Genetic and environment-induced pathwaysto innovation: on the possibility of a universalrelationship between robustness and adaptationin complex biological systems
James M. Whitacre
Received: 8 September 2010/Accepted: 27 January 2011
Springer Science+Business Media B.V. 2011
Recently, there has been considerable interest in the idea that mutationalrobustness enhances the propensity for future adaptations, i.e. evolvability, if evolutionproceeds over a neutral network that extends far throughout a fitness landscape. While thegenetic neutral network (NN-G) model may have important implications to our under-standing of evolution, little has been done to integrate these theoretical developments withempirical evidence that heritable phenotypes can also srcinate and become fixated as aresult of changes in the environment. In this brief commentary, I reconsider the role of environmental change in the adaptation of species and ask whether positive robustness-evolvability relationships might exist not only for genetic but also environmental buffering.In particular, I ask whether the insensitivity of species fitness towards variability in itsenvironment can have a positive influence on the likelihood of future environment-inducedadaptations (i.e. ecological opportunities) in a manner analogous to that proposed by theNN-G model. After outlining scenarios where such a counter-intuitive relationship appearsplausible, I comment on the merits of evolutionary theories that can integrate comple-mentary pathways to adaptation under static and time-variant environments. I also spec-ulate on some of the features that such a theory might have.
Cryptic genetic variation
Neutral evolution theory
Phenotypic plasticity
Genetic assimilation
Genetic accommodation
Entropic barriers
Ecological inheritance
Text box: glossary
Cryptic genetic variation (CGV) CGV is a population property that involves the fol-lowing features: (1) in its native environment a population maintains high levels of genetic
J. M. Whitacre (
)School of Computer Science, University of Birmingham, Edgbaston, UK e-mail: J. M. WhitacreDepartment of Bioinformatics and Biophysics, National University of Mongolia, Ulan Bator, Mongolia
Evol EcolDOI 10.1007/s10682-011-9464-z
diversity but exhibits relatively few trait differences, i.e. genetic differences are cryptic and(2) when exposed to new environmental conditions (or systematically exposed to newalleles), the population displays new heritable phenotypic variability.Neutral network A neutral network is defined as a connected graph of nodes with equalfitness. One can consider it a connected set of external and internal conditions within whicha species has the same fitness. Notice that connectedness implies that each node within thenetwork can be reached by every other without changing the species fitness along the pathof arcs. Illustrations of genetic and environmental neutral networks are given in Fig.1.Genetic Neutral Network (NN-G) NN-G is a neutral network in which the class of condition changes is restricted to single gene mutations. Such networks represent fitness-neutral regions within a classic fitness landscape.Environmental neutral network (NN-E) NN-E is a neutral network in which the class of condition changes is restricted to changes in the environment experienced by an organismduring development.Evolvability Evolvability refers to the propensity of a species to discover heritable andbeneficial phenotypes. Evolvability requires access to distinct heritable traits and it requiresthat some heritable differences can be transformed into beneficial innovations duringdevelopment within a particular environment. The first requirement—the ability to accessheritable phenotypic variation—is an important precondition and often used proxy forevolvability.Robustness Robustness describes the insensitivity of some functionality or measuredbiological trait to a set of distinct conditions. This article focuses primarily on therobustness of high level traits that influence survival and fecundity.Mutational robustness This refers to the extent that species fitness is robust towardsgenetic mutations.
The genetic neutral network hypothesis for adaptationThere are a growing number of studies reporting evidence of a positive relationshipbetween mutational robustness and evolvability at microevolutionary scales (Aldana et al.2007; Bloom et al.2006; Babajide et al.1997; van Nimwegen and Crutchfield2000; Ciliberti et al.2007; Wagner2008; Whitacre and Bender2010) with possible repercussions to our understanding of macroevolution and speciation (Gavrilets1997) (for reviews see(Wagner2008; Wagner2008). The hypothesis put forth is that networks of fitness neutral genotypes result in mutational robustness and reduced accessibility of heritable phenotypesover short timescales. With little genetic variation expressed as phenotypic variation,natural selection has few immediate options for modifying traits. On the other hand,genetic drift over neutral/buffered mutations can also provide mutational access to manydistinct heritable phenotypes that are reached from directly off the genetic neutral network over longer periods of time. This leads to the seemingly paradoxical conclusion (resolvedthrough a separation of timescales) that the suppression of heritable phenotypic variationcan ultimately increase the accessibility of distinct heritable phenotypes (Wagner2008).
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Because access to distinct heritable phenotypes is a prerequisite for adaptation, muta-tional robustness has thus been described as a potential facilitator of evolvability, i.e. thepropensity for a species to adapt. This genetic neutral network (NN-G) hypothesis has beensupported by recent computer models of biological systems (Aldana et al.2007; Bloomet al.2006; Babajide et al.1997; van Nimwegen and Crutchfield2000; Ciliberti et al.2007;
Fig. 1 a
Nodes represent genotypes and connections between nodes indicate that two genotypes differ byonly a single mutation. The connected graph of 
black nodes
illustrates a genetic neutral network (NN-G).The neutral network implies that for a particular environment, none of these genotypes are selectivelydistinguishable.
Square grey nodes
represent genotypes that are mutationally accessible from the NN-G butthat have phenotypic and selective differences when compared to members of NN-G. As observed in generegulatory network simulations (Ciliberti et al.2007) and abstract genome:proteome models (Whitacre andBender2010), it is assumed that the phenotypes associated with grey nodes will change depending on theirposition in genotype space. Thus, as NN-G grows and extends throughout larger regions of genotype space,it is assumed that the number of unique phenotypes accessible from NN-G will also grow (
illustrated inbottom figure
Nodes represent environmental patches and connections between nodes indicate that twopatches are physically connected so that a population can move directly from one patch to the other. Theconnected graph of black nodes illustrates an environmental neutral network (NN-E). The neutral network implies that a population can move to different patches without consequences to survival or reproductivesuccess. While this does not preclude the possibility that different patches in NN-E are associated withmildly distinct trait distributions, it is assumed that these distinctions do not result in changes to selectionthat have evolutionary consequences. As with the NN-G pathway, positive associations may exist betweenthe number of accessible environments in which species fitness is robust (NN-E) and the number of accessible environments that induce heritable (and sometimes selectively relevant) phenotypic differences ina population (
illustrated in bottom figure
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Wagner2008; Whitacre and Bender2010) and appears consistent with the available data related to biomolecular evolution (Bloom et al.2006; Wagner2008). The model clearly relies on a gene-centric view of evolution where novel alleles are encountered and occa-sionally result in novel and selectively relevant phenotypes.Environment-induced adaptationWhile the genetic basis of heredity is not disputed, the introduction of novel alleles is notthe only way that heritable phenotypes srcinate (Palmer2004; Gibson and Dworkin2004; Schlichting2008; Waddington1953; Waddington1957; Schmalhausen and Dobzhansky 1949; West-Eberhard2005; West-Eberhard2003; Barrett and Schluter2008). Because the phenotype is the result of self-environment organization, those conditions provided by anorganism’s genetic background, environmental background, and their interaction duringdevelopment, will determine the qualitative character, quantitative attributes, and thetiming of expressed traits. Changes in environmental inheritance due to movement (e.g.migration, seed dispersal), external perturbation [e.g. geologic cycles, ecological regimeshifts, epigenetic inheritance (Anway et al.2005)], and various forms of local environmentshaping [e.g. niche construction (Odling-Smee et al.1996; Day et al.2003), sexual selection (West-Eberhard2003), behavioural and genetic coevolution (Agrawal2001), parental inheritance (Uller2008; Jablonka et al.1995), cultural inheritance (Dawkins1983; Dennett1995)] can expose the conditional plasticity of a trait, i.e. phenotypic plasticity.The role that the environment plays in the srcination of new traits and its consequences toadaption have been discussed at length in (West-Eberhard2003; Pfennig et al.2010; Sultan 2007) [but also see (Agrawal2001; Schlichting and Pigliucci1998; Newman1994)]. At the population level, the conditional exposure of trait variation is often discussed as aphenomena known as cryptic genetic variation (CGV) or ‘hidden reaction norms’or‘‘genetic charge’’ (Le Rouzic and Carlborg2008) [for reviews see (Gibson and Dworkin2004; Schlichting2008; McGuigan and Sgro `2009)]. CGV describes heritable phenotypicvariation that is hidden under ‘‘normal conditions’’ but that is released in the presence of novel conditions. Studies of CGV have found evidence that novel conditions can comeboth in the form of novel alleles and novel environments, and that the phenotypic con-sequences can be remarkably similar between these perturbation classes.For circumstances where the environment induces a new adaptive trait, the inheritanceof this trait is generally expected to depend on subsequent genetic modifications. While thepersistence of a change to the environment, exposure to similarly modified environments,and trans-generational carry-over effects after a short-lived environmental change (Jab-lonka et al.1995) can, in principle, induce and maintain novel traits, it is genetic assim-ilation (Waddington1953; Waddington1957; Schmalhausen and Dobzhansky1949) and genetic accommodation (West-Eberhard2005; West-Eberhard2003) that act to preserve the inheritance of phenotypic adaptations in the face of further environmental modifica-tions (West-Eberhard2003; Pigliucci et al.2006). At present, it is not clear whether the srcination of heritable phenotypes by genetic orenvironmental novelty has been more relevant to evolution (McGuigan and Sgro`2009)however, the clearest available evidence suggests that these pathways are equally common(Palmer2004).West-Eberhard (2003) and Schlichting and Pigliucci (1998) argue that environment-induced phenotypic variation is a more likely source of heritable change, atleast partly due to evidence that environment-induced trait variation is more common(Houle et al.1996; Gibson2008), and potentially orders of magnitude more common (Lynch1988), in populations and species compared to gene-induced trait variation.
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