Developmental plasticity for male secondary sexual traits in a group of polyphenic tropical butterflies

Abstract

Many organisms alter their investment in secondary sexual traits to optimise the fitness tradeoff between reproduction and survival. Though seasonal variation in the expression of sexual traits is evident (e.g. conspicuous breeding plumage in birds), little attention has been given to short‐lived organisms that inhabit relatively stable environments throughout their own lifetime but are exposed to strong environmental variation across generations. Some insects have evolved seasonal polyphenism to cope with intergenerational variation in environmental selection, yielding alternative phenotypes better suited for the environment in which they occur. Here we use mycalesine butterflies, which express distinct seasonal forms in response to wet‐dry seasonal environments, to explore whether seasonal polyphenism extends to secondary sexual traits. Sex pheromones, which are produced by androconial patches on the wings of males, are a key determinant of mating success in these species. Through a series of field sampling, reaction norm experiments, pheromone titre quantification, and mate competition experiments, this study reveals that the size of the androconial patch on the forewing is mediated by the temperatures experienced during development, which correspond to the ecological conditions during the alternative wet and dry seasons in the wild. Furthermore, in one of the species, Bicyclus anynana, larger forewing patches are associated with both an increase in the production of pheromone components as well as the likelihood of mating. Taken together, these findings indicate that plasticity in androconial patches may be an adaptation to seasonal fluctuations in the environment as it favours reproductive success in the conditions in which each seasonal form flies. We discuss our findings in the context of seasonal differences in the optimal tradeoff between reproduction and survival.

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

“…In contrast, MSP2 amount kept increasing across ages in both seasonal forms as previously observed in WS-27/27 [35]. Importantly, stable amounts of MSP2 component across developmental temperatures in our two experiments suggest that hexadecanal may matter for mating success for all males independently of their developmental history, extending the importance of the MSP2 component for mating success, which is so far established for WS-27/27 males [35,36,64,65]. Our results highlight the complexity of how sexual selection shapes the male sex pheromone composition in this polyphenic species that displays a sex role reversal across seasons [23,43].…”

Thermal Plasticity in Insects’ Response to Climate Change and to Multifactorial Environments

“…Finally, lab studies have also shed light onto the genetic architecture and constraints on the evolution of thermal reaction norms (Holloway and Brakefield, 1995;Brakefield, 1996;Wijngaarden and Brakefield, 2001;Wijngaarden et al, 2002). On the other hand, field collections allowed for characterization of differences in reaction norms between geographical populations of B. anynana (de Jong et al, 2010) and between Bicyclus species (van Bergen et al, 2017;Balmer et al, 2018).…”

Warm developmental temperatures induce non‐adaptive plasticity in the intrasexually selected colouration of a dragonfly

“…Because temperature experienced later in development should better predict the adult conditions than temperatures experienced prior to or during the previous winter, this would be surprising, although it remains possible. Additionally, in parts of the range where the flight season lasts beyond the end of summer (Paulson, , ), warmer larval temperatures could indicate that individuals will encounter cooler autumnal temperatures as adults (Prudic et al ., ; Stoehr & Wojan, ; Balmer et al ., ). Although the reproductive season concludes when it is still relatively hot for the focal population (see ‘Study Species and study overview’), the observed wing colour response could be favoured by intrasexual selection in other parts of the range, perhaps maintained by gene flow and only small thermal costs to territorial success.…”