Evolution of Phenotypic Plasticity and Gene Expression during Character Displacement

Abstract

Character displacement – trait evolution that arises as an adaptive response to competition between species – is central to the origins, abundance and distribution of biodiversity. Yet, until recently, little was known of character displacement's underlying mechanisms. Although character displacement is assumed to arise solely through changes in deoxyribonucleic acid (DNA) sequence, many species can also respond adaptively to competition by facultatively altering traits via phenotypic plasticity, which frequently entails changes in gene expression. New research has revealed that these two mechanisms might often act together during character displacement. In particular, character displacement might proceed through an initial phase in which trait (and gene expression) differences are environmentally induced to a latter phase in which such differences become fixed via changes in DNA sequence. This plasticity‐first hypothesis has increasing support, suggesting that it may be a common pathway to character displacement.

Key Concepts

  • Competition is a key driver of phenotypic divergence between species.
  • Character displacement is an evolutionary process in which natural selection causes a shift in phenotype production to reduce competition.
  • This shift often causes competing lineages to differ more where they occur together (sympatry) than where each occurs in the other's absence (allopatry).
  • Both DNA sequence changes and phenotypic plasticity can play a role in mediating character displacement.
  • Competitively mediated phenotypic plasticity involves environmentally induced changes in gene expression.
  • Character displacement might undergo plasticity‐first evolution, whereby it transitions from an environmentally induced phase to a genetically fixed one.
  • An example of plasticity‐mediated character displacement comes from spadefoot toad (genus Spea) tadpoles.
  • As a consequence of character displacement, sympatric populations of one species (Spea bombifrons) have lost diet‐dependent plasticity in gene expression.
  • Thus, character displacement has facilitated genetic assimilation at both the phenotypic and molecular levels in this species.
  • Further exploration of character displacement's underlying mechanisms might provide some of the most compelling cases of plasticity‐first evolution and genetic assimilation in nature.

Keywords: adaptive divergence; character displacement; competition; ecological developmental biology; gene expression; genetic accommodation; genetic assimilation; genetics of adaptation; maternal effects; phenotypic plasticity; spadefoot toads

Figure 1. How character displacement unfolds and is detected. (a) Initially, two species encounter each other and overlap in traits associated with resource use or reproduction, indicated here by the two overlapping bell‐shaped curves. Character displacement arises when individuals most dissimilar from the average resource‐use or reproductive phenotypes of another species are more successful at acquiring resources or at reproducing than other members of their population. (b) Consequently, the most divergent individuals should experience the highest fitness, and the two species should evolve to be less similar to each other. Character displacement is indicated when the difference between species in mean trait value is greater after selection (dA) than before selection (dB). In practice, this process is most often detected by a distinctive pattern of divergence (c) in which the two species are more dissimilar to each other in sympatry, where there is selection for divergence, than in allopatry, where there is no such selection.
Figure 2. An example of character displacement observed in the wild. (a) On a series of small islands off the east coast of Florida, USA, (a) the native lizard, A. carolinensis, prefers to perch in trees (b) about a meter above ground. However, when another species, A. sagrei, was introduced onto some of these islands, A. carolinensis shifted to a higher perch site, and thereby reduced competition with this lower perching introduced species. (c) Moreover, in only 20 generations, A. carolinensis on the invaded islands had adapted to their higher perch sites by evolving changes to their toes, which they use to grasp trees. Based on data in Stuart et al. . Photo by D. Pfennig.
Figure 3. An example of how phenotypic plasticity can initiate character displacement. In this example, (a) a bee feeding on flower is (b) joined by a superior competitor, a wasp, whose presence, in turn, (c) causes the bee to shift to an alternative type of flower. Such a sequence of events would constitute ecological character displacement if bees with different genotypes differ in their propensity to respond to wasps, and if those that leave a flower in response to wasps experience less competition and thereby come to predominate in the population. Moreover, as described in the main text, these induced responses might even promote fixed (i.e. constitutively expressed) differences between species in foraging behaviour. Redrawn from Pfennig, D. W., and K. S. Pfennig. 2012. Evolution's wedge: competition and the origins of diversity. University of California Press, Berkeley, CA.
Figure 4. Character displacement in spadefoot toads, Spea multiplicata and Sp. bombifrons. Each of these two species produces alternative tadpole resource‐use phenotypes: (a) a small‐headed omnivore morph, which feeds mostly on plants and detritus and (b) a large‐headed carnivore morph, which feeds mostly on large animal prey, such as anostracan fairy shrimp (shown here). (c) Where each species occurs in allopatry, they produce similar, intermediate frequencies of omnivores and carnivores. However, where they occur in sympatry, Sp. multiplicata shifts to producing mostly omnivores, whereas Sp. bombifrons shifts to producing mostly carnivores. By diverging in resource‐use phenotypes, these two species reduce competition for food. Photos by D. Pfennig.
Figure 5. Evidence of gene expression evolution during character displacement. (a) Examples of genes for which levels of expression were measured in alternative carnivore and omnivore morph tadpoles of spadefoot toads when all were reared under common conditions. Although most genes display no morph‐specific differences in expression level (such as the thrap3 gene shown here), some genes are expressed more highly in omnivores than in carnivores (e.g. pnlip), whereas other genes are expressed more highly in carnivores than in omnivores (e.g. pm20d2). Data from Leichty et al. . (b) Although different genes displayed different patterns of gene regulatory evolution in spadefoots, the combined gene expression profile of nine differentially expressed (biased) genes reveals that individuals derived from sympatry (that have undergone character displacement) have lost the diet‐induced gene expression plasticity present in individuals derived from allopatry (that have not undergone character displacement). Thus, during the evolution of character displacement, gene expression has evolved in parallel with changes in morphology. Data from Levis et al. . Photo by D. Pfennig.
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Levis, Nicholas A, and Pfennig, David W(Aug 2018) Evolution of Phenotypic Plasticity and Gene Expression during Character Displacement. In: eLS. John Wiley & Sons Ltd, Chichester. http://www.els.net [doi: 10.1002/9780470015902.a0028159]