The role of developmental plasticity in evolutionary innovation

Explaining the origins of novel traits is central to evolutionary biology. Longstanding theory suggests that developmental plasticity, the ability of an individual to modify its development in response to environmental conditions, might facilitate the evolution of novel traits. Yet whether and how such developmental flexibility promotes innovations that persist over evolutionary time remains unclear. Here, we examine three distinct ways by which developmental plasticity can promote evolutionary innovation. First, we show how the process of genetic accommodation provides a feasible and possibly common avenue by which environmentally induced phenotypes can become subject to heritable modification. Second, we posit that the developmental underpinnings of plasticity increase the degrees of freedom by which environmental and genetic factors influence ontogeny, thereby diversifying targets for evolutionary processes to act on and increasing opportunities for the construction of novel, functional and potentially adaptive phenotypes. Finally, we examine the developmental genetic architectures of environment-dependent trait expression, and highlight their specific implications for the evolutionary origin of novel traits. We critically review the empirical evidence supporting each of these processes, and propose future experiments and tests that would further illuminate the interplay between environmental factors, condition-dependent development, and the initiation and elaboration of novel phenotypes.     

Evolution of growth by genetic accommodation in Icelandic freshwater stickleback

Classical Darwinian adaptation to a change in environment can ensue when selection favours beneficial genetic variation. How plastic trait responses to new conditions affect this process depends on how plasticity reveals to selection the influence of genotype on phenotype. Genetic accommodation theory predicts that evolutionary rate may sharply increase when a new environment induces plastic responses and selects on sufficient genetic variation in those responses to produce an immediate evolutionary response, but natural examples are rare. In Iceland, marine threespine stickleback that have colonized freshwater habitats have evolved more rapid individual growth. Heritable variation in growth is greater for marine full-siblings reared at low versus high salinity, and genetic variation exists in plastic growth responses to low salinity. In fish from recently founded freshwater populations reared at low salinity, the plastic response was strongly correlated with growth. Plasticity and growth were not correlated in full-siblings reared at high salinity nor in marine fish at either salinity. In well-adapted lake populations, rapid growth evolved jointly with stronger plastic responses to low salinity and the persistence of strong plastic responses indicates that growth is not genetically assimilated. Thus, beneficial plastic growth responses to low salinity have both guided and evolved along with rapid growth as stickleback adapted to freshwater.     

Molecular mechanisms of canalization: Hsp90 and beyond

The Hsp90 chaperone machine facilitates the maturation of a diverse set of ‘client’ proteins. Many of these Hsp90 clients are essential nodes in signal transduction pathways and regulatory circuits, accounting for the important role Hsp90 plays in organismal development and responses to the environment. Recent findings suggest a broader impact of the chaperone on phenotype: fully functional Hsp90 canalizes wild-type phenotypes by suppressing underlying genetic and epigenetic variation. This variation can be expressed upon challenging the Hsp90 machinery by environmental stress, genetic or pharmaceutical targeting of Hsp90. The existence of Hsp90-buffered genetic and epigenetic variation together with plausible release mechanisms has wide-ranging implication for phenotype and possibly evolutionary processes. Here, we discuss the role of Hsp90 in canalization and organismal plasticity, and highlight important questions for future experimental inquiry.     

Environmentally induced phenotypes and DNA methylation: how to deal with unpredictable conditions until the next generation and after

Organisms often respond to environmental changes by producing alternative phenotypes. Epigenetic processes such as DNA methylation may contribute to environmentally induced phenotypic variation by modifying gene expression. Changes in DNA methylation, unlike DNA mutations, can be influenced by the environment; they are stable at the time scale of an individual and present different levels of heritability. These characteristics make DNA methylation a potentially important molecular process to respond to environmental change. The aim of this review is to present the implications of DNA methylation on phenotypic variations driven by environmental changes. More specifically, we explore epigenetic concepts concerning phenotypic change in response to the environment and heritability of DNA methylation, namely the Baldwin effect and genetic accommodation. Before addressing this point, we report major differences in DNA methylation across taxa and the role of this modification in producing and maintaining environmentally induced phenotypic variation. We also present the different methods allowing the detection of methylation polymorphism. We believe this review will be helpful to molecular ecologists, in that it highlights the importance of epigenetic processes in ecological and evolutionary studies.     

Cytosine methylation levels in the genome ofStellaria longipes

Environment-induced alteration of DNA methylation levels was investigated inStellaria longipes (Caryophyllaceae). Total cytosine methylation levels were measured using HPLC in 6 genets representing two ecotypes (alpine and prairie) grown in short day photoperiod and cold temperature (SDC) and long day photoperiod and warm temperature (LDW) conditions. The levels of methylated cytosine were 16.54-22.20% among the three genets from the alpine and 12.62–24.70% in the three prairie genets when they were grown in SDC conditions. After the plants were moved to the LDW conditions, all of the three genets from the alpine showed decreasing levels of DNA methylation up to 6 days of growing in LDW. When the plants continued to grow in LDW for 10 days the average methylation level in the prairie genotypes showed no significant change. Cytosine methylation level was also detected inHpall andSau3AI restriction sites using the coupled restriction enzyme digestion and random amplification (CRED-RA) procedure, in which 15 random primers were used. Fifty per cent of the amplified bands with either or both of these two restriction sites were identified as being methylated in an alpine genotype (1C) and approximately 66% were found to be methylated in a prairie genotype (7C). It was observed that the change in growing conditions from SDC to LDW induced a decrease of methylation levels inHpall sites.     

Diet and hormonal manipulation reveal cryptic genetic variation: implications for the evolution of novel feeding strategies

When experiencing resource competition or abrupt environmental change, animals often must transition rapidly from an ancestral diet to a novel, derived diet. Yet, little is known about the proximate mechanisms that mediate such rapid evolutionary transitions. Here, we investigated the role of diet-induced, cryptic genetic variation in facilitating the evolution of novel resource-use traits that are associated with a new feeding strategy—carnivory—in tadpoles of spadefoot toads (genus Spea). We specifically asked whether such variation in trophic morphology and fitness is present in Scaphiopus couchii, a species that serves as a proxy for ancestral Spea. We also asked whether corticosterone, a vertebrate hormone produced in response to environmental signals, mediates the expression of this variation. Specifically, we compared broad-sense heritabilities of tadpoles fed different diets or treated with exogenous corticosterone, and found that novel diets can expose cryptic genetic variation to selection, and that diet-induced hormones may play a role in revealing this variation. Our results therefore suggest that cryptic genetic variation may have enabled the evolutionary transition to carnivory in Spea tadpoles, and that such variation might generally facilitate rapid evolutionary transitions to novel diets.     

The genetic and environmental basis of adaptive differences in shoaling behaviour among populations of Trinidadian guppies,Poecilia reticulata

The degree of plasticity an individual expresses when moving into a new environment is likely to influence the probability of colonization and potential for subsequent evolution. Yet few empirical examples exist where the ancestral and derived conditions suggest a role for plasticity in adaptive genetic divergence of populations. Here we explore the genetic and plastic components of shoaling behaviour in two pairs of populations of Poecilia reticulata (Trinidadian guppies). We contrast shoaling behaviour of guppies derived from high‐ and low‐predation populations from two separate drainages by measuring the shoaling response of second generation laboratory‐reared individuals in the presence and absence of predator induced alarm pheromones. We find persistent differences in mean shoaling cohesion that suggest a genetic basis; when measured under the same conditions high‐predation guppies form more cohesive shoals than low‐predation guppies. Both high and low‐predation guppies also exhibit plasticity in the response to alarm pheromones, by forming tighter, more cohesive shoals. These patterns suggest a conserved capacity for adaptive behavioural plasticity when moving between variable predation communities that are consistent with models of genetic accommodation.     

PERSPECTIVE: GENETIC ASSIMILATION AND A POSSIBLE EVOLUTIONARY PARADOX: CAN MACROEVOLUTION SOMETIMES BE SO FAST AS TO PASS US BY?

Abstract.— The idea of genetic assimilation, that environmentally induced phenotypes may become genetically fixed and no longer require the original environmental stimulus, has had varied success through time in evolutionary biology research. Proposed by Waddington in the 1940s, it became an area of active empirical research mostly thanks to the efforts of its inventor and his collaborators. It was then attacked as of minor importance during the \"hardening\" of the neo-Darwinian synthesis and was relegated to a secondary role for decades. Recently, several papers have appeared, mostly independently of each other, to explore the likelihood of genetic assimilation as a biological phenomenon and its potential importance to our understanding of evolution. In this article we briefly trace the history of the concept and then discuss theoretical models that have newly employed genetic assimilation in a variety of contexts. We propose a typical scenario of evolution of genetic assimilation via an intermediate stage of phenotypic plasticity and present potential examples of the same. We also discuss a conceptual map of current and future lines of research aimed at exploring the actual relevance of genetic assimilation for evolutionary biology.     

Jack of all trades,master of some? On the role of phenotypic plasticity in plant invasions

Invasion biologists often suggest that phenotypic plasticity plays an important role in successful plant invasions. Assuming that plasticity enhances ecological niche breadth and therefore confers a fitness advantage, recent studies have posed two main hypotheses: (1) invasive species are more plastic than non-invasive or native ones; (2) populations in the introduced range of an invasive species have evolved greater plasticity than populations in the native range. These two hypotheses largely reflect the disparate interests of ecologists and evolutionary biologists. Because these sciences are typically interested in different temporal and spatial scales, we describe what is required to assess phenotypic plasticity at different levels. We explore the inevitable tradeoffs of experiments conducted at the genotype vs. species level, outline components of experimental design required to identify plasticity at different levels, and review some examples from the recent literature. Moreover, we suggest that a successful invader may benefit from plasticity as either (1) a Jack-of-all-trades, better able to maintain fitness in unfavourable environments; (2) a Master-of-some, better able to increase fitness in favourable environments; or (3) a Jack-and-master that combines some level of both abilities. This new framework can be applied when testing both ecological or evolutionary oriented hypotheses, and therefore promises to bridge the gap between the two perspectives.