Complex multi-trait responses to multivariate environmental cues in a seasonal butterfly

Abstract

Developmental plasticity in a seasonal environment allows an organism to optimally match its life-history traits with the fluctuating conditions. This critically relies on abiotic and biotic factors, such as temperature or food quality, that act as environmental cues and predict seasonal transitions. In most seasonal environments, multiple factors vary together, making it crucial to understand their combined effects on an organism’s phenotype. Here, we study plasticity in a multivariate environment in the butterfly Bicyclus anynana that exhibits two distinct seasonal phenotypes. Temperature is an important cue mediating plasticity in this species, but other environmental cues such as larval host plant quality could also be informative since plant quality deteriorates during the transition from wet to dry season in the field. We examine how temperature and host plant quality interact to affect life-history traits. Using a full-factorial design, we expose cohorts of larvae to either poor (old plants) or high (young plants) quality plants at different temperatures. Our results show that plant quality had a temperature and sex-dependent effect on life-history traits. At lower and intermediate temperatures, it decreased body mass and prolonged development time, indicating that poor plant quality acted as a stressor. However, metabolic rates in adults were not affected, indicating that individuals could, at least in part, compensate for stressful juvenile conditions. In contrast, at higher temperatures poor plant quality induced a partial dry-season phenotype, indicating that it may have acted as an environmental cue. Moreover, poor plant quality, particularly in males, also decreased the correlation between life history traits, signifying disrupted phenotypic integration. Our study reveals complex interactive effects of two environmental variables on seasonal plasticity, reflecting differences in their reliability as seasonal cues. This highlights the importance of studying the combined effects of multiple environmental factors to better understand the regulation of phenotypic plasticity in wild.

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

“…Laboratory studies have characterized thermal reaction norms for various traits (e.g., Oostra et al, 2011). Revealingly, lab thermal phenotypes do not include phenotypes as extreme as those seen in nature, where other variables combined with temperature might affect development outcomes (Bauerfeind and Fischer, 2005;Rodrigues et al, 2018;Singh et al, 2019), but do include intermediate phenotypes between the typical dry-and wet-season forms, which are rarely found in nature (Brakefield and Reitsma, 1991;Windig et al, 1994;Muller et al, 2019). Lab studies have also allowed characterization of the physiological and genetic basis of thermal plasticity.…”

Multidimensional plasticity in the Glanville fritillary butterfly: larval performance curves are temperature, host and family specific

“…Hence, plastic responses to one type of environmental stress may be dependent on the state of another external factor. Such non-additive multidimensional plasticity, in response to combinations of thermal and nutritional environments, has been demonstrated in moths [14], butterflies [18] and fruit flies [19]. For example, Singh et al showed that poor host plant quality mainly influenced development at intermediate temperatures the tropical butterfly Bicyclus anynana [18].…”

“…Such non-additive multidimensional plasticity, in response to combinations of thermal and nutritional environments, has been demonstrated in moths [14], butterflies [18] and fruit flies [19]. For example, Singh et al showed that poor host plant quality mainly influenced development at intermediate temperatures the tropical butterfly Bicyclus anynana [18]. Moreover, significant genetic variation for (multidimensional) plasticity is known to exist in both natural and laboratory populations [20-22].…”