Does phenotypic plasticity initiate developmental bias?

Abstract

The generation of variation is paramount for the action of natural selection. Although biologists are now moving beyond the idea that random mutation provides the sole source of variation for adaptive evolution, we still assume that variation occurs randomly. In this review, we discuss an alternative view for how phenotypic plasticity, which has become well accepted as a source of phenotypic variation within evolutionary biology, can generate nonrandom variation. Although phenotypic plasticity is often defined as a property of a genotype, we argue that it needs to be considered more explicitly as a property of developmental systems involving more than the genotype. We provide examples of where plasticity could be initiating developmental bias, either through direct active responses to similar stimuli across populations or as the result of programmed variation within developmental systems. Such biased variation can echo past adaptations that reflect the evolutionary history of a lineage but can also serve to initiate evolution when environments change. Such adaptive programs can remain latent for millions of years and allow development to harbor an array of complex adaptations that can initiate new bouts of evolution. Specifically, we address how ideas such as the flexible stem hypothesis and cryptic genetic variation overlap, how modularity among traits can direct the outcomes of plasticity, and how the structure of developmental signaling pathways is limited to a few outcomes. We highlight key questions throughout and conclude by providing suggestions for future research that can address how plasticity initiates and harbors developmental bias.

Keywords: cryptic genetic variation; developmental signaling pathways; flexible stem; plasticity integration.

Figure 1

The preorbital region of fishes appears to possess developmental bias affecting its size and length. This is apparent across examples of adaptive radiation, population‐level adaptive divergence or resource polymorphism, and in morphological plasticity. In some cases, patterns of evolution match patterns of plasticity. Also, plasticity can show a similar pattern of response in spite of widely different environmental cues. In (a,b), we see that major trends in the adaptive radiations of cyprinids comprising over 3,000 (adapted from Hernandez & Staab, 2015) and African cichlids comprising over 1,200 species (adapted from Cooper et al., 2010) respectively, involve changes in the preorbital region of the craniofacial apparatus. Similarly, at the level of populations in (c,e), we see that adaptive divergence or resource polymorphisms involve changes in the preorbital region. Specifically, in (c,d), we see two cases of divergence in three‐spined sticklebacks showing a similar change in preorbital length. However, in (c), divergence is occurring along a thermal habitat gradient between geothermally warmed and ambient populations (red = warmed, blue = ambient; Pilakouta et al., 2019), whereas in (d) divergence is occurring along a limnetic (long side) and benthic (short side) gradient (image credit, Elizabeth Carefoot). In (e), planktivorous (long side) and benthivorous (ecomorphs) of arctic charr (Salvelinus alpinus) from Lake Thingvallavatn, Iceland are depicted (drawn by Eggert Petursson). In (f,g), we see the outcome of plasticity experiments, with the effects of limnetic (long side) and benthic (short side) foraging treatments in F3 hybrid cichlids (from Parsons et al., 2016). In (g), we see the morphological responses of juvenile sticklebacks to rearing at 18°C (long side) and 12°C (short side) (Campbell and Parsons, unpublished), which follow a similar pattern to limnetic (long side) and benthic (short side) treatments in sticklebacks depicted in (g); (from Wund et al., 2008) [Color figure can be viewed at wileyonlinelibrary.com]

Figure 2

Four scenarios (a–d) for how systems with three developmental pathways (red, purple, and blue) may respond to environmental inputs (green arrowheads). In (a), an open developmental system exists whereby any possible phenotype can be produced by any type of environmental input. There are numerous connections between elements of the pathways (colored blocks), allowing for a high degree of flexibility. The outcomes of these processes are likely to be highly variable (indicated by error bars) and thus provide a high degree of evolutionary potential. Though these phenotypes can provide adaptive variation, they are unrefined responses that can be improved through selective processes that alter developmental systems. In (b), a developmental system is presented that has been exposed to a single and constant environmental input. This environment has selectively favored a directional adaptive response, which is reflected in a loss of connections between pathway elements that are infrequently used or cause antagonistic pleiotropy. This has resulted in a more refined phenotypic response (note the more extreme body shape relative to the blue phenotype in (a)). Further, while the other phenotypes are still possible, the adaptive process has resulted in a relatively small degree of phenotypic variation for the most frequently expressed phenotype. The differences between (a) and (b) may be representative of processes such as genetic accommodation or genetic assimilation. Similarly, in (c), connections between pathway elements have been lost to optimize the frequency of two phenotypes in response to two distinct environmental inputs. These inputs could occur simultaneously or as an oscillating system that both favor the refinement of two phenotypes (reflected in more‐extreme body shapes of the red and blue phenotypes) with low levels of variation. Finally, in (d), a shift in environmental parameters has favored the development of a single phenotype but the connections for the ancestral adaptive phenotype remain latent in the developmental system (gray arrows). In this case, developmental trade‐offs and antagonistic pleiotropy are environmentally dependent and avoided over evolutionary time by stable environmental cues that favor a single phenotype different from the “potential” phenotype (gray). The latent program can be reactivated by a further shift in environmental inputs (or mutation) and elicit a phenotype that reflects the past adaptation. However, the re‐emerged phenotype possesses a high degree of variation due to the loss of refinement over evolutionary time whereas these aspects of the developmental system were silent and effectively neutral to selection [Color figure can be viewed at wileyonlinelibrary.com]

Figure 3

Potential mechanisms of developmental bias in the preorbital region of Malawi cichlids could lie in patterns of modularity (a, b), and the reliance of phenotypic variation on a limited number of developmental pathways (c, d). (a) Depiction of the landmarks used to assess both covariance and shape in the craniofacial region of over 80% of the genera of African cichlids from Lake Malawi (from Cooper et al., 2010). The preorbital region (blue lines connecting landmarks) comprises a distinct variational module in Malawi cichlids (b). The projection of plastic variation on such a “scaffold” for development lends itself well to the observations of bias in the preorbital region (see Figure 1). Further, the projection of variation on a developmental system that relies on few pathways would be more likely to result in similar phenotypes. This is seen in the similar production of a “lockjaw” phenotype in Labeotropheus fuelleborni embryos (control group = C) in response to lithium chloride (d), which is an agonist of Wnt/β‐catenin signaling (from Parsons, Trent Taylor, Powder, & Albertson, 2014), as well as to bepridil (e), which is an inhibitor of calcium signaling (Walker, McWhinnie, and Parsons, unpublished). These relatively similar phenotypic responses to different molecular targets suggest that craniofacial development in cichlids is developmentally limited with particularly strong effects on the preorbital region. Note that the orbital bone has been highlighted in these pictures, and that swelling of the eye has occurred due to staining and preservation methods [Color figure can be viewed at wileyonlinelibrary.com]