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

Singh, Putan; Bergen, Erik van; Brattström, Oskar; Osbaldeston, Dave; Brakefield, Paul M.; Oostra, Vicencio

doi:10.1007/s10682-020-10062-0

Cited by 15 publications

(16 citation statements)

References 124 publications

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“…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 [18] showed that poor host plant quality mainly influenced development at intermediate temperatures in the tropical butterfly Bicyclus anynana. Moreover, significant genetic variation for (multidimensional) plasticity is known to exist in both natural and laboratory populations [20][21][22].…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2020

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Variation in environmental conditions during development can lead to changes in life-history traits with long-lasting effects. Here, we study how variation in temperature and host plant (i.e. the consequences of potential maternal oviposition choices) affects a suite of life-history traits in pre-diapause larvae of the Glanville fritillary butterfly. We focus on offspring survival, larval growth rates and relative fat reserves, and pay specific attention to intraspecific variation in the responses (G × E × E). Globally, thermal performance and survival curves varied between diets of two host plants, suggesting that host modifies the temperature impact, or vice versa. Additionally, we show that the relative fat content has a host-dependent, discontinuous response to developmental temperature. This implies that a potential switch in resource allocation, from more investment in growth at lower temperatures to storage at higher temperatures, is dependent on the larval diet. Interestingly, a large proportion of the variance in larval performance is explained by differences among families, or interactions with this variable. Finally, we demonstrate that these family-specific responses to the host plant remain largely consistent across thermal environments. Together, the results of our study underscore the importance of paying attention to intraspecific trait variation in the field of evolutionary ecology.

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Section: Introductionmentioning

confidence: 99%

“…For example, Singh et al . [ 18 ] showed that poor host plant quality mainly influenced development at intermediate temperatures in the tropical butterfly Bicyclus anynana . Moreover, significant genetic variation for (multidimensional) plasticity is known to exist in both natural and laboratory populations [ 20 – 22 ].…”

Section: Introductionmentioning

confidence: 99%

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

et al. 2020

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“…Furthermore, rather than a single cue, but possibly an interaction between multiple cues may provide a better prediction of the seasonal change (e.g. Goehring & Oberhauser, 2002; Morehouse et al., 2013; Singh et al., 2020). For example, high temperature and low humidity can result in deteriorating plant quality, and larvae of Mycalesina butterflies growing on low host plant quality tend to have smaller eyespots (Kooi et al., 1996; Singh et al., 2020).…”

Section: Discussionmentioning

confidence: 99%

“…Goehring & Oberhauser, 2002; Morehouse et al., 2013; Singh et al., 2020). For example, high temperature and low humidity can result in deteriorating plant quality, and larvae of Mycalesina butterflies growing on low host plant quality tend to have smaller eyespots (Kooi et al., 1996; Singh et al., 2020). In nature, host plant quality generally declines towards the end of the wet season, which may result in the expression of DSF (Brakefield & Reitsma, 1991).…”

Section: Discussionmentioning

confidence: 99%

“…Lindestad et al., 2019; Roskam & Brakefield, 1999). In addition, strong temperature‐dependent expression of seasonal forms in Mycalesina butterflies as revealed by laboratory experiments may provide biased results since the temperature is often the only variable tested (but see Mayekar & Kodandaramaiah, 2017; Singh et al., 2020). Future reaction norm studies using multiple factors such as temperature, humidity or host plant quality in a full factorial design will be important in helping to understand the regulation of seasonal polyphenism in the wild.…”

Section: Discussionmentioning

confidence: 99%

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Predictability of temporal variation in climate and the evolution of seasonal polyphenism in tropical butterfly communities

Halali

Barlow³

et al. 2021

J of Evolutionary Biology

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Phenotypic plasticity in heterogeneous environments can provide tight environment‐phenotype matching. However, the prerequisite is a reliable environmental cue(s) that enables organisms to use current environmental information to induce the development of a phenotype with high fitness in a forthcoming environment. Here, we quantify predictability in the timing of precipitation and temperature change to examine how this is associated with seasonal polyphenism in tropical Mycalesina butterflies. Seasonal precipitation in the tropics typically results in distinct selective environments, the wet and dry seasons, and changes in temperature can be a major environmental cue. We sampled communities of Mycalesina butterflies from two seasonal locations and one aseasonal location. Quantifying environmental predictability using wavelet analysis and Colwell's indices confirmed a strong periodicity of precipitation over a 12‐month period at both seasonal locations compared to the aseasonal one. However, temperature seasonality and periodicity differed between the two seasonal locations. We further show that: (a) most females from both seasonal locations synchronize their reproduction with the seasons by breeding in the wet season but arresting reproduction in the dry season. In contrast, all species breed throughout the year in the aseasonal location and (b) species from the seasonal locations, but not those from the aseasonal location, exhibited polyphenism in wing pattern traits (eyespot size). We conclude that seasonal precipitation and its predictability are primary factors shaping the evolution of polyphenism in Mycalesina butterflies, and populations or species secondarily evolve local adaptations for cue use that depend on the local variation in the environment.

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Limited sex differences in plastic responses suggest evolutionary conservatism of thermal reaction norms: A meta-analysis in insects

et al. 2022

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Temperature has a profound effect on the growth and development of ectothermic animals. However, the extent to which ecologically driven selection pressures can adjust thermal plastic responses in growth schedules is not well understood. Comparing temperature‐induced plastic responses between sexes provides a promising but underexploited approach to evaluating the evolvability of thermal reaction norms: males and females share largely the same genes and immature environments but typically experience different ecological selection pressures. We proceed from the idea that substantial sex differences in plastic responses could be interpreted as resulting from sex‐specific life‐history optimization, whereas similarity among the sexes should rather be seen as evidence of an essential role of physiological constraints. In this study, we performed a meta‐analysis of sex‐specific thermal responses in insect development times, using data on 161 species with comprehensive phylogenetic and ecological coverage. As a reference for judging the magnitude of sex specificity in thermal plasticity, we compared the magnitude of sex differences in plastic responses to temperature with those in response to diet. We show that sex‐specific responses of development times to temperature variation are broadly similar. We also found no strong evidence for sex specificity in thermal responses to depend on the magnitude or direction of sex differences in development time. Sex differences in temperature‐induced plastic responses were systematically less pronounced than sex differences in responses induced by variations in larval diet. Our results point to the existence of substantial constraints on the evolvability of thermal reaction norms in insects as the most likely explanation. If confirmed, the low evolvability of thermal response is an essential aspect to consider in predicting evolutionary responses to climate warming.

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

Abstract: We would like to thank Andrew Balmer for help with the plant measurements, and the Radiating Butterflies Group for helpful discussions. This study was

Cited by 15 publications

References 124 publications

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

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

Predictability of temporal variation in climate and the evolution of seasonal polyphenism in tropical butterfly communities

Limited sex differences in plastic responses suggest evolutionary conservatism of thermal reaction norms: A meta-analysis in insects

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