sexual selection affects chemical sexually-selected traits. We used the butterfly Bicyclus anynana (Lepidoptera: Nymphalidae) as a model system, because this species is one of the best studied butterflies with regard to sexual, including olfactory, communication (Costanzo and Monteiro, 2007;Nieberding et al, 2008Nieberding et al, , 2012Nieberding et al, , 2018Brakefield et al, 2009;Prudic et al, 2011;San Martin et al, 2011;Westerman et al, 2012Westerman et al, , 2014van Bergen et al, 2013;Heuskin et al, 2014;Bacquet et al, 2015;Dion et al, 2016;Nieberding and Holveck, 2017). In B. anynana, males compete for access to females and perform a stereotyped courtship sequence during which the sex pheromone is emitted by wing pheromone-producing structures called androconia (Figure 1).…”