The dangers of irreversibility in an age of increased uncertainty: revisiting plasticity in invertebrates

Abstract

Plasticity in traits in response to environmental conditions can increase fitness, expanding the range of environments within which a genotype can generate viable and productive phenotypes, and therefore when and where populations can persist and diversify in ecological space. Adaptive forms of plasticity in invertebrates are diverse, ranging from polyphenism and diapause to behavioural thermoregulation and optimal foraging. Local patterns of environmental variation and developmental constraints will dictate which of these forms evolves. Here we review the core idea that the use of narrow developmental windows by invertebrates to attain specific types of phenotypic changes reduces their reversibility, while increasing their magnitude. These tradeoffs dictate the costs and effectiveness of plasticity in buffering environmental variation. In particular, plastic responses to narrow developmental or environmental windows increase fitness costs when predicted environmental challenges do not materialise, or when the environment changes in unpredictable ways. We then explore the converse idea that increasing trait reversibility depends on extending the period for which genotypes are sensitive to the environment, but also narrows the range of plastic phenotypes that can be generated. Considering these findings together, we would expect that the costs, benefits and constraints of reversible versus irreversible plasticity affect the rate and magnitude of adaptive responses to rapidly changing and novel environments. However, such predictions have rarely been tested or included in theoretical models. Identifying this knowledge gap leads us to propose new research directions to provide a deeper understanding of the evolution of plasticity in invertebrates and other organisms. We illustrate these possible directions through examples of Drosophila adapting to thermal stress.

Environmental variation and biotic interactions limit adaptation at ecological margins: lessons from rainforestDrosophilaand European butterflies

“…Including such behaviour in our measurements of [A] and [B] steepness may make local adaptation less (or sometimes more) likely at ecological margins than we might otherwise predict, as has been demonstrated in experimental studies of local adaptation in unicellular ciliates [84][85][86]. These considerations remind us that traits which come under selection in the field are the product of differences in the environmental sensitivity of genotypes and populations, which tend to evolve to make environmental variation as predictable (and often as smooth) as possible [60,87]. Increased awareness of this has focused attention on how genotypes respond to environments within and outside their historical distribution.…”

“…adaptive potential of standing variation as well as its effect in reducing mean fitness); and on [B], which represents the change in trait mean demanded by the change in the environment ( [10]; figure 1b). However, both dimensions [A] and [B] are shaped by the way that alleles and genotypes are sensitive to environmental variation, and how this affects their experience of ecological gradients, particularly in terms of the phenotypes that these genotypes create, and their behaviour in distributing these phenotypes in space (dispersal) or time ( phenology) [60], as we have seen through variation in brown argus oviposition preference, both at a regional [80] and microclimate [83] scale. Such non-random movement of gametes (by mate or fertilization choice) or genotypes (by seed dispersal, or by oviposition preference) to areas where they have high fitness may make ecological gradients very patchy (i.e.…”

The evolution of novel biotic interactions at ecological margins in response to climate change involves alleles from across the geographical range of the UK Brown Argus butterfly

“…2021). Increased environmental unpredictability as well as variation are key in shaping the life history and behavioural strategies that evolve during adaptation to novel climates (Hoffmann & Bridle 2021). In this context, the Brown Argus example is also important, given its rapid range expansion is likely to have reduced its capacity to cope with increasingly unpredictable conditions in coming decades, by favouring specialisation on a host plant that is only productive during clement years (Stewart et al, in press).…”

Biogeographical history shapes evolution of reproduction in a global warming scenario

“…Another possible explanation is that a part of the population’s response to the thermal conditions might be environmentally-based, resulting, for instance, from epigenetic and/or maternal environmental effects ( e . g ., (Hoffmann and Bridle 2021). That being true, such effects would not be detected in our experimental setup as they could have been mitigated or removed by the one-generation common garden protocol at 18ºC imposed prior to the plasticity assays.…”