Constraints and Opportunities for the Evolution of Metamorphic Organisms in a Changing Climate

We argue that developmental hormones facilitate the evolution of novel phenotypic innovations and timing of life history events by genetic accommodation. Within an individual’s life cycle, metamorphic hormones respond readily to environmental conditions and alter adult phenotypes. Across generations, the many effects of hormones can bias and at times constrain the evolution of traits during metamorphosis; yet, hormonal systems can overcome constraints through shifts in timing of, and acquisition of tissue specific responses to, endocrine regulation. Because of these actions of hormones, metamorphic hormones can shape the evolution of metamorphic organisms. We present a model called a developmental goblet, which provides a visual representation of how metamorphic organisms might evolve. In addition, because developmental hormones often respond to environmental changes, we discuss how endocrine regulation of postembryonic development may impact how organisms evolve in response to climate change. Thus, we propose that developmental hormones may provide a mechanistic link between climate change and organismal adaptation.

Are individuals consistent? Endocrine reaction norms under different ecological challenges

Quantifying organismal capacity for compensatory mechanisms is essential to forecast response to environmental change. Despite accumulating evidence for individual variation in physiological plasticity, the causes and consequences of this variation remain unclear. An outstanding question is whether individual reaction norms are consistent across different environmental challenges, i.e., whether an individual that is responsive to one environmental variable will be equally responsive to a different environmental variable. Additionally, are these reaction norms themselves consistent over time, i.e., repeatable? Here, we quantified individual baseline glucocorticoid responses in house sparrows, Passer domesticus, to sequential manipulations of temperature, wind speed, and food unpredictability that were repeated in discrete blocks of sampling under both control and stressor-exposed conditions. Individuals significantly decreased their baseline corticosterone levels and increased their mass during treatment exposure. This response was consistent across environmental challenge types. There was high repeatability in the intercept and slope of the baseline corticosterone reaction norm between environmental challenges but broad credible intervals in the repeatability of the reaction norm slope, suggesting that although glucocorticoid levels during baseline conditions are repeatable, among-individual variation in the shape of the glucocorticoid response may be higher than within-individual variation. Within-subject variation in baseline corticosterone levels was mainly explained by within-individual variation in body mass during stressor exposure. Despite the high lability in physiological traits, endocrine plasticity is repeatable across environmental challenges and may be able to evolve due to genetic accommodation, in which selection acts on genetic variation of reaction norms.

The evolution of human life course

Homo sapiens’ life history pattern possesses both fast and slow components, in a combination that is unique among the extant great apes. One of the issues debated in current evolutionary research is the role played by phenotypic plasticity as a non-genetic means of adaptation to evolutionary challenges. While life history parameters are shaped at a species level by genetic adaptations via natural selection, they remain very sensitive to changes in the environment. Relying on updated evidence and on key explanatory tools of the Extended Evolutionary Synthesis (phenotypic plasticity, niche construction, and inclusive inheritance), it is likely that environmentally induced plasticity led the way in human life history evolution, promoting subsequent genetic accommodation. To the extent that culturally transmitted behaviors altered the selective pressures that acted on life history traits across generations during human evolution, a culturally driven plasticity dynamic shaping human life history traits can be identified. Two case studies in particular are discussed: the human adaptations to the domestication of fire and the self-domestication hypothesis.

Evolution of, and via, Developmental Plasticity: Insights through the Study of Scaling Relationships

Scaling relationships emerge from differential growth of body parts relative to each other. As such, scaling relationships are at least in part the product of developmental plasticity. While some of the developmental genetic mechanisms underlying scaling relationships are starting to be elucidated, how these mechanisms evolve and give rise to the enormous diversity of allometric scaling observed in nature is less understood. Furthermore, developmental plasticity has itself been proposed as a mechanism that facilitates adaptation and diversification, yet its role in the developmental evolution of scaling relationships remains largely unknown. In this review, we first explore how the mechanisms of scaling relationships have evolved. We primarily focus on insect development and review how pathway components and pathway interactions have evolved across taxa to regulate scaling relationships across diverse traits. We then discuss the potential role of developmental plasticity in the evolution of scaling relationships. Specifically, we address the potential role of allometric plasticity and cryptic genetic variation in allometry in facilitating divergence via genetic accommodation. Collectively, in this article, we aim to bring together two aspects of developmental plasticity: the mechanistic underpinnings of scaling relationships and their evolution, and the potential role that plasticity plays in the evolutionary diversification of scaling relationships.

Rapid, ultra-local adaptation facilitated by phenotypic plasticity

Models of ‘plasticity-first’ evolution are attractive because they explain the rapid evolution of new complex adaptations. Nevertheless, it is unclear whether plasticity can still facilitate rapid evolution when diverging populations are connected by gene flow. Here we show how plasticity has generated adaptive divergence in fecundity in wild populations of burying beetlesNicrophorus vespilloides, which are still connected by gene flow, which occupy distinct Cambridgeshire woodlands that are just 2.5km apart and which diverged from a common ancestral population c. 1000-4000 years ago. We show that adaptive divergence is duetothe coupling of an evolved increase in the elevation of the reaction norm linking clutch size to carrion size (i.e. genetic accommodation) with plastic secondary elimination of surplus offspring. Working in combination, these two processes have facilitated rapid adaptation to fine-scale environmental differences, despite ongoing gene flow.

Facultative parasites as evolutionary stepping-stones towards parasitic lifestyles

Parasites and parasitic lifestyles have evolved from free-living organisms multiple times. How such a key evolutionary transition occurred remains puzzling. Facultative parasites represent potential transitional states between free-living and fully parasitic lifestyles because they can be either free-living or parasitic depending on environmental conditions. We suggest that facultative parasites with phenotypically plastic life-history strategies may serve as evolutionary stepping-stones towards obligate parasitism. Pre-adaptations provide a starting point for the transition towards opportunistic or facultative parasitism, but what evolutionary mechanism underlies the transition from facultative to obligate parasitism? In this Opinion Piece, we outline how facultative parasites could evolve towards obligate parasites via genetic assimilation, either alone or in combination with the Baldwin effect. We further describe the key predictions stemming from each of these evolutionary pathways. The importance of genetic assimilation in evolution has been hotly debated. Studies on facultative parasites may not only provide key insights regarding the evolution of parasitism, but also provide ideal systems in which to test evolutionary theory on genetic accommodation.

Evolution

This chapter takes up the Extended Evolutionary Synthesis in order to empirically enrich the nature-culture theory developed thus far. It considers three themes in the EES—phenotypic plasticity, genetic accommodation, and niche construction—and uses these to argue that the agency of organisms has a nontrivial influence on the evolutionary futures of species. The upshot of this argument is that habits are heritable (though this Lamarckian theme is now to be understood in a Darwinian context). The evolutionary influence of organism agency implies a phylogenetic expression of art in nature. An evolutionary extension of Poinsot’s customary sign is also suggested here, so that nature is ‘habituated’ in its forms and ‘customised’ in its meanings by the natural art of evolution. There is, then, a cultural dimension present through the whole biological order and through all of evolutionary history.

Adaptation to climate change through genetic accommodation and assimilation of plastic phenotypes

Theory suggests that evolutionary changes in phenotypic plasticity could either hinder or facilitate evolutionary rescue in a changing climate. Nevertheless, the actual role of evolving plasticity in the responses of natural populations to climate change remains unresolved. Direct observations of evolutionary change in nature are rare, making it difficult to assess the relative contributions of changes in trait means versus changes in plasticity to climate change responses. To address this gap, this review explores several proxies that can be used to understand evolving plasticity in the context of climate change, including space for time substitutions, experimental evolution and tests for genomic divergence at environmentally responsive loci. Comparisons among populations indicate a prominent role for divergence in environmentally responsive traits in local adaptation to climatic gradients. Moreover, genomic comparisons among such populations have identified pervasive divergence in the regulatory regions of environmentally responsive loci. Taken together, these lines of evidence suggest that divergence in plasticity plays a prominent role in adaptation to climatic gradients over space, indicating that evolving plasticity is also likely to play a key role in adaptive responses to climate change through time. This suggests that genetic variation in plastic responses to the environment (G × E) might be an important predictor of species' vulnerabilities to climate-driven decline or extinction.This article is part of the theme issue ‘The role of plasticity in phenotypic adaptation to rapid environmental change’.

Cognitive gadgets and genetic accommodation

Heyes argues that human metacognitive strategies (cognitive gadgets) evolved through cultural rather than genetic evolution. Although we agree that increased plasticity is the hallmark of human metacognition, we suggest cognitive malleability required the genetic accommodation of gadget-specific processes that enhanced the overall cognitive flexibility of humans.