Ecdysteroid Hormones Link the Juvenile Environment to Alternative Adult Life Histories in a Seasonal Insect

Journal of Animal Ecology

Collins³

et al. 2020

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Many tropical environments experience cyclical seasonal changes, frequently with pronounced wet and dry seasons, leading to a highly uneven temporal distribution of resources. Short‐lived animals inhabiting such environments often show season‐specific adaptations to cope with alternating selection pressures. African Bicyclus butterflies show strong seasonal polyphenism in a suite of phenotypic and life‐history traits, and their adults are thought to undergo reproductive diapause associated with the lack of available larval host plants during the dry season. Using 3 years of longitudinal field data for three species in Malawi, dissections demonstrated that one forest species reproduces continuously, whereas two savannah species undergo reproductive diapause in the dry season, either with or without pre‐diapause mating. Using additional data from field‐collected and museum samples, we then documented the same three mating strategies for a further 37 species. Phylogenetic analyses indicated that the ancestral state was a non‐diapausing forest species, and that habitat preference and mating strategy evolved in a correlated fashion. Bicyclus butterflies underwent rapid diversification during the Late Miocene, coinciding with expansions into more open savannah habitat. We conclude that the ability to undergo reproductive diapause was a key trait that facilitated colonization and eventual radiation into savannahs in the Late Miocene.

Section: Species Of the African Mycalesina Genus Bicyclus Inhabit Bothmentioning

confidence: 99%

mentioning

confidence: 99%

To mate, or not to mate: The evolution of reproductive diapause facilitates insect radiation into African savannahs in the Late Miocene

Halali

Journal of Animal Ecology

Collins³

et al. 2020

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“…Temperature experienced during the late larval stage is an important environmental inducer of the seasonal forms both in the field and in the laboratory; lower or higher temperatures act as a cue for forthcoming dry or wet seasons, respectively (Kooi andBrakefield 1999, Brakefield et al 2007). Moreover, developmental plasticity in mycalesine butterflies involves coordinated responses of morphological, physiological, behavioural and life history traits which together provide an adaptive response to climate instability (Oostra et al 2014, Mateus et al 2014, Nokelainen et al 2018, van Bergen and Beldade 2018.…”

Section: Introductionmentioning

confidence: 99%

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

Balmer

Brattström

et al. 2018

Oikos

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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.

“…Both adult wing pattern and life history are determined by developmental temperature, although life-history traits retain the ability to acclimatize over the course of several weeks when environmental conditions change during adult life (e.g., Fischer et al 2003). Recently, we showed that Ecdysteroid hormones during the pupal stage play a functional role in regulating developmental plasticity of adult reproductive strategy, a role for this hormone that had already been established for wing pattern plasticity (Oostra et al 2014b). This indicates that, at least in B. anynana, developmental plasticity of wing pattern and of life history share developmental-physiological mechanisms.…”

Section: Introductionmentioning

confidence: 99%

On the fate of seasonally plastic traits in a rainforest butterfly under relaxed selection

Oostra

Hiltemann

et al. 2014

Ecology and Evolution

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Many organisms display phenotypic plasticity as adaptation to seasonal environmental fluctuations. Often, such seasonal responses entails plasticity of a whole suite of morphological and life-history traits that together contribute to the adaptive phenotypes in the alternative environments. While phenotypic plasticity in general is a well-studied phenomenon, little is known about the evolutionary fate of plastic responses if natural selection on plasticity is relaxed. Here, we study whether the presumed ancestral seasonal plasticity of the rainforest butterfly Bicyclus sanaos (Fabricius, 1793) is still retained despite the fact that this species inhabits an environmentally stable habitat. Being exposed to an atypical range of temperatures in the laboratory revealed hidden reaction norms for several traits, including wing pattern. In contrast, reproductive body allocation has lost the plastic response. In the savannah butterfly, B. anynana (Butler, 1879), these traits show strong developmental plasticity as an adaptation to the contrasting environments of its seasonal habitat and they are coordinated via a common developmental hormonal system. Our results for B. sanaos indicate that such integration of plastic traits – as a result of past selection on expressing a coordinated environmental response – can be broken when the optimal reaction norms for those traits diverge in a new environment.